Multicausal etiology of the enteric syndrome in rabbits from Mexico

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García-Rubio, Linda G. Bautista-Gómez, José S. Martínez-Castañeda, Camilo Romero-Núñez" "autores" => array:4 [ 0 => array:3 [ "nombre" => "Virginia G." "apellidos" => "García-Rubio" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] ] ] 1 => array:4 [ "nombre" => "Linda G." "apellidos" => "Bautista-Gómez" "email" => array:2 [ 0 => "lgbautista@uaemex.mx" 1 => "lin_bag@yahoo.com.mx" ] "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "*" "identificador" => "cor0005" ] ] ] 2 => array:3 [ "nombre" => "José S." "apellidos" => "Martínez-Castañeda" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "b" "identificador" => "aff0010" ] ] ] 3 => array:3 [ "nombre" => "Camilo" "apellidos" => "Romero-Núñez" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] ] ] ] "afiliaciones" => array:2 [ 0 => array:3 [ "entidad" => "Centro Universitario UAEM Amecameca, Universidad Autónoma del Estado de México, Km 2.5 Carretera Amecameca-Ayapango, C.P. 56900 Amecameca, Estado de México, México" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Centro de Investigación y Estudios Avanzados en Salud Animal, Facultad de Medicina Veterinaria y Zootecnia, Universidad Autónoma del Estado de México. Carretera de Cuota Toluca-Atlacomulco km 15.5, C.P. 50200, Toluca, Estado de México, México" "etiqueta" => "b" "identificador" => "aff0010" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Multicausalidad del síndrome entérico en conejos de México" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1399 "Ancho" => 1633 "Tamanyo" => 118619 ] ] "descripcion" => array:1 [ "en" => "Agents isolated from enteric profiles in rabbits from Mexico." ] ] ] "textoCompleto" => "IntroductionThe enteritis complex was introduced by Whitney in 1976 to designate a group of diseases that include mucoid enteritis, typhlitis, typhlitis-diarrhea and hemorrhagic enteritis. Commonly observed symptoms include teeth grinding, anorexia, polydipsia, weakness, abdominal distension, profuse diarrhea, dehydration, hypothermia and death<a class="elsevierStyleCrossRef" href="#bib0290">18</a>. Enteropathies are recognized as a problem for domestic rabbits, being their etiology and pathogenesis poorly understood<a class="elsevierStyleCrossRef" href="#bib0220">4</a>. In commercial rabbit production, enteropathies are hard to diagnose; they can have a multifactorial etiology (hence the term “multifactorial enteritis”) and are also known as “enteric syndrome”<a class="elsevierStyleCrossRef" href="#bib0270">14</a>. This syndrome is a pathological complex characterized by various stressing and pathogenic factors acting synergistically, possessing varying degrees of virulence which can enhance their pathogenicity and cause damage to the intestinal tissue. Numerous studies have reported the isolation of Clostridium perfringens, Clostridium piliformis, Clostridium spiriforme, Escherichia coli<a class="elsevierStyleCrossRefs" href="#bib0305">21,35</a>, Salmonella spp., Klebsiella spp., Pseudomonas spp., Streptococcus aureus, Streptococcus spp., Campylobacter and Eimeria spp.,<a class="elsevierStyleCrossRefs" href="#bib0270">14,19,23,24</a>. Viruses seem to have an important but non-crucial role; overall, they are mild pathogens that do not induce severe clinical profiles<a class="elsevierStyleCrossRef" href="#bib0270">14</a>. Rotavirus<a class="elsevierStyleCrossRef" href="#bib0280">16</a>, Coronavirus<a class="elsevierStyleCrossRef" href="#bib0220">4</a>, and Parvovirus<a class="elsevierStyleCrossRef" href="#bib0285">17</a> have been reported and it has been suggested that they could exert direct pathogenic activity by initiating the development of bacterial infections and/or of other viral pathogens by inducing minimal alterations in the intestinal epithelium<a class="elsevierStyleCrossRef" href="#bib0285">17</a>. Enteric diseases are important in rabbit production and cause severe economic losses, due to high mortality indexes, decrease in growth and reduction in the feed conversion ratio<a class="elsevierStyleCrossRef" href="#bib0270">14</a>. Studies in Cuba, Japan and Argentina have reported digestive pathologies as the main cause of mortality with percentages of 57.9%, 48.9% and 43% respectively<a class="elsevierStyleCrossRef" href="#bib0320">24</a>. In Mexico there are few reports concerning the agents involved in these pathologies<a class="elsevierStyleCrossRef" href="#bib0395">39</a>. Because of this reason, the aim of this study was to isolate pathogens from enteric disease in rabbits from Mexico.Material and methodsFifty-eight rabbits with an enteric clinical profile were obtained from several rabbit meat production from the southeastern part of the State of Mexico, Mexico. The animals exhibited an enteric clinical profile that included depression, anorexia, dehydration, abdominal distension, liquid-to-mucoid diarrhea and death within 24h. Isolates were recovered from the intestinal contents through the necropsy service of the Amphitheater of Veterinary Medicine and Zootechnics of the Centro Universitario Amecameca (CU Amecameca), of the Universidad Autónoma del Estado de México (UAEMex). This study was authorized by the Bioethics Committee of the CU Amecameca (CBE/06/2013).Eimeria spp. were identified by microscopy and the parasitological flotation technique<a class="elsevierStyleCrossRef" href="#bib0345">29</a>. DNA was extracted from the stool samples using the ZR Fecal DNA MiniPrep™ (ZYMO Research, USA), according to the manufacturer's instructions. DNA samples were assessed quantitatively and qualitatively by measurements of absorbance in a Nano Drop 2000c (Thermo Scientific, USA). A PCR was also performed, using primers for the amplification of the ribosomal cistron, ITS1 region (400–500bp long) of Eimeria tenella, as reported by Oliveira et al.<a class="elsevierStyleCrossRef" href="#bib0295">19</a> (accession number AFO26388). The following reagents were added to 1mg of DNA to make 25μl PCR solution: 2.5mM MgCl2, 100mM each dATP, dCTP, dGTP, dTTP, 1.5U GoTaq Flexi DNA Polymerase (PROMEGA, USA), 5μl 5× Green GoTaq Flexi Buffer, and 0.8mM of each primer. The amplification conditions included 35 cycles of denaturation at 96°C for 45s, annealing at 54°C for 45s and extension at 72°C for 60s. A sequenced sample was included as positive control and DNA obtained from rabbit blood was used as negative control.The bacteriological analyses involved primary isolation in blood agar; identification was performed by colonial morphology and Gram staining. Gram negative bacteria were cultured in the following selective media: MacConkey, Salmonella-Shigella and brilliant green agar at 37°C incubation temperature and aerobiosis for 24–48h<a class="elsevierStyleCrossRef" href="#bib0210">2</a>. To identify Salmonella, the samples were previously inoculated in peptone water and tetrathionate broth. A colony of each growth produced was selected as a representative isolate and subcultured for further biochemical identification. Biochemical tests of oxidase, catalase, triple sugar iron, ornithine decarboxylase, sulfide indol motility and urease were performed<a class="elsevierStyleCrossRefs" href="#bib0225">5,10,14</a>. Gram positive bacteria were analyzed for evidence of catalase, coagulase, hemolysis, and cultured in mannitol salt agar<a class="elsevierStyleCrossRef" href="#bib0400">40</a>.To determine the E. coli pathotypes, we used a pathogen-specific multiplex PCR to detect enterotoxigenic E. coli (ETEC), enteropathogenic E. coli (EPEC), enteroinvasive E. coli (EIEC) and Shiga-toxin-producing or enterohemorrhagic E. coli (EHEC o STEC o VTEC), using specific primers, by the amplification of 150–650bp fragments for diverse virulence traits as reported by López-Saucedo et al.<a class="elsevierStyleCrossRef" href="#bib0275">15</a> Representative positive PCR products were purified and sequenced using an ABI PRISM 3500 genetic analyzer (Life Technologies, Carlsbad, CA).Rotavirus detection was accomplished by the amplification of a 380bp fragment of capsid protein VP6, employing primers as reported by Iturriza-Gomora et al.<a class="elsevierStyleCrossRef" href="#bib0260">12</a> RNA extraction was performed using GeneJET Viral DNA and the RNA Purification Kit (Thermo Scientific, USA). The two-step RT-PCR technique was implemented; complementary DNA (cDNA) was obtained by means of the SuperScript III Reverse Transcriptase (RT) (Thermo Scientific, USA). PCR conditions were as follows: Initial denaturation at 96°C for 10min, follow by 45 cycles of denaturation at 96°C for 45s, annealing at 61°C for 45s and an extension at 72°C for 30s, the final extension at 72°C for 5 min. As a positive control, we used the Rota teq pentavalent vaccine (MSD SNC, Lyon, France).In order to test the association between the presence of the identified agents and the clinical profiles, we used the Fisher's exact test, with a significance threshold of (p<0.05).ResultsOut of 58 intestine content samples, 35/58 (60.4%) were positive for at least one identification and 23 (39.6%) were in concurrence, including: 3/58 (5.2%) with two identifications and 14/58 (24.0%) with three identifications. Rotavirus was identified for the first time in rabbits from Mexico in 6/58 samples (10.3%), of which 5/6 samples (83.3%) showed the identification of concomitant infection by Rotavirus and other pathogens.We identified six highly pathogenic Eimeria species in 45/58 rabbits (77.5%); mildly pathogenic E. intestinalis in 2/58 rabbits (4.4%) and E. flavescens in 2/58 (4.4%); lowly pathogenic E. magna in 35/58 (77.7%), E. media in 8/58 (17.7%); E. perforans in 12/58 (26.6%) and E. vejdovsky in 4/58 (8.8%), followed by Aeromona spp. (15.5%) and E. coli in 5/58 (8.6%), corresponding to enteropathogenic E. coli (EPEC) while the other strains were non-diarrheagenic by PCR, using primers for bfpA detection<a class="elsevierStyleCrossRef" href="#bib0275">15</a>.There were 86 identifications in the 58 samples. <a class="elsevierStyleCrossRef" href="#fig0005">Figure 1</a> shows the frequency of detection per agent. The concurring presence of pathogenic agents identified in the intestine content samples is shown in <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>. Results of the Fisher's exact test showed a statistically significant association of the clinical profiles and the presence of Eimeria spp. (p=0.000), E. coli EPEC (p=0.09), Mannheimia spp. (p=0.001), Salmonella spp., Klebsiella spp., S. aureus and Enterococcus spp. (p=0.006) (<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>). In relation to the clinical profile observed, diarrhea (with varying characteristics) was the most frequent sign, followed by abdominal distension.<elsevierMultimedia ident="fig0005"></elsevierMultimedia><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><elsevierMultimedia ident="tbl0010"></elsevierMultimedia>DiscussionIn contrast with the results obtained by Szalo et al.<a class="elsevierStyleCrossRef" href="#bib0370">34</a>, who suggested that the enteropathy in rabbits is a bacterial disease and does not have a viral or parasitic etiology and with Martella et al.<a class="elsevierStyleCrossRef" href="#bib0280">16</a>, where rotavirus was the most frequent agent isolated from enteric profiles in rabbits, in the present study, Eimeria spp. was the most frequently recovered agent, both on its own and in association with other pathogens. Studies in other countries have reported the presence of eleven Eimeria species that affect rabbits in up to 70% of enteropathies, and, according to their level of pathogenicity, can cause reduced growth rate and feed conversion, and increased mortality<a class="elsevierStyleCrossRefs" href="#bib0295">19,21</a>. In this work we only identified by PCR six of the eleven Eimeria species in the samples, being E. magna and E. perforans the most frequently found, considered as mildly and lowly pathogenic respectively; however, although all the rabbits presented enteric disease, the association with other pathogens had not been reported. Interestingly in the present study, we found an association of Eimeria spp. with gram negative bacteria and less frequently with Gram positive bacteria. These results provide epidemiological evidence of synergism among Eimeria spp. and E. coli and other enteric pathogens. It seems that by being simultaneously present in the enteric profiles, these pathogens can increase their pathogenic potential<a class="elsevierStyleCrossRef" href="#bib0215">3</a>.The replication of Eimeria spp. within the epithelial cells of the intestine, alters the natural resistance barrier<a class="elsevierStyleCrossRef" href="#bib0350">30</a>, which is intensified due to various factors such as the production of inflammatory cytokines, mainly interleukin 6 (IL-6) and to a lesser degree interleukin 8 (IL-8) released as a result of massive cell lysis. These mechanisms are used by gram negative bacteria such as E. coli and Salmonella spp. to increase intestinal wall disorganization, consequently invading the tissue<a class="elsevierStyleCrossRefs" href="#bib0230">6,22</a>, facilitating bacterial adherence and penetration<a class="elsevierStyleCrossRef" href="#bib0335">27</a>. Further, some Eimeria species enhance host mucogenesis since the mucus layer of the gastrointestinal tract is an excellent source of nutrients for some bacteria<a class="elsevierStyleCrossRef" href="#bib0300">20</a>. Blankets and globular particles of mucus associated with numerous bacteria on villi and extensive inflammatory lesions have been observed in rabbits with an enteric profile and bacteria were observed attached to the site of serious cell damage<a class="elsevierStyleCrossRef" href="#bib0230">6</a>. They can take advantage of this scenario for synergies and exercise their mechanisms of pathogenicity or may be considered as secondary invaders.Aeromonas spp. are members of the microbiota of warm-blooded animals and have been reported to cause septicemia and gastroenteritis (with self-limiting acute diarrhea)<a class="elsevierStyleCrossRef" href="#bib0205">1</a>. Their mechanism of pathogenicity is through type III secretion systems, with production of cytotoxic, hemolytic, enterotoxic and lethal enterotoxin, which also alters the cytoskeletal signaling cascades and promotes bacterial growth<a class="elsevierStyleCrossRefs" href="#bib0325">25,28</a>. The pathogenic role of this bacterium in enteric disease has been demonstrated and studied in the present study, Aeromonas spp. occurred with a frequency of 10.47%. The isolation of Aeromonas spp., on their own or in association with other pathogens from the intestinal contents suggests their involvement in the enteric profiles.In our study, enteropathogenic E. coli (EPEC) was found in five animals (8.6%), which is very similar to Swennes et al.’s findings<a class="elsevierStyleCrossRefs" href="#bib0360">32,33</a>, who described 10.5 and 4.3% EPEC in laboratory rabbits. Lavazza et al.<a class="elsevierStyleCrossRef" href="#bib0270">14</a> found that E. coli was the only pathogen in about 40.0% of cases of domestic rabbits. Dewrée et al.<a class="elsevierStyleCrossRef" href="#bib0230">6</a> found that the most commonly isolated digestive tract bacteria pathogens were E. coli, but they did not find EPEC. This bacterium is a member of the intestinal microbiota and possibly several factors generate a state of immunosuppression, which allows significant replication of some opportunistic agents or performing synergy with other competing agents<a class="elsevierStyleCrossRefs" href="#bib0250">10,14,23,36</a>.We found that 60.4% of intestinal content samples were positive for one identification, 5.2% for two and 24% for three. Other studies in human detected enteropathogens in 66.4% of patients with diarrhea, a single enteric pathogen in 50.9% and multiple pathogens in 15.5%; concomitant infection by more than one enteric pathogen occurred in 18.6% of the infants and 29% contained multiple pathogens<a class="elsevierStyleCrossRef" href="#bib0240">8</a>.The enteric syndrome has a large impact on rabbit production. Several authors suggest that rotavirus could be the main cause of enteric disease in rabbits and also be implicated as the etiological agent of severe enteric outbreaks<a class="elsevierStyleCrossRefs" href="#bib0280">16,35</a>. Lavazza et al.<a class="elsevierStyleCrossRef" href="#bib0270">14</a> identified rotavirus in rabbits by electron microscopy (16.0%), detecting 3.3% to 36.6% in humans<a class="elsevierStyleCrossRefs" href="#bib0240">8,27,37</a>, our findings show the presence of rotavirus in fewer cases (10.3%). The concomitant identification of rotavirus and other pathogens was detected in 5/6 (83.3%) samples. In vitro models of pathogenesis indicate that synergism between rotavirus and invasive bacteria involve specific biologic pathways: the attachment of, or the invasion through an up-regulation of specific receptors<a class="elsevierStyleCrossRef" href="#bib0355">31</a>. Bhavnani et al.<a class="elsevierStyleCrossRef" href="#bib0215">3</a> found epidemiologic evidence of synergism between rotavirus and other enteric pathogens for producing enteric clinical profiles, either by enhancing attachment and bacterial invasion of intestinal epithelial cells or by producing inflammation promoting the development of bacteria by the release of fluid, mucin, cellular detritus and the secretion of antimicrobials, which could alter the composition of the gut microbiota, allowing pathogens to occupy their commensal niche. Lavazza et al.<a class="elsevierStyleCrossRef" href="#bib0270">14</a>, conclude that there was no association between viral positivity or negativity and the presence of bacteria. Our results agree with those of Dewrée et al.<a class="elsevierStyleCrossRef" href="#bib0230">6</a> and Rodriguez De Lara et al.<a class="elsevierStyleCrossRef" href="#bib0315">23</a>, about rotaviruses as the main cause of the epizootic outbreaks of diarrheas is questionable, particularly if considering that rotavirus are considered endemic and mildly pathogenic in commercial rabbitries. However, this is the first molecular report confirming the presence of rotavirus in the enteric profiles of rabbits from Mexico.In the bacteriological results in rabbits, Lavazza et al.<a class="elsevierStyleCrossRef" href="#bib0270">14</a> included E. coli, S. aureus, Klebsiella spp., Yersinia spp., Pasteurella multocida, C. perfringens and C. spiriforme. This study found E. coli, Aeromonas spp., Salmonella spp., Enterococcus spp., Streptococcus spp., S. aureus, Mannheimia spp., and Klebsiella spp. In humans, the results of several research works were similar: in Jordan, enteropathogenic E. coli (12.8%), enteroaggregative E. coli (10.2%), enterotoxigenic E. coli (5.7%), Shigella spp. (4.9%), Entamoeba histolytica (4.9%), Salmonella spp. (4.5%), Campylobacter jejuni/coli (1.5%), Cryptosporidium spp. (1.5%), enteroinvasive E. coli (1.5%), Giardia lamblia (0.8%) and Yersinia enterocolitica (0.4%)<a class="elsevierStyleCrossRef" href="#bib0395">39</a>; in Colombia, enteropathogenic E. coli (6.0%), enterohemorragic E. coli (2.8%), Aeromonas hydrophila (2.0%) and other pathogens (52.6%)<a class="elsevierStyleCrossRef" href="#bib0380">36</a> were identified; in the Netherlands, enteropathogenic E. coli were detected in 19.9%, and Salmonella enterica in 0.3%<a class="elsevierStyleCrossRef" href="#bib0240">8</a>; in Papua New Guinea, Shigella spp. (26.6%), enteropathogenic E. coli (8.5%), Salmonella spp. were found below the limit of detection<a class="elsevierStyleCrossRef" href="#bib0335">27</a>.Staphylococcus spp. make up the microbiota of the upper respiratory tract and lower urogenital tract, are transitory in the digestive tract and predominant in the small intestine and cecum; it has been observed that S. aureus produces yellow diarrhea in nursing rabbits<a class="elsevierStyleCrossRef" href="#bib0260">12</a>. Lavazza et al.<a class="elsevierStyleCrossRef" href="#bib0270">14</a> found Staphylococcus both in isolation and associated with E. coli and P. multocida; with and without viral presence. Furthermore, they found Streptococcus as single isolates from rabbits with enteritis. Our results show the presence of S. aureus in association with Eimeria spp. in 5.2%. Streptococcus spp., were found both on their own (1.7%) and in a concurrent manner with protozoa parasite Eimeria spp. (1.7%). Isolation frequency was not as high as in the case of other pathogen, however, their presence indicates involvement in promoting enteric profiles in rabbits.Enterococcus spp. are ubiquitous and are consistently found in animal gastrointestinal tracts. In pigs, the co-occurrence of Enterococcus genus and E. coli has been previously reported and this interaction has been found to contribute to the development of new neonatal porcine diarrhea<a class="elsevierStyleCrossRef" href="#bib0255">11</a>. Specifically, Enterococcus hirae has been associated with enteropathy in cats and with diarrhea in rats and nursing kittens<a class="elsevierStyleCrossRefs" href="#bib0235">7,9,13</a>. It has also been isolated from an outbreak of diarrhea in nursing rabbits with 85% morbidity and 50% mortality; rabbits died within a 3 day period<a class="elsevierStyleCrossRef" href="#bib0390">38</a>. In the present study, we found Enterococcus spp., without any associated pathogenic agent in two samples of intestinal content (3.5%) related to diarrhea episodes, which suggests they could be etiologic agents.Dewrée et al.<a class="elsevierStyleCrossRef" href="#bib0230">6</a> studied the epizootic rabbit enteropathy and found several bacteria adhering to the epithelial surface and inside the enterocytes in a few animals; none of the bacteria isolated from the intestinal mixed contents and cultivated on usual media were known as rabbit pathogens. There are several specific cases suggesting that pathogens can have significant impact upon each other, sometimes directly but at other times through the changes they cause to particular body systems and processes, including layers and components of the immune system<a class="elsevierStyleCrossRefs" href="#bib0330">26,30</a>. The presence of several pathogens in more than half of the intestinal content samples of the rabbits with enteric clinical profiles required to determine if these pathogens found concomitantly can act synergistically, and interestingly, if these clinical enteric profiles are different when they are produced by a single pathogen and if the presence of two or more pathogens, increasing pathogenicity.Ethical disclosuresProtection of human and animal subjectsThe authors declare that the procedures followed were in accordance with the regulations of the relevant clinical research ethics committee and with those of the Code of Ethics of the World Medical Association (Declaration of Helsinki).Confidentiality of dataThe authors declare that no patient data appear in this article.Right to privacy and informed consentThe authors declare that no patient data appear in this article.Conflict of interestThe authors declare no conflict of interest in the present study." "textoCompletoSecciones" => array:1 [ "secciones" => array:12 [ 0 => array:3 [ "identificador" => "xres848621" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec843741" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres848622" "titulo" => "Resumen" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0010" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec843740" "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:3 [ "identificador" => "sec0025" "titulo" => "Ethical disclosures" "secciones" => array:3 [ 0 => array:2 [ "identificador" => "sec0030" "titulo" => "Protection of human and animal subjects" ] 1 => array:2 [ "identificador" => "sec0035" "titulo" => "Confidentiality of data" ] 2 => array:2 [ "identificador" => "sec0040" "titulo" => "Right to privacy and informed consent" ] ] ] 9 => array:2 [ "identificador" => "sec0045" "titulo" => "Conflict of interest" ] 10 => array:2 [ "identificador" => "xack284613" "titulo" => "Acknowledgements" ] 11 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2015-08-25" "fechaAceptado" => "2016-10-11" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec843741" "palabras" => array:4 [ 0 => "Enteropathies" 1 => "Pathogens" 2 => "Rabbits" 3 => "Mexico" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec843740" "palabras" => array:4 [ 0 => "Enteropatías" 1 => "Agentes patógenos" 2 => "Conejos" 3 => "México" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "Enteropathies in rabbits are difficult to diagnose; their etiology involves pathogens that act synergistically, causing damage to the intestine. The aim of the present study was isolate enteric pathogens from rabbits in Mexico. Using parasitological, bacteriological and molecular analyses, we screened 58 samples of the intestinal content of rabbits having a clinical history of enteric disease from the southeastern part of the State of Mexico. Out of the 58 samples analyzed, a total of 86 identifications were made, Eimeria spp. were found in 77.5%, followed by Aeromonas spp. in 15.5% and Escherichia coli in 8.6%, which were identified as enteropathogenic E. coli (EPEC), and the presence of the following agents was also confirmed: Salmonella spp., Klebsiella spp., Streptococcus spp., Staphylococcus aureus, Enterococcus spp., Mannheimia spp. and Rotavirus. The concurrent presence of Eimeria spp. with Aeromonas was frequent (15.5%); there was statistical significance for the presence of an association between the clinical profiles and Eimeria spp. (p=0.000), Mannheimia spp. (p=0.001), Salmonella spp., Klebsiella spp., Streptococcus spp. and Enterococcus spp. (p=0.006)." ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "Las enteropatías en conejos son difíciles de diagnosticar, debido a que en su etiología participan patógenos que actúan en sinergia y causan daño al intestino. El objetivo de este estudio fue el aislamiento de patógenos de cuadros entéricos en conejos de México. Mediante métodos parasitológicos, bacteriológicos y moleculares, se analizaron 58 muestras de contenido intestinal de conejos con el antecedente de cuadro clínico entérico procedentes de granjas cunícolas de la zona suroriente del Estado de México. A partir de las 58 muestras se realizaron un total de 86 identificaciones, los patógenos más frecuentes fueron Eimeria spp. (77,6%), seguidas de Aeromonas spp. (15,5%) y de Escherichia coli (8,6%), identificadas como E. coli enterpatogénicas (EPEC). También se determinó la presencia de otros agentes: Salmonella spp., Klebsiella spp., Streptococcus spp., Staphylococcus aureus, Enterococcus spp., Mannheimia spp. y Rotavirus. La presencia concurrente de Eimeria spp. y Aeromonas spp. (15,5%) fue la observación más frecuente. Se encontró asociación estadísticamente significativa entre la presentación del cuadro clínico en conejos y la presencia de Eimeria spp. (p=0,000), Mannheimia spp. (p=0,001), Salmonella spp., Klebsiella spp., Streptococcus spp. y Enterococcus spp. (p=0,006)." ] ] "multimedia" => array:3 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1399 "Ancho" => 1633 "Tamanyo" => 118619 ] ] "descripcion" => array:1 [ "en" => "Agents isolated from enteric profiles in rabbits from Mexico." ] ] 1 => array:8 [ "identificador" => "tbl0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at1" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:1 [ "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Concurrent identification \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Frequency \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Percentage \t\t\t\t\t\t\n \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Enteropathogenic Escherichia coli (EPEC) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">5 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">8.7 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Eimeria magna \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">25 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">43.1 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Enterococcus spp. \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3.5 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Streptococcus spp. \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.7 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Rotavirus \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.7 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Mannheimia spp. \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.7 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Eimeria magna+E. perforans+Aeromona spp. \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">9 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">15.5 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Eimeria media+Sthapylococcus aureus \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.7 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Eimeria media+E. intestinalis+E. perforans+Staphylococcus aureus \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3.5 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Eimeria magna+E. perforans+E. vejdovsky+Streptococcus spp. \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.7 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Eimeria vejdovsky+Klebsiella spp. \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.7 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Eimeria vejdovsky+Salmonella spp. \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.7 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Eimeria media+E. flavescens+Rotavirus \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3.4 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Eimeria media+E. vejdovsky+Rotavirus \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.7 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Eimeria media+Klebsiella spp.+Rotavirus \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.7 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Eimeria media+Salmonella spp.+Rotavirus \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">17.0 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Without isolation \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">5.2 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " colspan="3" align="left" valign="top"></td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">58 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">100.0 \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1432252.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Identification of concurring agents in rabbit intestine samples from Mexico." ] ] 2 => array:8 [ "identificador" => "tbl0010" "etiqueta" => "Table 2" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at2" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:3 [ "leyenda" => "Fisher's exact test, p<0.05." "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Pathogen \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Positive \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Negative \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">p \t\t\t\t\t\t\n \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Eimeria spp. \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">45 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">13 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.000<a class="elsevierStyleCrossRef" href="#tblfn0005">a</a> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Enteropathogenic E. coli (EPEC) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">5 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">53 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.09 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Salmonella spp. \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">56 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.006<a class="elsevierStyleCrossRef" href="#tblfn0005">a</a> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Mannheimia spp. \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">57 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.001<a class="elsevierStyleCrossRef" href="#tblfn0005">a</a> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Staphylococcus aureus \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">55 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.084 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Streptococcus spp. \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">56 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.006<a class="elsevierStyleCrossRef" href="#tblfn0005">a</a> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Enterococcus spp. \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">56 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.006<a class="elsevierStyleCrossRef" href="#tblfn0005">a</a> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Aeromonas spp. \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">9 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">49 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.14 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Klebsiella spp. \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">56 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.006<a class="elsevierStyleCrossRef" href="#tblfn0005">a</a> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Rotavirus \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">6 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">52 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.11 \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1432253.png" ] ] ] "notaPie" => array:1 [ 0 => array:3 [ "identificador" => "tblfn0005" "etiqueta" => "a" "nota" => "Samples with statistical significance." ] ] ] "descripcion" => array:1 [ "en" => "Comparison of rabbits positive and negative to enteropathogens from intestine samples from Mexico." ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:40 [ 0 => array:3 [ "identificador" => "bib0205" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Aeromonas spp. as a causal agent of acute diarrheic syndrome in children under six years of age" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:3 [ 0 => "L. 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Multicausalidad del síndrome entérico en conejos de México

Virginia G. García-Rubioa, Linda G. Bautista-Gómeza,

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lgbautista@uaemex.mx
lin_bag@yahoo.com.mx

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, José S. Martínez-Castañedab, Camilo Romero-Núñeza

a Centro Universitario UAEM Amecameca, Universidad Autónoma del Estado de México, Km 2.5 Carretera Amecameca-Ayapango, C.P. 56900 Amecameca, Estado de México, México

b Centro de Investigación y Estudios Avanzados en Salud Animal, Facultad de Medicina Veterinaria y Zootecnia, Universidad Autónoma del Estado de México. Carretera de Cuota Toluca-Atlacomulco km 15.5, C.P. 50200, Toluca, Estado de México, México

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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">The enteritis complex was introduced by Whitney in 1976 to designate a group of diseases that include mucoid enteritis&#44; typhlitis&#44; typhlitis-diarrhea and hemorrhagic enteritis&#46; Commonly observed symptoms include teeth grinding&#44; anorexia&#44; polydipsia&#44; weakness&#44; abdominal distension&#44; profuse diarrhea&#44; dehydration&#44; hypothermia and death<a class="elsevierStyleCrossRef" href="#bib0290"><span class="elsevierStyleSup">18</span></a>&#46; Enteropathies are recognized as a problem for domestic rabbits&#44; being their etiology and pathogenesis poorly understood<a class="elsevierStyleCrossRef" href="#bib0220"><span class="elsevierStyleSup">4</span></a>&#46; In commercial rabbit production&#44; enteropathies are hard to diagnose&#59; they can have a multifactorial etiology &#40;hence the term &#8220;multifactorial enteritis&#8221;&#41; and are also known as &#8220;enteric syndrome&#8221;<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">14</span></a>&#46; This syndrome is a pathological complex characterized by various stressing and pathogenic factors acting synergistically&#44; possessing varying degrees of virulence which can enhance their pathogenicity and cause damage to the intestinal tissue&#46; Numerous studies have reported the isolation of <span class="elsevierStyleItalic">Clostridium perfringens</span>&#44; <span class="elsevierStyleItalic">Clostridium piliformis</span>&#44; <span class="elsevierStyleItalic">Clostridium spiriforme</span>&#44; <span class="elsevierStyleItalic">Escherichia coli</span><a class="elsevierStyleCrossRefs" href="#bib0305"><span class="elsevierStyleSup">21&#44;35</span></a>&#44; <span class="elsevierStyleItalic">Salmonella</span> spp&#46;&#44; <span class="elsevierStyleItalic">Klebsiella</span> spp&#46;&#44; <span class="elsevierStyleItalic">Pseudomonas</span> spp&#46;&#44; Streptococcus <span class="elsevierStyleItalic">aureus</span>&#44; <span class="elsevierStyleItalic">Streptococcus</span> spp&#46;&#44; <span class="elsevierStyleItalic">Campylobacter</span> and <span class="elsevierStyleItalic">Eimeria</span> spp&#46;&#44;<a class="elsevierStyleCrossRefs" href="#bib0270"><span class="elsevierStyleSup">14&#44;19&#44;23&#44;24</span></a>&#46; Viruses seem to have an important but non-crucial role&#59; overall&#44; they are mild pathogens that do not induce severe clinical profiles<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">14</span></a>&#46; Rotavirus<a class="elsevierStyleCrossRef" href="#bib0280"><span class="elsevierStyleSup">16</span></a>&#44; Coronavirus<a class="elsevierStyleCrossRef" href="#bib0220"><span class="elsevierStyleSup">4</span></a>&#44; and Parvovirus<a class="elsevierStyleCrossRef" href="#bib0285"><span class="elsevierStyleSup">17</span></a> have been reported and it has been suggested that they could exert direct pathogenic activity by initiating the development of bacterial infections and&#47;or of other viral pathogens by inducing minimal alterations in the intestinal epithelium<a class="elsevierStyleCrossRef" href="#bib0285"><span class="elsevierStyleSup">17</span></a>&#46; Enteric diseases are important in rabbit production and cause severe economic losses&#44; due to high mortality indexes&#44; decrease in growth and reduction in the feed conversion ratio<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">14</span></a>&#46; Studies in Cuba&#44; Japan and Argentina have reported digestive pathologies as the main cause of mortality with percentages of 57&#46;9&#37;&#44; 48&#46;9&#37; and 43&#37; respectively<a class="elsevierStyleCrossRef" href="#bib0320"><span class="elsevierStyleSup">24</span></a>&#46; In Mexico there are few reports concerning the agents involved in these pathologies<a class="elsevierStyleCrossRef" href="#bib0395"><span class="elsevierStyleSup">39</span></a>&#46; Because of this reason&#44; the aim of this study was to isolate pathogens from enteric disease in rabbits from Mexico&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Material and methods</span><p id="par0010" class="elsevierStylePara elsevierViewall">Fifty-eight rabbits with an enteric clinical profile were obtained from several rabbit meat production from the southeastern part of the State of Mexico&#44; Mexico&#46; The animals exhibited an enteric clinical profile that included depression&#44; anorexia&#44; dehydration&#44; abdominal distension&#44; liquid-to-mucoid diarrhea and death within 24<span class="elsevierStyleHsp" style=""></span>h&#46; Isolates were recovered from the intestinal contents through the necropsy service of the Amphitheater of Veterinary Medicine and Zootechnics of the Centro Universitario Amecameca &#40;CU Amecameca&#41;&#44; of the Universidad Aut&#243;noma del Estado de M&#233;xico &#40;UAEMex&#41;&#46; This study was authorized by the Bioethics Committee of the CU Amecameca &#40;CBE&#47;06&#47;2013&#41;&#46;</p><p id="par0015" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Eimeria</span> spp&#46; were identified by microscopy and the parasitological flotation technique<a class="elsevierStyleCrossRef" href="#bib0345"><span class="elsevierStyleSup">29</span></a>&#46; DNA was extracted from the stool samples using the ZR Fecal DNA MiniPrep&#8482; &#40;ZYMO Research&#44; USA&#41;&#44; according to the manufacturer&#39;s instructions&#46; DNA samples were assessed quantitatively and qualitatively by measurements of absorbance in a Nano Drop 2000c &#40;Thermo Scientific&#44; USA&#41;&#46; A PCR was also performed&#44; using primers for the amplification of the ribosomal cistron&#44; ITS1 region &#40;400&#8211;500<span class="elsevierStyleHsp" style=""></span>bp long&#41; of Eimeria tenella&#44; as reported by Oliveira et al&#46;<a class="elsevierStyleCrossRef" href="#bib0295"><span class="elsevierStyleSup">19</span></a> &#40;accession number AFO26388&#41;&#46; The following reagents were added to 1<span class="elsevierStyleHsp" style=""></span>mg of DNA to make 25<span class="elsevierStyleHsp" style=""></span>&#956;l PCR solution&#58; 2&#46;5<span class="elsevierStyleHsp" style=""></span>mM MgCl<span class="elsevierStyleInf">2</span>&#44; 100<span class="elsevierStyleHsp" style=""></span>mM each dATP&#44; dCTP&#44; dGTP&#44; dTTP&#44; 1&#46;5<span class="elsevierStyleHsp" style=""></span>U GoTaq Flexi DNA Polymerase &#40;PROMEGA&#44; USA&#41;&#44; 5<span class="elsevierStyleHsp" style=""></span>&#956;l 5&#215; Green GoTaq Flexi Buffer&#44; and 0&#46;8<span class="elsevierStyleHsp" style=""></span>mM of each primer&#46; The amplification conditions included 35 cycles of denaturation at 96<span class="elsevierStyleHsp" style=""></span>&#176;C for 45<span class="elsevierStyleHsp" style=""></span>s&#44; annealing at 54<span class="elsevierStyleHsp" style=""></span>&#176;C for 45<span class="elsevierStyleHsp" style=""></span>s and extension at 72<span class="elsevierStyleHsp" style=""></span>&#176;C for 60<span class="elsevierStyleHsp" style=""></span>s&#46; A sequenced sample was included as positive control and DNA obtained from rabbit blood was used as negative control&#46;</p><p id="par0020" class="elsevierStylePara elsevierViewall">The bacteriological analyses involved primary isolation in blood agar&#59; identification was performed by colonial morphology and Gram staining&#46; Gram negative bacteria were cultured in the following selective media&#58; MacConkey&#44; Salmonella-Shigella and brilliant green agar at 37<span class="elsevierStyleHsp" style=""></span>&#176;C incubation temperature and aerobiosis for 24&#8211;48<span class="elsevierStyleHsp" style=""></span>h<a class="elsevierStyleCrossRef" href="#bib0210"><span class="elsevierStyleSup">2</span></a>&#46; To identify <span class="elsevierStyleItalic">Salmonella</span>&#44; the samples were previously inoculated in peptone water and tetrathionate broth&#46; A colony of each growth produced was selected as a representative isolate and subcultured for further biochemical identification&#46; Biochemical tests of oxidase&#44; catalase&#44; triple sugar iron&#44; ornithine decarboxylase&#44; sulfide indol motility and urease were performed<a class="elsevierStyleCrossRefs" href="#bib0225"><span class="elsevierStyleSup">5&#44;10&#44;14</span></a>&#46; Gram positive bacteria were analyzed for evidence of catalase&#44; coagulase&#44; hemolysis&#44; and cultured in mannitol salt agar<a class="elsevierStyleCrossRef" href="#bib0400"><span class="elsevierStyleSup">40</span></a>&#46;</p><p id="par0025" class="elsevierStylePara elsevierViewall">To determine the <span class="elsevierStyleItalic">E&#46; coli</span> pathotypes&#44; we used a pathogen-specific multiplex PCR to detect enterotoxigenic <span class="elsevierStyleItalic">E&#46; coli</span> &#40;ETEC&#41;&#44; enteropathogenic <span class="elsevierStyleItalic">E&#46; coli</span> &#40;EPEC&#41;&#44; enteroinvasive <span class="elsevierStyleItalic">E&#46; coli</span> &#40;EIEC&#41; and Shiga-toxin-producing or enterohemorrhagic <span class="elsevierStyleItalic">E&#46; coli</span> &#40;EHEC o STEC o VTEC&#41;&#44; using specific primers&#44; by the amplification of 150&#8211;650<span class="elsevierStyleHsp" style=""></span>bp fragments for diverse virulence traits as reported by L&#243;pez-Saucedo et al&#46;<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">15</span></a> Representative positive PCR products were purified and sequenced using an ABI PRISM 3500 genetic analyzer &#40;Life Technologies&#44; Carlsbad&#44; CA&#41;&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">Rotavirus detection was accomplished by the amplification of a 380<span class="elsevierStyleHsp" style=""></span>bp fragment of capsid protein VP6&#44; employing primers as reported by Iturriza-Gomora et al&#46;<a class="elsevierStyleCrossRef" href="#bib0260"><span class="elsevierStyleSup">12</span></a> RNA extraction was performed using GeneJET Viral DNA and the RNA Purification Kit &#40;Thermo Scientific&#44; USA&#41;&#46; The two-step RT-PCR technique was implemented&#59; complementary DNA &#40;cDNA&#41; was obtained by means of the SuperScript III Reverse Transcriptase &#40;RT&#41; &#40;Thermo Scientific&#44; USA&#41;&#46; PCR conditions were as follows&#58; Initial denaturation at 96<span class="elsevierStyleHsp" style=""></span>&#176;C for 10<span class="elsevierStyleHsp" style=""></span>min&#44; follow by 45 cycles of denaturation at 96<span class="elsevierStyleHsp" style=""></span>&#176;C for 45<span class="elsevierStyleHsp" style=""></span>s&#44; annealing at 61<span class="elsevierStyleHsp" style=""></span>&#176;C for 45<span class="elsevierStyleHsp" style=""></span>s and an extension at 72<span class="elsevierStyleHsp" style=""></span>&#176;C for 30<span class="elsevierStyleHsp" style=""></span>s&#44; the final extension at 72<span class="elsevierStyleHsp" style=""></span>&#176;C for 5 min&#46; As a positive control&#44; we used the Rota teq pentavalent vaccine &#40;MSD SNC&#44; Lyon&#44; France&#41;&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">In order to test the association between the presence of the identified agents and the clinical profiles&#44; we used the Fisher&#39;s exact test&#44; with a significance threshold of &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41;&#46;</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Results</span><p id="par0040" class="elsevierStylePara elsevierViewall">Out of 58 intestine content samples&#44; 35&#47;58 &#40;60&#46;4&#37;&#41; were positive for at least one identification and 23 &#40;39&#46;6&#37;&#41; were in concurrence&#44; including&#58; 3&#47;58 &#40;5&#46;2&#37;&#41; with two identifications and 14&#47;58 &#40;24&#46;0&#37;&#41; with three identifications&#46; Rotavirus was identified for the first time in rabbits from Mexico in 6&#47;58 samples &#40;10&#46;3&#37;&#41;&#44; of which 5&#47;6 samples &#40;83&#46;3&#37;&#41; showed the identification of concomitant infection by Rotavirus and other pathogens&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">We identified six highly pathogenic <span class="elsevierStyleItalic">Eimeria</span> species in 45&#47;58 rabbits &#40;77&#46;5&#37;&#41;&#59; mildly pathogenic <span class="elsevierStyleItalic">E&#46; intestinalis</span> in 2&#47;58 rabbits &#40;4&#46;4&#37;&#41; and <span class="elsevierStyleItalic">E&#46; flavescens</span> in 2&#47;58 &#40;4&#46;4&#37;&#41;&#59; lowly pathogenic <span class="elsevierStyleItalic">E&#46; magna</span> in 35&#47;58 &#40;77&#46;7&#37;&#41;&#44; <span class="elsevierStyleItalic">E&#46; media</span> in 8&#47;58 &#40;17&#46;7&#37;&#41;&#59; <span class="elsevierStyleItalic">E&#46; perforans</span> in 12&#47;58 &#40;26&#46;6&#37;&#41; and <span class="elsevierStyleItalic">E&#46; vejdovsky</span> in 4&#47;58 &#40;8&#46;8&#37;&#41;&#44; followed by <span class="elsevierStyleItalic">Aeromona</span> spp&#46; &#40;15&#46;5&#37;&#41; and <span class="elsevierStyleItalic">E&#46; coli</span> in 5&#47;58 &#40;8&#46;6&#37;&#41;&#44; corresponding to enteropathogenic <span class="elsevierStyleItalic">E&#46; coli</span> &#40;EPEC&#41; while the other strains were non-diarrheagenic by PCR&#44; using primers for <span class="elsevierStyleItalic">bfp</span>A detection<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">15</span></a>&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">There were 86 identifications in the 58 samples&#46; <a class="elsevierStyleCrossRef" href="#fig0005">Figure 1</a> shows the frequency of detection per agent&#46; The concurring presence of pathogenic agents identified in the intestine content samples is shown in <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#46; Results of the Fisher&#39;s exact test showed a statistically significant association of the clinical profiles and the presence of <span class="elsevierStyleItalic">Eimeria</span> spp&#46; &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;000&#41;&#44; <span class="elsevierStyleItalic">E&#46; coli</span> EPEC &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;09&#41;&#44; <span class="elsevierStyleItalic">Mannheimia</span> spp&#46; &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;001&#41;&#44; <span class="elsevierStyleItalic">Salmonella</span> spp&#46;&#44; <span class="elsevierStyleItalic">Klebsiella</span> spp&#46;&#44; <span class="elsevierStyleItalic">S&#46; aureus</span> and <span class="elsevierStyleItalic">Enterococcus</span> spp&#46; &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;006&#41; &#40;<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>&#41;&#46; In relation to the clinical profile observed&#44; diarrhea &#40;with varying characteristics&#41; was the most frequent sign&#44; followed by abdominal distension&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><elsevierMultimedia ident="tbl0010"></elsevierMultimedia></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Discussion</span><p id="par0055" class="elsevierStylePara elsevierViewall">In contrast with the results obtained by Szalo et al&#46;<a class="elsevierStyleCrossRef" href="#bib0370"><span class="elsevierStyleSup">34</span></a>&#44; who suggested that the enteropathy in rabbits is a bacterial disease and does not have a viral or parasitic etiology and with Martella et al&#46;<a class="elsevierStyleCrossRef" href="#bib0280"><span class="elsevierStyleSup">16</span></a>&#44; where rotavirus was the most frequent agent isolated from enteric profiles in rabbits&#44; in the present study&#44; <span class="elsevierStyleItalic">Eimeria</span> spp&#46; was the most frequently recovered agent&#44; both on its own and in association with other pathogens&#46; Studies in other countries have reported the presence of eleven <span class="elsevierStyleItalic">Eimeria</span> species that affect rabbits in up to 70&#37; of enteropathies&#44; and&#44; according to their level of pathogenicity&#44; can cause reduced growth rate and feed conversion&#44; and increased mortality<a class="elsevierStyleCrossRefs" href="#bib0295"><span class="elsevierStyleSup">19&#44;21</span></a>&#46; In this work we only identified by PCR six of the eleven <span class="elsevierStyleItalic">Eimeria</span> species in the samples&#44; being <span class="elsevierStyleItalic">E&#46; magna</span> and <span class="elsevierStyleItalic">E&#46; perforans</span> the most frequently found&#44; considered as mildly and lowly pathogenic respectively&#59; however&#44; although all the rabbits presented enteric disease&#44; the association with other pathogens had not been reported&#46; Interestingly in the present study&#44; we found an association of <span class="elsevierStyleItalic">Eimeria</span> spp&#46; with gram negative bacteria and less frequently with Gram positive bacteria&#46; These results provide epidemiological evidence of synergism among <span class="elsevierStyleItalic">Eimeria</span> spp&#46; and <span class="elsevierStyleItalic">E&#46; coli</span> and other enteric pathogens&#46; It seems that by being simultaneously present in the enteric profiles&#44; these pathogens can increase their pathogenic potential<a class="elsevierStyleCrossRef" href="#bib0215"><span class="elsevierStyleSup">3</span></a>&#46;</p><p id="par0060" class="elsevierStylePara elsevierViewall">The replication of <span class="elsevierStyleItalic">Eimeria</span> spp&#46; within the epithelial cells of the intestine&#44; alters the natural resistance barrier<a class="elsevierStyleCrossRef" href="#bib0350"><span class="elsevierStyleSup">30</span></a>&#44; which is intensified due to various factors such as the production of inflammatory cytokines&#44; mainly interleukin 6 &#40;IL-6&#41; and to a lesser degree interleukin 8 &#40;IL-8&#41; released as a result of massive cell lysis&#46; These mechanisms are used by gram negative bacteria such as <span class="elsevierStyleItalic">E&#46; coli</span> and <span class="elsevierStyleItalic">Salmonella</span> spp&#46; to increase intestinal wall disorganization&#44; consequently invading the tissue<a class="elsevierStyleCrossRefs" href="#bib0230"><span class="elsevierStyleSup">6&#44;22</span></a>&#44; facilitating bacterial adherence and penetration<a class="elsevierStyleCrossRef" href="#bib0335"><span class="elsevierStyleSup">27</span></a>&#46; Further&#44; some <span class="elsevierStyleItalic">Eimeria</span> species enhance host mucogenesis since the mucus layer of the gastrointestinal tract is an excellent source of nutrients for some bacteria<a class="elsevierStyleCrossRef" href="#bib0300"><span class="elsevierStyleSup">20</span></a>&#46; Blankets and globular particles of mucus associated with numerous bacteria on villi and extensive inflammatory lesions have been observed in rabbits with an enteric profile and bacteria were observed attached to the site of serious cell damage<a class="elsevierStyleCrossRef" href="#bib0230"><span class="elsevierStyleSup">6</span></a>&#46; They can take advantage of this scenario for synergies and exercise their mechanisms of pathogenicity or may be considered as secondary invaders&#46;</p><p id="par0065" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Aeromonas</span> spp&#46; are members of the microbiota of warm-blooded animals and have been reported to cause septicemia and gastroenteritis &#40;with self-limiting acute diarrhea&#41;<a class="elsevierStyleCrossRef" href="#bib0205"><span class="elsevierStyleSup">1</span></a>&#46; Their mechanism of pathogenicity is through type III secretion systems&#44; with production of cytotoxic&#44; hemolytic&#44; enterotoxic and lethal enterotoxin&#44; which also alters the cytoskeletal signaling cascades and promotes bacterial growth<a class="elsevierStyleCrossRefs" href="#bib0325"><span class="elsevierStyleSup">25&#44;28</span></a>&#46; The pathogenic role of this bacterium in enteric disease has been demonstrated and studied in the present study&#44; <span class="elsevierStyleItalic">Aeromonas</span> spp&#46; occurred with a frequency of 10&#46;47&#37;&#46; The isolation of <span class="elsevierStyleItalic">Aeromonas</span> spp&#46;&#44; on their own or in association with other pathogens from the intestinal contents suggests their involvement in the enteric profiles&#46;</p><p id="par0070" class="elsevierStylePara elsevierViewall">In our study&#44; enteropathogenic <span class="elsevierStyleItalic">E&#46; coli</span> &#40;EPEC&#41; was found in five animals &#40;8&#46;6&#37;&#41;&#44; which is very similar to Swennes et al&#46;&#8217;s findings<a class="elsevierStyleCrossRefs" href="#bib0360"><span class="elsevierStyleSup">32&#44;33</span></a>&#44; who described 10&#46;5 and 4&#46;3&#37; EPEC in laboratory rabbits&#46; Lavazza et al&#46;<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">14</span></a> found that <span class="elsevierStyleItalic">E&#46; coli</span> was the only pathogen in about 40&#46;0&#37; of cases of domestic rabbits&#46; Dewr&#233;e et al&#46;<a class="elsevierStyleCrossRef" href="#bib0230"><span class="elsevierStyleSup">6</span></a> found that the most commonly isolated digestive tract bacteria pathogens were <span class="elsevierStyleItalic">E&#46; coli</span>&#44; but they did not find EPEC&#46; This bacterium is a member of the intestinal microbiota and possibly several factors generate a state of immunosuppression&#44; which allows significant replication of some opportunistic agents or performing synergy with other competing agents<a class="elsevierStyleCrossRefs" href="#bib0250"><span class="elsevierStyleSup">10&#44;14&#44;23&#44;36</span></a>&#46;</p><p id="par0075" class="elsevierStylePara elsevierViewall">We found that 60&#46;4&#37; of intestinal content samples were positive for one identification&#44; 5&#46;2&#37; for two and 24&#37; for three&#46; Other studies in human detected enteropathogens in 66&#46;4&#37; of patients with diarrhea&#44; a single enteric pathogen in 50&#46;9&#37; and multiple pathogens in 15&#46;5&#37;&#59; concomitant infection by more than one enteric pathogen occurred in 18&#46;6&#37; of the infants and 29&#37; contained multiple pathogens<a class="elsevierStyleCrossRef" href="#bib0240"><span class="elsevierStyleSup">8</span></a>&#46;</p><p id="par0080" class="elsevierStylePara elsevierViewall">The enteric syndrome has a large impact on rabbit production&#46; Several authors suggest that rotavirus could be the main cause of enteric disease in rabbits and also be implicated as the etiological agent of severe enteric outbreaks<a class="elsevierStyleCrossRefs" href="#bib0280"><span class="elsevierStyleSup">16&#44;35</span></a>&#46; Lavazza et al&#46;<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">14</span></a> identified rotavirus in rabbits by electron microscopy &#40;16&#46;0&#37;&#41;&#44; detecting 3&#46;3&#37; to 36&#46;6&#37; in humans<a class="elsevierStyleCrossRefs" href="#bib0240"><span class="elsevierStyleSup">8&#44;27&#44;37</span></a>&#44; our findings show the presence of rotavirus in fewer cases &#40;10&#46;3&#37;&#41;&#46; The concomitant identification of rotavirus and other pathogens was detected in 5&#47;6 &#40;83&#46;3&#37;&#41; samples&#46; <span class="elsevierStyleItalic">In vitro</span> models of pathogenesis indicate that synergism between rotavirus and invasive bacteria involve specific biologic pathways&#58; the attachment of&#44; or the invasion through an up-regulation of specific receptors<a class="elsevierStyleCrossRef" href="#bib0355"><span class="elsevierStyleSup">31</span></a>&#46; Bhavnani et al&#46;<a class="elsevierStyleCrossRef" href="#bib0215"><span class="elsevierStyleSup">3</span></a> found epidemiologic evidence of synergism between rotavirus and other enteric pathogens for producing enteric clinical profiles&#44; either by enhancing attachment and bacterial invasion of intestinal epithelial cells or by producing inflammation promoting the development of bacteria by the release of fluid&#44; mucin&#44; cellular detritus and the secretion of antimicrobials&#44; which could alter the composition of the gut microbiota&#44; allowing pathogens to occupy their commensal niche&#46; Lavazza et al&#46;<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">14</span></a>&#44; conclude that there was no association between viral positivity or negativity and the presence of bacteria&#46; Our results agree with those of Dewr&#233;e et al&#46;<a class="elsevierStyleCrossRef" href="#bib0230"><span class="elsevierStyleSup">6</span></a> and Rodriguez De Lara et al&#46;<a class="elsevierStyleCrossRef" href="#bib0315"><span class="elsevierStyleSup">23</span></a>&#44; about rotaviruses as the main cause of the epizootic outbreaks of diarrheas is questionable&#44; particularly if considering that rotavirus are considered endemic and mildly pathogenic in commercial rabbitries&#46; However&#44; this is the first molecular report confirming the presence of rotavirus in the enteric profiles of rabbits from Mexico&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">In the bacteriological results in rabbits&#44; Lavazza et al&#46;<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">14</span></a> included <span class="elsevierStyleItalic">E&#46; coli</span>&#44; <span class="elsevierStyleItalic">S&#46; aureus</span>&#44; <span class="elsevierStyleItalic">Klebsiella</span> spp&#46;&#44; <span class="elsevierStyleItalic">Yersinia</span> spp&#46;&#44; Pasteurella <span class="elsevierStyleItalic">multocida&#44; C&#46; perfringens</span> and <span class="elsevierStyleItalic">C&#46; spiriforme</span>&#46; This study found <span class="elsevierStyleItalic">E&#46; coli&#44; Aeromonas</span> spp&#46;&#44; <span class="elsevierStyleItalic">Salmonella</span> spp&#46;&#44; <span class="elsevierStyleItalic">Enterococcus</span> spp&#46;&#44; <span class="elsevierStyleItalic">Streptococcus</span> spp&#46;&#44; <span class="elsevierStyleItalic">S&#46; aureus</span>&#44; <span class="elsevierStyleItalic">Mannheimia</span> spp&#46;&#44; and <span class="elsevierStyleItalic">Klebsiella</span> spp&#46; In humans&#44; the results of several research works were similar&#58; in Jordan&#44; enteropathogenic <span class="elsevierStyleItalic">E&#46; coli</span> &#40;12&#46;8&#37;&#41;&#44; enteroaggregative <span class="elsevierStyleItalic">E&#46; coli</span> &#40;10&#46;2&#37;&#41;&#44; enterotoxigenic <span class="elsevierStyleItalic">E&#46; coli</span> &#40;5&#46;7&#37;&#41;&#44; <span class="elsevierStyleItalic">Shigella</span> spp&#46; &#40;4&#46;9&#37;&#41;&#44; <span class="elsevierStyleItalic">Entamoeba histolytica</span> &#40;4&#46;9&#37;&#41;&#44; <span class="elsevierStyleItalic">Salmonella</span> spp&#46; &#40;4&#46;5&#37;&#41;&#44; <span class="elsevierStyleItalic">Campylobacter jejuni&#47;coli</span> &#40;1&#46;5&#37;&#41;&#44; <span class="elsevierStyleItalic">Cryptosporidium</span> spp&#46; &#40;1&#46;5&#37;&#41;&#44; enteroinvasive <span class="elsevierStyleItalic">E&#46; coli</span> &#40;1&#46;5&#37;&#41;&#44; <span class="elsevierStyleItalic">Giardia lamblia</span> &#40;0&#46;8&#37;&#41; and <span class="elsevierStyleItalic">Yersinia enterocolitica</span> &#40;0&#46;4&#37;&#41;<a class="elsevierStyleCrossRef" href="#bib0395"><span class="elsevierStyleSup">39</span></a>&#59; in Colombia&#44; enteropathogenic <span class="elsevierStyleItalic">E&#46; coli</span> &#40;6&#46;0&#37;&#41;&#44; enterohemorragic <span class="elsevierStyleItalic">E&#46; coli</span> &#40;2&#46;8&#37;&#41;&#44; <span class="elsevierStyleItalic">Aeromonas hydrophila</span> &#40;2&#46;0&#37;&#41; and other pathogens &#40;52&#46;6&#37;&#41;<a class="elsevierStyleCrossRef" href="#bib0380"><span class="elsevierStyleSup">36</span></a> were identified&#59; in the Netherlands&#44; enteropathogenic <span class="elsevierStyleItalic">E&#46; coli</span> were detected in 19&#46;9&#37;&#44; and <span class="elsevierStyleItalic">Salmonella enterica</span> in 0&#46;3&#37;<a class="elsevierStyleCrossRef" href="#bib0240"><span class="elsevierStyleSup">8</span></a>&#59; in Papua New Guinea&#44; <span class="elsevierStyleItalic">Shigella</span> spp&#46; &#40;26&#46;6&#37;&#41;&#44; enteropathogenic <span class="elsevierStyleItalic">E&#46; coli</span> &#40;8&#46;5&#37;&#41;&#44; <span class="elsevierStyleItalic">Salmonella</span> spp&#46; were found below the limit of detection<a class="elsevierStyleCrossRef" href="#bib0335"><span class="elsevierStyleSup">27</span></a>&#46;</p><p id="par0090" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Staphylococcus</span> spp&#46; make up the microbiota of the upper respiratory tract and lower urogenital tract&#44; are transitory in the digestive tract and predominant in the small intestine and cecum&#59; it has been observed that <span class="elsevierStyleItalic">S&#46; aureus</span> produces yellow diarrhea in nursing rabbits<a class="elsevierStyleCrossRef" href="#bib0260"><span class="elsevierStyleSup">12</span></a>&#46; Lavazza et al&#46;<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">14</span></a> found <span class="elsevierStyleItalic">Staphylococcus</span> both in isolation and associated with <span class="elsevierStyleItalic">E&#46; coli</span> and <span class="elsevierStyleItalic">P&#46; multocida</span>&#59; with and without viral presence&#46; Furthermore&#44; they found <span class="elsevierStyleItalic">Streptococcus</span> as single isolates from rabbits with enteritis&#46; Our results show the presence of <span class="elsevierStyleItalic">S&#46; aureus</span> in association with <span class="elsevierStyleItalic">Eimeria</span> spp&#46; in 5&#46;2&#37;&#46; <span class="elsevierStyleItalic">Streptococcus</span> spp&#46;&#44; were found both on their own &#40;1&#46;7&#37;&#41; and in a concurrent manner with protozoa parasite <span class="elsevierStyleItalic">Eimeria</span> spp&#46; &#40;1&#46;7&#37;&#41;&#46; Isolation frequency was not as high as in the case of other pathogen&#44; however&#44; their presence indicates involvement in promoting enteric profiles in rabbits&#46;</p><p id="par0095" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Enterococcus</span> spp&#46; are ubiquitous and are consistently found in animal gastrointestinal tracts&#46; In pigs&#44; the co-occurrence of <span class="elsevierStyleItalic">Enterococcus</span> genus and <span class="elsevierStyleItalic">E&#46; coli</span> has been previously reported and this interaction has been found to contribute to the development of new neonatal porcine diarrhea<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">11</span></a>&#46; Specifically&#44; <span class="elsevierStyleItalic">Enterococcus hirae</span> has been associated with enteropathy in cats and with diarrhea in rats and nursing kittens<a class="elsevierStyleCrossRefs" href="#bib0235"><span class="elsevierStyleSup">7&#44;9&#44;13</span></a>&#46; It has also been isolated from an outbreak of diarrhea in nursing rabbits with 85&#37; morbidity and 50&#37; mortality&#59; rabbits died within a 3 day period<a class="elsevierStyleCrossRef" href="#bib0390"><span class="elsevierStyleSup">38</span></a>&#46; In the present study&#44; we found <span class="elsevierStyleItalic">Enterococcus</span> spp&#46;&#44; without any associated pathogenic agent in two samples of intestinal content &#40;3&#46;5&#37;&#41; related to diarrhea episodes&#44; which suggests they could be etiologic agents&#46;</p><p id="par0100" class="elsevierStylePara elsevierViewall">Dewr&#233;e et al&#46;<a class="elsevierStyleCrossRef" href="#bib0230"><span class="elsevierStyleSup">6</span></a> studied the epizootic rabbit enteropathy and found several bacteria adhering to the epithelial surface and inside the enterocytes in a few animals&#59; none of the bacteria isolated from the intestinal mixed contents and cultivated on usual media were known as rabbit pathogens&#46; There are several specific cases suggesting that pathogens can have significant impact upon each other&#44; sometimes directly but at other times through the changes they cause to particular body systems and processes&#44; including layers and components of the immune system<a class="elsevierStyleCrossRefs" href="#bib0330"><span class="elsevierStyleSup">26&#44;30</span></a>&#46; The presence of several pathogens in more than half of the intestinal content samples of the rabbits with enteric clinical profiles required to determine if these pathogens found concomitantly can act synergistically&#44; and interestingly&#44; if these clinical enteric profiles are different when they are produced by a single pathogen and if the presence of two or more pathogens&#44; increasing pathogenicity&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Ethical disclosures</span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Protection of human and animal subjects</span><p id="par0105" class="elsevierStylePara elsevierViewall">The authors declare that the procedures followed were in accordance with the regulations of the relevant clinical research ethics committee and with those of the Code of Ethics of the World Medical Association &#40;Declaration of Helsinki&#41;&#46;</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Confidentiality of data</span><p id="par0110" class="elsevierStylePara elsevierViewall">The authors declare that no patient data appear in this article&#46;</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Right to privacy and informed consent</span><p id="par0115" class="elsevierStylePara elsevierViewall">The authors declare that no patient data appear in this article&#46;</p></span></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Conflict of interest</span><p id="par0120" class="elsevierStylePara elsevierViewall">The authors declare no conflict of interest in the present study&#46;</p></span></span>"
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        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Enteropathies in rabbits are difficult to diagnose&#59; their etiology involves pathogens that act synergistically&#44; causing damage to the intestine&#46; The aim of the present study was isolate enteric pathogens from rabbits in Mexico&#46; Using parasitological&#44; bacteriological and molecular analyses&#44; we screened 58 samples of the intestinal content of rabbits having a clinical history of enteric disease from the southeastern part of the State of Mexico&#46; Out of the 58 samples analyzed&#44; a total of 86 identifications were made&#44; <span class="elsevierStyleItalic">Eimeria</span> spp&#46; were found in 77&#46;5&#37;&#44; followed by <span class="elsevierStyleItalic">Aeromonas</span> spp&#46; in 15&#46;5&#37; and <span class="elsevierStyleItalic">Escherichia coli</span> in 8&#46;6&#37;&#44; which were identified as enteropathogenic <span class="elsevierStyleItalic">E&#46; coli</span> &#40;EPEC&#41;&#44; and the presence of the following agents was also confirmed&#58; <span class="elsevierStyleItalic">Salmonella</span> spp&#46;&#44; <span class="elsevierStyleItalic">Klebsiella</span> spp&#46;&#44; <span class="elsevierStyleItalic">Streptococcus</span> spp&#46;&#44; <span class="elsevierStyleItalic">Staphylococcus aureus</span>&#44; <span class="elsevierStyleItalic">Enterococcus</span> spp&#46;&#44; <span class="elsevierStyleItalic">Mannheimia</span> spp&#46; and <span class="elsevierStyleItalic">Rotavirus</span>&#46; The concurrent presence of <span class="elsevierStyleItalic">Eimeria</span> spp&#46; with <span class="elsevierStyleItalic">Aeromonas</span> was frequent &#40;15&#46;5&#37;&#41;&#59; there was statistical significance for the presence of an association between the clinical profiles and <span class="elsevierStyleItalic">Eimeria</span> spp&#46; &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;000&#41;&#44; <span class="elsevierStyleItalic">Mannheimia</span> spp&#46; &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;001&#41;&#44; <span class="elsevierStyleItalic">Salmonella</span> spp&#46;&#44; <span class="elsevierStyleItalic">Klebsiella</span> spp&#46;&#44; <span class="elsevierStyleItalic">Streptococcus</span> spp&#46; and <span class="elsevierStyleItalic">Enterococcus</span> spp&#46; &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;006&#41;&#46;</p></span>"
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        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Las enteropat&#237;as en conejos son dif&#237;ciles de diagnosticar&#44; debido a que en su etiolog&#237;a participan pat&#243;genos que act&#250;an en sinergia y causan da&#241;o al intestino&#46; El objetivo de este estudio fue el aislamiento de pat&#243;genos de cuadros ent&#233;ricos en conejos de M&#233;xico&#46; Mediante m&#233;todos parasitol&#243;gicos&#44; bacteriol&#243;gicos y moleculares&#44; se analizaron 58 muestras de contenido intestinal de conejos con el antecedente de cuadro cl&#237;nico ent&#233;rico procedentes de granjas cun&#237;colas de la zona suroriente del Estado de M&#233;xico&#46; A partir de las 58 muestras se realizaron un total de 86 identificaciones&#44; los pat&#243;genos m&#225;s frecuentes fueron <span class="elsevierStyleItalic">Eimeria</span> spp&#46; &#40;77&#44;6&#37;&#41;&#44; seguidas de <span class="elsevierStyleItalic">Aeromonas</span> spp&#46; &#40;15&#44;5&#37;&#41; y de <span class="elsevierStyleItalic">Escherichia coli</span> &#40;8&#44;6&#37;&#41;&#44; identificadas como <span class="elsevierStyleItalic">E&#46; coli</span> enterpatog&#233;nicas &#40;EPEC&#41;&#46; Tambi&#233;n se determin&#243; la presencia de otros agentes&#58; <span class="elsevierStyleItalic">Salmonella</span> spp&#46;&#44; <span class="elsevierStyleItalic">Klebsiella</span> spp&#46;&#44; <span class="elsevierStyleItalic">Streptococcus</span> spp&#46;&#44; <span class="elsevierStyleItalic">Staphylococcus aureus&#44; Enterococcus</span> spp&#46;&#44; <span class="elsevierStyleItalic">Mannheimia</span> spp&#46; y <span class="elsevierStyleItalic">Rotavirus</span>&#46; La presencia concurrente de <span class="elsevierStyleItalic">Eimeria</span> spp&#46; y <span class="elsevierStyleItalic">Aeromonas</span> spp&#46; &#40;15&#44;5&#37;&#41; fue la observaci&#243;n m&#225;s frecuente&#46; Se encontr&#243; asociaci&#243;n estad&#237;sticamente significativa entre la presentaci&#243;n del cuadro cl&#237;nico en conejos y la presencia de <span class="elsevierStyleItalic">Eimeria</span> spp&#46; &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#44;000&#41;&#44; <span class="elsevierStyleItalic">Mannheimia</span> spp&#46; &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#44;001&#41;&#44; <span class="elsevierStyleItalic">Salmonella</span> spp&#46;&#44; <span class="elsevierStyleItalic">Klebsiella</span> spp&#46;&#44; <span class="elsevierStyleItalic">Streptococcus</span> spp&#46; y <span class="elsevierStyleItalic">Enterococcus</span> spp&#46; &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#44;006&#41;&#46;</p></span>"
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          "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Agents isolated from enteric profiles in rabbits from Mexico&#46;</p>"
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                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Concurrent identification&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Frequency&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Percentage&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Enteropathogenic <span class="elsevierStyleItalic">Escherichia coli</span> &#40;EPEC&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">5&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">8&#46;7&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Eimeria magna</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">25&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">43&#46;1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Enterococcus</span> spp&#46;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">3&#46;5&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Streptococcus</span> spp&#46;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;7&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Rotavirus</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;7&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Mannheimia</span> spp&#46;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;7&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Eimeria magna</span><span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">E&#46; perforans</span><span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">Aeromona</span> spp&#46;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">9&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">15&#46;5&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Eimeria media</span><span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">Sthapylococcus aureus</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;7&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Eimeria media</span><span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">E&#46; intestinalis</span><span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">E&#46; perforans</span><span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">Staphylococcus aureus</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">3&#46;5&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Eimeria magna</span><span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">E&#46; perforans</span><span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">E&#46; vejdovsky</span><span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">Streptococcus</span> spp&#46;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;7&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Eimeria vejdovsky</span><span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">Klebsiella</span> spp&#46;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;7&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Eimeria vejdovsky</span><span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">Salmonella</span> spp&#46;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;7&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Eimeria media</span><span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">E&#46; flavescens</span><span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">Rotavirus</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">3&#46;4&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Eimeria media</span><span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">E&#46; vejdovsky</span><span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">Rotavirus</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;7&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Eimeria media</span><span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">Klebsiella</span> spp&#46;<span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">Rotavirus</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;7&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Eimeria media</span><span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">Salmonella</span> spp&#46;<span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">Rotavirus</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">17&#46;0&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Without isolation&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">3&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">5&#46;2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " colspan="3" align="left" valign="top"><span class="elsevierStyleVsp" style="height:0.5px"></span></td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">58&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">100&#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="spar0020" class="elsevierStyleSimplePara elsevierViewall">Identification of concurring agents in rabbit intestine samples from Mexico&#46;</p>"
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                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Pathogen&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Positive&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Negative&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">p</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Eimeria</span> spp&#46;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">45&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">13&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;000<a class="elsevierStyleCrossRef" href="#tblfn0005"><span class="elsevierStyleSup">a</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Enteropathogenic <span class="elsevierStyleItalic">E&#46; coli</span> &#40;EPEC&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">5&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">53&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;09&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Salmonella</span> spp&#46;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">56&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;006<a class="elsevierStyleCrossRef" href="#tblfn0005"><span class="elsevierStyleSup">a</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Mannheimia</span> spp&#46;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">57&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;001<a class="elsevierStyleCrossRef" href="#tblfn0005"><span class="elsevierStyleSup">a</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Staphylococcus aureus</span>&nbsp;\t\t\t\t\t\t\n
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Article information

ISSN: 03257541
Original language: English

DOI:10.1016/j.ram.2017.03.001

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Year/Month	Html	Pdf	Total

2024 October	9	1	10
2024 September	35	13	48
2024 August	36	6	42
2024 July	18	12	30
2024 June	39	9	48
2024 May	37	1	38
2024 April	23	7	30
2024 March	22	9	31
2024 February	18	10	28
2024 January	16	10	26
2023 December	12	14	26
2023 November	26	10	36
2023 October	21	29	50
2023 September	21	9	30
2023 August	29	14	43
2023 July	21	12	33
2023 June	25	9	34
2023 May	42	13	55
2023 April	49	13	62
2023 March	35	10	45
2023 February	43	19	62
2023 January	38	17	55
2022 December	19	8	27
2022 November	23	15	38
2022 October	13	8	21
2022 September	10	12	22
2022 August	16	6	22
2022 July	15	17	32
2022 June	14	10	24
2022 May	6	12	18
2022 April	12	28	40
2022 March	16	21	37
2022 February	24	5	29
2022 January	43	12	55
2021 December	11	13	24
2021 November	17	12	29
2021 October	18	30	48
2021 September	21	16	37
2021 August	30	6	36
2021 July	22	16	38
2021 June	15	11	26
2021 May	17	6	23
2021 April	13	47	60
2021 March	43	9	52
2021 February	18	13	31
2021 January	21	8	29
2020 December	30	6	36
2020 November	16	16	32
2020 October	12	8	20
2020 September	14	6	20
2020 August	17	9	26
2020 July	18	2	20
2020 June	13	13	26
2020 May	9	9	18
2020 April	10	8	18
2020 March	16	5	21
2020 February	16	7	23
2020 January	17	3	20
2019 December	10	19	29
2019 November	9	6	15
2019 October	11	6	17
2019 September	19	8	27
2019 August	8	3	11
2019 July	9	8	17
2019 June	97	12	109
2019 May	151	17	168
2019 April	105	21	126
2019 March	81	12	93
2019 February	74	4	78
2019 January	76	0	76
2018 December	104	4	108
2018 November	56	3	59
2018 October	97	16	113
2018 September	136	4	140
2018 August	135	3	138
2018 July	109	6	115
2018 June	6	2	8
2018 May	6	9	15
2018 April	7	5	12
2018 March	6	6	12
2018 February	8	1	9
2018 January	10	0	10
2017 December	5	3	8
2017 November	13	2	15
2017 October	5	2	7
2017 September	12	10	22
2017 August	14	3	17
2017 July	21	1	22
2017 June	36	13	49
2017 May	1	12	13
2017 April	0	5	5

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