An Stx-EAEC O59:NM[H19] strain isolated from a hemolytic uremic syndrome case in Argentina

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López Daneri, Silvia Relloso, Leandro Jorge Zarlenga, Mónica Alejandra Vinante, María Teresa Mujica" "autores" => array:6 [ 0 => array:2 [ "nombre" => "María Fernanda" "apellidos" => "Landaburu" ] 1 => array:2 [ "nombre" => "Gabriela A." "apellidos" => "López Daneri" ] 2 => array:2 [ "nombre" => "Silvia" "apellidos" => "Relloso" ] 3 => array:2 [ "nombre" => "Leandro Jorge" "apellidos" => "Zarlenga" ] 4 => array:2 [ "nombre" => "Mónica Alejandra" "apellidos" => "Vinante" ] 5 => array:2 [ "nombre" => "María Teresa" "apellidos" => "Mujica" ] ] ] ] ] "idiomaDefecto" => "en" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S0325754119300513?idApp=UINPBA00004N" "url" => "/03257541/0000005200000001/v1_202003120635/S0325754119300513/v1_202003120635/en/main.assets" ] "en" => array:20 [ "idiomaDefecto" => true "cabecera" => "Brief report" "titulo" => "An Stx-EAEC O59:NM[H19] strain isolated from a hemolytic uremic syndrome case in Argentina" "tieneTextoCompleto" => true "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "31" "paginaFinal" => "35" ] ] "autores" => array:1 [ 0 => array:4 [ "autoresLista" => "Claudia C. Carbonari, Miriam Ricciardi, Ana Rodríguez Calvo, Alejandro Montes, Natalia L. Deza, María A. Conde Valentino, Gisela Zolezzi, Ariela Baschkier, Mariano Vago, Denise Acosta, Eduardo A. Manfredi, Elizabeth S. Miliwebsky, Isabel Chinen, Marta Rivas" "autores" => array:14 [ 0 => array:3 [ "nombre" => "Claudia C." "apellidos" => "Carbonari" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] ] ] 1 => array:3 [ "nombre" => "Miriam" "apellidos" => "Ricciardi" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "b" "identificador" => "aff0010" ] ] ] 2 => array:3 [ "nombre" => "Ana Rodríguez" "apellidos" => "Calvo" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "b" "identificador" => "aff0010" ] ] ] 3 => array:3 [ "nombre" => "Alejandro" "apellidos" => "Montes" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "b" "identificador" => "aff0010" ] ] ] 4 => array:3 [ "nombre" => "Natalia L." 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"apellidos" => "Manfredi" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] ] ] 11 => array:3 [ "nombre" => "Elizabeth S." "apellidos" => "Miliwebsky" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] ] ] 12 => array:3 [ "nombre" => "Isabel" "apellidos" => "Chinen" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] ] ] 13 => array:4 [ "nombre" => "Marta" "apellidos" => "Rivas" "email" => array:1 [ 0 => "martarivas170@gmail.com" ] "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "*" "identificador" => "cor0005" ] ] ] ] "afiliaciones" => array:2 [ 0 => array:3 [ "entidad" => "Servicio Fisiopatogenia, Departamento Bacteriología, Instituto Nacional de Enfermedades Infecciosas-ANLIS “Dr. Carlos G. Malbrán”, Av. Vélez Sarsfield 563, 1281 Ciudad Autónoma de Buenos Aires, Argentina" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Hospital Zonal de Puerto Madryn “Dr. Andrés Ísola”, Roberto Gómez 299, U9120 Puerto Madryn, Chubut, Argentina" "etiqueta" => "b" "identificador" => "aff0010" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Cepa EAEC-Stx O59:NM[H19] aislada de un caso de síndrome urémico hemolítico en Argentina" ] ] "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" => 980 "Ancho" => 2502 "Tamanyo" => 184176 ] ] "descripcion" => array:1 [ "en" => "Clonal relation between Stx-EAEC O59:NM[H19] strains isolated in Germany and Argentina by XbaI-PFGE." ] ] ] "textoCompleto" => "IntroductionShiga toxin (Stx)-producing Escherichia coli (STEC) are a heterogeneous group of foodborne pathogens causing diarrhea, hemorrhagic colitis and hemolytic uremic syndrome (HUS). Argentina has the highest incidence of HUS globally, with approximately 400 new cases each year. During the period 2005–2015, the incidence in children under 5 years of age was 8.5 cases per 100000 annually. Evidence of STEC infection is found in around 70% of HUS cases and O157:H7 is the predominant serotype isolated<a class="elsevierStyleCrossRef" href="#bib0120">8</a>. In 2011, a STEC O104:H4 strain caused a large outbreak in Germany with more than 4000 infections, including 900 HUS cases and 50 deaths<a class="elsevierStyleCrossRef" href="#bib0090">2</a>. The outbreak strain, besides the production of Stx, possessed the adhesion determinants of Enteroaggregative E. coli (EAEC). This new pathotype was named as Enteroaggregative Hemorrhagic E. coli (EAHEC)<a class="elsevierStyleCrossRefs" href="#bib0085">1,4</a>, hybrid of EAEC/STEC<a class="elsevierStyleCrossRef" href="#bib0125">9</a> and Stx-EAEC<a class="elsevierStyleCrossRef" href="#bib0095">3</a> by different authors, in order to better define the virulence profile.In this report, we describe the isolation and characterization of a Stx-EAEC strain that was associated with an HUS case in Argentina and compare the strain to similar strains isolated in Germany.Clinical and laboratory findingsOn January 15, 2015, a boy who was 7 years and 8 months old was seen by his pediatrician for fever (38°C), and vomiting. The child presented severe headache, irritability, photophobia, abdominal pain, but no upper tract catarrh, and was sent home with dietary and general instructions. Only a nonsteroidal anti-inflammatory drug was given as treatment. As the general condition worsened, the next day he was seen by his pediatrician again, who sent him to the emergency room of Hospital Zonal de Puerto Madryn “Dr. Andrés Ísola”. Upon admission, he exhibited generalized pallor, jaundice of skin and mucous membranes, an episode of loose stool, dehydration, arterial hypertension (blood pressure 150/90mmHg [greater than 95th percentile of systolic blood pressure for age]) and sleepiness, and, given his condition, he was hospitalized in the intensive care unit (ICU). In the ICU, the child had oliguria and dark urine, with an initial diagnostic impression of acute renal failure, anemia and thrombocytopenia. A presumptive diagnosis of atypical HUS (D-) was established. Initial laboratory findings included: hematocrit, 28%; hemoglobin level, 9.2g/dl; leukocyte count, 10700/mm3; platelet count, 33000/mm3; serum glucose, 106mg/dl; blood urea nitrogen (BUN), 206mg/dl; serum creatinine, 1.9mg/dl; albumin, 4.1g/dl; uric acid, 7.5mg/dl; calcium, 9.4mg/dl; phosphorus, 6.5mg/dl; magnesium, 2.8mg/dl; sodium, 134mEq/l; potassium, 4.4mEq/l; pH, 7.36; bicarbonate, 16mmol/l; base excess, −8mmol/l; AST, 133U/l; ALT, 16U/l; total bilirubin, 4mg/dl; direct bilirubin, 1mg/dl; indirect bilirubin, 3mg/dl; prothrombin time, 12.7s; lactic acid, 1.1mmol/l; lactate dehydrogenase (LDH), 5130UI/l. A stool culture was requested. During hospitalization, the patient received hydration, omeprazole, nifedipine, allopurinol, calcium carbonate, bicarbonate, and three infusions of packed red blood cells, but did not require dialysis. Antimicrobial therapy was not provided. The blood and urine cultures were negative. On the 8th day, he had a seizure episode with paresis of the left hemisphere that improved with lorazepam treatment. He continued the treatment with clobazan, and remained with left hemiparesis and ataxia that improved in the following days. Cranial magnetic resonance imaging (MRI) and X-ray computed tomography (CT) scans showed normal parameters. The patient was discharged after 11 days of hospitalization. Since the hospital discharge and until now, he has been periodically controlled by a pediatric nephrologist, confirming on February 2018 absence of proteinuria and microalbuminuria and normal renal function.Epidemiological investigationAs part of the epidemiological study conducted at the hospital to identify the risk factors associated with the disease, the parents were interviewed using a standardized questionnaire. Information was collected about potential exposure in the 7 days before the onset of symptoms, and demographic issues. On January 11, the child and his family (parents and a 42-months-old sister) had eaten well-done roast meat and sausages purchased at a local market. No other family members reported gastrointestinal symptoms. The parents referred good practices of food handling and hygiene in the home. Informed consent was obtained from the adult primary caregiver, who was interviewed in person.Microbiological investigationA stool sample was collected on January 16 and routinely cultured for E. coli, Salmonella, and Shigella species. The stool sample and a culture on MacConkey (MAC) agar (Difco Laboratories, Detroit, MI) were sent to the Servicio Fisiopatogenia, as National Reference Laboratory (NRL), for STEC and free fecal Stx (FFStx) detection, as previously described<a class="elsevierStyleCrossRef" href="#bib0135">11</a>. The material was sent with the respective hospital charts (records), from which the clinical, laboratory and epidemiological data were reviewed. The bacterial confluent growth zone on MAC was positive for stx2 gene by a multiplex polymerase chain reaction (mPCR)<a class="elsevierStyleCrossRef" href="#bib0135">11</a>. The isolate (EC-90 #1) identified as E. coli by standard biochemical methods, was defined as non-O157/stx2 by the mPCR. The strain was negative for eae (intimin encoded protein) and ehxA (enterohemolysin) genes by PCR<a class="elsevierStyleCrossRef" href="#bib0135">11</a>. FFStx2 was detected by specific cytotoxicity assays on Vero cells.From a second stool sample, collected on March 17, 61 days after the onset of symptoms, E. colistx2-positive (EC-90 #2) and FFStx2 were detected. Due to the prolonged STEC shedding, virulence factors of other diarrheagenic E. coli pathotypes were analyzed by PCR<a class="elsevierStyleCrossRef" href="#bib0145">13</a>. Both isolates (EC-90 #1 and EC-90 #2), corresponding to the first and second samples, were positive for the regulator AggR, which drives the expression of AraC, and also the expression of the different aggregative adherence fimbriae (AAF) responsible of the characteristic stacked brick-like adherence pattern of EAEC and other proteins<a class="elsevierStyleCrossRef" href="#bib0095">3</a>. A third E. coli strain (EC-90 #3) with the same virulence profile was recovered from feces 115 days after the onset of symptoms and the stool sample was also FFStx2-positive.The full characterization done by PCR as previously described<a class="elsevierStyleCrossRefs" href="#bib0115">7,9,14,15</a>, showed that the three strains harbored stx2a (Shiga toxin variant 2a), iha (gene for IrgA adhesion homolog), lpfAO26 (gene for structural subunit of long polar fimbriae (LPF) of STEC O26), lpfAO113 (gene for structural subunit of LPF of STEC O113) genes frequently associated with STEC, and aatA (dispersin transporter protein), aap (dispersin, antiaggregation protein), pic (protein involved in intestinal colonization), sigA (gene for the SPATE protein) genes typically associated with EAEC. The presence of type IV AAF was established by the amplification of the agg4A fimbrial subunit gene. The EC-90 #1, EC-90 #2 and EC-90 #3 strains, were phenotypically serotyped as O59:NM and the fliCH19 gene was determined by PCR, using primers described previously<a class="elsevierStyleCrossRef" href="#bib0105">5</a>. The strains showed a cytotoxicity of 600 CD50/90μl on Vero cells, and were resistant to streptomycin and trimethoprim/sulfonamides. Stool samples collected at 145 and 162 days were negative for Stx-EAEC and FFStx.DiscussionUntil recent years, the ability to produce Stx and to cause the attaching-and-effacing (A/E) lesion was the paradigm for severe HUS-associated STEC. The Stx-EAEC O59:NM[H19] strain, described in the present study, had the ability to produce HUS and to cause a long-term shedding in the patient. Although the strain showed low cytotoxicity on Vero cells, its pathogenicity and prolonged excretion could be attributed to the fact that it has characteristics of EAEC; therefore it is a better colonizer of the intestine due to its aggregative phenotype. This property could facilitate the systemic absorption of Stx.Since the large German outbreak associated with a Stx-EAEC O104:H4 strain, attention has been focusing on this new E. coli pathotype. Prager et al. screened 2435 strains of the STEC collection from the German National Reference Centre for Salmonella and other Bacterial Enteric Pathogens (NRC), corresponding to the period 2008–2012, for the presence of stx1, stx2, eae and ehxA genes<a class="elsevierStyleCrossRef" href="#bib0130">10</a>. Among 268 eae- and ehxA-negative strains, two strains exhibited both STEC and EAEC marker genes and were stx2- and aatA-positive. One strain, isolated from a case of bloody diarrhea in 2010 and serotyped as O59:NM[H19], harbored stx2a, belonged to the sequence type (ST) 1136 by multiple locus sequence typing (MLST), and exhibited genes for type IV aggregative AAF fimbriae, with resistance toward sulfonamides, streptomycin, and trimethoprim/sulfonamide and low cytotoxicity on Vero cells.The German O59:NM[H19] strain harbored the same genes as the Argentine O59:NM[H19] strain plus the following genes: irp2 (component of iron uptake system on high pathogenicity island) gene of STEC, and set1a (Shigella enterotoxin subunit A), set1b (Shigella enterotoxin subunit B), iucA (siderophore aerobactin) genes of EAEC. The second German strain, isolated from a patient with diarrhea in 2012, harbored stx2b, was typed as Orough:H2 and belonged to MLST ST26.A comparison between the properties of both Stx-EAEC O59:NM[H19] strains is shown in <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>.<elsevierMultimedia ident="tbl0005"></elsevierMultimedia>By pulsed-field gel electrophoresis using the restriction enzyme XbaI (XbaI-PFGE), the three Argentine strains showed the same macrorestriction pattern, named AREEF901.0001, with 100% similarity<a class="elsevierStyleCrossRef" href="#bib0135">11</a>. A high clonal relationship (>85%) with the Stx-EAEC O59:NM[H19] German strain was established. The dendrogram of the German and Argentine strains is shown in <a class="elsevierStyleCrossRef" href="#fig0005">Figure 1</a>.<elsevierMultimedia ident="fig0005"></elsevierMultimedia>The impact of the German outbreak was so important to become the responsible E. coli strain as a prototype of the new Stx-EAEC pathotype. The emergence of Stx-EAEC O104:H4 suggests that either certain EAEC serotypes might be more susceptible to acquire STEC determinants or that there are certain Stx-EAEC ancestors which successfully adapted to survive specific selection conditions, which represents a new challenge for the entire scientific community. There is evidence that shows that the Stx-EAEC O104:H4 could have evolved by the uptake of a stx2-phage originated from the bovine reservoir by an EAEC O104:H4 strain<a class="elsevierStyleCrossRef" href="#bib0085">1</a>.Other Stx-EAEC strains of different serotypes were previously described in association with human disease. During an HUS outbreak in France in 1996, an O111:H2 strain was characterized as stx2- and AAF-positive, and eaeA- and ehxA-negative, being the first Stx-EAEC hybrid described. In 1999, an O86:NM[H2] strain with stx2 and AAF marker genes but no eae was isolated from a child with HUS and bloody diarrhea in Japan. Later, in 2011, an O111:H21 strain associated with a household outbreak in Northern Ireland was detected. The strain harbored the stx2c gene and the type V AAF fimbriae, but was eae-negative with a low level of resistance to ampicillin<a class="elsevierStyleCrossRef" href="#bib0110">6</a>. In 2013 in a school in northern Italy, an outbreak caused by a Stx-EAEC- O127:H4 strain was reported. Five Stx-EAEC strains were isolated from 76 fecal samples from children and school staff. The strains were characterized as O127:H4 and ST678 and possessed the stx2a gene and other EAEC virulence genes such as aggR, aap, aat, aaiC, sigA, pic and astA. The stx2-phage was inserted in wrbA site, as well as it was described for O104:H4 outbreak strain<a class="elsevierStyleCrossRef" href="#bib0140">12</a>.Tozzoli et al. have demonstrated that, at laboratory level, all stx2-phages used in their study were able to infect a range of bacterial hosts, including both diarrheagenic (DEC) and extraintestinal pathogenic E. coli (ExPEC), suggesting that STEC might represent multiple pathogroups whose virulence has been increased by the event of a stx-phage acquisition<a class="elsevierStyleCrossRef" href="#bib0160">16</a>. Regarding the Stx-EAEC, it was demonstrated by genomics sequencing, that EAEC strain was infected by stx2-phage and yield this new pathotype<a class="elsevierStyleCrossRef" href="#bib0095">3</a>. On the other hand Nyholm et al. also described hybrid Shigatoxigenic and Enterotoxigenic Escherichia coli (STEC/ETEC) strains, and 1% of the strains belonging to a STEC collection harbored genes typically present in ETEC and some of them being isolated from patients with HUS<a class="elsevierStyleCrossRef" href="#bib0125">9</a>.In Argentina, this is the first report of an HUS case associated with a Stx-EAEC infection. A distinct characteristic was the prolonged shedding during 4 months. Although O59:NM[H19] is an unusual serotype in the country, these results open new questions and pose a challenge for the Surveillance System.Conflict of interestThe authors declare that they have no conflicts of interest." "textoCompletoSecciones" => array:1 [ "secciones" => array:12 [ 0 => array:3 [ "identificador" => "xres1316946" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec1215366" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres1316945" "titulo" => "Resumen" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0010" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec1215365" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 5 => array:2 [ "identificador" => "sec0010" "titulo" => "Clinical and laboratory findings" ] 6 => array:2 [ "identificador" => "sec0015" "titulo" => "Epidemiological investigation" ] 7 => array:2 [ "identificador" => "sec0020" "titulo" => "Microbiological investigation" ] 8 => array:2 [ "identificador" => "sec0025" "titulo" => "Discussion" ] 9 => array:2 [ "identificador" => "sec0030" "titulo" => "Conflict of interest" ] 10 => array:2 [ "identificador" => "xack453982" "titulo" => "Acknowledgments" ] 11 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2018-10-19" "fechaAceptado" => "2019-03-20" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec1215366" "palabras" => array:4 [ 0 => "Stx-EAEC" 1 => "O59:NM[H19]" 2 => "HUS" 3 => "Surveillance system" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec1215365" "palabras" => array:4 [ 0 => "EAEC-Stx" 1 => "O59:NM[H19]" 2 => "SUH" 3 => "Sistema de vigilancia" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "Shiga toxin-producing Escherichia coli (STEC) are a heterogeneous group of foodborne pathogens causing a broad spectrum of human disease, from uncomplicated diarrhea to hemolytic uremic syndrome (HUS). In this study, we report an HUS case associated with an O59:NM[H19] strain, harboring stx2a, iha, lpfAO26, lpfAO113 genes associated with STEC, and aatA, aap, pic, sigA, agg4A genes associated with enteroaggregative E. coli (EAEC), named Stx-EAEC. The strain showed low toxicity on Vero cells, and was resistant to streptomycin and trimethoprim/sulfonamides. The child carried the bacteria for more than 100 days. Since the large outbreak associated with Stx-EAEC O104:H4, many strains with similar profiles have been described. In Germany, an O59:NM[H19] strain, with comparable characteristics to the Argentine strain, was isolated from a bloody diarrhea case. In Argentina, this is the first report of an HUS case associated with a Stx-EAEC infection, and represents a new challenge for the surveillance system." ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "Escherichia coli productor de la toxina Shiga (STEC) es un grupo heterogéneo de patógenos transmitidos por alimentos que causan un amplio espectro de enfermedades humanas, desde diarrea no complicada hasta síndrome urémico hemolítico (SUH). Nosotros informamos de un caso de SUH por O59:NM[H19], que portaba los genes stx2a, iha, lpfAO26, lpfAO113 asociados con STEC, y los genes aatA, aap, pic, sigA, agg4A de E. coli enteroagregativo (EAEC), llamado EAEC-Stx. La cepa mostró baja citotoxicidad en las células Vero, y fue resistente a estreptomicina y trimetoprima/sulfonamidas. El niño excretó la bacteria durante más de 100 días. Desde el brote asociado con EAEC-Stx O104:H4, se describieron muchas cepas con perfiles similares. En Alemania se aisló una cepa O59:NM[H19] de una diarrea sanguinolenta, con características comparables a la cepa argentina. Este es el primer informe de un caso de SUH asociado a una infección por EAEC-Stx, y representa un nuevo desafío para el sistema de vigilancia." ] ] "multimedia" => array:2 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 980 "Ancho" => 2502 "Tamanyo" => 184176 ] ] "descripcion" => array:1 [ "en" => "Clonal relation between Stx-EAEC O59:NM[H19] strains isolated in Germany and Argentina by XbaI-PFGE." ] ] 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:2 [ "leyenda" => "a,b Both strains, isolated from bloody diarrhea (BD) and hemolytic uremic syndrome (HUS) cases, showed resistance to streptomycin and trimethoprim/sulfamethoxazole and low cytotoxicity on Vero cells." "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-with-role" title="\n \t\t\t\t\ttable-head\n \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Genes \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Description of the genes \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Pathotype \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Germany BDa/2010 \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Argentina HUSb/2015 \t\t\t\t\t\t\n \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">stx2a \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Shiga toxin variant 2a \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">EAEC/EHEC \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">+ \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">iha \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">IrgA adhesion homolog \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">STEC \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">+ \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">lpfO26 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">subunit of long polar fimbriae of EHEC O26 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">STEC/EHEC \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">+ \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">lpfO113 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">subunit of long polar fimbriae of EHEC O113 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">STEC/EHEC \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">+ \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">ehxA \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">enterohemolysin \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">STEC \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">− \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">− \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">eae \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">intimin \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">STEC/EPEC \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">− \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">− \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">terA \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">tellurium resistance protein \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">STEC/EHEC \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">− \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">− \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">irp2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">iron uptake system \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">STEC \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Unknown \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">aggR \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">transcriptional activator \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">EAEC \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">+ \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">aatA \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">dispersin transporter protein \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">EAEC \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">+ \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">aap \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">dispersin, antiaggregation protein \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">EAEC \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">+ \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">st1a/b \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Shigella enterotoxin subunit A and B \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">EAEC \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Unknown \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">pic \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">serine protease precursor \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">EAEC \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">+ \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">pet \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">plasmid-encoded toxin \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">EAEC \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Unknown \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">+ \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">sigA \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">IgA protease-like homolog \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">EAEC/Shigella \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">+ \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">iucA/C \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">siderophore aerobactin \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">EAEC \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Unknown \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">agg4A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">AAF/IV fimbrial subunit \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">EAEC \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Unknown \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">+ \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">astA \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">EAST-1 heat-stable toxin \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">EAEC/ETEC \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">− \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">− \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab2257463.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Properties of Stx-EAEC O59:NM[H19] strains isolated in Germany and Argentina" ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0015" "bibliografiaReferencia" => array:16 [ 0 => array:3 [ "identificador" => "bib0085" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Outbreak of Shiga toxin-producing Escherichia coli (STEC) O104:H4 infection in Germany causes a paradigm shift with regard to human pathogenicity of STEC strains" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:2 [ 0 => "L. 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Cepa EAEC-Stx O59:NM[H19] aislada de un caso de síndrome urémico hemolítico en Argentina

Claudia C. Carbonaria, Miriam Ricciardib, Ana Rodríguez Calvob, Alejandro Montesb, Natalia L. Dezaa, María A. Conde Valentinob, Gisela Zolezzia, Ariela Baschkiera, Mariano Vagob, Denise Acostab, Eduardo A. Manfredia, Elizabeth S. Miliwebskya, Isabel Chinena, Marta Rivasa,

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martarivas170@gmail.com

Corresponding author.

a Servicio Fisiopatogenia, Departamento Bacteriología, Instituto Nacional de Enfermedades Infecciosas-ANLIS “Dr. Carlos G. Malbrán”, Av. Vélez Sarsfield 563, 1281 Ciudad Autónoma de Buenos Aires, Argentina

b Hospital Zonal de Puerto Madryn “Dr. Andrés Ísola”, Roberto Gómez 299, U9120 Puerto Madryn, Chubut, Argentina

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        "titulo" => "Cepa EAEC-Stx O59&#58;NM&#91;H19&#93; aislada de un caso de s&#237;ndrome ur&#233;mico hemol&#237;tico en Argentina"
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          "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Clonal relation between Stx-EAEC O59&#58;NM&#91;H19&#93; strains isolated in Germany and Argentina by <span class="elsevierStyleItalic">Xba</span>I-PFGE&#46;</p>"
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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">Shiga toxin &#40;Stx&#41;-producing <span class="elsevierStyleItalic">Escherichia coli</span> &#40;STEC&#41; are a heterogeneous group of foodborne pathogens causing diarrhea&#44; hemorrhagic colitis and hemolytic uremic syndrome &#40;HUS&#41;&#46; Argentina has the highest incidence of HUS globally&#44; with approximately 400 new cases each year&#46; During the period 2005&#8211;2015&#44; the incidence in children under 5 years of age was 8&#46;5 cases per 100<span class="elsevierStyleHsp" style=""></span>000 annually&#46; Evidence of STEC infection is found in around 70&#37; of HUS cases and O157&#58;H7 is the predominant serotype isolated<a class="elsevierStyleCrossRef" href="#bib0120"><span class="elsevierStyleSup">8</span></a>&#46; In 2011&#44; a STEC O104&#58;H4 strain caused a large outbreak in Germany with more than 4000 infections&#44; including 900 HUS cases and 50 deaths<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">2</span></a>&#46; The outbreak strain&#44; besides the production of Stx&#44; possessed the adhesion determinants of Enteroaggregative <span class="elsevierStyleItalic">E&#46; coli</span> &#40;EAEC&#41;&#46; This new pathotype was named as Enteroaggregative Hemorrhagic <span class="elsevierStyleItalic">E&#46; coli</span> &#40;EAHEC&#41;<a class="elsevierStyleCrossRefs" href="#bib0085"><span class="elsevierStyleSup">1&#44;4</span></a>&#44; hybrid of EAEC&#47;STEC<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">9</span></a> and Stx-EAEC<a class="elsevierStyleCrossRef" href="#bib0095"><span class="elsevierStyleSup">3</span></a> by different authors&#44; in order to better define the virulence profile&#46;</p><p id="par0010" class="elsevierStylePara elsevierViewall">In this report&#44; we describe the isolation and characterization of a Stx-EAEC strain that was associated with an HUS case in Argentina and compare the strain to similar strains isolated in Germany&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Clinical and laboratory findings</span><p id="par0015" class="elsevierStylePara elsevierViewall">On January 15&#44; 2015&#44; a boy who was 7 years and 8 months old was seen by his pediatrician for fever &#40;38<span class="elsevierStyleHsp" style=""></span>&#176;C&#41;&#44; and vomiting&#46; The child presented severe headache&#44; irritability&#44; photophobia&#44; abdominal pain&#44; but no upper tract catarrh&#44; and was sent home with dietary and general instructions&#46; Only a nonsteroidal anti-inflammatory drug was given as treatment&#46; As the general condition worsened&#44; the next day he was seen by his pediatrician again&#44; who sent him to the emergency room of Hospital Zonal de Puerto Madryn &#8220;Dr&#46; Andr&#233;s &#205;sola&#8221;&#46; Upon admission&#44; he exhibited generalized pallor&#44; jaundice of skin and mucous membranes&#44; an episode of loose stool&#44; dehydration&#44; arterial hypertension &#40;blood pressure 150&#47;90<span class="elsevierStyleHsp" style=""></span>mmHg &#91;greater than 95th percentile of systolic blood pressure for age&#93;&#41; and sleepiness&#44; and&#44; given his condition&#44; he was hospitalized in the intensive care unit &#40;ICU&#41;&#46; In the ICU&#44; the child had oliguria and dark urine&#44; with an initial diagnostic impression of acute renal failure&#44; anemia and thrombocytopenia&#46; A presumptive diagnosis of atypical HUS &#40;D-&#41; was established&#46; Initial laboratory findings included&#58; hematocrit&#44; 28&#37;&#59; hemoglobin level&#44; 9&#46;2<span class="elsevierStyleHsp" style=""></span>g&#47;dl&#59; leukocyte count&#44; 10<span class="elsevierStyleHsp" style=""></span>700&#47;mm<span class="elsevierStyleSup">3</span>&#59; platelet count&#44; 33<span class="elsevierStyleHsp" style=""></span>000&#47;mm<span class="elsevierStyleSup">3</span>&#59; serum glucose&#44; 106<span class="elsevierStyleHsp" style=""></span>mg&#47;dl&#59; blood urea nitrogen &#40;BUN&#41;&#44; 206<span class="elsevierStyleHsp" style=""></span>mg&#47;dl&#59; serum creatinine&#44; 1&#46;9<span class="elsevierStyleHsp" style=""></span>mg&#47;dl&#59; albumin&#44; 4&#46;1<span class="elsevierStyleHsp" style=""></span>g&#47;dl&#59; uric acid&#44; 7&#46;5<span class="elsevierStyleHsp" style=""></span>mg&#47;dl&#59; calcium&#44; 9&#46;4<span class="elsevierStyleHsp" style=""></span>mg&#47;dl&#59; phosphorus&#44; 6&#46;5<span class="elsevierStyleHsp" style=""></span>mg&#47;dl&#59; magnesium&#44; 2&#46;8<span class="elsevierStyleHsp" style=""></span>mg&#47;dl&#59; sodium&#44; 134<span class="elsevierStyleHsp" style=""></span>mEq&#47;l&#59; potassium&#44; 4&#46;4<span class="elsevierStyleHsp" style=""></span>mEq&#47;l&#59; pH&#44; 7&#46;36&#59; bicarbonate&#44; 16<span class="elsevierStyleHsp" style=""></span>mmol&#47;l&#59; base excess&#44; &#8722;8<span class="elsevierStyleHsp" style=""></span>mmol&#47;l&#59; AST&#44; 133<span class="elsevierStyleHsp" style=""></span>U&#47;l&#59; ALT&#44; 16<span class="elsevierStyleHsp" style=""></span>U&#47;l&#59; total bilirubin&#44; 4<span class="elsevierStyleHsp" style=""></span>mg&#47;dl&#59; direct bilirubin&#44; 1<span class="elsevierStyleHsp" style=""></span>mg&#47;dl&#59; indirect bilirubin&#44; 3<span class="elsevierStyleHsp" style=""></span>mg&#47;dl&#59; prothrombin time&#44; 12&#46;7<span class="elsevierStyleHsp" style=""></span>s&#59; lactic acid&#44; 1&#46;1<span class="elsevierStyleHsp" style=""></span>mmol&#47;l&#59; lactate dehydrogenase &#40;LDH&#41;&#44; 5130<span class="elsevierStyleHsp" style=""></span>UI&#47;l&#46; A stool culture was requested&#46; During hospitalization&#44; the patient received hydration&#44; omeprazole&#44; nifedipine&#44; allopurinol&#44; calcium carbonate&#44; bicarbonate&#44; and three infusions of packed red blood cells&#44; but did not require dialysis&#46; Antimicrobial therapy was not provided&#46; The blood and urine cultures were negative&#46; On the 8<span class="elsevierStyleSup">th</span> day&#44; he had a seizure episode with paresis of the left hemisphere that improved with lorazepam treatment&#46; He continued the treatment with clobazan&#44; and remained with left hemiparesis and ataxia that improved in the following days&#46; Cranial magnetic resonance imaging &#40;MRI&#41; and X-ray computed tomography &#40;CT&#41; scans showed normal parameters&#46; The patient was discharged after 11 days of hospitalization&#46; Since the hospital discharge and until now&#44; he has been periodically controlled by a pediatric nephrologist&#44; confirming on February 2018 absence of proteinuria and microalbuminuria and normal renal function&#46;</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Epidemiological investigation</span><p id="par0020" class="elsevierStylePara elsevierViewall">As part of the epidemiological study conducted at the hospital to identify the risk factors associated with the disease&#44; the parents were interviewed using a standardized questionnaire&#46; Information was collected about potential exposure in the 7 days before the onset of symptoms&#44; and demographic issues&#46; On January 11&#44; the child and his family &#40;parents and a 42-months-old sister&#41; had eaten well-done roast meat and sausages purchased at a local market&#46; No other family members reported gastrointestinal symptoms&#46; The parents referred good practices of food handling and hygiene in the home&#46; Informed consent was obtained from the adult primary caregiver&#44; who was interviewed in person&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Microbiological investigation</span><p id="par0025" class="elsevierStylePara elsevierViewall">A stool sample was collected on January 16 and routinely cultured for <span class="elsevierStyleItalic">E&#46; coli</span>&#44; <span class="elsevierStyleItalic">Salmonella</span>&#44; and <span class="elsevierStyleItalic">Shigella</span> species&#46; The stool sample and a culture on MacConkey &#40;MAC&#41; agar &#40;Difco Laboratories&#44; Detroit&#44; MI&#41; were sent to the Servicio Fisiopatogenia&#44; as National Reference Laboratory &#40;NRL&#41;&#44; for STEC and free fecal Stx &#40;FFStx&#41; detection&#44; as previously described<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">11</span></a>&#46; The material was sent with the respective hospital charts &#40;records&#41;&#44; from which the clinical&#44; laboratory and epidemiological data were reviewed&#46; The bacterial confluent growth zone on MAC was positive for <span class="elsevierStyleItalic">stx</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">2</span></span> gene by a multiplex polymerase chain reaction &#40;mPCR&#41;<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">11</span></a>&#46; The isolate &#40;EC-90 &#35;1&#41; identified as <span class="elsevierStyleItalic">E&#46; coli</span> by standard biochemical methods&#44; was defined as non-O157&#47;<span class="elsevierStyleItalic">stx</span><span class="elsevierStyleInf">2</span> by the mPCR&#46; The strain was negative for <span class="elsevierStyleItalic">eae</span> &#40;intimin encoded protein&#41; and <span class="elsevierStyleItalic">ehx</span>A &#40;enterohemolysin&#41; genes by PCR<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">11</span></a>&#46; FFStx2 was detected by specific cytotoxicity assays on Vero cells&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">From a second stool sample&#44; collected on March 17&#44; 61 days after the onset of symptoms&#44; <span class="elsevierStyleItalic">E&#46; coli</span><span class="elsevierStyleItalic">stx</span><span class="elsevierStyleInf">2</span>-positive &#40;EC-90 &#35;2&#41; and FFStx2 were detected&#46; Due to the prolonged STEC shedding&#44; virulence factors of other diarrheagenic <span class="elsevierStyleItalic">E&#46; coli</span> pathotypes were analyzed by PCR<a class="elsevierStyleCrossRef" href="#bib0145"><span class="elsevierStyleSup">13</span></a>&#46; Both isolates &#40;EC-90 &#35;1 and EC-90 &#35;2&#41;&#44; corresponding to the first and second samples&#44; were positive for the regulator AggR&#44; which drives the expression of AraC&#44; and also the expression of the different aggregative adherence fimbriae &#40;AAF&#41; responsible of the characteristic stacked brick-like adherence pattern of EAEC and other proteins<a class="elsevierStyleCrossRef" href="#bib0095"><span class="elsevierStyleSup">3</span></a>&#46; A third <span class="elsevierStyleItalic">E&#46; coli</span> strain &#40;EC-90 &#35;3&#41; with the same virulence profile was recovered from feces 115 days after the onset of symptoms and the stool sample was also FFStx2-positive&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">The full characterization done by PCR as previously described<a class="elsevierStyleCrossRefs" href="#bib0115"><span class="elsevierStyleSup">7&#44;9&#44;14&#44;15</span></a>&#44; showed that the three strains harbored <span class="elsevierStyleItalic">stx</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">2a</span></span> &#40;Shiga toxin variant 2a&#41;&#44; <span class="elsevierStyleItalic">iha</span> &#40;gene for IrgA adhesion homolog&#41;&#44; <span class="elsevierStyleItalic">lpfA</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">O26</span></span> &#40;gene for structural subunit of long polar fimbriae &#40;LPF&#41; of STEC O26&#41;&#44; <span class="elsevierStyleItalic">lpfA</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">O113</span></span> &#40;gene for structural subunit of LPF of STEC O113&#41; genes frequently associated with STEC&#44; and <span class="elsevierStyleItalic">aatA</span> &#40;dispersin transporter protein&#41;&#44; <span class="elsevierStyleItalic">aap</span> &#40;dispersin&#44; antiaggregation protein&#41;&#44; <span class="elsevierStyleItalic">pic</span> &#40;protein involved in intestinal colonization&#41;&#44; <span class="elsevierStyleItalic">sigA</span> &#40;gene for the SPATE protein&#41; genes typically associated with EAEC&#46; The presence of type IV AAF was established by the amplification of the <span class="elsevierStyleItalic">agg4A</span> fimbrial subunit gene&#46; The EC-90 &#35;1&#44; EC-90 &#35;2 and EC-90 &#35;3 strains&#44; were phenotypically serotyped as O59&#58;NM and the <span class="elsevierStyleItalic">fliC</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">H19</span></span> gene was determined by PCR&#44; using primers described previously<a class="elsevierStyleCrossRef" href="#bib0105"><span class="elsevierStyleSup">5</span></a>&#46; The strains showed a cytotoxicity of 600 CD50&#47;90<span class="elsevierStyleHsp" style=""></span>&#956;l on Vero cells&#44; and were resistant to streptomycin and trimethoprim&#47;sulfonamides&#46; Stool samples collected at 145 and 162 days were negative for Stx-EAEC and FFStx&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Discussion</span><p id="par0040" class="elsevierStylePara elsevierViewall">Until recent years&#44; the ability to produce Stx and to cause the attaching-and-effacing &#40;A&#47;E&#41; lesion was the paradigm for severe HUS-associated STEC&#46; The Stx-EAEC O59&#58;NM&#91;H19&#93; strain&#44; described in the present study&#44; had the ability to produce HUS and to cause a long-term shedding in the patient&#46; Although the strain showed low cytotoxicity on Vero cells&#44; its pathogenicity and prolonged excretion could be attributed to the fact that it has characteristics of EAEC&#59; therefore it is a better colonizer of the intestine due to its aggregative phenotype&#46; This property could facilitate the systemic absorption of Stx&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">Since the large German outbreak associated with a Stx-EAEC O104&#58;H4 strain&#44; attention has been focusing on this new <span class="elsevierStyleItalic">E&#46; coli</span> pathotype&#46; Prager et al&#46; screened 2435 strains of the STEC collection from the German National Reference Centre for <span class="elsevierStyleItalic">Salmonella</span> and other Bacterial Enteric Pathogens &#40;NRC&#41;&#44; corresponding to the period 2008&#8211;2012&#44; for the presence of <span class="elsevierStyleItalic">stx</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">1</span></span>&#44; <span class="elsevierStyleItalic">stx</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">2</span></span>&#44; <span class="elsevierStyleItalic">eae</span> and <span class="elsevierStyleItalic">ehxA</span> genes<a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">10</span></a>&#46; Among 268 <span class="elsevierStyleItalic">eae</span>- and <span class="elsevierStyleItalic">ehxA</span>-negative strains&#44; two strains exhibited both STEC and EAEC marker genes and were <span class="elsevierStyleItalic">stx</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">2</span></span>- and <span class="elsevierStyleItalic">aatA</span>-positive&#46; One strain&#44; isolated from a case of bloody diarrhea in 2010 and serotyped as O59&#58;NM&#91;H19&#93;&#44; harbored <span class="elsevierStyleItalic">stx</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">2a</span></span>&#44; belonged to the sequence type &#40;ST&#41; 1136 by multiple locus sequence typing &#40;MLST&#41;&#44; and exhibited genes for type IV aggregative AAF fimbriae&#44; with resistance toward sulfonamides&#44; streptomycin&#44; and trimethoprim&#47;sulfonamide and low cytotoxicity on Vero cells&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">The German O59&#58;NM&#91;H19&#93; strain harbored the same genes as the Argentine O59&#58;NM&#91;H19&#93; strain plus the following genes&#58; <span class="elsevierStyleItalic">irp2</span> &#40;component of iron uptake system on high pathogenicity island&#41; gene of STEC&#44; and <span class="elsevierStyleItalic">set1a</span> &#40;<span class="elsevierStyleItalic">Shigella</span> enterotoxin subunit A&#41;&#44; <span class="elsevierStyleItalic">set1b</span> &#40;<span class="elsevierStyleItalic">Shigella</span> enterotoxin subunit B&#41;&#44; <span class="elsevierStyleItalic">iucA</span> &#40;siderophore aerobactin&#41; genes of EAEC&#46; The second German strain&#44; isolated from a patient with diarrhea in 2012&#44; harbored <span class="elsevierStyleItalic">stx</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">2b</span></span>&#44; was typed as Orough&#58;H2 and belonged to MLST ST26&#46;</p><p id="par0055" class="elsevierStylePara elsevierViewall">A comparison between the properties of both Stx-EAEC O59&#58;NM&#91;H19&#93; strains is shown in <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0060" class="elsevierStylePara elsevierViewall">By pulsed-field gel electrophoresis using the restriction enzyme <span class="elsevierStyleItalic">Xba</span>I &#40;<span class="elsevierStyleItalic">Xba</span>I-PFGE&#41;&#44; the three Argentine strains showed the same macrorestriction pattern&#44; named AREEF901&#46;0001&#44; with 100&#37; similarity<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">11</span></a>&#46; A high clonal relationship &#40;&#62;85&#37;&#41; with the Stx-EAEC O59&#58;NM&#91;H19&#93; German strain was established&#46; The dendrogram of the German and Argentine strains is shown in <a class="elsevierStyleCrossRef" href="#fig0005">Figure 1</a>&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0065" class="elsevierStylePara elsevierViewall">The impact of the German outbreak was so important to become the responsible <span class="elsevierStyleItalic">E&#46; coli</span> strain as a prototype of the new Stx-EAEC pathotype&#46; The emergence of Stx-EAEC O104&#58;H4 suggests that either certain EAEC serotypes might be more susceptible to acquire STEC determinants or that there are certain Stx-EAEC ancestors which successfully adapted to survive specific selection conditions&#44; which represents a new challenge for the entire scientific community&#46; There is evidence that shows that the Stx-EAEC O104&#58;H4 could have evolved by the uptake of a <span class="elsevierStyleItalic">stx</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">2</span></span>-phage originated from the bovine reservoir by an EAEC O104&#58;H4 strain<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">1</span></a>&#46;</p><p id="par0070" class="elsevierStylePara elsevierViewall">Other Stx-EAEC strains of different serotypes were previously described in association with human disease&#46; During an HUS outbreak in France in 1996&#44; an O111&#58;H2 strain was characterized as <span class="elsevierStyleItalic">stx</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">2</span></span>- and AAF-positive&#44; and <span class="elsevierStyleItalic">eaeA</span>- and <span class="elsevierStyleItalic">ehxA</span>-negative&#44; being the first Stx-EAEC hybrid described&#46; In 1999&#44; an O86&#58;NM&#91;H2&#93; strain with <span class="elsevierStyleItalic">stx</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">2</span></span> and AAF marker genes but no <span class="elsevierStyleItalic">eae</span> was isolated from a child with HUS and bloody diarrhea in Japan&#46; Later&#44; in 2011&#44; an O111&#58;H21 strain associated with a household outbreak in Northern Ireland was detected&#46; The strain harbored the <span class="elsevierStyleItalic">stx</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">2c</span></span> gene and the type V AAF fimbriae&#44; but was <span class="elsevierStyleItalic">eae</span>-negative with a low level of resistance to ampicillin<a class="elsevierStyleCrossRef" href="#bib0110"><span class="elsevierStyleSup">6</span></a>&#46; In 2013 in a school in northern Italy&#44; an outbreak caused by a Stx-EAEC- O127&#58;H4 strain was reported&#46; Five Stx-EAEC strains were isolated from 76 fecal samples from children and school staff&#46; The strains were characterized as O127&#58;H4 and ST678 and possessed the <span class="elsevierStyleItalic">stx</span><span class="elsevierStyleInf">2a</span> gene and other EAEC virulence genes such as <span class="elsevierStyleItalic">aggR</span>&#44; <span class="elsevierStyleItalic">aap</span>&#44; <span class="elsevierStyleItalic">aat</span>&#44; <span class="elsevierStyleItalic">aaiC</span>&#44; <span class="elsevierStyleItalic">sigA</span>&#44; <span class="elsevierStyleItalic">pic</span> and <span class="elsevierStyleItalic">astA</span>&#46; The <span class="elsevierStyleItalic">stx</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">2</span></span>-phage was inserted in <span class="elsevierStyleItalic">wrbA</span> site&#44; as well as it was described for O104&#58;H4 outbreak strain<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">12</span></a>&#46;</p><p id="par0075" class="elsevierStylePara elsevierViewall">Tozzoli et al&#46; have demonstrated that&#44; at laboratory level&#44; all <span class="elsevierStyleItalic">stx</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">2</span></span>-phages used in their study were able to infect a range of bacterial hosts&#44; including both diarrheagenic &#40;DEC&#41; and extraintestinal pathogenic <span class="elsevierStyleItalic">E&#46; coli</span> &#40;ExPEC&#41;&#44; suggesting that STEC might represent multiple pathogroups whose virulence has been increased by the event of a <span class="elsevierStyleItalic">stx</span>-phage acquisition<a class="elsevierStyleCrossRef" href="#bib0160"><span class="elsevierStyleSup">16</span></a>&#46; Regarding the Stx-EAEC&#44; it was demonstrated by genomics sequencing&#44; that EAEC strain was infected by <span class="elsevierStyleItalic">stx</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">2</span></span>-phage and yield this new pathotype<a class="elsevierStyleCrossRef" href="#bib0095"><span class="elsevierStyleSup">3</span></a>&#46; On the other hand Nyholm et al&#46; also described hybrid Shigatoxigenic and Enterotoxigenic <span class="elsevierStyleItalic">Escherichia coli</span> &#40;STEC&#47;ETEC&#41; strains&#44; and 1&#37; of the strains belonging to a STEC collection harbored genes typically present in ETEC and some of them being isolated from patients with HUS<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">9</span></a>&#46;</p><p id="par0080" class="elsevierStylePara elsevierViewall">In Argentina&#44; this is the first report of an HUS case associated with a Stx-EAEC infection&#46; A distinct characteristic was the prolonged shedding during 4 months&#46; Although O59&#58;NM&#91;H19&#93; is an unusual serotype in the country&#44; these results open new questions and pose a challenge for the Surveillance System&#46;</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conflict of interest</span><p id="par0085" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflicts of interest&#46;</p></span></span>"
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          "titulo" => "Acknowledgments"
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          "titulo" => "References"
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    "fechaRecibido" => "2018-10-19"
    "fechaAceptado" => "2019-03-20"
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          "clase" => "keyword"
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            0 => "Stx-EAEC"
            1 => "O59&#58;NM&#91;H19&#93;"
            2 => "HUS"
            3 => "Surveillance system"
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          "palabras" => array:4 [
            0 => "EAEC-Stx"
            1 => "O59&#58;NM&#91;H19&#93;"
            2 => "SUH"
            3 => "Sistema de vigilancia"
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        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Shiga toxin-producing <span class="elsevierStyleItalic">Escherichia coli</span> &#40;STEC&#41; are a heterogeneous group of foodborne pathogens causing a broad spectrum of human disease&#44; from uncomplicated diarrhea to hemolytic uremic syndrome &#40;HUS&#41;&#46; In this study&#44; we report an HUS case associated with an O59&#58;NM&#91;H19&#93; strain&#44; harboring <span class="elsevierStyleItalic">stx</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">2a</span></span>&#44; <span class="elsevierStyleItalic">iha</span>&#44; <span class="elsevierStyleItalic">lpfA</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">O26</span></span>&#44; <span class="elsevierStyleItalic">lpfA</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">O113</span></span> genes associated with STEC&#44; and <span class="elsevierStyleItalic">aatA</span>&#44; <span class="elsevierStyleItalic">aap</span>&#44; <span class="elsevierStyleItalic">pic</span>&#44; <span class="elsevierStyleItalic">sigA</span>&#44; <span class="elsevierStyleItalic">agg4A</span> genes associated with enteroaggregative <span class="elsevierStyleItalic">E&#46; coli</span> &#40;EAEC&#41;&#44; named Stx-EAEC&#46; The strain showed low toxicity on Vero cells&#44; and was resistant to streptomycin and trimethoprim&#47;sulfonamides&#46; The child carried the bacteria for more than 100 days&#46; Since the large outbreak associated with Stx-EAEC O104&#58;H4&#44; many strains with similar profiles have been described&#46; In Germany&#44; an O59&#58;NM&#91;H19&#93; strain&#44; with comparable characteristics to the Argentine strain&#44; was isolated from a bloody diarrhea case&#46; In Argentina&#44; this is the first report of an HUS case associated with a Stx-EAEC infection&#44; and represents a new challenge for the surveillance system&#46;</p></span>"
      ]
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        "titulo" => "Resumen"
        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleItalic">Escherichia coli</span> productor de la toxina Shiga &#40;STEC&#41; es un grupo heterog&#233;neo de pat&#243;genos transmitidos por alimentos que causan un amplio espectro de enfermedades humanas&#44; desde diarrea no complicada hasta s&#237;ndrome ur&#233;mico hemol&#237;tico &#40;SUH&#41;&#46; Nosotros informamos de un caso de SUH por O59&#58;NM&#91;H19&#93;&#44; que portaba los genes <span class="elsevierStyleItalic">stx</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">2a</span></span>&#44; <span class="elsevierStyleItalic">iha</span>&#44; <span class="elsevierStyleItalic">lpfA</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">O26</span></span>&#44; <span class="elsevierStyleItalic">lpfA</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">O113</span></span> asociados con STEC&#44; y los genes <span class="elsevierStyleItalic">aatA</span>&#44; <span class="elsevierStyleItalic">aap</span>&#44; <span class="elsevierStyleItalic">pic</span>&#44; <span class="elsevierStyleItalic">sigA</span>&#44; <span class="elsevierStyleItalic">agg4A</span> de <span class="elsevierStyleItalic">E&#46; coli</span> enteroagregativo &#40;EAEC&#41;&#44; llamado EAEC-Stx&#46; La cepa mostr&#243; baja citotoxicidad en las c&#233;lulas Vero&#44; y fue resistente a estreptomicina y trimetoprima&#47;sulfonamidas&#46; El ni&#241;o excret&#243; la bacteria durante m&#225;s de 100 d&#237;as&#46; Desde el brote asociado con EAEC-Stx O104&#58;H4&#44; se describieron muchas cepas con perfiles similares&#46; En Alemania se aisl&#243; una cepa O59&#58;NM&#91;H19&#93; de una diarrea sanguinolenta&#44; con caracter&#237;sticas comparables a la cepa argentina&#46; Este es el primer informe de un caso de SUH asociado a una infecci&#243;n por EAEC-Stx&#44; y representa un nuevo desaf&#237;o para el sistema de vigilancia&#46;</p></span>"
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          "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Clonal relation between Stx-EAEC O59&#58;NM&#91;H19&#93; strains isolated in Germany and Argentina by <span class="elsevierStyleItalic">Xba</span>I-PFGE&#46;</p>"
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          "leyenda" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleSup">a&#44;b</span> Both strains&#44; isolated from bloody diarrhea &#40;BD&#41; and hemolytic uremic syndrome &#40;HUS&#41; cases&#44; showed resistance to streptomycin and trimethoprim&#47;sulfamethoxazole and low cytotoxicity on Vero cells&#46;</p>"
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                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Genes&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Pathotype&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Germany BD<span class="elsevierStyleSup">a</span>&#47;2010&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Argentina HUS<span class="elsevierStyleSup">b</span>&#47;2015&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">stx<span class="elsevierStyleInf">2a</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">Shiga toxin variant 2a&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">EAEC&#47;EHEC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">iha</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">IrgA adhesion homolog&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">STEC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">lpf</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">O26</span></span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">subunit of long polar fimbriae of EHEC O26&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">STEC&#47;EHEC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">lpf</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">O113</span></span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">subunit of long polar fimbriae of EHEC O113&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">STEC&#47;EHEC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">ehxA</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">enterohemolysin&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">STEC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">&#8722;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">&#8722;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">eae</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">intimin&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">STEC&#47;EPEC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#8722;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#8722;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">terA</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">tellurium resistance protein&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">STEC&#47;EHEC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#8722;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#8722;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">irp2</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">iron uptake system&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">STEC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Unknown&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">aggR</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">transcriptional activator&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">EAEC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">aatA</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">dispersin transporter protein&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">EAEC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">aap</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">dispersin&#44; antiaggregation protein&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">EAEC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">st1a&#47;b</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Shigella</span> enterotoxin subunit A and B&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">EAEC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Unknown&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">pic</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">serine protease precursor&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">EAEC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">pet</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">plasmid-encoded toxin&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">EAEC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Unknown&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">sigA</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">IgA protease-like homolog&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">EAEC&#47;<span class="elsevierStyleItalic">Shigella</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">iucA&#47;C</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">siderophore aerobactin&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">EAEC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Unknown&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">agg4A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">AAF&#47;IV fimbrial subunit&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">EAEC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Unknown&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">astA</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">EAST-1 heat-stable toxin&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">EAEC&#47;ETEC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#8722;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#8722;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
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        "descripcion" => array:1 [
          "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Properties of Stx-EAEC O59&#58;NM&#91;H19&#93; strains isolated in Germany and Argentina</p>"
        ]
      ]
    ]
    "bibliografia" => array:2 [
      "titulo" => "References"
      "seccion" => array:1 [
        0 => array:2 [
          "identificador" => "bibs0015"
          "bibliografiaReferencia" => array:16 [
            0 => array:3 [
              "identificador" => "bib0085"
              "etiqueta" => "1"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Outbreak of Shiga toxin-producing <span class="elsevierStyleItalic">Escherichia coli</span> &#40;STEC&#41; O104&#58;H4 infection in Germany causes a paradigm shift with regard to human pathogenicity of STEC strains"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:2 [
                            0 => "L&#46; Beutin"
                            1 => "A&#46; Martin"
                          ]
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                      ]
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                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.4315/0362-028X.JFP-11-452"
                      "Revista" => array:6 [
                        "tituloSerie" => "J Food Prot"
                        "fecha" => "2012"
                        "volumen" => "75"
                        "paginaInicial" => "408"
                        "paginaFinal" => "418"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/22289607"
                            "web" => "Medline"
                          ]
                        ]
                      ]
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              "identificador" => "bib0090"
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Article information

ISSN: 03257541
Original language: English

DOI:10.1016/j.ram.2019.03.006

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2023 August	21	9	30
2023 July	16	4	20
2023 June	35	3	38
2023 May	45	8	53
2023 April	42	4	46
2023 March	26	0	26
2023 February	29	8	37
2023 January	20	2	22
2022 December	21	16	37
2022 November	24	9	33
2022 October	28	9	37
2022 September	19	10	29
2022 August	21	9	30
2022 July	30	9	39
2022 June	32	7	39
2022 May	47	14	61
2022 April	43	7	50
2022 March	112	12	124
2022 February	86	6	92
2022 January	67	10	77
2021 December	55	14	69
2021 November	70	11	81
2021 October	45	12	57
2021 September	42	14	56
2021 August	40	9	49
2021 July	27	14	41
2021 June	20	12	32
2021 May	16	12	28
2021 April	45	9	54
2021 March	26	11	37
2021 February	15	16	31
2021 January	18	15	33
2020 December	30	10	40
2020 November	22	7	29
2020 October	18	9	27
2020 September	17	12	29
2020 August	22	13	35
2020 July	20	10	30
2020 June	28	20	48
2020 May	25	17	42
2020 April	22	14	36
2020 March	24	16	40
2020 February	13	14	27
2020 January	4	9	13
2019 December	13	9	22
2019 November	9	8	17
2019 October	7	16	23
2019 September	7	10	17
2019 August	3	4	7
2019 July	10	19	29
2019 June	1	4	5

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