Hepatitis E Virus Genotype 1 Cases Imported to Portugal from India, 2016
João R. Mesquita
, Madalena Almeida-Santos†, Maria Fernandes†, Fernando Maltez‡, Sara Lino†, Liliana Alves†, Joana Abreu-Silva§, Ricardo M.S. Oliveira§, Martin D. Curran||, Maria S.J. Nascimento§
,
Corresponding author
* Instituto Politécnico de Viseu, Viseu, Portugal. Epidemiology ReserchUnit (EPIUnit), Institute of Public Health, University of Porto, 4050-313 Porto, Portugal
† Laboratório de Patologia Clínica Centro Hospitalar Lisboa Central (CHLC) - Hospital Curry Cabral, 1069-166 Lisboa, Portugal
‡ Serviço de Doenças Infeciosas CHLC - Hospital Curry Cabral, 1069-166 Lisboa, Portugal
§ Laboratório de Microbiologia, Departamento de Ciências Biológicas, Faculdade de Farmácia, Universidade do Porto, 4050-313 Porto, Portugal
|| Clinical Microbiology and Public Health Laboratory, Public Health England, Addenbrooke’s Hospital, Cambridge, UK
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"apellidos" => "Mesquita" "email" => array:1 [ 0 => "jmesquita@esav.ipv.pt" ] "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">*</span>" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">*</span>" "identificador" => "cor0005" ] ] ] 1 => array:3 [ "nombre" => "Madalena" "apellidos" => "Almeida-Santos" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">†</span>" "identificador" => "aff0010" ] ] ] 2 => array:3 [ "nombre" => "Maria" "apellidos" => "Fernandes" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">†</span>" "identificador" => "aff0010" ] ] ] 3 => array:3 [ "nombre" => "Fernando" "apellidos" => "Maltez" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">‡</span>" "identificador" => "aff0015" ] ] ] 4 => array:3 [ "nombre" => "Sara" "apellidos" => "Lino" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">†</span>" "identificador" => "aff0010" ] ] ] 5 => array:3 [ "nombre" => "Liliana" "apellidos" => "Alves" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">†</span>" "identificador" => "aff0010" ] ] ] 6 => array:3 [ "nombre" => "Joana" "apellidos" => "Abreu-Silva" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">§</span>" "identificador" => "aff0020" ] ] ] 7 => array:3 [ "nombre" => "Ricardo M.S." "apellidos" => "Oliveira" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">§</span>" "identificador" => "aff0020" ] ] ] 8 => array:3 [ "nombre" => "Martin D." "apellidos" => "Curran" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">||</span>" "identificador" => "aff0025" ] ] ] 9 => array:3 [ "nombre" => "Maria S.J." "apellidos" => "Nascimento" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">§</span>" "identificador" => "aff0020" ] ] ] ] "afiliaciones" => array:5 [ 0 => array:3 [ "entidad" => "Instituto Politécnico de Viseu, Viseu, Portugal. Epidemiology ReserchUnit (EPIUnit), Institute of Public Health, University of Porto, 4050-313 Porto, Portugal" "etiqueta" => "*" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Laboratório de Patologia Clínica Centro Hospitalar Lisboa Central (CHLC) - Hospital Curry Cabral, 1069-166 Lisboa, Portugal" "etiqueta" => "†" "identificador" => "aff0010" ] 2 => array:3 [ "entidad" => "Serviço de Doenças Infeciosas CHLC - Hospital Curry Cabral, 1069-166 Lisboa, Portugal" "etiqueta" => "‡" "identificador" => "aff0015" ] 3 => array:3 [ "entidad" => "Laboratório de Microbiologia, Departamento de Ciências Biológicas, Faculdade de Farmácia, Universidade do Porto, 4050-313 Porto, Portugal" "etiqueta" => "§" "identificador" => "aff0020" ] 4 => array:3 [ "entidad" => "Clinical Microbiology and Public Health Laboratory, Public Health England, Addenbrooke’s Hospital, Cambridge, UK" "etiqueta" => "||" "identificador" => "aff0025" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "*" "correspondencia" => "Corresponding author." ] ] ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "f0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 463 "Ancho" => 543 "Tamanyo" => 39458 ] ] "descripcion" => array:1 [ "en" => "<p id="sp0005" class="elsevierStyleSimplePara elsevierViewall">Phylogenetic tree based on partial RNA-dependent RNA-polimerase region of open reading frame 1 (330 bp) using neighbor-joining method based on the Jukes-Cantor model and 1000 bootstrap ressamplings. Scale bar indicates substitutions per nucleotide position. Sequences are defined in tree as Strain|Host|Origin|Subgenotype (accession number). Sequences characterized in this study are in bold.</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><span id="s0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="st0015">Introduction</span><p id="p0005" class="elsevierStylePara elsevierViewall">In industrialized countries hepatitis E virus (HEV) infection has usually been associated with travellers to endemic areas but it is now known that locally acquired HEV infection is common in industrialized regions. However, autochthonous HEV infections in these areas contrasts from those in developing countries presenting distinct clinical and epidemiologic profiles.<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> Hepatitis E in industrialized countries is mainly associated with genotype 3 and normally cause sporadic self-limiting disease in immunocompetent individuals, but may progress to chronic hepatitis in the immunocompromised patients or be associated with a range of extra-hepatic manifestations.<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a>,<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a> Genotypes 1 and 2 that circulate in developing countries are normally associated with more severe disease<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a> and occur in the epidemic form with mortality rates in epidemics ranging from 0.2% to 4.0%.<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a> For unknown reasons, mortality is higher in infants under 2 years of age and in pregnant women during the third trimester (reaching 10% to 25%), causing fulminant hepatic failure and obstetric complications such as eclampsia or haemorrhage.<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a></p><p id="p0010" class="elsevierStylePara elsevierViewall">In Portugal HEV genotype 3 is the only genotype detected so far, and closely related isolates have been detected in both animals and humans.<a class="elsevierStyleCrossRefs" href="#bib0025"><span class="elsevierStyleSup">5</span></a><span class="elsevierStyleSup">–</span><a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a> Up until this report no case of HEV genotype 1 infection has ever been documented in Portugal. Here we report the first cases of HEV genotype 1 in Portugal, associated to severe acute hepatitis that required hospitalization in two migrants from India that had recently entered the country. This report highlights the possibility of introduction of exotic HEV genotypes into the Portuguese territory with different pathogenic profiles and with the potential to cause severe disease in more susceptible groups, namely in children and pregnant women.</p></span><span id="s0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="st0020">Case Report</span><span id="s0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="st0025">Case 1</span><p id="p0015" class="elsevierStylePara elsevierViewall">On 14th January 2016, a 31-year-old Indian man was admitted to the Emergency Unit (EU) of Centro Hospitalar Lisboa Central (CHLC), Lisboa, Portugal, with abdominal pain in the epigastric and right hipochondrium regions associated with coluria, nausea and jaundice. Upon admission he reported he had resided in the North of India until coming to Portugal 6 weeks previously. He had no history of risky sexual behaviour or drug addiction. Abdominal ultrasonography and radiography, as well as electrocardiography were performed and none showed abnormalities. Liver function tests (<a class="elsevierStyleCrossRef" href="#t0005">Table 1</a>) showed a marked elevation of hepatic enzymes (AST and ALT ≥ 400 IU/L) with ALT typically higher than AST, supporting the presumptive diagnosis of viral hepatitis. The patient was transferred to the Infectious Diseases Unit (IDU) on the following day (15th January) where he stayed for 6 days until discharge (20th January). During the stay at the IDU a blood sample was collected (18th January) and submitted to the current diagnostic algorithm of acute viral hepatitis, that focus on HAV, HBV, HCV, EBV and CMV. All the viral serologic markers of acute infection (IgM anti-HAV, AgHBs, IgM anti-HBc, anti-HCV/RNA HCV, IgM anti-VCA, IgM anti-CMV) were negative. He also tested negative for HIV, <span class="elsevierStyleItalic">Fasciola hepática</span> and syphilis. IgM anti-HEV was not performed but HEV RNA was detected in this serum sample by real-time RT-PCR using the generic primers/probe targeting the open reading frame (ORF) 2 region that covers all HEV genotypes.<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> Patient management comprised supportive measures that included hypolipidemic diet. Clinical evolution was favourable making a progressive improvement of cutaneous/sclerotic jaundice and subsequent discharge a week after admission.</p><elsevierMultimedia ident="t0005"></elsevierMultimedia></span><span id="s0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="st0030">Case 2</span><p id="p0020" class="elsevierStylePara elsevierViewall">On 17th February 2016, a 50-year-old Indian man was admitted to the EU of CHLC, Lisboa, Portugal, with abdominal pain in the epigastric region, anorexia and asthenia. Upon admission he reported his previous residence as Jalandhar, North of India, until coming to Portugal one month previously. He had no history of drug addiction and was a moderate consumer of alcohol, having been abstinent for the past five days. Abdominal ultrasonography and radiography, as well as electrocardiography were performed and none showed abnormalities. On that day blood was taken for analysis and liver function tests (<a class="elsevierStyleCrossRef" href="#t0005">Table 1</a>) and showed elevated levels of transaminases (≥ 400 IU/ L) with the typically higher profile of ALT compatible with the diagnosis of viral hepatitis. The patient was transferred to the IDU on the 19th February where he stayed for seven days until discharge (26th February). The blood sample collected on 19th February was also submitted to the diagnostic algorithm of acute viral hepatitis but all the viral serologic markers of acute infection were negative. IgM anti-HEV was not performed but serum was found positive for HEV RNA by real-time RT-PCR.<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> The patient tested negative for HIV but was positive for Fasciola hepatica (antibody titer 320). Since the patient was non-eosinophilic and showed normal abdominal ecographic patterns a diagnosis of fasiolosis was ruled out. Patient management comprised supportive measures that included hypolipidemic diet. Clinical evolution was favourable and he was discharged a week after admission.</p></span><span id="s0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="st0035">Genotypic characterization of HEV detected in patients</span><p id="p0025" class="elsevierStylePara elsevierViewall">To characterize the HEV sequences retrieved from the two patients a nested broad-spectrum RT-PCR with amplification within the ORF 1 was used.<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a> The final 330 bp amplified products were sequenced and compared with HEV reference strains, using a neighbor-joining method based on the Jukes-Cantor model for selected HEV isolates representing genotypes 1–4 and including sequences with highest nucleotide identity, according to nucleotide BLAST (Basic Local Alignment Search Tool). The phylogenetic analysis indicated that the two HEV sequences retrieved from these patients were nearly identical, sharing 99.7% nucleotide sequence identity between them, and clustering with HEV genotype 1 sequences isolated in 2013 and 2014 in Jabalpur District, India, and from an HEV outbreak in Nepal, 2014 (<a class="elsevierStyleCrossRef" href="#f0005">Figure 1</a>) with which they shared 99.0% nucleotide identity. The obtained sequences were deposited in GenBank (PoHuG12016; GenBank accession no. KX815297 and Po2HUG12016; GenBank accession no. KX815298).</p><elsevierMultimedia ident="f0005"></elsevierMultimedia></span></span><span id="s0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="st0040">Discussion</span><p id="p0030" class="elsevierStylePara elsevierViewall">The present report describes two cases of severe acute hepatitis that required hospitalization for 6 and 9 days in two individuals of Indian nationality that had recently migrated to Portugal. HEV genotype 1 was identified as the cause of the acute hepatitis in both patients that most likely acquired the HEV infection in the North of India where they lived, before coming to Portugal. There was no com- mon link between them and they now live in Lisbon in separate accommodations. The sequences of HEV identified in these patients showed a high degree of identity clustering with strains retrieved from India and Nepal, in 2013 and 2014. Hepatitis E occurring in travellers returning from HEV endemic areas is not a novel epidemiological occurrence, however the vast majority of cases remain to be genetically studied. Genetic characterization of imported HEV genotype 1 isolates have been scarcely documented with reports from travellers returning to UK,<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">11</span></a> Spain<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a> and Germany.<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a>,<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">14</span></a> HEV genotypes circulating in developing countries such as India are considered a serious public health problem<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">15</span></a> and are known to cause an estimated 20.1 million infections with 3.4 million acute cases and 3 000 stillbirths annually worldwide with an estimated 70 000 deaths.<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">16</span></a></p><p id="p0035" class="elsevierStylePara elsevierViewall">Over the past few decades there has been growing concerns about population migration flows from low- to high-income countries and its impact on infectious disease emergence. If HEV genotypes of increased pathogenicity like genotype 1 are being introduced in otherwise naïve populations of industrialized countries such as European countries, the consequences of such imported events are difficult to predict. Our findings demonstrate the need to implement and improve strategic HEV surveillance in high-income countries with substantial migration flows.</p></span><span id="s0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="st0045">Abbreviations</span><p id="p0040" class="elsevierStylePara elsevierViewall"><ul class="elsevierStyleList" id="l0005"><li class="elsevierStyleListItem" id="u0005"><span class="elsevierStyleLabel">•</span><p id="p0045" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleBold">CHLC:</span> Centro Hospitalar Lisboa Central.</p></li><li class="elsevierStyleListItem" id="u0010"><span class="elsevierStyleLabel">•</span><p id="p0050" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleBold">EU:</span> Emergency Unit.</p></li><li class="elsevierStyleListItem" id="u0015"><span class="elsevierStyleLabel">•</span><p id="p0055" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleBold">HEV:</span> hepatitis E virus.</p></li><li class="elsevierStyleListItem" id="u0020"><span class="elsevierStyleLabel">•</span><p id="p0060" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleBold">IDU:</span> Infectious Diseases Unit.</p></li><li class="elsevierStyleListItem" id="u0025"><span class="elsevierStyleLabel">•</span><p id="p0065" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleBold">ORF:</span> open reading frame.</p></li></ul></p></span><span id="s0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="st0050">Conflicts of Interest</span><p id="p0070" class="elsevierStylePara elsevierViewall">None.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:8 [ 0 => array:3 [ "identificador" => "xres1190056" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abs0010" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec1109534" "titulo" => "Keywords" ] 2 => array:2 [ "identificador" => "s0005" "titulo" => "Introduction" ] 3 => array:3 [ "identificador" => "s0010" "titulo" => "Case Report" "secciones" => array:3 [ 0 => array:2 [ "identificador" => "s0015" "titulo" => "Case 1" ] 1 => array:2 [ "identificador" => "s0020" "titulo" => "Case 2" ] 2 => array:2 [ "identificador" => "s0025" "titulo" => "Genotypic characterization of HEV detected in patients" ] ] ] 4 => array:2 [ "identificador" => "s0030" "titulo" => "Discussion" ] 5 => array:2 [ "identificador" => "s0035" "titulo" => "Abbreviations" ] 6 => array:2 [ "identificador" => "s0040" "titulo" => "Conflicts of Interest" ] 7 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2017-03-10" "fechaAceptado" => "2017-04-10" "PalabrasClave" => array:1 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec1109534" "palabras" => array:3 [ 0 => "Acute hepatitis E" 1 => "Travel" 2 => "India" ] ] ] ] "tieneResumen" => true "resumen" => array:1 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "<span id="abs0010" class="elsevierStyleSection elsevierViewall"><p id="sp0015" class="elsevierStyleSimplePara elsevierViewall">Hepatitis E in industrialized countries is mainly associated with genotype 3 hepatitis E virus (HEV) and normally causes a sporadic self-limiting disease in immunocompetent individuals. Unlike genotype 3, genotypes 1 and 2 circulate in developing countries, produce severe disease and occur in the epidemic form. Hepatitis E occurring in travellers returning from endemic areas in developing countries is not a novel epidemiological occurrence, however the vast majority of cases remain to be genetically studied. The present study describes two cases of severe acute hepatitis E that required hospitalization for 6 and 9 days in two individuals of Indian nationality that had recently migrated to Portugal to work. The retrieved HEV sequences both belonged to genotype 1 and had a high degree of nucleotide sequence identity, clustering with strains isolated in India and Nepal, in 2013 and 2014. Confirmed HEV genotypes of increased pathogenicity like genotype 1 are being introduced into otherwise naïve populations of industrialized countries such as European countries with consequences difficult to predict. As far as we know the present study is the first in Portugal to describe and genetically characterize imported cases of hepatitis E infection caused by HEV genotype 1.</p></span>" ] ] "multimedia" => array:2 [ 0 => array:7 [ "identificador" => "f0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 463 "Ancho" => 543 "Tamanyo" => 39458 ] ] "descripcion" => array:1 [ "en" => "<p id="sp0005" class="elsevierStyleSimplePara elsevierViewall">Phylogenetic tree based on partial RNA-dependent RNA-polimerase region of open reading frame 1 (330 bp) using neighbor-joining method based on the Jukes-Cantor model and 1000 bootstrap ressamplings. Scale bar indicates substitutions per nucleotide position. Sequences are defined in tree as Strain|Host|Origin|Subgenotype (accession number). Sequences characterized in this study are in bold.</p>" ] ] 1 => array:7 [ "identificador" => "t0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "tabla" => array:2 [ "leyenda" => "<p id="np0005" class="elsevierStyleSimplePara elsevierViewall">EU: Emergency Unit, IDU: Infectious Diseases Unit, AST: aspartate aminotransferase. ALT: alanine aminotransferase. G-GT: gamma-glutamyl transpeptidase. TB: total bilirubin. LDH: lactate dehydrogenase. The dashes indicate that the test was not done.</p>" "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Laboratory data (units) \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " colspan="3" align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Case 1</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " colspan="3" align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Case 2</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Normal range limits, adults adults \t\t\t\t\t\t\n \t\t\t\t\t\t</th></tr><tr title="table-row"><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black"> \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Day 1 (EU Jan 14 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Day 2 (IDU) Jan 15 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Day 4 (IDU) Jan 17 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Day 1 (EU) Feb 17 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Day 3 (IDU) Feb 19 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Day 10 (Discharge) Feb 26 \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black"> \t\t\t\t\t\t\n \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Haemoglobin (g/dL) \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">15.4 \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="left" 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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">15.2 \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="left" 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="left" 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="left" 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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">13.5 - 17.5 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Leukocytes (x 19<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a>/L) \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">7.4 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><span class="elsevierStyleInf">-</span> \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">6.2 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><span class="elsevierStyleInf">-</span> \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><span class="elsevierStyleInf">-</span> \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><span class="elsevierStyleInf">-</span> \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">4.5 - 11.0 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Platelets (x 19<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a>/L) \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">221 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><span class="elsevierStyleInf">-</span> \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">186 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><span class="elsevierStyleInf">-</span> \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><span class="elsevierStyleInf">-</span> \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><span class="elsevierStyleInf">-</span> \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">150 - 450 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">AST (IU/L) \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">2,560 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1974 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">505 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">909 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1,093 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">244 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">5.0 - 34.0 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">ALT (IU/L) \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">3,795 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">3274 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1,760 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1,100 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1,188 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">452 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0.0 - 55.0 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">G-GT (IU/L) \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">361 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">298 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">276 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">266 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">216 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">163 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">12.0 - 64.0 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">TB (mg/dL) \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">6.93 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">7.22 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">5.6 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">5.96 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">844 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">4.26 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0.20 - 1.2 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">LDH (IU/L) \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1,299 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">692 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">266 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">409 \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">501 \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="left" 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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">125 - 220 \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab2030552.png" ] ] ] ] "descripcion" => array:1 [ "en" => "<p id="sp0010" class="elsevierStyleSimplePara elsevierViewall">Laboratory findings of the two Indian patients (case 1 and 2) with acute hepatitis E.</p>" ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bs0010" "bibliografiaReferencia" => array:16 [ 0 => array:3 [ "identificador" => "bib0005" "etiqueta" => "1." "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Hepatitis E Virus: Time to Change the Textbooks" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:4 [ 0 => "Dalton H.R." 1 => "Webb G.W." 2 => "Norton B.C." 3 => "Woolson K.L." ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.1159/000444468" "Revista" => array:6 [ "tituloSerie" => "Digestive Diseases" "fecha" => "2016" "volumen" => "34" "paginaInicial" => "308" "paginaFinal" => "316" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/27170383" "web" => "Medline" ] ] ] ] ] ] ] ] 1 => array:3 [ "identificador" => "bib0010" "etiqueta" => "2." 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| Year/Month | Html | Total | |
|---|---|---|---|
| 2024 November | 1 | 0 | 1 |
| 2024 October | 10 | 2 | 12 |
| 2024 September | 8 | 1 | 9 |
| 2024 August | 9 | 2 | 11 |
| 2024 July | 7 | 3 | 10 |
| 2024 June | 6 | 2 | 8 |
| 2024 May | 12 | 1 | 13 |
| 2024 April | 11 | 3 | 14 |
| 2024 March | 6 | 4 | 10 |
| 2024 February | 5 | 3 | 8 |
| 2024 January | 8 | 5 | 13 |
| 2023 December | 2 | 4 | 6 |
| 2023 November | 4 | 6 | 10 |
| 2023 October | 7 | 4 | 11 |
| 2023 September | 7 | 0 | 7 |
| 2023 August | 11 | 2 | 13 |
| 2023 July | 6 | 6 | 12 |
| 2023 June | 15 | 2 | 17 |
| 2023 May | 22 | 2 | 24 |
| 2023 April | 25 | 2 | 27 |
| 2023 March | 11 | 4 | 15 |
| 2023 February | 5 | 5 | 10 |
| 2023 January | 8 | 4 | 12 |
| 2022 December | 10 | 5 | 15 |
| 2022 November | 9 | 2 | 11 |
| 2022 October | 10 | 5 | 15 |
| 2022 September | 7 | 9 | 16 |
| 2022 August | 11 | 5 | 16 |
| 2022 July | 11 | 8 | 19 |
| 2022 June | 5 | 6 | 11 |
| 2022 May | 4 | 4 | 8 |
| 2022 April | 9 | 11 | 20 |
| 2022 March | 8 | 11 | 19 |
| 2022 February | 4 | 3 | 7 |
| 2022 January | 12 | 5 | 17 |
| 2021 December | 28 | 15 | 43 |
| 2021 November | 19 | 8 | 27 |
| 2021 October | 14 | 12 | 26 |
| 2021 September | 8 | 8 | 16 |
| 2021 August | 7 | 5 | 12 |
| 2021 July | 6 | 10 | 16 |
| 2021 June | 8 | 6 | 14 |
| 2021 May | 8 | 11 | 19 |
| 2021 April | 28 | 5 | 33 |
| 2021 March | 26 | 7 | 33 |
| 2021 February | 14 | 7 | 21 |
| 2021 January | 26 | 7 | 33 |
| 2020 December | 19 | 4 | 23 |
| 2020 November | 10 | 2 | 12 |
| 2020 October | 6 | 2 | 8 |
| 2020 September | 11 | 11 | 22 |
| 2020 August | 6 | 6 | 12 |
| 2020 July | 6 | 9 | 15 |
| 2020 June | 4 | 5 | 9 |
| 2020 May | 5 | 9 | 14 |
| 2020 April | 2 | 1 | 3 |
| 2020 March | 2 | 1 | 3 |
| 2020 February | 7 | 7 | 14 |
| 2020 January | 3 | 2 | 5 |
| 2019 December | 7 | 3 | 10 |
| 2019 November | 2 | 3 | 5 |
| 2019 October | 1 | 8 | 9 |
| 2019 September | 7 | 1 | 8 |
| 2019 August | 3 | 1 | 4 |
| 2019 July | 4 | 1 | 5 |
| 2019 June | 1 | 4 | 5 |
| 2019 May | 12 | 8 | 20 |
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