Scientific Letter
Acute neurological disease due to enterovirus: A review of clinical cases in a tertiary hospital in Andalusia after an outbreak in Catalonia
Patología neurológica aguda por enterovirus: revisión de casos clínicos en un hospital andaluz de tercer nivel tras brote epidémico de Cataluña
Ana Isabel Valdivielso Martíneza,
, Begoña Carazo Gallegob, Zaira Cubiles Ariloa, David Moreno-Pérezb,c, Antonio Urda Cardonaa
Corresponding author
a Unidad de Gestión Clínica de Pediatría, Hospital Materno-Infantil, Hospital Regional Universitario de Málaga, Málaga, Spain
b Infectología Pediátrica e Inmunodeficiencias, Unidad de Gestión Clínica de Pediatría, Hospital Materno-Infantil, Hospital Regional Universitario de Málaga, Málaga, Spain
c Grupo de Investigación IBIMA, Departamento de Pediatría y Farmacología, Facultad de Medicina, Universidad de Málaga, Red de Investigación Translacional en Infectología Pediátrica (RITIP), Málaga, Spain
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"nombre" => "Ana Isabel" "apellidos" => "Valdivielso Martínez" "email" => array:1 [ 0 => "avaldivielsom@gmail.com" ] "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">*</span>" "identificador" => "cor0005" ] ] ] 1 => array:3 [ "nombre" => "Begoña" "apellidos" => "Carazo Gallego" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] ] ] 2 => array:3 [ "nombre" => "Zaira" "apellidos" => "Cubiles Arilo" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] ] ] 3 => array:3 [ "nombre" => "David" "apellidos" => "Moreno-Pérez" "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] 1 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">c</span>" "identificador" => "aff0015" ] ] ] 4 => array:3 [ "nombre" => "Antonio" "apellidos" => "Urda Cardona" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] ] ] ] "afiliaciones" => array:3 [ 0 => array:3 [ "entidad" => "Unidad de Gestión Clínica de Pediatría, Hospital Materno-Infantil, Hospital Regional Universitario de Málaga, Málaga, Spain" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Infectología Pediátrica e Inmunodeficiencias, Unidad de Gestión Clínica de Pediatría, Hospital Materno-Infantil, Hospital Regional Universitario de Málaga, Málaga, Spain" "etiqueta" => "b" "identificador" => "aff0010" ] 2 => array:3 [ "entidad" => "Grupo de Investigación IBIMA, Departamento de Pediatría y Farmacología, Facultad de Medicina, Universidad de Málaga, Red de Investigación Translacional en Infectología Pediátrica (RITIP), Málaga, Spain" "etiqueta" => "c" "identificador" => "aff0015" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Patología neurológica aguda por enterovirus: revisión de casos clínicos en un hospital andaluz de tercer nivel tras brote epidémico de Cataluña" ] ] "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" => 1046 "Ancho" => 950 "Tamanyo" => 78969 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Case 2 patient: T2-weighted hyperintensity at mesencephalon.</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0005" class="elsevierStylePara elsevierViewall">Enterovirus (EV) infections are common in childhood. They usually cause benign diseases such as herpangina or hand, foot and mouth disease, and are the most frequent cause of lymphocytic meningitis. Occasionally there is an outbreak that includes cases with neurologic involvement that manifests with acute flaccid paralysis and/or rhombencephalic involvement, as occurred in a 2016 outbreak in Catalonia.</p><p id="par0010" class="elsevierStylePara elsevierViewall">Our aim was to describe the cases of the 4 patients admitted to our hospital with neurologic disease secondary to infection by EV between June and December 2016.</p><p id="par0015" class="elsevierStylePara elsevierViewall"><a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a> shows the main characteristics of the patients. At admission, all of them presented with fever of several days’ duration and a constellation of neurologic symptoms that ranged from depression and somnolence to instability, ataxia and involuntary tremors. All patients underwent a lumbar puncture, and microscopic examination of the specimens revealed lymphomononuclear pleocytosis in 3 cases (1, 2 and 3). Testing of cerebrospinal fluid (CSF), respiratory secretion and stool samples by polymerase chain reaction (PCR) detected EV in at least 1 of the samples in all 4 patients. The virus was detected in the CSF in only 1 case, and in the stool sample in all cases. In 3 of the 4 cases, cranial MRI revealed hyperintense lesions at the level of the rhombencephalon (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>). When it came to treatment, 2 patients received corticosteroids, 2 intravenous immunoglobulin therapy, and only 1 symptomatic treatment. All patients had favourable outcomes, as they were either asymptomatic or their symptoms had greatly improved compared to admission at the time of discharge.</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0020" class="elsevierStylePara elsevierViewall">In Europe, unlike China, infection by EV serotype 71 had been rare until recently and was associated with fever or hand, food and mouth disease. The virus is transmitted by the faecal–oral route or the oral–oral route. Certain EV serotypes, such as A71, are particularly neurotropic, and it has been hypothesised that neuroinvasion occurs through retrograde axonal transport.<a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">1</span></a> Starting in March 2016, there were 100 cases in Catalonia that met the case definition criterion of “presentation with rhombencephalic involvement or myelitis with detection of EV.”<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">2</span></a> However, isolation of EV is not always associated with neurologic disease, and in fact, one study described that out of a total of 2788 respiratory samples from children with respiratory infections, 148 (5%) corresponded to EV infections, of which only 8 were by the EV-A71 serotype. Among these 8, there was only 1 case with neurologic involvement, which manifested as lymphocytic meningitis; this patient had a favourable outcome.<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">3</span></a></p><p id="par0025" class="elsevierStylePara elsevierViewall">In children, the presence of fever and neurologic involvement at the level of the rhombencephalon (myoclonic jerks, tremors and/or ataxia) and/or the medulla oblongata (cranial nerve involvement, abnormalities in swallowing or speech, apnoeic episodes and neurogenic pulmonary oedema)<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">4</span></a> should be assessed by examination of the CSF, which usually reveals lymphocytic pleocytosis, and by performance of a MRI exam in the acute stage of disease, whose typical findings are the presence of hyperintense lesions on T2-weighted images, especially at the level of the pons, cervical spinal cord, mesencephalon, dentate nucleus and hypothalamus.<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">5</span></a></p><p id="par0030" class="elsevierStylePara elsevierViewall">The most sensitive and quick technique to establish the aetiological diagnosis, which is also currently the gold standard, is PCR. Despite the severity of the presentation, detection of EV in the CSF is rare. In fact, in our series only 1 of the 4 patients had a positive result, case 2, a female patient who had more severe neurologic manifestations. Therefore, suspicion of this disease should be approached by the collection of respiratory and stool samples, and detection of enterovirus alone does not suffice to rule out other diseases that may cause acute neurologic symptoms.</p><p id="par0035" class="elsevierStylePara elsevierViewall">Unfortunately, we were unable to perform a serotype analysis of the enteroviruses found in our sample, and therefore, while the clinical and epidemiological data were mainly suggestive of EV-A71, we are unable to state that this was the involved type with certainty.</p><p id="par0040" class="elsevierStylePara elsevierViewall">There is no specific treatment that is effective against infection by EV. Following the guidelines recommended by Spanish scientific societies, patients with severe symptoms received polyvalent immunoglobulins intravenously, as it has been proposed that they have an immunomodulator effect on the release of cytokines involved in the development of severe neurologic symptoms associated with infection by EV, although the evidence on the use of immunoglobulin is scarce and not from randomised controlled trials. Megadose corticosteroid therapy (30<span class="elsevierStyleHsp" style=""></span>mg/kg/day, 3–5 days) has been used in patients with severe neurologic involvement, although its use is not supported by evidence from randomised controlled trials<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">6</span></a> and has been extrapolated from previous use in cases of acute myelitis.</p><p id="par0045" class="elsevierStylePara elsevierViewall">Enterovirus A71 spread from the site of its earlier identification in Germany to France and Catalonia,<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">2</span></a> causing an outbreak that has not recurred in our province, which suggests that there are environmental and microbiological factors that play a role in the infection rate and virulence that have yet to be identified.</p></span>" "pdfFichero" => "main.pdf" "tienePdf" => true "NotaPie" => array:1 [ 0 => array:2 [ "etiqueta" => "☆" "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Please cite this article as: Valdivielso Martínez AI, Carazo Gallego B, Cubiles Arilo Z, Moreno-Pérez D, Urda Cardona A. Patología neurológica aguda por enterovirus: revisión de casos clínicos en un hospital andaluz de tercer nivel tras brote epidémico de Cataluña. An Pediatr (Barc). 2018;89:249–251.</p>" ] ] "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" => 1046 "Ancho" => 950 "Tamanyo" => 78969 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Case 2 patient: T2-weighted hyperintensity at mesencephalon.</p>" ] ] 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" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">CSF, cerebrospinal fluid; EV, enterovirus; GM, grey matter; IVIg, nonspecific intravenous immunoglobulin therapy; PCR, polymerase chain reaction.</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="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Case \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Month \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Age \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Symptoms \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Samples from which EV was isolated with PCR \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Magnetic resonance imaging \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Treatment \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Outcome (1 month) \t\t\t\t\t\t\n \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">June \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">10 months \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">6-Day fever<br>Somnolence<br>Ataxia<br>Tremors \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Stools<br>Respiratory \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Normal \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Symptomatic \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Gradual improvement<br>Full resolution of symptoms \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">June \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">9 years \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">4-Day fever<br>Somnolence<br>Ataxia<br>Nystagmus<br>Weakness<br>Vomiting \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Stool<br>Respiratory<br>CSF \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">T2-weighted hyperintensity in mesencephalon extending to the pons, with GM involvement \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">IVIg 1<span class="elsevierStyleHsp" style=""></span>g/kg/day, 2 days<br>Methylprednisolone 30<span class="elsevierStyleHsp" style=""></span>mg/kg/day, 3 days \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Improvement<br>No resolution \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">3 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">September \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">22 months \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">2-Day fever<br>Ataxia<br>Vomiting<br>Diarrhoea \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Stool<br>Respiratory \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Altered T2-weighted signal with bilateral hyperintensity of GM in the mesencephalon \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Methylprednisolone 2<span class="elsevierStyleHsp" style=""></span>mg/kg/day, 5 days \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Gradual improvement<br>Full resolution of symptoms \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">4 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">December \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">21 months \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">5-Day fever<br>Somnolence<br>Ataxia<br>Conjunctivitis \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Stool \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">T2-weighted hyperintensity at the medulla oblongata and junction of medulla and spinal cord \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">IVIg 1<span class="elsevierStyleHsp" style=""></span>g/kg/day, 2 days \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Gradual improvement<br>Full resolution of symptoms \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1862806.png" ] ] ] ] "descripcion" => array:1 [ "en" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Main characteristics of cases of acute neurologic disease due to enterovirus.</p>" ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0015" "bibliografiaReferencia" => array:6 [ 0 => array:3 [ "identificador" => "bib0035" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Understanding enterovirus 71 neuropathogenesis and its impact on other neurotropic enteroviruses" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:2 [ 0 => "K.C. 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| Year/Month | Html | Total | |
|---|---|---|---|
| 2024 November | 7 | 11 | 18 |
| 2024 October | 47 | 44 | 91 |
| 2024 September | 51 | 34 | 85 |
| 2024 August | 50 | 58 | 108 |
| 2024 July | 43 | 41 | 84 |
| 2024 June | 52 | 37 | 89 |
| 2024 May | 44 | 26 | 70 |
| 2024 April | 43 | 31 | 74 |
| 2024 March | 43 | 21 | 64 |
| 2024 February | 32 | 29 | 61 |
| 2024 January | 28 | 14 | 42 |
| 2023 December | 63 | 23 | 86 |
| 2023 November | 30 | 31 | 61 |
| 2023 October | 43 | 21 | 64 |
| 2023 September | 30 | 21 | 51 |
| 2023 August | 32 | 29 | 61 |
| 2023 July | 39 | 27 | 66 |
| 2023 June | 41 | 27 | 68 |
| 2023 May | 35 | 20 | 55 |
| 2023 April | 18 | 16 | 34 |
| 2023 March | 41 | 22 | 63 |
| 2023 February | 32 | 16 | 48 |
| 2023 January | 19 | 15 | 34 |
| 2022 December | 49 | 13 | 62 |
| 2022 November | 54 | 31 | 85 |
| 2022 October | 62 | 32 | 94 |
| 2022 September | 32 | 23 | 55 |
| 2022 August | 45 | 47 | 92 |
| 2022 July | 34 | 38 | 72 |
| 2022 June | 33 | 47 | 80 |
| 2022 May | 44 | 27 | 71 |
| 2022 April | 36 | 29 | 65 |
| 2022 March | 61 | 50 | 111 |
| 2022 February | 30 | 22 | 52 |
| 2022 January | 39 | 34 | 73 |
| 2021 December | 47 | 40 | 87 |
| 2021 November | 53 | 33 | 86 |
| 2021 October | 70 | 58 | 128 |
| 2021 September | 54 | 41 | 95 |
| 2021 August | 38 | 41 | 79 |
| 2021 July | 35 | 19 | 54 |
| 2021 June | 43 | 37 | 80 |
| 2021 May | 56 | 38 | 94 |
| 2021 April | 146 | 44 | 190 |
| 2021 March | 60 | 30 | 90 |
| 2021 February | 55 | 36 | 91 |
| 2021 January | 66 | 20 | 86 |
| 2020 December | 49 | 15 | 64 |
| 2020 November | 47 | 15 | 62 |
| 2020 October | 52 | 21 | 73 |
| 2020 September | 41 | 19 | 60 |
| 2020 August | 45 | 19 | 64 |
| 2020 July | 33 | 24 | 57 |
| 2020 June | 72 | 8 | 80 |
| 2020 May | 44 | 16 | 60 |
| 2020 April | 23 | 12 | 35 |
| 2020 March | 29 | 9 | 38 |
| 2020 February | 44 | 10 | 54 |
| 2020 January | 61 | 12 | 73 |
| 2019 December | 39 | 16 | 55 |
| 2019 November | 43 | 6 | 49 |
| 2019 October | 53 | 8 | 61 |
| 2019 September | 53 | 3 | 56 |
| 2019 August | 57 | 14 | 71 |
| 2019 July | 44 | 26 | 70 |
| 2019 June | 26 | 16 | 42 |
| 2019 May | 49 | 17 | 66 |
| 2019 April | 53 | 22 | 75 |
| 2019 March | 23 | 8 | 31 |
| 2019 February | 30 | 13 | 43 |
| 2019 January | 43 | 13 | 56 |
| 2018 December | 41 | 24 | 65 |
| 2018 November | 46 | 25 | 71 |
| 2018 October | 169 | 31 | 200 |
| 2018 September | 33 | 21 | 54 |
| 2018 August | 0 | 3 | 3 |
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