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Oculomotor nerve palsy in herpes zoster ophthalmicus: Presentation of 4 cases
Parálisis oculomotoras en el contexto de una reactivación del virus varicela-zóster: a propósito de 4 casos
J. Pascual-Prieto
, B. Benito-Pascual, E. Hernández-García, B. Domingo-Gordo, R. Gómez-de-Liaño
Corresponding author
Servicio de Oftalmología, Hospital Clínico San Carlos, Madrid, Spain
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Pascual-Prieto, B. Benito-Pascual, E. Hernández-García, B. Domingo-Gordo, R. Gómez-de-Liaño" "autores" => array:5 [ 0 => array:4 [ "nombre" => "J." "apellidos" => "Pascual-Prieto" "email" => array:1 [ 0 => "jpascualprieto@gmail.com" ] "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "*" "identificador" => "cor0005" ] ] ] 1 => array:2 [ "nombre" => "B." "apellidos" => "Benito-Pascual" ] 2 => array:2 [ "nombre" => "E." "apellidos" => "Hernández-García" ] 3 => array:2 [ "nombre" => "B." "apellidos" => "Domingo-Gordo" ] 4 => array:2 [ "nombre" => "R." "apellidos" => "Gómez-de-Liaño" ] ] "afiliaciones" => array:1 [ 0 => array:2 [ "entidad" => "Servicio de Oftalmología, Hospital Clínico San Carlos, Madrid, Spain" "identificador" => "aff0005" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "<span class="elsevierStyleItalic">Corresponding author</span>." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Parálisis oculomotoras en el contexto de una reactivación del virus varicela-zóster: a propósito de 4 casos" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:8 [ "identificador" => "fig0015" "etiqueta" => "Fig. 3" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr3.jpeg" "Alto" => 990 "Ancho" => 905 "Tamanyo" => 65660 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0015" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Magnetic resonance with intravenous gadolinium. Note the contrast enhancement increase in Meckel's <span class="elsevierStyleItalic">cavum</span> and Gasser's ganglion on the left side.</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Varicella zoster virus (VZV) is a herpes alpha virus with high infectivity and worldwide prevalence. During primary infection, known as chickenpox, the virus accesses nerve nodes by retrograde transport from the skin infection. VZV can remain latent in nerve ganglia for years. Its reactivation, usually a single episode, is due to the virus anterograde spread through the axon. Advanced age and suppressed immune state are the main risk factors for its reactivation.<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> The main reservoirs are spinal cord dorsal ganglia.</p><p id="par0010" class="elsevierStylePara elsevierViewall">Herpes zoster ophthalmicus (HZO) is VZVs spread from the Gasser ganglion through the trigeminal nerves cutaneous sensory branches in its V<span class="elsevierStyleInf">1</span> territory. HZO represents approximately 10%–20% of all herpes zoster cases.<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a></p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Clinical case 1</span><p id="par0015" class="elsevierStylePara elsevierViewall">A 79-year-old man presented herpetic keratouveitis in the left eye (LE). Three days later he develops cutaneous herpes in the trigeminal branch V<span class="elsevierStyleInf">1</span>. Two days after onset of vesicles, ophthalmoplegia, reactive LE mydriasis and ptosis on the same side were developed (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>). A complete III cranial nerve mononeuritis was diagnosed with a cranial computed tomography (CAT) scan without significant findings.</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0020" class="elsevierStylePara elsevierViewall">Hospital admission for the administration of intravenous acyclovir and treatment of herpetic keratouveitis was decided. After a few days, the patient exhibited partial recovery of ocular motility with external eye movements improved. The pupil remained unresponsive and mydriatic at hospital discharge.</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Clinical case 2</span><p id="par0025" class="elsevierStylePara elsevierViewall">A 68-year-old woman developed diplopia 4 days after the onset of vesicular lesions in V<span class="elsevierStyleInf">1</span> nerve territory. Partial paralysis of the III cranial nerve with preserved pupillary reflexes and a slight ptosis (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>) were observed.</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia><p id="par0030" class="elsevierStylePara elsevierViewall">Following intravenous acyclovir administration, the patient partially recovered ocular motility. During admission, a gadolinium-enhanced magnetic resonance showing an increased contrast enhancement in Meckel's <span class="elsevierStyleItalic">cavum</span> and Gasser's ganglion region (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>) was performed.</p><elsevierMultimedia ident="fig0015"></elsevierMultimedia></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Clinical case 3</span><p id="par0035" class="elsevierStylePara elsevierViewall">An 89-year-old woman presented skin involvement in V<span class="elsevierStyleInf">1</span> left side due to VZV. Two weeks later, horizontal diplopia was developed. Left VI cranial nerve mononeuritis was diagnosed. CAT scan was performed without significant findings. Given the elevated ESR evidence, hospital admission was determined and oral prednisone was prescribed for 3 weeks due to suspicion of polymyalgia rheumatica. After normalization of ESR values and partial recovery of ocular motility, hospital discharge was decided.</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Clinical case 4</span><p id="par0040" class="elsevierStylePara elsevierViewall">A 48-year-old woman visited the ER for bifrontal headache with oppressive characteristics that did not subside with regular analgesia. A cranial CAT scan was performed without findings that could explainthe symptoms. On ocular motility examination, the patient reported diplopia in levoversion. Left VI cranial nerve paresis was evident. Five days later the patient presented herpetic keratitis on the LE and 2 days later cutaneous vesicles in V<span class="elsevierStyleInf">1</span> trigeminal region of the same side were evident.</p><p id="par0045" class="elsevierStylePara elsevierViewall">After prescribing systemic acyclovir, the patient fully recovered ocular motility.</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Discussion</span><p id="par0050" class="elsevierStylePara elsevierViewall">VZV reactivation usually occurs in the area where the cutaneous expressions of the primary infection (chickenpox) were most noticeable, usually in thoracic dermatome and the V trigeminal cranial nerve innervation area.</p><p id="par0055" class="elsevierStylePara elsevierViewall">Depending on the bibliographic sources consulted, the frequency of oculomotor involvement can vary between 5 and 29% according to the cases. The most described oculomotor paralysis is that of the III cranial nerve, followed by the VI nerve, and occasionally, isolated paralysis of the IV nerve has been described in this context.<a class="elsevierStyleCrossRefs" href="#bib0015"><span class="elsevierStyleSup">3–6</span></a></p><p id="par0060" class="elsevierStylePara elsevierViewall">Most authors recognize vesicle appearance as one of the first signs of the process. However, it is to be noted how in the fourth clinical case the vesicles were one of the last signs to manifest, the patient only presented anodyne headache and horizontal diplopia at first. In cases like this, early etiologic diagnosis is particularly complicated.</p><p id="par0065" class="elsevierStylePara elsevierViewall">The different ophthalmological involvement that VZV reactivation may produce in the trigeminal region is related to nerve path in the cavernous sinus, superior orbital fissure and Zinn ring, where the virus spread through axons can extend to other cranial pairs such as II, III, IV and VI due to the anatomical relations between them. In the cavernous sinus, the trigeminal nerve is anatomically related to the III and IV cranial nerves. Through the superior orbital fissure, branches of the trigeminal nerve pass next to the superior ophthalmic vein and IV cranial nerve. In the Zinn ring, the trigeminal nerve is once again related to the III and VI cranial nerves.</p><p id="par0070" class="elsevierStylePara elsevierViewall">The pathogenic mechanisms that cause VZV paralysis are not clear yet. Some authors propose that the cause could be processes such as meninges inflammation, occlusive vasculitis microinfarcts and demyelination processes.<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a> In our case series, only one presented evidence compatible with VZV reactivation through the Gasser ganglion by means of imaging test. Immune phenomena such as occlusive vasculitis or small localized demyelination defects described in literature may have caused the paralysis we present.</p><p id="par0075" class="elsevierStylePara elsevierViewall">Imaging tests that rule out other causes such as ischemic etiology or life-threatening complications such as herpetic encephalitis are essential in the management of oculomotor paralysis with suspected VZV reactivation.</p><p id="par0080" class="elsevierStylePara elsevierViewall">Regarding treatment, all authors agree on the need to establish systemic antivirals, choosing acyclovir treatment. The selection of oral or intravenous administration does not seem to be very well defined. Some authors propose the use of corticosteroids along with antivirals. This decision could be related to the proposed pathogenic mechanisms of inflammation and immune processes. In our series of patients, all were treated with systemic antivirals, evolving favorably. We have not found published evidence that the adjuvant use of systemic corticosteroids improves the prognosis and evolution of these patients.</p><p id="par0085" class="elsevierStylePara elsevierViewall">In Spain, for a decade or so, chickenpox vaccine has been administered in 2 doses: the first between 12 and 15 months and the later between 4 and 6 years. Contact of adults that had chickenpox with children who present chickenpox has a booster effect that reinforces this immunity. Widespread vaccination has dramatically reduced the primary infection of VZV or it turns it into a version with latent symptomatology. This new epidemiological circumstance could be behind an increase in virus reactivations even in people under the age of 50.<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a></p><p id="par0090" class="elsevierStylePara elsevierViewall">Currently, there are 2 types of vaccines that combat VZV reactivation; one live attenuated virus vaccine and another recombinant subunit vaccine. Both seem to be effective in VZV reactivation and post-herpetic neuralgia incidence.<a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">7</span></a></p><p id="par0095" class="elsevierStylePara elsevierViewall">In conclusion, ophthalmological manifestations of VZV reactivation are multiple. Appearance of sudden diplopia in the context of herpetic vesicles should suggest an associated oculomotor paralysis. An imaging test that rules out other causes or complications is mandatory. The treatment of choice is systemic acyclovir.</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Funding</span><p id="par0100" class="elsevierStylePara elsevierViewall">The authors declare that they have not received funding to carry out this work.</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Conflict of interest</span><p id="par0105" class="elsevierStylePara elsevierViewall">No conflict of interests was declared by the authors.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:13 [ 0 => array:3 [ "identificador" => "xres1371333" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec1260321" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres1371334" "titulo" => "Resumen" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0010" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec1260320" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 5 => array:2 [ "identificador" => "sec0010" "titulo" => "Clinical case 1" ] 6 => array:2 [ "identificador" => "sec0015" "titulo" => "Clinical case 2" ] 7 => array:2 [ "identificador" => "sec0020" "titulo" => "Clinical case 3" ] 8 => array:2 [ "identificador" => "sec0025" "titulo" => "Clinical case 4" ] 9 => array:2 [ "identificador" => "sec0030" "titulo" => "Discussion" ] 10 => array:2 [ "identificador" => "sec0035" "titulo" => "Funding" ] 11 => array:2 [ "identificador" => "sec0040" "titulo" => "Conflict of interest" ] 12 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2020-01-14" "fechaAceptado" => "2020-04-09" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec1260321" "palabras" => array:3 [ 0 => "Varicella zoster virus" 1 => "Herpes zoster ophthalmicus" 2 => "Oculomotor palsy" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec1260320" "palabras" => array:3 [ 0 => "Virus varicela zóster" 1 => "Herpes zóster oftálmico" 2 => "Parálisis oculomotora" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Varicella zoster virus (VZV) infection has a high prevalence worldwide. Within the multiple ophthalmologic manifestations that VZV can cause, sudden diplopia is among them. A review is presented of four clinical cases of 3rd and 4th oculomotor nerve palsies in herpes zoster ophthalmicus. A review is also presented of the physiopathology and most important clinical manifestations. Imaging tests are essential in order to rule out complications. Systemic antiviral administration is the correct treatment.</p></span>" ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">La infección por el virus varicela zóster (VVZ) tiene una alta prevalencia a nivel mundial. De las muchas manifestaciones oftalmológicas que puede manifestar, la diplopía de aparición brusca es una de ellas. Revisamos cuatro casos clínicos de mononeuritis del III y VI par craneales en el contexto de vesículas herpéticas por el VVZ y revisamos la fisiopatología y manifestaciones clínicas más importantes. Es obligado para el oftalmólogo descartar complicaciones mediante pruebas de imagen y el correcto tratamiento con antivirales sistémicos.</p></span>" ] ] "NotaPie" => array:2 [ 0 => array:2 [ "etiqueta" => "☆" "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Please cite this article as: Pascual-Prieto J, Benito-Pascual B, Hernández-García E, Domingo-Gordo B, Gómez-de-Liaño R. Parálisis oculomotoras en el contexto de una reactivación del virus varicela-zóster: a propósito de 4 casos. Arch Soc Esp Oftalmol. 2020. <span class="elsevierStyleInterRef" id="intr0005" href="https://doi.org/10.1016/j.oftal.2020.04.011">https://doi.org/10.1016/j.oftal.2020.04.011</span></p>" ] 1 => array:2 [ "etiqueta" => "☆☆" "nota" => "<p class="elsevierStyleNotepara" id="npar0010">This paper was awarded the First Panels Prize at the 95th Congress of the Ophthalmology Society of Spain.</p>" ] ] "multimedia" => array:3 [ 0 => array:8 [ "identificador" => "fig0005" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1291 "Ancho" => 1805 "Tamanyo" => 362909 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0005" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Left III cranial nerve paralysis with ptosis. Note ciliary hyperemia due to associated herpetic keratouveitis.</p>" ] ] 1 => array:8 [ "identificador" => "fig0010" "etiqueta" => "Fig. 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 1289 "Ancho" => 1805 "Tamanyo" => 305070 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0010" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Left III cranial nerve paralysis with mild ptosis. Pharmacological mydriasis.</p>" ] ] 2 => array:8 [ "identificador" => "fig0015" "etiqueta" => "Fig. 3" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr3.jpeg" "Alto" => 990 "Ancho" => 905 "Tamanyo" => 65660 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0015" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Magnetic resonance with intravenous gadolinium. 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