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Permanent damage of the inner retinal layers in a patient with migraine: a different case of paracentral acute middle maculopathy
Lesión permanente de las capas internas de la retina en una paciente con migraña: un caso diferente de maculopatía paracentral aguda media
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Monera Lucas, J. Escolano Serrano, D. Romero Valero, G. Castilla Martínez, S. Pardo López, R. Toledano Martos" "autores" => array:6 [ 0 => array:4 [ "nombre" => "C.E." "apellidos" => "Monera Lucas" "email" => array:1 [ 0 => "carlosmonera@gmail.com" ] "referencia" => array:3 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] 2 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">*</span>" "identificador" => "cor0005" ] ] ] 1 => array:3 [ "nombre" => "J." "apellidos" => "Escolano Serrano" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] ] ] 2 => array:3 [ "nombre" => "D." "apellidos" => "Romero Valero" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] ] ] 3 => array:3 [ "nombre" => "G." "apellidos" => "Castilla Martínez" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] ] ] 4 => array:3 [ "nombre" => "S." "apellidos" => "Pardo López" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] ] ] 5 => array:3 [ "nombre" => "R." "apellidos" => "Toledano Martos" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] ] ] ] "afiliaciones" => array:2 [ 0 => array:3 [ "entidad" => "Servicio de Oftalmología, Hospital General Universitario de Elche, Elche, Alicante, Spain" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Universidad Miguel Hernández, Elche, Alicante, Spain" "etiqueta" => "b" "identificador" => "aff0010" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "<span class="elsevierStyleItalic">Corresponding author</span>." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Lesión permanente de las capas internas de la retina en una paciente con migraña: un caso diferente de maculopatía paracentral aguda media" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:8 [ "identificador" => "fig0010" "etiqueta" => "Fig. 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 1291 "Ancho" => 2500 "Tamanyo" => 294545 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0010" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Visual field test of the left eye performed with a Humphrey perimeter and the SITA 24-2 strategy. The image A shows the existence of a paracentral scotoma at the moment of the diagnosis, wich persists one year later (image B).</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Migraine headache disorder is very prevalent and disabling. It can occur spontaneously or be triggered by stress, physical exercise, or the intake of certain toxics, such as alcohol. In some cases, it is accompanied by neurological or visual symptoms, called auras. The visual symptoms are usually positive, such as photopsia, scintillations or more rarely, hallucinations. However, sometimes the visual symptoms can be sometimes negative, such as transient monocular blindness or transitory scotomas. Positive symptoms generally originate in the occipital cortex and are usually bilateral. Negative symptoms, for their part, originate in most cases in the anterior visual pathway and are generally unilateral.<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">Retinal migraine was defined as recurrent episodes of monocular visual loss, scotoma, or reversible blindness in association with typical migraine headache.<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">However, retinal migraine is an ambiguous concept, and it is rejected by some researchers. Hill et al.,<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a> concluded that the diagnosis of retinal migraine was probably wrong in most reported cases and proposed that most of cases of transient monocular vision loss associated to headache should be considered as a different diagnosis. Furthermore, they suggested to be careful before making a diagnosis of retinal migraine in the absence of personal or family history of migraine. On the other hand, Petzold et al.,<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a> described that in cases of transient monocular vision loss due to vasospasm a migraine attack could act as a trigger factor. Generally, these phenomena are painless and last between ten to twenty minutes, although cases of longer duration have been reported. In most cases they resolve spontaneously and completely.</p><p id="par0020" class="elsevierStylePara elsevierViewall">It has been demonstrated that during migraine attacks, microvascular vasospasms exist in cortical areas corresponding topographically with visual symptoms.<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a> Retinal arteriole vasospasms are infrequent and a rare cause of visual disturbance. They generally produce a transient, painless and monocular visual decrease, lasting less than twenty minutes, with subsequent progressive spontaneous complete resolution. The most frequent sign found in retinal vasospasms is the appearance of pale areas of the retina dependent on the affected arterioles, that usually disappear within the following four to six weeks and generally do not produce any type of chronic injury.<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1,5</span></a> OCT is useful in these cases because pale areas can be observed early as hyperreflective focal retinal edema, and later as a disruption or thinning of inner retinal layers.<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">6</span></a></p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Case report</span><p id="par0025" class="elsevierStylePara elsevierViewall">The case is that of a 20-year-old woman with a history of migraine headache with visual aura. Her aura symptoms used to appear as a paracentral scotoma in the left eye lasting approximately ten minutes. She went to the emergency department for a consultation because the scotoma had not disappeared after a migraine attack two days before. The patient did not report any other type of symptoms and denied any relevant personal or family pathological history. She was not taking any treatment and denied use of amphetamines and cocaine.</p><p id="par0030" class="elsevierStylePara elsevierViewall">Best corrected visual acuity (BCVA) was 20/20 in both eyes. Intraocular pressures (IOP) by Goldmann tonometry measured 15<span class="elsevierStyleHsp" style=""></span>mmHg bilaterally. Both the neurological examination and the anterior chamber examination with slit lamp were normal. Pupillary reflexes were normal. Fundoscopy revealed the existence of two pale paracentral areas in the left eye suggestive of an ischemic disturbance (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>A). The scotoma described by the patient was evidenced by a visual field test (Humphrey 24-2) (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>A). The optical coherence tomography (OCT) showed a well-defined foveal profile and the absence of subretinal fluid. However, focal hyper-reflective lesion at the level of the inner and outer plexiform layers and inner nuclear layer of the retina in the areas affected by ischemia was observed (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>A). A fluorescein angiography (FA) was performed the next day and it did not reveal any relevant findings (<a class="elsevierStyleCrossRef" href="#fig0020">Fig. 4</a>).</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><elsevierMultimedia ident="fig0010"></elsevierMultimedia><elsevierMultimedia ident="fig0015"></elsevierMultimedia><elsevierMultimedia ident="fig0020"></elsevierMultimedia><p id="par0035" class="elsevierStylePara elsevierViewall">A blood test was requested to rule out autoimmune and thrombophilic diseases, as well as different serologies (toxoplasma, syphilis, toxocara, tuberculosis, herpes simplex virus, herpes zoster virus, cytomegalovirus and Epstein-Barr virus) to rule out infectious pathology. All laboratory tests were normal, including HLA-B27, HLA-B29, HLA-B52, anti-neutrophil antibodies (ANCA), rheumatoid factor, anti-cardiolipin antibodies and antiglycoprotein antibody. The neurology department was consulted, and a general study was proposed. Several neurological and imaging studies were performed. Magnetic resonance imaging (MRI) of the brain and spinal cord, visual evoked potentials (VEP), transesophageal echocardiography (TEE) and transthoracic echocardiography (TTE) were normal. In addition, a hearing study with brainstem auditory evoked potentials (BEAP) and audiometry was conducted in order to exclude Susac Syndrome. All the assessments returned normal results. She was given acetylsalicylic acid 100<span class="elsevierStyleHsp" style=""></span>mg daily.</p><p id="par0040" class="elsevierStylePara elsevierViewall">Six weeks after the first diagnosis, the BCVA was 20/20 in both eyes, and the pale retinal areas had disappeared (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>B). However, the patient was still complaining about the scotoma in her left eye without any significant subjective changes. The OCT of the posterior pole evidenced an atrophy of the inner retinal layers in the area affected by ischemia (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>B).</p><p id="par0045" class="elsevierStylePara elsevierViewall">Twelve months later, the inner retinal layers atrophy was persistent without any significant changes (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>C). The patient has remained clinically stable without changes in her symptoms, and she has a chronic paracentral scotoma in her left eye a year after the episode (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>B).</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Discussion</span><p id="par0050" class="elsevierStylePara elsevierViewall">The mechanism by which focal retinal vasospasms occur remains unknown, although it is believed to be due to an alteration in the autoregulation of blood flow in the retinal circulation. Normally there is a balance between vasoconstrictor factors, such as Endothelin-1 (ET-1), and vasodilator factors, such as endothelium derived nitric oxide (NO).<a class="elsevierStyleCrossRefs" href="#bib0020"><span class="elsevierStyleSup">4,5</span></a> ET-1 increases in autoimmune diseases and migraine, which could explain the vasoconstriction of retinal arterioles due to loss of autoregulation.<a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">7</span></a></p><p id="par0055" class="elsevierStylePara elsevierViewall">Loss of blood supply to the retina during retinal vasospasms produces tissue hypoxia. An enzymatic cascade thereby occurs involving neuronal depolarisation, increased calcium concentration, increasing of free radicals and oxidative stress that results in apoptosis and cellular necrosis.<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a></p><p id="par0060" class="elsevierStylePara elsevierViewall">Although most studies have been conducted on animal models, the retina is known to be more resistant to ischemic insult than the brain. This can be explained due to the autoregulation of blood flow in retinal circulation. A few minutes of cerebral hypoxia results in irreversible injury. However, it has been demonstrated that the primate retina can endure up to 100<span class="elsevierStyleHsp" style=""></span>min of ischemia without causing permanent injury.<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1,8</span></a> Moreover, the retina has a regionalised sensitivity to ischemia with the inner layers being less resistant than the outer layers,<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a> because the outer retina receives its blood supply directly from the choroid. This explains why the inner retinal layers are the most affected area in cases of deficient blood supply due to arteriolar vasoconstriction.</p><p id="par0065" class="elsevierStylePara elsevierViewall">The main causes of retinal ischemia were ruled out, and the patient was diagnosed with probable vasospastic syndrome secondary to migraine disorder as a predisposing condition. The existence of negative visual symptoms secondary to retinal arteriolar vasospasms has been reported previously. Killer et al.<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">5</span></a> reported the case of a 40-year-old woman with clinical scotoma and a complete vasospasm in the inferotemporal retinal artery, which totally resolved within a few hours, with normal fundus and no visual symptoms. Gutteridge et al. reported the case a 60-year-old male with evidence of branch retinal arterial occlusion that developed during a migraine attack, and Abdul-Rahman et al.<a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">7</span></a> reported a 48-year-old man with a left superior hemiretinal artery spasm which resolved completely over two months. On the other hand, Doyle et al.,<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> reported the case of a 22-year-old man with an episode of transient monocular blindness and evidence of retinal arterial and vein vasospasm.</p><p id="par0070" class="elsevierStylePara elsevierViewall">Nevertheless, in our case report, the tissue hypoxia secondary to retinal vasospasm resulted in a permanent injury of the inner retinal layers, which manifests as a chronic paracentral scotoma. This is a very unusual clinical entity because the time hath hypoxia lasts in retinal vasospasms is usually quite short, and it is usually insufficient to produce irreversible lesions. However, the presence of permanent ischemic complications in association with migraine has been described in recent clinical reports.</p><p id="par0075" class="elsevierStylePara elsevierViewall">In recent years a new tomographic finding in retinal image studies named paracentral acute middle maculopathy (PAMM) has been introduced. It was first described in 2013 by Sarraf et al.,<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a> and it is characterized by a hyper-reflective band-like lesion involving the inner nuclear layer (INL), resulting in permanent INL thinning in patients that typically present with sudden onset of one or multiple paracentral scotoma. Although the pathophysiology of PAMM is not well defined, it has been associated with some vascular dysfunctions and systemic diseases. Different cardiovascular risk factors<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a> have been related to PAMM, including dyslipidemia, hypotension, intensive exercise, pregnancy, migraine and drug or caffeine intake. The finding of typical OCT lesions and the history of migraine could be compatible with the diagnosis of PAMM in our patient.</p><p id="par0080" class="elsevierStylePara elsevierViewall">The chronic scotoma is not having a very disabling impact on our patient’s normal life. However, this case report demonstrates that retinal vasospasms can cause irreversible injuries due to ischemia and cell destruction. It may be interesting to take this into account when conducting the differential diagnosis in cases of negative visual symptoms, because it can potentially produce permanent lesions, thus having an impact on the patient’s normal autonomy and quality of life.</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Conflict of interest</span><p id="par0085" class="elsevierStylePara elsevierViewall">None.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:9 [ 0 => array:3 [ "identificador" => "xres1813810" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec1583700" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres1813809" "titulo" => "Resumen" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0010" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec1583701" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 5 => array:2 [ "identificador" => "sec0010" "titulo" => "Case report" ] 6 => array:2 [ "identificador" => "sec0015" "titulo" => "Discussion" ] 7 => array:2 [ "identificador" => "sec0020" "titulo" => "Conflict of interest" ] 8 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2022-06-06" "fechaAceptado" => "2022-09-07" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec1583700" "palabras" => array:5 [ 0 => "Migraine" 1 => "Retina" 2 => "Scotoma" 3 => "Neuro-ophthalmology" 4 => "Headache" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec1583701" "palabras" => array:5 [ 0 => "Migraña" 1 => "Retina" 2 => "Escotoma" 3 => "Neuro-oftalmología" 4 => "Cefalea" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">We report the case of a 20-year-old patient who presented a paracentral scotoma in her left eye that had not disappeared after a migraine attack two days before. Ocular examination showed two pale paracentral areas suggesting an acute ischemia insult. Several causes of retinal ischemia were ruled out and the patient was diagnosed with secondary retinal vasospasm. One year later, the patient suffers an atrophy of the inner layers of the affected retina and has a paracentral chronic scotoma in her left eye. Retinal vasospasms can result in irreversible lesions and chronic symptoms due to ischemia and cell destruction. This unusual case reports a permanent damage due to retinal vasospasm secondary to migraine attack. The finding of typical lesions and the history of migraine could be compatible with the diagnosis of paracentral acute middle maculopathy (PAMM).</p></span>" ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Presentamos el caso de una paciente mujer de 20 años que consultó por un escotoma paracentral en su ojo izquierdo que no había desaparecido después de una crisis de migraña dos días antes. La exploración realizada evidenció la presencia de dos áreas de palidez retiniana sugestivas de isquemia aguda. Tras descartar varias causas de isquemia retiniana aguda se llegó al diagnóstico de un síndrome vasoespástico retiniano. Un año después, la paciente presenta una atrofia de las capas internas de la retina afectada y sufre un escotoma paracentral crónico en su ojo izquierdo. Los vasoespasmos retinianos pueden provocar un daño irreversible y crónico debido a la destrucción tisular por la isquemia. Este inusual caso describe una lesión permanente secundaria a un vasoespasmo arterial tras una crisis de migraña. El hallazgo de lesiones retinianas características y la historia de migraña hace el diagnóstico compatible con un episodio de maculopatía paracentral aguda media.</p></span>" ] ] "multimedia" => array:4 [ 0 => array:8 [ "identificador" => "fig0005" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 425 "Ancho" => 855 "Tamanyo" => 53187 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0005" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Fundoscopy of the left eye. The image A shows the existence of two pale paracentral areas at the moment of the diagnosis. Image B shows that the pale areas had disappeared six weeks later.</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" => 1291 "Ancho" => 2500 "Tamanyo" => 294545 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0010" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Visual field test of the left eye performed with a Humphrey perimeter and the SITA 24-2 strategy. The image A shows the existence of a paracentral scotoma at the moment of the diagnosis, wich persists one year later (image B).</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" => 1141 "Ancho" => 1005 "Tamanyo" => 126112 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0015" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Optical coherence tomography (OCT) of the left eye. The image A shows a focal edema of the inner retinal layers in the parafovea at the moment of the diagnosis. The image B shows a focal damage in the inner retinal layers six weeks later, which persists after one year (image C).</p>" ] ] 3 => array:8 [ "identificador" => "fig0020" "etiqueta" => "Fig. 4" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr4.jpeg" "Alto" => 633 "Ancho" => 1255 "Tamanyo" => 129514 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0020" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Fuorescein Angiography (FA) of both eyes. 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