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Letter to the Editor
Amyotrophic lateral sclerosis and myasthenia gravis overlap syndrome: 3 new cases
Esclerosis lateral amiotrófica y miastenia gravis (síndrome overlap): presentación de 3 nuevos casos
S. Santos-Lasaosa
Corresponding author
ssantos@salud.aragon.es

Corresponding author.
, A. López-Bravo, M. Garcés-Redondo, S. Atienza-Ayala, P. Larrodé-Pellicer
Servicio de Neurología, Hospital Clínico Universitario Lozano Blesa, Zaragoza, Spain
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    "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0005" class="elsevierStylePara elsevierViewall">The association of myasthenia gravis &#40;MG&#41; and amyotrophic lateral sclerosis &#40;ALS&#41; &#40;overlap syndrome&#41; is infrequent in clinical practice&#46; The available evidence suggests that immunomodulatory therapy has a protective effect in the early stages of motor neuron disease &#40;MND&#41;&#46;<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1&#44;2</span></a> We present 3 cases of this overlap syndrome&#59; <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a> summarises the characteristics of these patients&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0005">Patient 1</span><p id="par0010" class="elsevierStylePara elsevierViewall">The patient was a 52-year-old man with initial symptoms of bilateral ptsosis&#44; diplopia&#44; and dysphagia&#59; 6-8 months later&#44; he presented left brachial paresis with thenar atrophy&#44; global hyperreflexia&#44; and increased jaw jerk reflex&#46; 3-Hz repetitive stimulation obtained a decrement of &#62; 10&#37; in the fifth potential in the abductor digiti minimi&#46; Anti-acetylcholine receptor &#40;anti-AChR&#41; antibody titre was 0&#46;74 &#40;positive results&#44; &#62; 0&#46;7&#41;&#44; and remained stable in subsequent determinations&#46; Fasciculations and denervation potentials were observed in an electromyography study &#40;EMG&#41; performed 4 months after the initial assessment&#46; At 24 months&#44; the patient met diagnostic criteria for class IIb MG<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a> and definite ALS&#44; according to the El Escorial criteria&#46;<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a></p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Patient 2</span><p id="par0015" class="elsevierStylePara elsevierViewall">The patient was a 77-year-old man who developed dysphonia and neurogenic dysphagia with fatigue&#46; He was initially diagnosed class IIb MG&#58; anti-AChR antibody titre was &#62; 20 and 3-Hz repetitive stimulation of the abductor digiti minimi obtained a decrement of &#62; 10&#37; in the fifth potential&#46; Treatment was started with pyridostigmine and oral prednisone&#44; with good clinical response&#59; at 15 months&#44; he presented atrophy of the shoulder and pelvic girdles and right quadriceps&#44; and exacerbation of bulbar symptoms and hyperreflexia&#46; The EMG revealed fasciculations and denervation potentials in the deltoids&#44; medial head of the left gastrocnemius&#44; and the left vastus&#44; and in the tongue&#46;</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Patient 3</span><p id="par0020" class="elsevierStylePara elsevierViewall">The patient was a 73-year-old woman with dysphonia&#44; neurogenic dysphagia&#44; fatigue&#44; and exertion dyspnoea of progressive onset in the previous 2 months&#46; 3-Hz repetitive stimulation of the facial and accessory nerves obtained a decrement of &#62; 10&#37; in the fifth potential&#46; Anti-AChR antibody titre was 7&#46;6&#46; After diagnosis of class IIb MG&#44;<span class="elsevierStyleSup">3</span> combined treatment with pyridostigmine and prednisone was started&#46; Five months after onset&#44; the patient presented anarthria&#46; An EMG study revealed denervation activity and fasciculations in the masseter&#44; tongue&#44; right first interosseous muscle&#44; abductor digiti minimi&#44; and vastus lateralis&#46; The subsequent clinical progression&#44; with lack of response to treatment with immunoglobulins and plasmapheresis&#44; as well as the findings of the neurophysiological study&#44; confirmed the diagnosis of definite ALS&#46;<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a></p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Discussion</span><p id="par0025" class="elsevierStylePara elsevierViewall">This association is infrequent&#44; with only 28 cases reported in the literature&#44;<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1&#44;5</span></a> and represents 2&#37; of patients in our series&#46; Both processes feature an immune-mediated pathogenic mechanism&#46;<a class="elsevierStyleCrossRefs" href="#bib0030"><span class="elsevierStyleSup">6&#44;7</span></a> A decrease in CD4&#43; Foxp3&#43; regulatory T cells &#40;Tregs&#41;<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a> has been described&#59; levels of these cells are associated with ALS progression and altered nitric oxide synthesis&#46;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> It is also reported that muscle and neuromuscular junction involvement may already be apparent in the initial stage of ALS&#46;<a class="elsevierStyleCrossRefs" href="#bib0030"><span class="elsevierStyleSup">6&#44;10&#44;11</span></a></p><p id="par0030" class="elsevierStylePara elsevierViewall">Mulder et al&#46;<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a> describe a decrease in action potentials in patients with ALS&#44; which varies according to muscle analysed&#46;<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a> For example&#44; Wang et al&#46;<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">14</span></a> observed a decrease &#62; 10&#37; in 43&#37; of patients with ALS and in 70&#37; of those with MG&#46; This finding was associated with disease progression and predominantly affected proximal muscles &#40;frequently the trapezius&#41; in patients with ALS&#44; whereas distal muscles showed greater involvement in MG&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">When both entities coexist&#44; MG symptoms are mainly ocular and bulbar&#46; In these cases&#44; immunomodulatory treatment should be considered as a diagnostic and therapeutic option&#46;<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> Furthermore&#44; positive anti-AChR antibody titres have been reported in up to 5&#37; of patients with ALS&#46; Although the cause is unclear&#44; this may be related to the early involvement of the neuromuscular junction&#44; which may also explain the higher levels of anti&#8211;low-density lipoprotein receptor&#8211;related protein 4 &#40;anti-LRP4&#41; antibodies in this disease&#46;<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> Okuyama et al&#46;<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">15</span></a> detected higher titres during periods of more aggressive disease activity and lower titres in stages of clinical stability&#46;</p><p id="par0040" class="elsevierStylePara elsevierViewall">Therefore&#44; we conclude that although the available evidence suggests that early treatment of symptoms of neuromuscular junction involvement improves survival in patients with ALS&#44; diagnosis of ALS&#47;MG overlap syndrome should only be considered when signs and symptoms of MND are observed in association with clinical signs of neuromuscular junction involvement &#40;preferably ocular or bulbar signs&#41; or positive titres of anti-AChR&#44; anti-MuSK&#44; or anti-LRP10 antibodies&#59; and response to acetylcholinesterase inhibitors&#46;<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a></p></span></span>"
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        "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Please cite this article as&#58; Santos-Lasaosa S&#44; L&#243;pez-Bravo A&#44; Garc&#233;s-Redondo M&#44; Atienza-Ayala S&#44; Larrod&#233;-Pellicer P&#46; Esclerosis lateral amiotr&#243;fica y miastenia gravis &#40;s&#237;ndrome <span class="elsevierStyleItalic">overlap</span>&#41;&#58; presentaci&#243;n de 3 nuevos casos&#46; Neurolog&#237;a&#46; 2020&#59;35&#58;595&#8211;597&#46;</p>"
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          "leyenda" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">AChR&#58; acetylcholine receptor&#59; CT&#58; computed tomography&#59; M&#58; man&#59; MND&#58; motor neuron disease&#59; MuSK&#58; muscle-specific receptor tyrosine kinase&#59; W&#58; woman&#46;</p>"
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                  <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
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Patient&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">1&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">2&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">3&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">Sex&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">M&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">M&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">W&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Age of symptom onset &#40;years&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">52&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">77&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">73&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">First symptoms&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Ptosis&#47;diplopia&#47;dysphagia&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Diplopia&#47;dysphagia&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Diplopia&#47;dysphagia&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Time to MND symptom onset&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">6-8 months&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">10-12 months&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">5 months&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Time to diagnosis of overlap syndrome&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">24 months&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">15 months&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">7 months&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Anti-AChR antibodies&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;74&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#62; 20&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">7&#46;6&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Anti-MuSK antibodies&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Negative&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Negative&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Negative&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Mediastinum CT&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">Normal thymus&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">Normal thymus&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Normal thymus&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
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          "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Demographic and clinical characteristics of the patients&#46;</p>"
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                        0 => array:2 [
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                      "titulo" => "Transformation of myasthenia gravis into amyotrophic lateral sclerosis or their concomitance&#63; &#40;case review&#41;"
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                          "autores" => array:3 [
                            0 => "N&#46; Kvirkvelia"
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                        "tituloSerie" => "Georgian Med News&#46;"
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                          "autores" => array:3 [
                            0 => "A&#46; Malaspina"
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                      "doi" => "10.1093/intimm/dxu099"
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                        "tituloSerie" => "Int Immunol&#46;"
                        "fecha" => "2015"
                        "volumen" => "27"
                        "paginaInicial" => "117"
                        "paginaFinal" => "129"
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                      "titulo" => "Autoimmune disease preceding amyotrophic lateral sclerosis&#58; an epidemiologic study"
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                          "etal" => false
                          "autores" => array:5 [
                            0 => "M&#46;R&#46; Turner"
                            1 => "R&#46; Goldacre"
                            2 => "S&#46; Ramagopalan"
                            3 => "K&#46; Talbot"
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                        "fecha" => "2013"
                        "volumen" => "81"
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                      "titulo" => "Association of regulatory T-cell expansion with progresion of amyotrophic lateral sclerosis&#58; a study of humans and a transgenic mouse model"
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                          "etal" => true
                          "autores" => array:6 [
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                            1 => "F&#46;C&#46; McKay"
                            2 => "E&#46; Cretney"
                            3 => "C&#46;R&#46; Bye"
                            4 => "N&#46;D&#46; Perera"
                            5 => "D&#46; Tomas"
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                      "Revista" => array:5 [
                        "tituloSerie" => "JAMA&#46;"
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