Case Report
Extranodal marginal zone B cell lymphoma: An unexpected complication in children with Sjögren's syndrome
Linfoma no Hodgkin de linfocitos B de la zona marginal, extranodal: una complicación inesperada en niños con síndrome de Sjögren
Paz Colladoa,◊,
, Aml Keladab,◊, Maria Cámarac, Andrew Zeftd, Aron Flaggb
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a Department of Rheumatology/Paediatric Rheumatology Unit, Hospital Universitario Severo Ochoa, Madrid, Spain
b Department of Pediatric Hematology/Oncology and Blood & Marrow Transplant, Cleveland Clinic, OH, USA
c Pathologic Anatomy Department, Hospital Universitario Severo Ochoa, Madrid, Spain
d Center for Pediatric Rheumatology and Immunology Cleveland Clinic, OH, USA
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CD 20 stain showing sheets of B cells in case 2.</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Sjögren's syndrome (SS) is a systemic autoimmune disease characterized by the infiltration of lymphocytes in exocrine glands.<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">1</span></a> SS is a rare condition in childhood and ocular and oral symptoms are uncommon.<a class="elsevierStyleCrossRefs" href="#bib0060"><span class="elsevierStyleSup">2,3</span></a> The risk of lymphoma development during the course of SS has been described in adults, but it is extremely rare in childhood.<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">1</span></a> We report the association of lymphoma to SS in two children, as an unexpected complication.</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Case reports</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Case 1</span><p id="par0010" class="elsevierStylePara elsevierViewall">A teenager followed since the age of 14 years for intermittent swelling of the knee with negative image and laboratory investigations. She developed SS at the age of 18 year showing intermittent swelling of parotid glands, positive RF, antinuclear antibodies (ANA) and anti-SSA antibodies, elevated erythrocyte sedimentation rate (ESR, 25<span class="elsevierStyleHsp" style=""></span>mm/1<span class="elsevierStyleHsp" style=""></span>h), but normal serum level of cryoglobulins, IgG4 and complement. The Schirmer test and serologic testing for virus were negative. The minor SG biopsy showed focal lymphocytic sialadenitis but the histopathologic diagnosis did not meet SS-criteria. Her follow-up showed the detection of a nodule on the hard palate with the diagnosis of B-cell lymphoma based on morphologic and immunohistochemical staining (CD20+ B cells) from nodule biopsy. Gastrointestinal endoscopy showed chronic gastritis (<span class="elsevierStyleItalic">Helicobacter pylori</span> negative). The computerized tomography (CT) of neck, chest, abdomen, and pelvis, showed no additional evidence of disease. Recently a new episode of right parotitis along with a biopsied cervical lymph node confirmed persistent lymphoma after 6 months of rituximab.</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Case 2</span><p id="par0015" class="elsevierStylePara elsevierViewall">A 16-year-old boy presented with intermittent painless cervical lymphadenopathy and bilateral parotid swelling for more than 5 years. Neck CT demonstrated enlargement of the parotids. A fine needle aspiration showed a benign lymphoid tissue with no evidence of malignancy. Laboratory data showed an increased ESR (122<span class="elsevierStyleHsp" style=""></span>mm/h). Histopathology analysis showed infiltration of the salivary gland by a lymphocytic proliferation forming confluent nodular masses and follicular hyperplasia of the attached lymph nodes, indicative of a lymphoid malignancy (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>). Immunohistochemical stains demonstrated sheets of CD20+ B cells that were negative for CD5, CD43, and cyclin-D1, confirming B-cell clonal proliferation (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>). CD10 and BCL-6 stains highlighted germinal centers which were negative for BCL-2. A Ki-67 stain showed numerous positive cells within and between germinal centers (20–30% cells). Parotidectomy and radiotherapy was performed. Serologic testing revealed only a remote infection by CMV and EBV. Immunological tests showed positive RF, ANA, anti-SSA and anti-SSB antibodies. Despite only vague sicca symptoms, ophthalmology exam revealed corneal and conjunctival erosions, and the diagnosis of SS was made. Hydroxychloroquine and rituximab were started. There was no evidence of tumor recurrence after >14 months follow-up.</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><elsevierMultimedia ident="fig0010"></elsevierMultimedia></span></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Discussion</span><p id="par0020" class="elsevierStylePara elsevierViewall">In childhood, recurrent parotid swelling is the most common hallmark of SS, usually proceeding to sicca symptoms as in our patients.<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">2</span></a> Diagnostic criteria are similar to those proposed in adults<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">3</span></a>; however, it showed low sensitivity and histological findings of the minor SG criteria (>1 focus of 50 lymphocytes/4<span class="elsevierStyleHsp" style=""></span>mm<span class="elsevierStyleSup">2</span>) are often negative in children.<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">4</span></a> It explains delayed diagnosis in the case 1, despite exclusion of infectious diseases at onset. The sensitivity increases by using a lesser score in childhood.<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">5</span></a></p><p id="par0025" class="elsevierStylePara elsevierViewall">The occurrence of lymphoma in SS is extremely rare in childhood. EMZL is a low-grade lymphoma that usually occurs in the setting of a benign myoepithelial sialadenitis (MESA) and biopsy confirms the diagnosis. Clonal expansion to EMZL is believed to be triggered by chronic immune stimulation in the context of a preexisting inflammatory response from autoimmune diseases or chronic infections, amyloidosis, some translocations and common variable immunodeficiency.<a class="elsevierStyleCrossRefs" href="#bib0080"><span class="elsevierStyleSup">6–9</span></a> Differences in Rituximab response might be a higher pretreatment number of CD20+ B cells/mm<span class="elsevierStyleSup">2</span> parotid gland parenchyma.<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">10</span></a></p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conclusion</span><p id="par0030" class="elsevierStylePara elsevierViewall">SS requires child-specific criteria to role out lymphoma as unusual complication in children, particularly for timely and appropriate referral.</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Ethical disclosures</span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Protection of human and animal subjects</span><p id="par0035" class="elsevierStylePara elsevierViewall">The authors declare that the procedures followed were in accordance with the regulations of the relevant clinical research ethics committee and with those of the Code of Ethics of the World Medical Association (Declaration of Helsinki).</p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Confidentiality of data</span><p id="par0040" class="elsevierStylePara elsevierViewall">The authors declare that they have followed the protocols of their work centre on the publication of patient data.</p></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Right to privacy and informed consent</span><p id="par0045" class="elsevierStylePara elsevierViewall">The authors have obtained the written informed consent of the patients or subjects mentioned in the article. The corresponding author is in possession of this document.</p></span></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Conflict of interest</span><p id="par0050" class="elsevierStylePara elsevierViewall">None.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:11 [ 0 => array:3 [ "identificador" => "xres1067587" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec1015088" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres1067586" "titulo" => "Resumen" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0010" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec1015089" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 5 => array:3 [ "identificador" => "sec0010" "titulo" => "Case reports" "secciones" => array:2 [ 0 => array:2 [ "identificador" => "sec0015" "titulo" => "Case 1" ] 1 => array:2 [ "identificador" => "sec0020" "titulo" => "Case 2" ] ] ] 6 => array:2 [ "identificador" => "sec0025" "titulo" => "Discussion" ] 7 => array:2 [ "identificador" => "sec0030" "titulo" => "Conclusion" ] 8 => array:3 [ "identificador" => "sec0035" "titulo" => "Ethical disclosures" "secciones" => array:3 [ 0 => array:2 [ "identificador" => "sec0040" "titulo" => "Protection of human and animal subjects" ] 1 => array:2 [ "identificador" => "sec0045" "titulo" => "Confidentiality of data" ] 2 => array:2 [ "identificador" => "sec0050" "titulo" => "Right to privacy and informed consent" ] ] ] 9 => array:2 [ "identificador" => "sec0055" "titulo" => "Conflict of interest" ] 10 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2016-11-09" "fechaAceptado" => "2017-01-26" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec1015088" "palabras" => array:3 [ 0 => "Sjögren's syndrome" 1 => "Child" 2 => "B-cell lymphoma" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec1015089" "palabras" => array:3 [ 0 => "Síndrome de Sjögren" 1 => "Niño" 2 => "Linfoma de células B" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Sjögren's syndrome (SS) is a systemic autoimmune disease characterized by the infiltration of lymphocytes into exocrine glands, resulting in the typical sicca symptoms. Unlike adults, primary SS is a very rare condition in childhood, and the risk of malignancy in juvenile SS (JSS) has not been defined.</p><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">We report the detection of extranodal marginal zone B-cell lymphoma (EMZL) occurring in two children with SS. Fine needle aspiration of the salivary glands (SG) showed nonspecific findings that led to delayed diagnosis of SS. The diagnosis of B-cell lymphoma associated with JSS was based on morphologic and immunohistochemical staining done during the biopsy.</p><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">To highlight awareness of EMZL as a timely and appropriate update of an unusual complication in children with SS.</p></span>" ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">El síndrome de Sjögren (SS) es una enfermedad sistémica autoinmune caracterizada por la infiltración de linfocitos en glándulas exocrinas, provocando el típico síndrome seco. A diferencia de los adultos, el SS es una afección rara en niños, y el riesgo de malignización no ha sido descrito.</p><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Describimos la detección de linfoma B de la zona marginal extranodal de tejido linfoide asociado a mucosa (linfoma MALT) en 2 niños con SS. La aspiración con aguja fina de las glándulas salivares (SG) mostró hallazgos inespecíficos que retrasaron el diagnóstico de SS. El diagnóstico de linfoma B asociado a SS juvenil se realizó con base en los hallazgos morfológicos e inmunohistoquímicos detectados en biopsia.</p><p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Hay que tomar conciencia de que un linfoma B puede acontecer en el curso de un SS como una complicación inesperada en niños, principalmente para realizar una derivación correcta a oncología.</p></span>" ] ] "NotaPie" => array:1 [ 0 => array:3 [ "etiqueta" => "◊" "nota" => "<p class="elsevierStyleNotepara" id="npar0005">These authors contributed equally to this work.</p>" "identificador" => "fn0005" ] ] "multimedia" => array:2 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1122 "Ancho" => 2049 "Tamanyo" => 666134 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Biopsy of extranodal marginal zone lymphoma of mucosa-associated lymphoid tissue of the parotid gland in case 2. Left image shows Hematoxylin & Eosin (H&E) stain in low-power view. Right image shows H&E stain in high-power view.</p>" ] ] 1 => array:7 [ "identificador" => "fig0010" "etiqueta" => "Fig. 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 768 "Ancho" => 1020 "Tamanyo" => 265102 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">Biopsy of low grade B-cell lymphoma of MALT type of the parotid gland. CD 20 stain showing sheets of B cells in case 2.</p>" ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:10 [ 0 => array:3 [ "identificador" => "bib0055" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Primary Sjogren's syndrome: clinical phenotypes, outcome and the development of biomarkers" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:2 [ 0 => "A.V. Goules" 1 => "A.G. 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| año/Mes | Html | Total | |
|---|---|---|---|
| 2024 Noviembre | 4 | 1 | 5 |
| 2024 Octubre | 49 | 30 | 79 |
| 2024 Septiembre | 43 | 15 | 58 |
| 2024 Agosto | 65 | 31 | 96 |
| 2024 Julio | 44 | 32 | 76 |
| 2024 Junio | 59 | 26 | 85 |
| 2024 Mayo | 59 | 35 | 94 |
| 2024 Abril | 45 | 24 | 69 |
| 2024 Marzo | 43 | 37 | 80 |
| 2024 Febrero | 34 | 31 | 65 |
| 2024 Enero | 32 | 28 | 60 |
| 2023 Diciembre | 24 | 32 | 56 |
| 2023 Noviembre | 36 | 27 | 63 |
| 2023 Octubre | 34 | 26 | 60 |
| 2023 Septiembre | 63 | 34 | 97 |
| 2023 Agosto | 26 | 13 | 39 |
| 2023 Julio | 41 | 23 | 64 |
| 2023 Junio | 33 | 22 | 55 |
| 2023 Mayo | 43 | 29 | 72 |
| 2023 Abril | 37 | 17 | 54 |
| 2023 Marzo | 89 | 37 | 126 |
| 2023 Febrero | 70 | 30 | 100 |
| 2023 Enero | 57 | 18 | 75 |
| 2022 Diciembre | 82 | 25 | 107 |
| 2022 Noviembre | 77 | 41 | 118 |
| 2022 Octubre | 73 | 31 | 104 |
| 2022 Septiembre | 44 | 37 | 81 |
| 2022 Agosto | 40 | 47 | 87 |
| 2022 Julio | 35 | 48 | 83 |
| 2022 Junio | 40 | 90 | 130 |
| 2022 Mayo | 38 | 50 | 88 |
| 2022 Abril | 42 | 48 | 90 |
| 2022 Marzo | 44 | 81 | 125 |
| 2022 Febrero | 78 | 31 | 109 |
| 2022 Enero | 93 | 53 | 146 |
| 2021 Diciembre | 43 | 46 | 89 |
| 2021 Noviembre | 46 | 48 | 94 |
| 2021 Octubre | 53 | 53 | 106 |
| 2021 Septiembre | 36 | 40 | 76 |
| 2021 Agosto | 27 | 41 | 68 |
| 2021 Julio | 26 | 46 | 72 |
| 2021 Junio | 48 | 46 | 94 |
| 2021 Mayo | 68 | 51 | 119 |
| 2021 Abril | 165 | 106 | 271 |
| 2021 Marzo | 80 | 41 | 121 |
| 2021 Febrero | 45 | 34 | 79 |
| 2021 Enero | 42 | 21 | 63 |
| 2020 Diciembre | 39 | 24 | 63 |
| 2020 Noviembre | 33 | 27 | 60 |
| 2020 Octubre | 31 | 25 | 56 |
| 2020 Septiembre | 48 | 41 | 89 |
| 2020 Agosto | 40 | 36 | 76 |
| 2020 Julio | 33 | 18 | 51 |
| 2020 Junio | 33 | 28 | 61 |
| 2020 Mayo | 47 | 15 | 62 |
| 2020 Abril | 36 | 36 | 72 |
| 2020 Marzo | 56 | 37 | 93 |
| 2020 Febrero | 66 | 24 | 90 |
| 2020 Enero | 42 | 37 | 79 |
| 2019 Diciembre | 40 | 21 | 61 |
| 2019 Noviembre | 51 | 24 | 75 |
| 2019 Octubre | 73 | 23 | 96 |
| 2019 Septiembre | 46 | 26 | 72 |
| 2019 Agosto | 59 | 20 | 79 |
| 2019 Julio | 53 | 19 | 72 |
| 2019 Junio | 56 | 27 | 83 |
| 2019 Mayo | 120 | 68 | 188 |
| 2019 Abril | 69 | 30 | 99 |
| 2019 Marzo | 49 | 20 | 69 |
| 2019 Febrero | 24 | 8 | 32 |
| 2019 Enero | 45 | 24 | 69 |
| 2018 Diciembre | 1 | 2 | 3 |
| 2018 Septiembre | 2 | 0 | 2 |
| 2018 Agosto | 4 | 1 | 5 |
| 2018 Julio | 0 | 4 | 4 |
| 2018 Abril | 0 | 15 | 15 |
| 2018 Marzo | 0 | 14 | 14 |
| 2018 Febrero | 0 | 9 | 9 |
| 2018 Enero | 0 | 12 | 12 |
| 2017 Diciembre | 0 | 17 | 17 |
| 2017 Noviembre | 0 | 16 | 16 |
| 2017 Octubre | 0 | 20 | 20 |
| 2017 Septiembre | 0 | 22 | 22 |
| 2017 Agosto | 0 | 14 | 14 |
| 2017 Julio | 0 | 24 | 24 |
| 2017 Junio | 0 | 25 | 25 |
| 2017 Mayo | 0 | 20 | 20 |
| 2017 Abril | 0 | 29 | 29 |
| 2017 Marzo | 0 | 45 | 45 |
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