Letter to the Editor
Nodular Regenerative Hyperplasia of the Liver as a Complication of Long-standing Systemic-onset Juvenile Idiopathic Arthritis
Hiperplasia nodular regenerativa hepática como complicación tardía de la artritis idiopática juvenil de inicio sistémico
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A mayor aumento, los sinusoides se encuentran comprimidos por las placas hepatocitarias engrosadas (hematoxilina-eosina 40×) (B). En la tomografía computarizada abdominal, se evidencia la dilatación de la vena porta y sus ramas (flecha) (C).</p>" ] ] ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "Walter Alberto Sifuentes Giraldo, Ana Burdaspal Moratilla, Alberto Moreno Caparrós, María Luz Gámir Gámir" "autores" => array:4 [ 0 => array:2 [ "nombre" => "Walter Alberto" "apellidos" => "Sifuentes Giraldo" ] 1 => array:2 [ "nombre" => "Ana" "apellidos" => "Burdaspal Moratilla" ] 2 => array:2 [ "nombre" => "Alberto" "apellidos" => "Moreno Caparrós" ] 3 => array:2 [ "nombre" => "María Luz" "apellidos" => "Gámir Gámir" ] ] ] ] ] "idiomaDefecto" => "es" "Traduccion" => array:1 [ "en" => array:9 [ "pii" => "S2173574314000148" "doi" => "10.1016/j.reumae.2013.09.001" "estado" => "S300" "subdocumento" => "" "abierto" => array:3 [ "ES" => false "ES2" => false "LATM" => false ] "gratuito" => false "lecturas" => array:1 [ "total" => 0 ] "idiomaDefecto" => "en" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S2173574314000148?idApp=UINPBA00004M" ] ] "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S1699258X1300199X?idApp=UINPBA00004M" "url" => "/1699258X/0000001000000003/v1_201405040016/S1699258X1300199X/v1_201405040016/es/main.assets" ] ] "itemSiguiente" => array:19 [ "pii" => "S217357431300138X" "issn" => "21735743" "doi" => "10.1016/j.reumae.2013.12.007" "estado" => "S300" "fechaPublicacion" => "2014-05-01" "aid" => "598" "copyright" => "Elsevier España, S.L." 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"autores" => array:1 [ 0 => array:4 [ "autoresLista" => "Walter Alberto Sifuentes Giraldo, Ana Burdaspal Moratilla, Alberto Moreno Caparrós, María Luz Gámir Gámir" "autores" => array:4 [ 0 => array:4 [ "nombre" => "Walter Alberto" "apellidos" => "Sifuentes Giraldo" "email" => array:1 [ 0 => "albertosifuentesg@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" => "Ana" "apellidos" => "Burdaspal Moratilla" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] ] ] 2 => array:3 [ "nombre" => "Alberto" "apellidos" => "Moreno Caparrós" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] ] ] 3 => array:3 [ "nombre" => "María Luz" "apellidos" => "Gámir Gámir" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] ] ] ] "afiliaciones" => array:2 [ 0 => array:3 [ "entidad" => "Unidad de Reumatología Pediátrica, Servicio de Reumatología, Hospital Universitario Ramón y Cajal, Madrid, Spain" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Servicio de Anatomía Patológica, Hospital Universitario Ramón y Cajal, Madrid, Spain" "etiqueta" => "b" "identificador" => "aff0010" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Hiperplasia nodular regenerativa hepática como complicación tardía de la artritis idiopática juvenil de inicio sistémico" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0005" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 345 "Ancho" => 1400 "Tamanyo" => 160504 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Liver biopsy in which a hyperplastic nodular zone (arrowheads) partially surrounded by dilated sinusoids (arrow) and absence of fibrosis (hematoxylin–eosin 2×) (A) is observed. At higher magnification, the sinusoids are compressed by the thickened hepatocyte plaques (hematoxylin–eosin 40×) (B). An abdominal CT scan shows dilation of the portal vein and its branches (arrow) (C).</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0005" class="elsevierStylePara elsevierViewall">Hepatic nodular regenerative hyperplasia (HNRH) is an entity characterized by a diffuse, benign transformation of the hepatic parenchyma into small regenerative nodules, which can lead to the development of non-cirrhotic portal hypertension (PH). It has been associated with several disorders, mainly autoimmune and hematologic diseases and immunosuppressive drugs, including azathioprine and cyclophosphamide.<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> The HNRH has been described in RA/Felty's syndrome, systemic lupus erythematosus (SLE), antiphospholipid syndrome (APS), Sjögren's syndrome, systemic sclerosis, sarcoidosis, polyarteritis nodosa and mixed cryoglobulinemia.<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1–3</span></a> However, only one case has been reported in systemic onset juvenile idiopathic arthritis (JIA).<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">A 33-year-old male was diagnosed with systemic onset JIA at 5 years of age based on fever, evanescent rash, joint pain, recurrent pericarditis, elevated acute phase reactants (C-reactive protein 22.5<span class="elsevierStyleHsp" style=""></span>mg/dl and erythrocyte sedimentation rate 39<span class="elsevierStyleHsp" style=""></span>mm/h) and negative for rheumatoid factor, antinuclear antibodies and HLA-B27. He was initially treated with low doses of corticosteroids and methotrexate 10<span class="elsevierStyleHsp" style=""></span>mg/week, but the latter was suspended at 20 years of age due to neurotoxicity. Since then, he has received varying doses of corticosteroids alone, maintaining an active disease, with a mild increase in alanine aminotransferase (ALT) (72<span class="elsevierStyleHsp" style=""></span>U/l), gamma-glutamyl transferase (GGT) (171<span class="elsevierStyleHsp" style=""></span>U/l) and alkaline phosphatase (AP) (146<span class="elsevierStyleHsp" style=""></span>U/l), in addition to thrombocytopenia (117×10<span class="elsevierStyleSup">3</span>/μl) with normal bone marrow study. Ultrasonography and abdominal computed tomography showed mild splenomegaly with no signs of PH. Tocilizumab (8<span class="elsevierStyleHsp" style=""></span>mg/kg every 14 days) was initiated in January 2011, with rapid improvement of systemic symptoms and standardization of the reactants. However, after the third infusion he presented worsening liver function, doubling previous levels of ALT and GGT, increasing aspartate aminotransferase (AST) (79<span class="elsevierStyleHsp" style=""></span>U/l) and total bilirubin (TB) (3.51<span class="elsevierStyleHsp" style=""></span>mg/dl) levels, presenting hypofibrinogenemia (122<span class="elsevierStyleHsp" style=""></span>mg/dl), abnormal INR (1.5) and an increase in the severity of thrombocytopenia (57×10<span class="elsevierStyleSup">3</span>/μl). He was admitted to the hospital with suspected Macrophage Activation Syndrome. The patient had not concomitantly received NSAIDs or other potentially hepatotoxic drugs. Serologic testing for hepatitis viruses B and C, Epstein Barr virus and human immunodeficiency virus were negative, and a bone marrow biopsy showed reactive changes and no hemophagocytosis. Endoscopy revealed the presence of grade <span class="elsevierStyleSmallCaps">i</span>–<span class="elsevierStyleSmallCaps">ii</span> esophageal varices and a biopsy confirmed the diagnosis of HNRH (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>A and B). Tocilizumab was suspended permanently, with normalization of AST, TB, fibrinogen and INR, but the levels of ALT, GGT, AP and thrombocytopenia remained unchanged. In successive imaging controls, an increased diameter of the portal vein (17<span class="elsevierStyleHsp" style=""></span>mm) was observed (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>C), with no evidence of thrombosis. Currently, the patient receives only steroids at a variable dose, with mild to moderate activity of JIA and without developing other complications of PH.</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0015" class="elsevierStylePara elsevierViewall">HNRH pathogenesis is unknown, but it is considered a nonspecific tissue adaptive response to an altered distribution of hepatic vascular flow with a multifactorial cause.<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">5</span></a> Among the identified factors which can cause this condition are thrombosis (thrombophilia, malignancies, myeloproliferative disorders, APS) and endothelial cell injury in the portal venules and hepatic sinusoids (drugs, autoimmune diseases, and viruses).<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> In this case, the underlying disease and drug therapy could have been involved. The chronic inflammatory state secondary to the long duration of systemic onset JIA is associated with high circulating levels of proinflammatory cytokines such as interleukin 6 (IL-6), which has been implicated in the development of HNRH.<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">6</span></a> This cytokine is important in the proliferation of hepatocytes and liver regeneration.<a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">7</span></a> However, transgenic mice expressing high levels of IL-6 and its soluble receptor (sIL-6R) exhibit hepatocellular hyperplastic nodules around the portal tracts, as do patients with HNRH.<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">6</span></a> There is also clinical evidence that the increase in IL-6 is associated HNRH in Castleman's disease.<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a> Other HNRH related disorders, such as SLE and hematological malignancies, have high levels of the IL-6/sIL-6R complex.<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">6</span></a> Although patients with systemic onset JIA have a higher concentration of these complexes.<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> HNRH has rarely been described in this disease, with only the case of a 17-year-old patient with hepatomegaly and PH<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a> having been published, but this is probably due to an underdiagnosis of this condition.<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> Drugs are also associated with the development of HNRH, mainly thiopurines (azathioprine, 6-mercaptopurine, 6-thioguanine), cyclophosphamide, busulfan, oxaliplatin and antiretroviral drugs.<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> Our patient did not receive any of these agents but was treated for 15 years with methotrexate, a drug that has been associated with hepatotoxicity and liver fibrosis but not HNRH, with only one case found in the literature of a patient with adult-onset Still's disease treated simultaneously with azathioprine and glucocorticoids, attributing its development to the combination of the latter 2 drugs,<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a> and another in a patient with Felty's syndrome who was diagnosed with HNRH after receiving methotrexate for a short period of time, leading the authors to conclude that there was no association.<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">11</span></a> This case also received varying doses of corticosteroids for 28 years. The association of these drugs with HNRH<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a> through an unknown mechanism has been suggested. However, chronic corticosteroid therapy is associated with the development of vascular lesions in autoimmune diseases, which could contribute to the development of liver vascular flow alterations that lead to the development of HNRH.</p><p id="par0020" class="elsevierStylePara elsevierViewall">The possibility of HNRH should be considered in patients with symptomatic PH (splenomegaly, ascites, esophageal varices), who have normal transaminases and no manifestations of cirrhosis. HNRH is estimated to represent 27% of all cases of non-cirrhotic PH in Europe, but its diagnosis suffers a significant delay because only 50% have a PH and 11%–25% have only mildly elevated liver enzymes, generally AP.<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> Our case probably developed HNRH insidiously during the prolonged course of systemic onset JIA and the emergence of hepatotoxicity during administration of tocilizumab finally led to the diagnosis, when the patient developed PH. Imaging tests have poor sensitivity and specificity for detecting HNRH, so a definitive diagnosis requires histologic confirmation.<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> Treating HNRH focuses on correcting the underlying cause (autoimmune disease, hematologic disorder, drugs) and, in patients in whom PH has developed, preventing and treating the complications, with esophageal varices bleeding constituting the leading cause of mortality in these patients.<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> In conclusion, HNRH is a complication that can occur during the development of autoimmune diseases, including systemic onset JIA, so it should be considered in cases with a persistent abnormal liver profile, even without other data from PH.</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: Sifuentes Giraldo WA, Burdaspal Moratilla A, Moreno Caparrós A, Gámir Gámir ML. Hiperplasia nodular regenerativa hepática como complicación tardía de la artritis idiopática juvenil de inicio sistémico. Reumatol Clin. 2014;10:194–195.</p>" ] ] "multimedia" => array:1 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 345 "Ancho" => 1400 "Tamanyo" => 160504 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Liver biopsy in which a hyperplastic nodular zone (arrowheads) partially surrounded by dilated sinusoids (arrow) and absence of fibrosis (hematoxylin–eosin 2×) (A) is observed. At higher magnification, the sinusoids are compressed by the thickened hepatocyte plaques (hematoxylin–eosin 40×) (B). 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| Year/Month | Html | Total | |
|---|---|---|---|
| 2024 November | 6 | 2 | 8 |
| 2024 October | 52 | 19 | 71 |
| 2024 September | 60 | 18 | 78 |
| 2024 August | 69 | 31 | 100 |
| 2024 July | 47 | 30 | 77 |
| 2024 June | 66 | 30 | 96 |
| 2024 May | 56 | 32 | 88 |
| 2024 April | 56 | 25 | 81 |
| 2024 March | 48 | 27 | 75 |
| 2024 February | 37 | 22 | 59 |
| 2024 January | 41 | 21 | 62 |
| 2023 December | 34 | 27 | 61 |
| 2023 November | 52 | 29 | 81 |
| 2023 October | 55 | 31 | 86 |
| 2023 September | 74 | 31 | 105 |
| 2023 August | 42 | 9 | 51 |
| 2023 July | 43 | 25 | 68 |
| 2023 June | 50 | 17 | 67 |
| 2023 May | 65 | 28 | 93 |
| 2023 April | 40 | 10 | 50 |
| 2023 March | 48 | 26 | 74 |
| 2023 February | 60 | 33 | 93 |
| 2023 January | 58 | 27 | 85 |
| 2022 December | 68 | 28 | 96 |
| 2022 November | 54 | 28 | 82 |
| 2022 October | 82 | 27 | 109 |
| 2022 September | 62 | 22 | 84 |
| 2022 August | 55 | 50 | 105 |
| 2022 July | 42 | 39 | 81 |
| 2022 June | 53 | 32 | 85 |
| 2022 May | 54 | 45 | 99 |
| 2022 April | 67 | 44 | 111 |
| 2022 March | 69 | 46 | 115 |
| 2022 February | 53 | 25 | 78 |
| 2022 January | 79 | 40 | 119 |
| 2021 December | 35 | 44 | 79 |
| 2021 November | 55 | 50 | 105 |
| 2021 October | 150 | 40 | 190 |
| 2021 September | 136 | 46 | 182 |
| 2021 August | 43 | 34 | 77 |
| 2021 July | 54 | 36 | 90 |
| 2021 June | 50 | 51 | 101 |
| 2021 May | 58 | 29 | 87 |
| 2021 April | 121 | 58 | 179 |
| 2021 March | 88 | 12 | 100 |
| 2021 February | 69 | 27 | 96 |
| 2021 January | 55 | 18 | 73 |
| 2020 December | 52 | 12 | 64 |
| 2020 November | 49 | 20 | 69 |
| 2020 October | 34 | 16 | 50 |
| 2020 September | 36 | 26 | 62 |
| 2020 August | 41 | 27 | 68 |
| 2020 July | 19 | 25 | 44 |
| 2020 June | 29 | 29 | 58 |
| 2020 May | 23 | 14 | 37 |
| 2020 April | 35 | 17 | 52 |
| 2020 March | 19 | 8 | 27 |
| 2018 July | 1 | 0 | 1 |
| 2018 May | 6 | 2 | 8 |
| 2018 April | 31 | 15 | 46 |
| 2018 March | 49 | 12 | 61 |
| 2018 February | 27 | 10 | 37 |
| 2018 January | 28 | 9 | 37 |
| 2017 December | 31 | 3 | 34 |
| 2017 November | 40 | 8 | 48 |
| 2017 October | 24 | 7 | 31 |
| 2017 September | 36 | 16 | 52 |
| 2017 August | 57 | 15 | 72 |
| 2017 July | 46 | 9 | 55 |
| 2017 June | 80 | 13 | 93 |
| 2017 May | 76 | 10 | 86 |
| 2017 April | 71 | 4 | 75 |
| 2017 March | 66 | 8 | 74 |
| 2017 February | 30 | 6 | 36 |
| 2017 January | 36 | 7 | 43 |
| 2016 December | 62 | 18 | 80 |
| 2016 November | 47 | 7 | 54 |
| 2016 October | 74 | 15 | 89 |
| 2016 September | 49 | 7 | 56 |
| 2016 August | 63 | 23 | 86 |
| 2016 July | 30 | 12 | 42 |
| 2015 December | 2 | 0 | 2 |
| 2015 September | 2 | 0 | 2 |
| 2015 August | 1 | 0 | 1 |
| 2015 July | 12 | 6 | 18 |
| 2015 June | 32 | 13 | 45 |
| 2015 May | 57 | 19 | 76 |
| 2015 April | 74 | 18 | 92 |
| 2015 March | 75 | 14 | 89 |
| 2015 February | 72 | 6 | 78 |
| 2015 January | 69 | 25 | 94 |
| 2014 December | 40 | 21 | 61 |
| 2014 November | 37 | 11 | 48 |
| 2014 October | 43 | 12 | 55 |
| 2014 September | 37 | 28 | 65 |
| 2014 August | 63 | 14 | 77 |
| 2014 July | 38 | 15 | 53 |
| 2014 June | 59 | 25 | 84 |
| 2014 May | 41 | 15 | 56 |
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