Cutaneous vasculitis in ulcerative colitis mimicking Henoch Schönlein purpura
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1 Journal of Crohn's and Colitis (2013) 7, e69 e73 Available online at SHORT REPORT Cutaneous vasculitis in ulcerative colitis mimicking Henoch Schönlein purpura Guilherme Trudes de Oliveira a, Sofia Simão Martins a, Mariana Deboni b, Patrícia Picciarelli c, Lúcia Maria Arruda Campos a, Adriana Almeida Jesus a, Yu Kar Ling Koda b, Clovis Artur Silva a, a Pediatric Rheumatology Unit, Children's Institute, Faculdade de Medicina da Universidade de São Paulo (FMUSP), São Paulo, Brazil b Pediatric Gastroenterology Unit, Children's Institute, FMUSP, São Paulo, Brazil c Department of Pathology, FMUSP, São Paulo, Brazil Received 2 February 2012; received in revised form 13 April 2012; accepted 1 May 2012 KEYWORDS Inflammatory bowel disease; Ulcerative colitis; Henoch Schönlein purpura; Children; Orchitis; Abdominal pain Abstract To the best of our knowledge, no cases of ulcerative colitis (UC) mimicking Henoch Schönlein purpura (HSP) have been reported so far. During a 28-year period 5635 patients were followed up at our Pediatric Rheumatology Unit and 357 had HSP according to the European League Against Rheumatism, the Paediatric Rheumatology International Trials Organisation and the Paediatric Rheumatology European Society validated classification criteria. At the same period, 148 patients with IBD according to the European Society for Paediatric Gastroenterology, Hepatology and Nutrition criteria were followed up at the Pediatric Gastroenterology Unit in our University Hospital. Only two of them had vasculitis, as an extra intestinal manifestation of UC mimicking HSP, and fulfilled both disease criteria. A 2-year old girl had bloody diarrhoea, severe abdominal pain, arthritis in ankles, petechiae and palpable purpura not related to thrombocytopenia in lower limbs. A 5-year old boy had bloody diarrhoea, palpable purpura in buttocks, lower limbs, penis and scrotum associated with arthritis in knees, orchitis in right testicle and periarticular swelling in hands and feet. Their ileocolonoscopy showed diffuse mucosal erythema, oedema, friability and multiple irregular ulcers, and histopathological examination of colonic specimen revealed diffuse chronic mucosal inflammation, crypt distortion and crypt abscesses suggesting ulcerative colitis. There were no signs of intestinal vasculitis in both cases. In conclusion, this is the first study in a paediatric population that evidenced palpable purpura associated with UC mimicking HSP European Crohn's and Colitis Organisation. Published by Elsevier B.V. All rights reserved. Corresponding author at: Rua Araioses, 152/81 Vila Madalena, São Paulo, SP, CEP , Brazil. Fax: address: clovis.silva@icr.usp.br (C.A. Silva) /$ - see front matter 2012 European Crohn's and Colitis Organisation. Published by Elsevier B.V. All rights reserved. doi: /j.crohns
2 e70 G.T. de Oliveira et al. 1. Introduction Inflammatory bowel disease (IBD) is a heterogeneous group of chronic inflammatory diseases of the intestinal tract. Crohn's disease and ulcerative colitis (UC) are the two major phenotypic forms and both may present extra intestinal manifestations. 1 Cutaneous lesions associated with IBD include erythema nodosum, pyoderma gangrenosum, vitiligo and, rarely, vasculitis. 2 Henoch Schönlein purpura (HSP), also known as anaphylactic purpura, nonthrombocytopenic purpura, rheumatic purpura or allergic purpura, is the most common type of vasculitis in children and adolescents. 3,4 It is characterized by cutaneous, articular, gastrointestinal and renal involvements, while orchitis, vasculitis of the central nervous system and pulmonary haemorrhage are rarely observed. 3 Recently, the European League Against Rheumatism (EULAR), and the Pediatric Rheumatology International Trials Organisation (PRINTO) proposed a new criteria to HSP diagnosis. 5 According to these, a patient is classified with HSP in the presence of purpura or petechiae particularly in the lower limb (mandatory criterion) and one out of four of the following findings: abdominal pain, arthritis or arthralgia, renal involvement (haematuria or proteinuria) and histopathology (leucocytoclastic vasculitis with predominant IgA deposits). 5 Of note, HSP mimicking UC has been rarely described, especially in children. 6,7 In contrast, no cases have been reported of UC mimicking HSP and the prevalence of cutaneous vasculitis in IBD patients has not been studied in a paediatric population. During a 28-year period (January 1983 to December 2011) 5635 patients were followed up at the Pediatric Rheumatology Unit of the Children's Institute, Faculdade de Medicina da Universidade de São Paulo and 357 had HSP according to EULAR/PRINTO/PRES criteria. 5 At the same period, 148 patients with IBD were followed up at the Pediatric Gastroenterology Unit in our University Hospital. They were all diagnosed according to the European Society for Paediatric Gastroenterology, Hepatology and Nutrition (ESPGHAN) criteria. 2 Only two of them had vasculitis, as an extra intestinal manifestation of UC mimicking HSP, and fulfilled both disease criteria. The local ethics committee of our Hospital approved this study. 2. Case reports 2.1. Case 1 A 2-year old girl was admitted to our University Hospital with bloody diarrhoea and severe abdominal pain associated with ankle arthritis, petechiae and palpable purpura in lower limbs. She had a previous history of intermittent bloody diarrhoea since 6 months old and an isolated episode of erythema nodosum and feet oedema. Laboratory tests performed at admission revealed a haemoglobin count of 12.0 g/dl, white blood cell count of 13,700/mm 3 and platelet count of 339,000/mm 3. The erythrocyte sedimentation rate (ESR) was 60 mm/h; C-reactive protein (CRP) was 25 mg/l, urea was 13 mg/dl and creatinine was 0.5 mg/dl. The immunological status evaluation showed IgA 230 mg/dl ( mg/dl), C3 1.3 g/dl ( g/dl) and C g/dl ( g/dl). Immunological assays were negative for serum antibodies: antinuclear antibodies (ANA), anti-doublestranded DNA (anti-ds DNA), anti-sm, anti-cardiolipin (ACL) IgM and IgG and antineutrophil cytoplasmic autoantibodies (ANCA). The HSP diagnosis was established according to EULAR/PRINTO/PRES classification criteria 5 and she was treated with prednisone (2.0 mg/kg/day) with progressive dose reduction. Two months later, while receiving 3.5 mg prednisone per day, she had a new flare of severe bloody diarrhoea, abdominal pain associated with palpable purpura, and inflammatory and painful subcutaneous nodules in lower limbs. The barium studies of small intestine revealed no abnormalities. Upper endoscopy was normal. The ileocolonoscopy obtained showed diffuse pancolonic mucosal erythema, oedema, friability and multiple irregular ulcers. The ileocecal valve was also affected with ulcers. The terminal ileum had normal aspect. Histopathologic examination of colon biopsies revealed diffuse chronic mucosal inflammation, crypt distortion and crypt abscesses suggesting UC. There was no evidence of vasculitis (Fig. 1). The skin biopsy specimens of palpable purpura lesions revealed leukocytoclastic vasculitis (Fig. 1) without positive staining for IgA in the capillaries. Therefore, the diagnosis of UC 2 mimicking was established. She was treated with prednisone (2.0 mg/kg/day), sulphasalazine and 6-mercaptopurine for two consecutive years, with improvement of all manifestations and maintenance of sulphasalazine and 6-mercaptopurine during follow-up Case 2 A 5-year old boy was admitted in our University Hospital. He had a previous history of intermittent bloody diarrhoea since the age of 6 months old and delayed growth since the age of 3 years old. A few days after admission he presented with palpable purpura in the buttocks, lower limbs (Fig. 2), penis and scrotum. There was also arthritis in both knees, and periarticular swelling in the hands and feet. The scrotum was swollen with oedema and there was tenderness of the right testicle. Laboratory tests showed haemoglobin count was 10 g/dl, white blood cell count was 17,300/mm 3, and platelet count was 417,000/mm 3, ESR was 54 mm/h and CRP was 106 mg/l. Immunological assays were negative for serum antibodies: ANA, anti-ds DNA, anti-sm, anti-acl IgM and IgG and ANCA. The immunological status evaluation showed IgG 1708 mg/dl, IgA 227 mg/dl, IgM 122 mg/dl, IgE 137 UI/mL, C g/dl and C g/dl. The HSP diagnosis was established according to EULAR/PRINTO/PRES classification criteria 5 and he received prednisone (2.0 mg/kg/day). During the follow up he was submitted to an upper endoscopy and a barium study of the small intestine, with normal results. The ileocolonoscopy revealed loss of vascular pattern, oedema, friability and granular-appearing mucosa. There were multiple fibrin-covered ulcers. This pattern was observed in all colonic segments. The ileocecal valve and terminal ileum segment were normal. The histologic examination of colonic specimens revealed diffuse chronic mucosal inflammation, with eosinophils and basal plasmocytosis, crypt distortion and crypt abscesses suggesting UC. The mucosal and submucosal vessels had normal appearance (Fig. 3). Therefore, the diagnosis of UC was defined according to ESPGHAN criteria. 2 He was treatedwithprednisone(2.0mg/kg/day), 6-mercaptopurine
3 Cutaneous vasculitis in ulcerative colitis mimicking Henoch Schönlein purpura e71 Figure 1 A. Ileum with chronic mild ileitis. B. Descending colon with chronic mild colitis. C. Skin biopsy with leukocytoclastic vasculitis. (A, B and C, haematoxylin and eosin, 200 ). D. Detail of a small vessel of dermis with perivascular infiltrate dominated by neutrophils, with destruction of vessel wall by migrating neutrophils with nuclear dust (haematoxylin and eosin, 400 ). and sulphasalazine for two months, with improvement of all the intestinal, cutaneous and articular symptoms. Sulphasalazine and 6-mercaptopurine were administered during follow-up. 3. Discussion To our knowledge, this is the first study in a paediatric population that evidenced cutaneous vasculitis associated with UC mimicking HSP. The prevalence of IBD associated with vasculitis was rarely observed in our university paediatric hospital. UC is a type of inflammatory bowel disease; a chronic illness especially characterized by digestive manifestations, especially abdominal pain, 6,7 diarrhoea and rectal bleeding. 2 As a systemic condition, the main extraintestinal involvement of UC includes: articular (arthralgia or arthritis) 2 and dermatologic Figure 2 Palpable purpura in lower limbs. (vasculitis, erythema nodosum), 8 as observed in our cases. Additionally, ocular and hepatic involvements may also be present. It is important to note that acute orchitis was observed in one of our patients, and to our knowledge this is the first case of IBD with this urologic manifestation. Orchitis occurs in 2 31% of patients with primary vasculitis, particularly Adamandiadis Behçet's disease (4 31%), HSP (7 21%) and polyarteritis nodosa (2 18%). 9 In addition, our two very young UC patients reported herein had intermittent gastrointestinal signs and symptoms, as also reported in a German-language paediatric IBD registry. 10 On the other hand, acute gastrointestinal involvement occurs in up to 62% of HSP patients 3 with disease onset varying from 4 to 10 years. 11 Furthermore, HSP has rarely been described in infants. 3 Interestingly, all of our UC patients presented cutaneous vasculitis (palpable purpura) and were initially misdiagnosed as HSP. The new EULAR/PRINTO/PRES criteria studied 827 patients worldwide, including also our Brazilian patients. The sensitivity and specificity observed according to these criteria were 100% and 87%, respectively. 5 Therefore, it seems that there are other differential diagnoses to be taken into consideration in all patients with primary or secondary vasculitis, especially with palpable purpura (most prominent or dependent on pressure-bearing surfaces). The most important differential diagnoses of palpable purpura in a paediatric population are: childhood-onset systemic lupus erythematosus, 12 juvenile dermatomyositis, 13 Churg Strauss syndrome, 14 and viral, bacterial or fungal infections, such as chronic active Epstein Barr virus infection, 15 as previously described by our paediatric rheumatology group. Vasculitis related to Crohn's disease 16,17 (as preceding, mimicking or complicating) and associated to anti-tnfα in IBD patients have been rarely reported (Table 1). The pathophysiologies of IBD, bowel vasculitis related to rheumatological
4 e72 G.T. de Oliveira et al. Figure 3 A. Rectum with chronic active colitis and cryptitis. B. Descending colon with chronic active colitis, cryptitis and crypt abscess. C. Ileum with chronic mild ileitis. (A, B and C, haematoxylin and eosin, 400 ). D. Detail of colon mucosa, without vasculitis (haematoxylin and eosin, 1000 ). disease and more specifically the HSP related bowel vasculitis are poorly understood. It is also commonplace that skin manifestations may precede IBD diagnosis for many years. In spite of our patients fulfilling the HSP and UC criteria, indicating a possible co-existence or overlap of both diseases, the histopathology of intestinal biopsies analysis confirmed only UC diagnosis and excluded intestinal vasculitis. Additionally,IgAdepositinskinbiopsyisfrequentlyobservedinHSP 5 and the absence of this immunoglobulin isotype in histopathologic analysis suggests IBD diagnosis in Case 1. Furthermore, the gastrointestinal involvement of HSP affects small and medium-sized vessels of mucosa and submucosa layers, with leucocytoclastic vasculitis and granular IgA deposition in 64% of patients. 18 Two cases of HSP had evidence of terminal ileal inflammation mimicking Crohn's disease, 6,7 and one of them presented bowel obstruction that was rarely described in this autoimmune systemic primary vasculitis. 6 A limitation that occurred in our reported cases was the absence of the rectum endoscopy pictures, although the intestinal histology alterations observed in the figures were compatible with UC in both cases. 2 Table 1 Reported cases of inflammatory bowel disease (IBD) and Henoch Schönlein purpura (HSP) in paediatric patients. Reported cases Age at diagnosis Gender Final diagnosis Cassater et al. (2006) years F CD+HSP Saulsbury and Hart (2000) years F CD+HSP Our two cases 2 and 5 years M and F UC Crohn's disease CD, ulcerative colitis UC, F female, M male. In conclusion, we have reported two cases of UC that mimic HSP with palpable purpura in lower limbs, abdominal pain, arthritis and/or orchitis, which has never been evidenced in our tertiary teaching paediatric hospital in both gastroenterology and rheumatology groups. Conflict of interest statement We declare no conflict of interest. Acknowledgments This study was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo FAPESP (grant #08/ to CAS) and by Conselho Nacional de Desenvolvimento Científico e Tecnológico CNPQ (302724/ to CAS) and Federico Foundation to CAS. Specific contribution 1. Acquisition of data GTD, SSM, LMAC, AAJ, MD, CAS 2. Drafting the article or revising it critically GTS, SSM, YKLK, CAS 3. Final approval of the version to be submitted GTD, SSM, LMAC, AAJ, MD, CAS. References 1. Ruemmele FM. Pediatric inflammatory bowel diseases: coming of age. Curr Opin Gastroenterol 2010;26: IBD Working Group of the European Society for Paediatric Gastroenterology, Hepatology and Nutrition. Inflammatory bowel disease in children and adolescents: recommendations for diagnosis the Porto criteria. J Pediatr Gastroenterol Nutr 2005;41:1 7.
5 Cutaneous vasculitis in ulcerative colitis mimicking Henoch Schönlein purpura e73 3. de Almeida JL, Campos LM, Paim LB, Leone C, Koch VH, Silva CA. Renal involvement in Henoch Schönlein purpura: a multivariate analysis of initial prognostic factors. J Pediatr (Rio J) 2007;83: Júnior CR, Yamaguti R, Ribeiro AM, Melo BA, Campos LA, Silva CA. Acute hemorrhagic edema of childhood. Acta Reumatol Port 2008;33: Ozen S, Pistorio A, Iusan SM, Bakkaloglu A, Herlin T, Brik R, et al. EULAR/PRINTO/PRES criteria for Henoch Schönlein purpura, childhood polyarteritis nodosa, childhood Wegener granulomatosis and childhood Takayasu arteritis: Ankara Part II: final classification criteria. Ann Rheum Dis 2010;69: Yavuz A, Yıldız M, Aydın A, Yıldırım AC, Buluş H, Köklü S. Henoch Schönlein purpura mimicking Crohn's ileitis. J Crohns Colitis 2011;5: Samuel S, Loftus Jr EV, Sandborn WJ. Henoch Schönlein purpura in an adult mimicking Crohn's disease and pyoderma gangrenosum. Dig Dis Sci 2011;56: Paller AS. Cutaneous changes associated with inflammatory bowel disease. Pediatr Dermatol 1986;6: Silva CA, Cocuzza M, Borba EF, Bonfá E. Cutting-edge issues in autoimmune orchitis. Clin Rev Allergy Immunol 2012;42: Timmer A, Behrens R, Buderus S, Findeisen A, Hauer A, Keller KM, et al. Childhood onset inflammatory bowel disease: predictors of delayed diagnosis from the CEDATA German-language pediatric inflammatory bowel disease registry. J Pediatr 2011;158: SohagiaAB,GunturuSG,TongTR,HertanHI.Henoch Schönlein purpura a case report and review of the literature. Gastroenterol Res Pract 2010;2010: Guissa VR, Trudes G, Jesus AA, Aikawa NE, Romiti R, Silva CA. Lupus erythematosus panniculitis in children and adolescents. Acta Reumatol Port 2012;37: Sallum AM, Silva MF, Michelin CM, Duarte RJ, Baroni RH, Aikawa NE, et al. Penile and scrotum swelling in juvenile dermatomyositis. Acta Reumatol Port 2011;36: Twardowsky AO, Paz JA, Pastorino AC, Jacob CM, Marques-Dias MJ, Silva CA. Chorea in a child with Churg Strauss syndrome. Acta Reumatol Port 2010;35: Guissa VR, Aragão PA, Marques HH, Jacob CM, Silva CA. Chronic active Epstein Barr virus infection mimicking Henoch Schönlein purpura. Acta Reumatol Port 2010;35: Cassater D, Gambaro G, Fabris A, et al. Henoch Schönlein purpura and Crohn's disease in a family. J Nephrol 2006;119: Saulsbury FT, Hart MH. Crohn's disease presenting with Henoch Schönlein purpura. JPGN 2000;31: Ebert EC. Gastrointestinal manifestations of Henoch Schönlein purpura. Dig Dis Sci 2008;53:
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