Kaposi's sarcoma: An opportunistic infection by human herpesvirus-8 in ulcerative colitis
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1 Journal of Crohn's and Colitis (2010) 4, available at SHORT REPORT Kaposi's sarcoma: An opportunistic infection by human herpesvirus-8 in ulcerative colitis María Rodríguez-Peláez a, María Soledad Fernández-García b, Natalia Gutiérrez-Corral c, Ruth de Francisco a, Sabino Riestra a,, Carmen García-Pravia b, José Ignacio Rodríguez c, Luis Rodrigo a a Department of Gastroenterology, Hospital Universitario Central de Asturias, Oviedo, Asturias, Spain b Department of Pathology, Hospital Universitario Central de Asturias, Oviedo, Asturias, Spain c Department of General Surgery, Hospital Universitario Central de Asturias, Oviedo, Asturias, Spain Received 17 February 2010; received in revised form 31 March 2010; accepted 31 March 2010 KEYWORDS Ulcerative colitis; Immunosuppressive treatment; Kaposi's sarcoma; Human herpesvirus-8; Opportunistic infections; Inflammatory bowel disease Abstract Kaposi's sarcoma is a vascular tumor caused by human herpesvirus-8 infection. Iatrogenic Kaposi's sarcoma often occurs in patients receiving immunosuppressive therapy. To date, a few cases of colonic Kaposi's sarcoma have been reported in ulcerative colitis patients treated with immunomodulators. We describe a 65-year-old male diagnosed with left-sided ulcerative colitis who was treated with methotrexate and low-dose steroids for greater than 6 years. He presented with several papular, violet lesions on both legs. Colonoscopy revealed the presence of multiple reddish, elevated lesions in the sigmoid colon and rectum. Histological evaluation of skin and colonic biopsies showed findings suggestive of Kaposi's sarcoma; immunohistochemistry for human herpesvirus-8 was positive in the colonic lesions. To avoid the need for further immunosuppressive treatment, the patient underwent a colectomy. Following immunomodulator discontinuation, the patient experienced spontaneous regression of his skin lesions. With the present case, we wish to stress the important interaction of immunosuppressive therapy (mainly corticosteroids) used in ulcerative colitis patients in relation to the development of colonic Kaposi's sarcoma. Human herpesvirus-8 infection should be recognized as a possible opportunistic infection in patients with inflammatory bowel disease European Crohn's and Colitis Organisation. Published by Elsevier B.V. All rights reserved. 1. Introduction Kaposi's sarcoma (KS) is a vascular tumor that arises predominantly in the skin but which can also affect internal Abbreviations (KS), Kaposi's sarcoma; (HHV-8), human herpesvirus-8; (UC), ulcerative colitis; (IBD), inflammatory bowel disease. Corresponding author. Tel.: ; fax: address: sriestram7@hotmail.com (S. Riestra). organs. Four KS variants have been described, each with distinct clinical and epidemiological characteristics: the classic or sporadic form: a symptomless tumor affecting the elderly in Mediterranean countries an endemic form found in African people an epidemic form related to HIV infection and AIDS an iatrogenic form associated with immunosuppressive therapy /$ - see front matter 2010 European Crohn's and Colitis Organisation. Published by Elsevier B.V. All rights reserved. doi: /j.crohns
2 Kaposi's sarcoma and ulcerative colitis 587 In 1994, Chang et al. 2 identified DNA sequences of a new herpes virus in KS tissue samples. This virus was termed human herpesvirus-8 (HHV-8), and has been detected in all four epidemiological variants of the disease. 3 Iatrogenic KS has mainly been described as occurring in kidney and liver transplant recipients, 4 although cases have also been reported in patients with autoimmune diseases. 5,6 In every case the development of KS was associated with the use of immunosuppressive drugs and, in most cases, tumor regression was observed following the discontinuation of immunosuppressive therapy. Patients with inflammatory bowel disease (IBD) often receive long-term immunomodulator therapy with medications such as steroids, azathioprine, and methotrexate. Several cases of colonic KS have been reported in ulcerative colitis (UC) patients whose only risk factor was the previous administration of immunosuppressives To date, a minority of these cases has been associated with HHV-8 infection Recently, a consensus document was published on the prevention, diagnosis and management of opportunistic infections in IBD patients. 13 This document addresses the role of selected chronic viral infections in the development of different tumors, such as Epstein-Barr virus/lymphoma and human papillomavirus/cervical cancer, in patients receiving long-term immunomodulator treatment. The present study describes a new case of colonic KS in a patient with UC, and serves to underscore the role of HHV-8 infection in the development of a neoplasm in these immunosuppressed patients. 2. Case report A 65-year-old male was diagnosed with left-sided UC and seronegative spondyloarthropathy in November Given the need for continued steroid treatment, immunomodulator therapy was also indicated; however, azathioprine and 6- mercaptopurine were discontinued due to gastrointestinal intolerance. Methotrexate was initiated in June 2001 and maintained until November 2007, when it was suspended to prevent potential treatment-related toxicities; during this period, the patient required continuous treatment with prednisone (5 mg/day). In 1996 and 2000, endoscopic exploration of the colon provided data regarding macroscopic and histological disease activity. In August 2008, the patient experienced an acute disease flare and was admitted to the hospital for intravenous steroid therapy. During his hospital stay, violaceous reddish-brown nodules developed on both legs. Samples of the skin lesions were obtained; hepatitis C and B, HIV and syphilis serological testing proved negative. Colonoscopy demonstrated active UC and the presence of multiple reddish, elevated lesions in the last 25 cm of the colon that were biopsied. A thoracoabdominal CT scan revealed thickening of the rectum and sigmoid colon walls, without evidence of adenopathy or other lesions. Histological studies of the skin revealed a small, nonencapsulated dermal lesion composed of dilated, irregular and spiculated blood vessels lined by scantly prominent endothelial cells, associated with an infiltrate composed of lymphocytes and hemosiderin-containing macrophages. Immunohistochemical analysis with CD31 and CD34 showed labeling of the vascular endothelial cells; immunohistochemistry for the detection of HHV-8, using a murine monoclonal antibody directed against the C-terminus of the latent nuclear antigen-1 molecule of HHV-8 (Novocastra Laboratories, Newcastle, UK), proved negative. The Ki67 proliferation index was less than 2%. The morphological findings were suggestive of KS, although the immunohistochemistry did not support this final diagnosis. Thus, the patient was ultimately diagnosed with a pseudo-kaposi type lesion. Colonic biopsies were consistent with UC. The lamina propria demonstrated focal proliferation of cleft-shaped vessels showing frequent extravasation, extending to the muscularis mucosae. Immunohistochemical studies with CD34 and CD31 were positive and the staining for HHV-8 revealed moderate and focal nuclear positivity. A preliminary diagnosis of colonic KS was made. Anti-HHV-8 serology, using an indirect immunofluorescence assay, achieved an IgG antibody titer of 1/40. Given the existence of steroid-dependent UC and KS a proctocolectomy was decided to be the definitive treatment. The surgical specimen confirmed the presence, in the sigmoid colon and rectum, of multiple reddish-black nodular lesions, limited to the submucosa although with focal involvement of the muscular layer. HHV-8 labeling proved positive (Fig. 1). The remainder of the colon demonstrated no tumorous lesions and there was no lymph node involvement. The final diagnosis was multifocal KS of the colon. Following surgery and steroid withdrawal, the patient's skin lesions resolved. At 12 months of follow-up, the patient remains free of symptoms, and no further skin lesions have appeared. 3. Discussion We report a case of iatrogenic KS of the colon in an UC patient previously treated with immunosuppressive drugs (steroids and methotrexate). To date, the association between UC and colonic KS in patients known to be free of HIV infection has been reported in only 6 male patients 7 12 (Table 1). In all cases, the patients clinical course was chronic-intermittent or chronic-continuous and corticosteroids were warranted to control the flares; two patients were receiving a combination of corticosteroids with other immunosuppressives such as cyclosporine 11 and azathioprine. 12 Our patient was prescribed prolonged concomitant treatment with methotrexate. In all of the published cases of KS in UC patients, steroid treatment was ubiquitous and neither the dose nor the duration of treatment appeared to influence tumor development, as both parameters varied greatly among cases. In previously described patients, the diagnosis of colonic KS was established post-surgically. Although in two cases 7,10 the existence of skin KS was known, the indication for colectomy was based on the poor response of UC to medical treatment or on the suspicion of a rectal tumor. Our case is the first in which colonic KS was diagnosed prior to colectomy; the presence of the typical KS skin lesions led us to specifically investigate whether they were evident in the endoscopic colonic samples. Colonic KS in patients with UC may be difficult to diagnose, because there are no specific symptoms, and the presence of the characteristic skin lesions has been documented in only three of the 7 cases; alternatively, the mainly submucosal involvement
3 588 M. Rodríguez-Peláez et al. Figure. 1 A Macroscopic view showing a reddened mucosa of angiomatous appearance. B CD31 labeling showing numerous vessels grouped in the lamina propria. X200. C Numerous cleft-shaped vessels in the lamina propria (arrows). Hematoxylin-eosin, X200. D Immunohistochemical labeling for HHV-8 (arrows). X400. may indicate that endoscopic biopsies are insufficient for establishing the diagnosis. HHV-8 infection is the underlying cause of all four epidemiological forms of KS. 3 The prevalence of HHV- 8 infection varies significantly by geography, race/ethnicity and risk group. The highest HHV-8 prevalence is found in groups with a high incidence of KS, such as sub-saharan Africans, individuals in Mediterranean countries, and individuals who are infected with HIV. 14 HHV-8 is mainly transmitted through sexual contact, although parenteral (blood-borne, organ transplantation) and horizontal transmission have also been reported mainly in areas where KS is endemic. 15 Of note is the fact that our patient did not belong to any of the previously described risk groups; in Spain, the seroprevalence of HHV-8 varies from 0% in children to 6.5% in blood donors. 16 There is limited data on HHV-8 infection in IBD patients. In a series of 24 UC patients who underwent colectomy due to resistance to medical treatment, HHV-8 was not detected by PCR testing in bowel tissue. 17 On the other hand, in a group of 60 patients with Crohn's disease assigned to receive infliximab Table 1 Characteristics of the patients with ulcerative colitis and Kaposi's sarcoma of the colon, without HIV infection associated. Authors and references Meltzer 7 Thompson 8 Tedesco 9 Bursics 10 Girelli 11 Svrcek 12 Present study Clinical characteristics Gender Male Male Male Male Male Male Male Age (years) UC extension Left Extensive Extensive Unknown Left Left Left UC duration (years) b b Immunosuppressive drug Steroids Steroids Steroids Steroids Steroids/ cyclosporine Steroids/ azathioprine Steroids/ methotrexate Skin lesion Yes Non Non Yes Non Non Yes HHV-8 status ND ND ND Skin: + Skin: Colon: Colon: + Colon: + Colon: + Serum: Serum: - Serum: + Serum: + UC: ulcerative colitis ; HHV-8: human herpes virus-8 ; and ND : not done.
4 Kaposi's sarcoma and ulcerative colitis 589 therapy, the presence of HHV-8 likewise could not be demonstrated by serum PCR. 18 HHV-8 and HIV co-infection has been associated with a 30% risk of developing KS within 10 years 19 ; although the risk of KS in patients with IBD receiving immunosuppressive treatment is very low, knowledge of HHV-8 serological status could help to define a subgroup of individuals at risk of developing KS. Iatrogenic KS is associated with immunosuppressive therapy. Similar to other viruses of the herpes family, HHV- 8 remains in a latent stage following primary infection and may undergo reactivation in individuals who are immunosuppressed. It has been recently observed that a lytic viral gene encoding for vgpcr (G protein coupled to the receptor) plays a key role in the genesis of KS. 20,21 A finding that supports the significant role of immune suppression in the development of KS is the fact that the characteristic skin lesions regress after stopping immunosuppressor therapy in both kidney transplant 22 and in UC patients 7,10 despite the persistence of HHV- 8DNA. 23 In our case, a colectomy was considered less a local treatment for colonic KS than an obligate measure to avoid the need for immunosuppressive treatment. Currently, the diagnosis of KS requires clinical and histologic evaluation; however, knowledge of its association with HHV-8 has made the detection of such infections important for the management of these patients. HHV- 8 infection can be identified by molecular (PCR) and serological methods (ELISA, IFA, Western blot, and immunohistochemistry). Immunohistochemistry has been used to locate HHV-8 proteins and to assess the involvement of HHV- 8 in malignancies. Thus, the expression of a specific HHV- 8 gene, in particular latent nuclear antigen-1 detection, 24 has led to clinical applications for the diagnosis of KS in tissue samples 25. In our case, immunohistochemistry for HHV-8 was decisive in confirming colonic KS. With this case, we wish to stress the importance of steroid therapy used in UC patients in relation to the development of KS. This tumor is associated with HHV-8 infection; consequently, this virus should be included among the possible opportunistic infections associated with immune suppression in patients with IBD. Since skin involvement is not frequent and the clinical and endoscopic findings may be similar to those of the inflammatory disease itself, a high degree of clinical suspicion is needed to diagnosis these patients. Acknowledgements Each author has participated sufficiently, intellectually or practically, in the work to take public responsibility for the content of the article, including the conception, design, and data interpretation. R-PM, defr, RS and RL provided clinical advice and consultation and participated in the design of the report; G-CN and RJI were the treating surgeons; F-GMS and G-PC performed the pathological studies; and R-PM, F-GMS and RS drafted the manuscript. All authors have read and approved the final manuscript. References 1. Antman K, Chang Y. Kaposi's sarcoma. N Engl J Med 2000;342: Chang Y, Cesarman E, Pessin MS, Lee F, Culpepper J, Knowles DM, et al. Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science 1994;266: Ablashi DV, Chatlynne LG, Whitman Jr JE, Cesarman E. Spectrum of Kaposi's sarcoma-associated herpesvirus, or human herpesvirus 8, diseases. Clin Microbiol Rev 2002;15: García- Astudillo LA, Leyva-Cobián F. Human herpesvirus- 8 infection and Kaposi s sarcoma after liver and kidney transplantation in different geographical areas of Spain. Transpl Immunol 2006;17: Trattner A, Hodak E, David M, Sandbank M. The appearance of Kaposi sarcoma during corticosteroid therapy. Cancer 1993;72: Klein MB, Pereira FA, Kantor I. Kaposi sarcoma complicating systemic lupus erythematosus treated with immunosuppression. Arch Dermatol 1974;110: Meltzer SJ, Rotterdam HZ, Korelitz BI. Kaposi's sarcoma in association with ulcerative colitis. Am J Gastroenterol 1987;82: Thompson GB, Pemberton JH, Morris S, Bustamante MA, Delong B, Carpenter HA, et al. Kaposi's sarcoma of the colon in a young HIV negative man with chronic ulcerative colitis. Report of a case. Dis Colon Rectum 1989;32: Tedesco M, Benevolo M, Frezza F, Mancini R, Carone MD, Mottolese M, et al. Colorectal Kaposi's sarcoma in an HIVnegative male in association with ulcerative rectocolitis: a case report. Anticancer Res 1999;19: Bursics A, Morvay K, Abrahám K, Marschalkó M, Kardos M, Járay B, et al. HHV-8 positive, HIV negative disseminated Kaposi's sarcoma complicating steroid dependent ulcerative colitis: a successfully treated case. Gut 2005;54: Serio G, Girelli CM, Rocca E, Rocca F. Refractory ulcerative colitis and iatrogenic colorectal Kaposi's sarcoma. Dig Liver Dis 2009;41(2): Svrcek M, Tiret E, Bennis M, Guyot P, Fléjou JF. KSHV/HHV8- Associated Intestinal Kaposi's sarcoma in patient with ulcerative colitis receiving immunosuppresive drugs: report of a case. Dis Colon Rectum 2009;52: Rahier JF, Ben-Horin S, Chowers Y, Conlon C, de Munter P, D Haens G, et al. European evidence-based Consensus on the prevention, diagnosis and management of opportunistic infections in inflammatory bowel disease. J Crohn s Colitis 2009;3: Edelman DC. Human herpesvirus-8. A novel human pathogen. Virol J 2005;2: Guttman-Yassky E, Kra-Oz Z, Dubnov J, Friedman-Birnbaum R, Segal I, Zaltzman N, et al. 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5 590 M. Rodríguez-Peláez et al. 21. Sodhi A, Chaisuparat R, Hu J, Ramsdell AK, Manning BD, Sausville EA, et al. The TSC2/mTOR pathway drives endothelial cell transformation induced by the Kaposi's sarcoma-associated herpesvirus G protein-coupled receptor. Cancer Cell 2006;10: Wijnveen AC, Persson H, Björck S, Blohmé I. Disseminated Kaposi's sarcoma-full regression after withdrawal of immunosuppressive therapy:report of a case. Transplant Proc 1987;19: Nagy S, Gyulai R, Kemeny L, Szenohradszky P, Dobozy A. Iatrogenic Kaposi's sarcoma. HHV8 positivity persists but the tumours regress almost completely without immunosupresive therapy. Transplant 2000;69: Rainbow L, Platt GM, Simpson GR, Sarid R, Gao SJ, Stoiber H, et al. The 222 -to 234-kilodalton latent nuclear protein (LNA) of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) is encoded by orf73 and is a component of the latencyassociated nuclear antigen. J Virol 1997;71: Cheuk W, Wong KO, Wong CS, Dinkel JE, Ben-Dor D, Chan JK. Immunostaining for human herpesvirus 8 latent nuclear antigen- 1 helps distinguish Kaposi sarcoma from its mimickers. Am J Clin Pathol 2004;121:
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