Primary hepatic Epstein–Barr virus-positive diffuse large B-cell lymphoma associated with azathioprine immunosuppression: a case report

go back to reference Cartwright SL, Knudson MP. Diagnostic imaging of acute abdominal pain in adults. Am Fam Physician. 2015;91(7):452–9.PubMed Cartwright SL, Knudson MP. Diagnostic imaging of acute abdominal pain in adults. Am Fam Physician. 2015;91(7):452–9.PubMed

go back to reference Marrero JA, Ahn J, Rajender Reddy K, Americal College of Gastroenterology. ACG clinical guideline: the diagnosis and management of focal liver lesions. Am J Gastroenterol. 2014;109(9):1328–47. https://doi.org/10.1038/ajg.2014.213.CrossRefPubMed Marrero JA, Ahn J, Rajender Reddy K, Americal College of Gastroenterology. ACG clinical guideline: the diagnosis and management of focal liver lesions. Am J Gastroenterol. 2014;109(9):1328–47. https://​doi.​org/​10.​1038/​ajg.​2014.​213.CrossRefPubMed

go back to reference Penn I, Starzl TE. Immunosuppression and cancer. Transplant Proc. 1973;5(1):943–7.PubMedPubMedCentral Penn I, Starzl TE. Immunosuppression and cancer. Transplant Proc. 1973;5(1):943–7.PubMedPubMedCentral

go back to reference Busnach G, Piselli P, Arbustini E, Baccarani U, Burra P, Carrieri MP, Citterio F, De Juli E, Bellelli S, Pradier C, Rezza G, Serraino D, Immunosuppression and Cancer Study Group. Immunosuppression and cancer: a comparison of risks in recipients of organ transplants and in HIV-positive individuals. Transplant Proc. 2006;38(10):3533–5. https://doi.org/10.1016/j.transproceed.2006.10.144.CrossRefPubMed Busnach G, Piselli P, Arbustini E, Baccarani U, Burra P, Carrieri MP, Citterio F, De Juli E, Bellelli S, Pradier C, Rezza G, Serraino D, Immunosuppression and Cancer Study Group. Immunosuppression and cancer: a comparison of risks in recipients of organ transplants and in HIV-positive individuals. Transplant Proc. 2006;38(10):3533–5. https://​doi.​org/​10.​1016/​j.​transproceed.​2006.​10.​144.CrossRefPubMed

go back to reference Beral V, Newton R. Overview of the epidemiology of immunodeficiency-associated cancers. J Natl Cancer Inst Monogr. 1998;23:1–6. https://doi.org/10.1093/oxfordjournals.jncimonographs.a024164.CrossRef Beral V, Newton R. Overview of the epidemiology of immunodeficiency-associated cancers. J Natl Cancer Inst Monogr. 1998;23:1–6. https://​doi.​org/​10.​1093/​oxfordjournals.​jncimonographs.​a024164.CrossRef

go back to reference Sehn LH, Gascoyne RD. Diffuse large B-cell lymphoma: optimizing outcome in the context of clinical and biologic heterogeneity. Blood. 2015;125(1):22–32. https://doi.org/10.1182/blood-2014-05-577189.CrossRefPubMed Sehn LH, Gascoyne RD. Diffuse large B-cell lymphoma: optimizing outcome in the context of clinical and biologic heterogeneity. Blood. 2015;125(1):22–32. https://​doi.​org/​10.​1182/​blood-2014-05-577189.CrossRefPubMed

go back to reference Martelli M, Ferreri AJ, Agostinelli C, Di Rocco A, Pfreundschuh M, Pileri SA. Diffuse large B-cell lymphoma. Crit Rev Oncol Hematol. 2013;87(2):146–71. https://doi.org/10.1016/j.critrevonc.2012.12.009.CrossRefPubMed Martelli M, Ferreri AJ, Agostinelli C, Di Rocco A, Pfreundschuh M, Pileri SA. Diffuse large B-cell lymphoma. Crit Rev Oncol Hematol. 2013;87(2):146–71. https://​doi.​org/​10.​1016/​j.​critrevonc.​2012.​12.​009.CrossRefPubMed

go back to reference Vangipuram R, Tyring SK. AIDS-associated malignancies. Cancer Treat Res. 2019;177:1–21. https://doi.org/10.1007/978-3-030-03502-0_1.CrossRefPubMed Vangipuram R, Tyring SK. AIDS-associated malignancies. Cancer Treat Res. 2019;177:1–21. https://​doi.​org/​10.​1007/​978-3-030-03502-0_​1.CrossRefPubMed

go back to reference Kinlen L. Immunosuppressive therapy and acquired immunological disorders. Cancer Res. 1992;52(19 Suppl):5474s–6s.PubMed Kinlen L. Immunosuppressive therapy and acquired immunological disorders. Cancer Res. 1992;52(19 Suppl):5474s–6s.PubMed

go back to reference Azathioprine. In: In-Depth Answers [database on the Internet]. Greenwood Village (CO): IBM Corporation; 2022 [cited 2022 Sept 14]. Available from: www.micromedexsolutions.com. Subscription required to view. Azathioprine. In: In-Depth Answers [database on the Internet]. Greenwood Village (CO): IBM Corporation; 2022 [cited 2022 Sept 14]. Available from: www.​micromedexsoluti​ons.​com. Subscription required to view.

go back to reference Confavreux C, Saddier P, Grimaud J, et al. Risk of cancer from azathioprine therapy in multiple sclerosis: a case-control study. Neurology. 1996;46:1607–12.CrossRefPubMed Confavreux C, Saddier P, Grimaud J, et al. Risk of cancer from azathioprine therapy in multiple sclerosis: a case-control study. Neurology. 1996;46:1607–12.CrossRefPubMed

go back to reference Arnold JA, Ranson SA, Abdalla SH. Azathioprine-associated acute myeloid leukaemia with trilineage dysplasia and complex karyotype: a case report and review of the literature. Clin Lab Haem. 1999;21:289–92.CrossRef Arnold JA, Ranson SA, Abdalla SH. Azathioprine-associated acute myeloid leukaemia with trilineage dysplasia and complex karyotype: a case report and review of the literature. Clin Lab Haem. 1999;21:289–92.CrossRef

go back to reference Au WY, Yuen MF, Lai KC, et al. Clonal marrow abnormalities after azathioprine and sulfasalazine exposure in Crohn’s disease: a cautionary tale. Leuk Lymphoma. 2002;43(8):1679–81.CrossRefPubMed Au WY, Yuen MF, Lai KC, et al. Clonal marrow abnormalities after azathioprine and sulfasalazine exposure in Crohn’s disease: a cautionary tale. Leuk Lymphoma. 2002;43(8):1679–81.CrossRefPubMed

go back to reference Offman J, Opelz G, Doehler B, et al. Defective DNA mismatch repair in acute myeloid leukemia/myelodysplastic syndrome after organ transplantation. Blood. 2004;104(3):822–8.CrossRefPubMed Offman J, Opelz G, Doehler B, et al. Defective DNA mismatch repair in acute myeloid leukemia/myelodysplastic syndrome after organ transplantation. Blood. 2004;104(3):822–8.CrossRefPubMed

go back to reference Urowitz MB, Lee P. The risks of antimalarial retinopathy, azathioprine lymphoma and methotrexate hepatotoxicity during the treatment of rheumatoid arthritis. Baillieres Clin Rheumatol. 1990;4(2):193–206. https://doi.org/10.1016/s0950-3579(05)80017-2.CrossRefPubMed Urowitz MB, Lee P. The risks of antimalarial retinopathy, azathioprine lymphoma and methotrexate hepatotoxicity during the treatment of rheumatoid arthritis. Baillieres Clin Rheumatol. 1990;4(2):193–206. https://​doi.​org/​10.​1016/​s0950-3579(05)80017-2.CrossRefPubMed

go back to reference Aguilar HI, Burgart LJ, Geller A, et al. Azathioprine-induced lymphoma manifesting as fulminant hepatic failure. Mayo Clin Proc. 1997;72:643–5.CrossRefPubMed Aguilar HI, Burgart LJ, Geller A, et al. Azathioprine-induced lymphoma manifesting as fulminant hepatic failure. Mayo Clin Proc. 1997;72:643–5.CrossRefPubMed

go back to reference Pitt PI, Sultan AH, Malone M, et al. Association between azathioprine therapy and lymphoma in rheumatoid disease. J R Soc Med. 1987;80:428–9.CrossRefPubMedPubMedCentral Pitt PI, Sultan AH, Malone M, et al. Association between azathioprine therapy and lymphoma in rheumatoid disease. J R Soc Med. 1987;80:428–9.CrossRefPubMedPubMedCentral

go back to reference US Food and Drug Administration: FDA Drug Safety Communication: Safety Review update on reports of Hepatosplenic T-Cell Lymphoma in adolescents and young adults receiving tumor necrosis factor (TNF) blockers, azathioprine and/or mercaptopurine. US Food and Drug Administration. Silver Spring, MD. 2011. Available from URL: http://www.fda.go. As accessed 2011–04–14. US Food and Drug Administration: FDA Drug Safety Communication: Safety Review update on reports of Hepatosplenic T-Cell Lymphoma in adolescents and young adults receiving tumor necrosis factor (TNF) blockers, azathioprine and/or mercaptopurine. US Food and Drug Administration. Silver Spring, MD. 2011. Available from URL: http://​www.​fda.​go. As accessed 2011–04–14.

go back to reference Beaugerie L, Brousse N, Bouvier AM, Colombel JF, Lémann M, Cosnes J, Hébuterne X, Cortot A, Bouhnik Y, Gendre JP, Simon T, Maynadié M, Hermine O, Faivre J, Carrat F, CESAME Study Group. Lymphoproliferative disorders in patients receiving thiopurines for inflammatory bowel disease: a prospective observational cohort study. Lancet. 2009;374(9701):1617–25. https://doi.org/10.1016/S0140-6736(09)61302-7.CrossRefPubMed Beaugerie L, Brousse N, Bouvier AM, Colombel JF, Lémann M, Cosnes J, Hébuterne X, Cortot A, Bouhnik Y, Gendre JP, Simon T, Maynadié M, Hermine O, Faivre J, Carrat F, CESAME Study Group. Lymphoproliferative disorders in patients receiving thiopurines for inflammatory bowel disease: a prospective observational cohort study. Lancet. 2009;374(9701):1617–25. https://​doi.​org/​10.​1016/​S0140-6736(09)61302-7.CrossRefPubMed

go back to reference Hiyama K, Terashima H, Nakano Y, Kamiga M, Harada K, Horiguchi H, Mamiya T. Primary rectal diffuse large B-cell lymphoma associated with ulcerative colitis: a case report. Clin Case Rep. 2015;3(3):150–5. https://doi.org/10.1002/ccr3.185.CrossRefPubMed Hiyama K, Terashima H, Nakano Y, Kamiga M, Harada K, Horiguchi H, Mamiya T. Primary rectal diffuse large B-cell lymphoma associated with ulcerative colitis: a case report. Clin Case Rep. 2015;3(3):150–5. https://​doi.​org/​10.​1002/​ccr3.​185.CrossRefPubMed

go back to reference Tan CW, Wilson GE, Howat JM, Shreeve DR. Rectal lymphoma in ulcerative colitis treated with azathioprine. Eur J Gastroenterol Hepatol. 2001;13(8):989–92. https://doi.org/10.1097/00042737-200108000-00022.CrossRefPubMed Tan CW, Wilson GE, Howat JM, Shreeve DR. Rectal lymphoma in ulcerative colitis treated with azathioprine. Eur J Gastroenterol Hepatol. 2001;13(8):989–92. https://​doi.​org/​10.​1097/​00042737-200108000-00022.CrossRefPubMed

go back to reference Lee LY, Namuduri R, Chan MMF, Quek JKS, Koh MJ. Epstein–Barr virus positive diffuse large B-cell lymphoma presenting with vaginal sloughing and ulcerated skin nodule. J Cutan Pathol. 2018;45(2):162–6. https://doi.org/10.1111/cup.13074.CrossRefPubMed Lee LY, Namuduri R, Chan MMF, Quek JKS, Koh MJ. Epstein–Barr virus positive diffuse large B-cell lymphoma presenting with vaginal sloughing and ulcerated skin nodule. J Cutan Pathol. 2018;45(2):162–6. https://​doi.​org/​10.​1111/​cup.​13074.CrossRefPubMed

go back to reference Barthelmes L, Thomas KJ, Seale JR. Prostatic involvement of a testicular lymphoma in a patient with myasthenia gravis on long-term azathioprine. Leuk Lymphoma. 2002;43(12):2425–6. https://doi.org/10.1080/1042819021000040189.CrossRefPubMed Barthelmes L, Thomas KJ, Seale JR. Prostatic involvement of a testicular lymphoma in a patient with myasthenia gravis on long-term azathioprine. Leuk Lymphoma. 2002;43(12):2425–6. https://​doi.​org/​10.​1080/​1042819021000040​189.CrossRefPubMed

go back to reference Termsarasab P, Katirji B. Brainstem lymphoma in a myasthenia gravis patient on azathioprine. J Clin Neurosci. 2015;22(2):415–8. https://doi.org/10.1016/j.jocn.2014.06.104.CrossRefPubMed Termsarasab P, Katirji B. Brainstem lymphoma in a myasthenia gravis patient on azathioprine. J Clin Neurosci. 2015;22(2):415–8. https://​doi.​org/​10.​1016/​j.​jocn.​2014.​06.​104.CrossRefPubMed

go back to reference McAleer MA, D’Arcy CA, Mulligan NJ, Sheahan K, Collins P. Primary cutaneous lymphoma associated with Epstein–Barr virus and azathioprine therapy. Clin Exp Dermatol. 2010;35(6):674–6. https://doi.org/10.1111/j.1365-2230.2010.03799.x.CrossRefPubMed McAleer MA, D’Arcy CA, Mulligan NJ, Sheahan K, Collins P. Primary cutaneous lymphoma associated with Epstein–Barr virus and azathioprine therapy. Clin Exp Dermatol. 2010;35(6):674–6. https://​doi.​org/​10.​1111/​j.​1365-2230.​2010.​03799.​x.CrossRefPubMed

go back to reference Bonder A, Afdhal N. Evaluation of liver lesions. Clin Liver Dis. 2012;16(2):271–83. https://doi.org/10.1016/j.cld.2012.03.001.CrossRefPubMed Bonder A, Afdhal N. Evaluation of liver lesions. Clin Liver Dis. 2012;16(2):271–83. https://​doi.​org/​10.​1016/​j.​cld.​2012.​03.​001.CrossRefPubMed

go back to reference O’Neill EK, Cogley JR, Miller FH. The ins and outs of liver imaging. Clin Liver Dis. 2015;19(1):99–121. https://doi.org/10.1016/j.cld.2014.09.006.CrossRefPubMed O’Neill EK, Cogley JR, Miller FH. The ins and outs of liver imaging. Clin Liver Dis. 2015;19(1):99–121. https://​doi.​org/​10.​1016/​j.​cld.​2014.​09.​006.CrossRefPubMed

go back to reference Silva TS, Sung M, Nelson DW, DiFronzo AL, O’Connor VV. A multicenter, 10-year experience with hepatocellular adenoma: risk factors and disease course. Am Surg. 2021. https://doi.org/10.1177/00031348211011084.CrossRefPubMed Silva TS, Sung M, Nelson DW, DiFronzo AL, O’Connor VV. A multicenter, 10-year experience with hepatocellular adenoma: risk factors and disease course. Am Surg. 2021. https://​doi.​org/​10.​1177/​0003134821101108​4.CrossRefPubMed

go back to reference Duran SR, Jaquiss RDB. Hepatocellular carcinoma. N Engl J Med. 2019;381(1):e2. https://doi.org/10.1056/NEJMc1906565.CrossRefPubMed Duran SR, Jaquiss RDB. Hepatocellular carcinoma. N Engl J Med. 2019;381(1):e2. https://​doi.​org/​10.​1056/​NEJMc1906565.CrossRefPubMed

go back to reference Khan AS, Dageforde LA. Cholangiocarcinoma. Surg Clin North Am. 2019;99(2):315–35. https://doi.org/10.1016/j.suc.2018.12.004.CrossRefPubMed Khan AS, Dageforde LA. Cholangiocarcinoma. Surg Clin North Am. 2019;99(2):315–35. https://​doi.​org/​10.​1016/​j.​suc.​2018.​12.​004.CrossRefPubMed

go back to reference Di Martino M, De Filippis G, De Santis A, Geiger D, Del Monte M, Lombardo CV, Rossi M, Corradini SG, Mennini G, Catalano C. Hepatocellular carcinoma in cirrhotic patients: prospective comparison of US, CT and MR imaging. Eur Radiol. 2013;23(4):887–96. https://doi.org/10.1007/s00330-012-2691-z.CrossRefPubMed Di Martino M, De Filippis G, De Santis A, Geiger D, Del Monte M, Lombardo CV, Rossi M, Corradini SG, Mennini G, Catalano C. Hepatocellular carcinoma in cirrhotic patients: prospective comparison of US, CT and MR imaging. Eur Radiol. 2013;23(4):887–96. https://​doi.​org/​10.​1007/​s00330-012-2691-z.CrossRefPubMed

go back to reference Agmon-Levin N, Berger I, Shtalrid M, Schlanger H, Sthoeger ZM. Primary hepatic lymphoma: a case report and review of the literature. Age Ageing. 2004;33(6):637–40. https://doi.org/10.1093/ageing/afh197.CrossRefPubMed Agmon-Levin N, Berger I, Shtalrid M, Schlanger H, Sthoeger ZM. Primary hepatic lymphoma: a case report and review of the literature. Age Ageing. 2004;33(6):637–40. https://​doi.​org/​10.​1093/​ageing/​afh197.CrossRefPubMed

go back to reference Forghani F, Masoodi M, Kadivar M. Primary hepatic lymphoma mimicking cholangiocarcinoma. Oman Med J. 2017;32(4):335–8. https://doi.org/10.5001/omj.2017.63.CrossRefPubMedPubMedCentral Forghani F, Masoodi M, Kadivar M. Primary hepatic lymphoma mimicking cholangiocarcinoma. Oman Med J. 2017;32(4):335–8. https://​doi.​org/​10.​5001/​omj.​2017.​63.CrossRefPubMedPubMedCentral

go back to reference El Nouwar R, El Murr T. Primary hepatic diffuse large B-cell lymphoma mimicking acute fulminant hepatitis: a case report and review of the literature. Eur J Case Rep Intern Med. 2018;5(6):000878. https://doi.org/10.12890/2018_000878.CrossRefPubMedPubMedCentral El Nouwar R, El Murr T. Primary hepatic diffuse large B-cell lymphoma mimicking acute fulminant hepatitis: a case report and review of the literature. Eur J Case Rep Intern Med. 2018;5(6):000878. https://​doi.​org/​10.​12890/​2018_​000878.CrossRefPubMedPubMedCentral

go back to reference Zelenetz AD, Gordon LI, Abramson JS, et al. B-cell Lymphomas. Version 4.2021. In: National Comprehensive Cancer Network (NCCN) Clinical Practice Guidelines in Oncology- B-Cell Lymphomas. NCCN 2021 May from NCCN.org/guidelines Zelenetz AD, Gordon LI, Abramson JS, et al. B-cell Lymphomas. Version 4.2021. In: National Comprehensive Cancer Network (NCCN) Clinical Practice Guidelines in Oncology- B-Cell Lymphomas. NCCN 2021 May from NCCN.org/guidelines

go back to reference Baecklund E, Smedby KE, Sutton LA, Askling J, Rosenquist R. Lymphoma development in patients with autoimmune and inflammatory disorders–what are the driving forces? Semin Cancer Biol. 2014;24:61–70. https://doi.org/10.1016/j.semcancer.2013.12.001.CrossRefPubMed Baecklund E, Smedby KE, Sutton LA, Askling J, Rosenquist R. Lymphoma development in patients with autoimmune and inflammatory disorders–what are the driving forces? Semin Cancer Biol. 2014;24:61–70. https://​doi.​org/​10.​1016/​j.​semcancer.​2013.​12.​001.CrossRefPubMed

go back to reference Alaggio R, Amador C, Anagnostopoulos I, Attygalle AD, Araujo IBO, Berti E, Bhagat G, Borges AM, Boyer D, Calaminici M, Chadburn A, Chan JKC, Cheuk W, Chng WJ, Choi JK, Chuang SS, Coupland SE, Czader M, Dave SS, de Jong D, Du MQ, Elenitoba-Johnson KS, Ferry J, Geyer J, Gratzinger D, Guitart J, Gujral S, Harris M, Harrison CJ, Hartmann S, Hochhaus A, Jansen PM, Karube K, Kempf W, Khoury J, Kimura H, Klapper W, Kovach AE, Kumar S, Lazar AJ, Lazzi S, Leoncini L, Leung N, Leventaki V, Li XQ, Lim MS, Liu WP, Louissaint A Jr, Marcogliese A, Medeiros LJ, Michal M, Miranda RN, Mitteldorf C, Montes-Moreno S, Morice W, Nardi V, Naresh KN, Natkunam Y, Ng SB, Oschlies I, Ott G, Parrens M, Pulitzer M, Rajkumar SV, Rawstron AC, Rech K, Rosenwald A, Said J, Sarkozy C, Sayed S, Saygin C, Schuh A, Sewell W, Siebert R, Sohani AR, Tooze R, Traverse-Glehen A, Vega F, Vergier B, Wechalekar AD, Wood B, Xerri L, Xiao W. The 5th edition of the World Health Organization Classification of haematolymphoid tumours: lymphoid neoplasms. Leukemia. 2022;36(7):1720–48. https://doi.org/10.1038/s41375-022-01620-2.CrossRefPubMedPubMedCentral Alaggio R, Amador C, Anagnostopoulos I, Attygalle AD, Araujo IBO, Berti E, Bhagat G, Borges AM, Boyer D, Calaminici M, Chadburn A, Chan JKC, Cheuk W, Chng WJ, Choi JK, Chuang SS, Coupland SE, Czader M, Dave SS, de Jong D, Du MQ, Elenitoba-Johnson KS, Ferry J, Geyer J, Gratzinger D, Guitart J, Gujral S, Harris M, Harrison CJ, Hartmann S, Hochhaus A, Jansen PM, Karube K, Kempf W, Khoury J, Kimura H, Klapper W, Kovach AE, Kumar S, Lazar AJ, Lazzi S, Leoncini L, Leung N, Leventaki V, Li XQ, Lim MS, Liu WP, Louissaint A Jr, Marcogliese A, Medeiros LJ, Michal M, Miranda RN, Mitteldorf C, Montes-Moreno S, Morice W, Nardi V, Naresh KN, Natkunam Y, Ng SB, Oschlies I, Ott G, Parrens M, Pulitzer M, Rajkumar SV, Rawstron AC, Rech K, Rosenwald A, Said J, Sarkozy C, Sayed S, Saygin C, Schuh A, Sewell W, Siebert R, Sohani AR, Tooze R, Traverse-Glehen A, Vega F, Vergier B, Wechalekar AD, Wood B, Xerri L, Xiao W. The 5th edition of the World Health Organization Classification of haematolymphoid tumours: lymphoid neoplasms. Leukemia. 2022;36(7):1720–48. https://​doi.​org/​10.​1038/​s41375-022-01620-2.CrossRefPubMedPubMedCentral