DOI QR코드

DOI QR Code

Approach to cytomegalovirus infections in patients with ulcerative colitis

  • Park, Sung Chul (Department of Internal Medicine, Kangwon National University Hospital) ;
  • Yoon, Mi Jeen (Department of Pathology, Soon Chun Hyang University Seoul Hospital) ;
  • Yoon, Tae Jeen (Department of Internal Medicine, Korea University Anam Hospital)
  • 투고 : 2017.02.09
  • 심사 : 2017.03.06
  • 발행 : 2017.05.01

초록

Cytomegalovirus (CMV) reactivation is common in patients with severe ulcerative colitis (UC), and may reflect exacerbation of mucosal inflammation and/or administration of immunosuppressants. The question of whether CMV is an active pathogen or 'an innocent bystander' in the exacerbation of UC remains controversial. Patients with UC exacerbated by reactivated CMV experience worse prognoses than those without CMV reactivation and antiviral therapy significantly reduces the need for colectomy in patients with severe UC and high-grade CMV infection, indicating that CMV plays a role in UC prognosis. Therefore, the CMV status of patients on immunosuppressants, particularly those with steroid-refractory or -dependent UC, should be tested. When CMV is detected, be performed based on should adequate treatment the extent of the viral load and the presence of certain clinical features including a large ulcer. Anti-tumor necrosis factor agents may be useful for treating CMV colitis complicating UC.

키워드

참고문헌

  1. Cannon MJ, Schmid DS, Hyde TB. Review of cytomegalovirus seroprevalence and demographic characteristics associated with infection. Rev Med Virol 2010;20:202-213. https://doi.org/10.1002/rmv.655
  2. Rowshani AT, Bemelman FJ, van Leeuwen EM, van Lier RA, ten Berge IJ. Clinical and immunologic aspects of cytomegalovirus infection in solid organ transplant recipients. Transplantation 2005;79:381-386. https://doi.org/10.1097/01.TP.0000148239.00384.F0
  3. Powell RD, Warner NE, Levine RS, Kirsner JB. Cytomegalic inclusion disease and ulcerative colitis: report of a case in a young adult. Am J Med 1961;30:334-340. https://doi.org/10.1016/0002-9343(61)90105-X
  4. Kishore J, Ghoshal U, Ghoshal UC, et al. Infection with cytomegalovirus in patients with inflammatory bowel disease: prevalence, clinical significance and outcome. J Med Microbiol 2004;53(Pt 11):1155-1160. https://doi.org/10.1099/jmm.0.45629-0
  5. Wada Y, Matsui T, Matake H, et al. Intractable ulcerative colitis caused by cytomegalovirus infection: a prospective study on prevalence, diagnosis, and treatment. Dis Colon Rectum 2003;46(10 Suppl):S59-S65. https://doi.org/10.1007/s10350-004-6497-1
  6. Domenech E, Vega R, Ojanguren I, et al. Cytomegalovirus infection in ulcerative colitis: a prospective, comparative study on prevalence and diagnostic strategy. Inflamm Bowel Dis 2008;14:1373-1379. https://doi.org/10.1002/ibd.20498
  7. Maconi G, Colombo E, Zerbi P, et al. Prevalence, detection rate and outcome of cytomegalovirus infection in ulcerative colitis patients requiring colonic resection. Dig Liver Dis 2005;37:418-423. https://doi.org/10.1016/j.dld.2005.01.011
  8. Cottone M, Pietrosi G, Martorana G, et al. Prevalence of cytomegalovirus infection in severe refractory ulcerative and Crohn's colitis. Am J Gastroenterol 2001;96:773-775. https://doi.org/10.1111/j.1572-0241.2001.03620.x
  9. Kambham N, Vij R, Cartwright CA, Longacre T. Cytomegalovirus infection in steroid-refractory ulcerative colitis: a case-control study. Am J Surg Pathol 2004;28:365-373. https://doi.org/10.1097/00000478-200403000-00009
  10. Kim YS, Kim YH, Kim JS, et al. The prevalence and efficacy of ganciclovir on steroid-refractory ulcerative colitis with cytomegalovirus infection: a prospective multicenter study. J Clin Gastroenterol 2012;46:51-56. https://doi.org/10.1097/MCG.0b013e3182160c9c
  11. Kim JJ, Simpson N, Klipfel N, Debose R, Barr N, Laine L. Cytomegalovirus infection in patients with active inflammatory bowel disease. Dig Dis Sci 2010;55:1059-1065. https://doi.org/10.1007/s10620-010-1126-4
  12. Knosel T, Schewe C, Petersen N, Dietel M, Petersen I. Prevalence of infectious pathogens in Crohn's disease. Pathol Res Pract 2009;205:223-230. https://doi.org/10.1016/j.prp.2008.04.018
  13. Nakase H, Yoshino T, Honzawa Y, Chiba T. Low prevalence of CMV infection in patients with Crohn's disease in comparison with ulcerative colitis: effect of different immune response on prevalence of CMV infection. Dig Dis Sci 2010;55:1498-1499. https://doi.org/10.1007/s10620-010-1162-0
  14. Pillet S, Pozzetto B, Jarlot C, Paul S, Roblin X. Management of cytomegalovirus infection in inflammatory bowel diseases. Dig Liver Dis 2012;44:541-548. https://doi.org/10.1016/j.dld.2012.03.018
  15. Rahier JF, Magro F, Abreu C, et al. Second European evidence-based consensus on the prevention, diagnosis and management of opportunistic infections in inflammatory bowel disease. J Crohns Colitis 2014;8:443-468. https://doi.org/10.1016/j.crohns.2013.12.013
  16. Mun JI, Shin SJ, Yu BH, et al. A case of hemophagocytic syndrome in a patient with fulminant ulcerative colitis superinfected by cytomegalovirus. Korean J Intern Med 2013;28:352-355. https://doi.org/10.3904/kjim.2013.28.3.352
  17. Matsumoto S, Yoshida Y. What are the factors that affect hospitalization and surgery for aggravation of ulcerative colitis? Eur J Gastroenterol Hepatol 2014;26:282-287. https://doi.org/10.1097/MEG.0000000000000028
  18. Park SH, Yang SK, Hong SM, et al. Severe disease activity and cytomegalovirus colitis are predictive of a nonresponse to infliximab in patients with ulcerative colitis. Dig Dis Sci 2013;58:3592-3599. https://doi.org/10.1007/s10620-013-2828-1
  19. Kim YS, Kim YH, Kim JS, et al. Long-term outcomes of cytomegalovirus reactivation in patients with moderate to severe ulcerative colitis: a multicenter study. Gut Liver 2014;8:643-647. https://doi.org/10.5009/gnl13427
  20. Matsuoka K, Iwao Y, Mori T, et al. Cytomegalovirus is frequently reactivated and disappears without antiviral agents in ulcerative colitis patients. Am J Gastroenterol 2007;102:331-337. https://doi.org/10.1111/j.1572-0241.2006.00989.x
  21. Yoshino T, Nakase H, Ueno S, et al. Usefulness of quantitative real-time PCR assay for early detection of cytomegalovirus infection in patients with ulcerative colitis refractory to immunosuppressive therapies. Inflamm Bowel Dis 2007;13:1516-1521. https://doi.org/10.1002/ibd.20253
  22. do Carmo AM, Santos FM, Ortiz-Agostinho CL, et al. Cytomegalovirus infection in inflammatory bowel disease is not associated with worsening of intestinal inflammatory activity. PLoS One 2014;9:e111574. https://doi.org/10.1371/journal.pone.0111574
  23. McCurdy JD, Jones A, Enders FT, et al. A model for identifying cytomegalovirus in patients with inflammatory bowel disease. Clin Gastroenterol Hepatol 2015;13:131-137. https://doi.org/10.1016/j.cgh.2014.05.026
  24. Gauss A, Rosenstiel S, Schnitzler P, et al. Intestinal cytomegalovirus infection in patients hospitalized for exacerbation of inflammatory bowel disease: a 10-year tertiary referral center experience. Eur J Gastroenterol Hepatol 2015;27:712-720. https://doi.org/10.1097/MEG.0000000000000361
  25. Sager K, Alam S, Bond A, Chinnappan L, Probert CS. Review article: cytomegalovirus and inflammatory bowel disease. Aliment Pharmacol Ther 2015;41:725-733. https://doi.org/10.1111/apt.13124
  26. Iida T, Ikeya K, Watanabe F, et al. Looking for endoscopic features of cytomegalovirus colitis: a study of 187 patients with active ulcerative colitis, positive and negative for cytomegalovirus. Inflamm Bowel Dis 2013;19:1156-1163. https://doi.org/10.1097/MIB.0b013e31828075ce
  27. Suzuki H, Kato J, Kuriyama M, Hiraoka S, Kuwaki K, Yamamoto K. Specific endoscopic features of ulcerative colitis complicated by cytomegalovirus infection. World J Gastroenterol 2010;16:1245-1251. https://doi.org/10.3748/wjg.v16.i10.1245
  28. Kim JW, Boo SJ, Ye BD, et al. Clinical utility of cytomegalovirus antigenemia assay and blood cytomegalovirus DNA PCR for cytomegaloviral colitis patients with moderate to severe ulcerative colitis. J Crohns Colitis 2014;8:693-701. https://doi.org/10.1016/j.crohns.2013.12.014
  29. Chun J, Lee C, Kwon JE, et al. Usefulness of the cytomegalovirus antigenemia assay in patients with ulcerative colitis. Intest Res 2015;13:50-59. https://doi.org/10.5217/ir.2015.13.1.50
  30. Chang S, Cheon JH. A clinical significance of assessing cytomegalovirus infection status in patients with ulcerative colitis. Intest Res 2015;13:2-3. https://doi.org/10.5217/ir.2015.13.1.2
  31. Kandiel A, Lashner B. Cytomegalovirus colitis complicating inflammatory bowel disease. Am J Gastroenterol 2006;101:2857-2865. https://doi.org/10.1111/j.1572-0241.2006.00869.x
  32. Beaugerie L, Cywiner-Golenzer C, Monfort L, et al. Definition and diagnosis of cytomegalovirus colitis in patients infected by human immunodeficiency virus. J Acquir Immune Defic Syndr Hum Retrovirol 1997;14:423-429. https://doi.org/10.1097/00042560-199704150-00005
  33. McCoy MH, Post K, Sen JD, et al. qPCR increases sensitivity to detect cytomegalovirus in formalin-fixed, paraffin-embedded tissue of gastrointestinal biopsies. Hum Pathol 2014;45:48-53. https://doi.org/10.1016/j.humpath.2013.07.040
  34. Cotte L, Drouet E, Bissuel F, Denoyel GA, Trepo C. Diagnostic value of amplification of human cytomegalovirus DNA from gastrointestinal biopsies from human immunodeficiency virus-infected patients. J Clin Microbiol 1993;31:2066-2069.
  35. Roblin X, Pillet S, Oussalah A, et al. Cytomegalovirus load in inflamed intestinal tissue is predictive of resistance to immunosuppressive therapy in ulcerative colitis. Am J Gastroenterol 2011;106:2001-2008. https://doi.org/10.1038/ajg.2011.202
  36. Ciccocioppo R, Racca F, Paolucci S, et al. Human cytomegalovirus and Epstein-Barr virus infection in inflammatory bowel disease: need for mucosal viral load measurement. World J Gastroenterol 2015;21:1915-1926. https://doi.org/10.3748/wjg.v21.i6.1915
  37. Zidar N, Ferkolj I, Tepes K, et al. Diagnosing cytomegalovirus in patients with inflammatory bowel disease: by immunohistochemistry or polymerase chain reaction? Virchows Arch 2015;466:533-539. https://doi.org/10.1007/s00428-015-1741-8
  38. McCurdy JD, Enders FT, Jones A, et al. Detection of cytomegalovirus in patients with inflammatory bowel disease: where to biopsy and how many biopsies? Inflamm Bowel Dis 2015;21:2833-2838. https://doi.org/10.1097/MIB.0000000000000556
  39. de la Hoz RE, Stephens G, Sherlock C. Diagnosis and treatment approaches of CMV infections in adult patients. J Clin Virol 2002;25 Suppl 2:S1-S12.
  40. Landry ML, Ferguson D. Comparison of quantitative cytomegalovirus antigenemia assay with culture methods and correlation with clinical disease. J Clin Microbiol 1993;31:2851-2856.
  41. Kornbluth A, Sachar DB; Practice Parameters Committee of the American College of Gastroenterology. Ulcerative colitis practice guidelines in adults: American College Of Gastroenterology, Practice Parameters Committee. Am J Gastroenterol 2010;105:501-523. https://doi.org/10.1038/ajg.2009.727
  42. Choi CH, Moon W, Kim YS, et al. Second Korean guideline for the management of ulcerative colitis. Korean J Gastroenterol 2017;69:1-28. https://doi.org/10.4166/kjg.2017.69.1.1
  43. Maconi G, Lombardini M, Furfaro F, Bezzio C, Zerbi P, Ardizzone S. Long-term outcome of inflammatory bowel diseases with cytomegalovirus colitis: effect of antiviral treatment. Eur J Gastroenterol Hepatol 2014;26:1146-1151. https://doi.org/10.1097/MEG.0000000000000175
  44. Shukla T, Singh S, Loftus EV Jr, Bruining DH, McCurdy JD. Antiviral therapy in steroid-refractory ulcerative colitis with cytomegalovirus: systematic review and meta-analysis. Inflamm Bowel Dis 2015;21:2718-2725. https://doi.org/10.1097/MIB.0000000000000489
  45. Jones A, McCurdy JD, Loftus EV Jr, et al. Effects of antiviral therapy for patients with inflammatory bowel disease and a positive intestinal biopsy for cytomegalovirus. Clin Gastroenterol Hepatol 2015;13:949-955. https://doi.org/10.1016/j.cgh.2014.09.042
  46. Omiya M, Matsushita M, Tanaka T, Kawamata S, Okazaki K. The absence of large ulcer predicts latent cytomegalovirus infection in ulcerative colitis with positive mucosal viral assay. Intern Med 2010;49:2277-2282. https://doi.org/10.2169/internalmedicine.49.3657
  47. Pillet S, Pozzetto B, Roblin X. Cytomegalovirus and ulcerative colitis: place of antiviral therapy. World J Gastroenterol 2016;22:2030-2045. https://doi.org/10.3748/wjg.v22.i6.2030
  48. Criscuoli V, Casa A, Orlando A, et al. Severe acute colitis associated with CMV: a prevalence study. Dig Liver Dis 2004;36:818-820. https://doi.org/10.1016/j.dld.2004.05.013
  49. Papadakis KA, Tung JK, Binder SW, et al. Outcome of cytomegalovirus infections in patients with inflammatory bowel disease. Am J Gastroenterol 2001;96:2137-2142. https://doi.org/10.1111/j.1572-0241.2001.03949.x
  50. Czock D, Scholle C, Rasche FM, Schaarschmidt D, Keller F. Pharmacokinetics of valganciclovir and ganciclovir in renal impairment. Clin Pharmacol Ther 2002;72:142-150. https://doi.org/10.1067/mcp.2002.126306
  51. Einsele H, Ehninger G, Steidle M, et al. Polymerase chain reaction to evaluate antiviral therapy for cytomegalovirus disease. Lancet 1991;338:1170-1172. https://doi.org/10.1016/0140-6736(91)92032-W
  52. Ciccocioppo R. Letter: cytomegalovirus infection in inflammatory bowel disease. Aliment Pharmacol Ther 2015;42:127-129.
  53. Landsman MJ, Sultan M, Stevens M, Charabaty A, Mattar MC. Diagnosis and management of common gastrointestinal tract infectious diseases in ulcerative colitis and Crohn's disease patients. Inflamm Bowel Dis 2014;20:2503-2510. https://doi.org/10.1097/MIB.0000000000000140
  54. D'Ovidio V, Vernia P, Gentile G, et al. Cytomegalovirus infection in inflammatory bowel disease patients undergoing anti-TNFalpha therapy. J Clin Virol 2008;43:180-183. https://doi.org/10.1016/j.jcv.2008.06.002
  55. Lavagna A, Bergallo M, Daperno M, et al. Infliximab and the risk of latent viruses reactivation in active Crohn's disease. Inflamm Bowel Dis 2007;13:896-902. https://doi.org/10.1002/ibd.20131
  56. Pillet S, Jarlot C, Courault M, et al. Infliximab does not worsen outcomes during flare-ups associated with cytomegalovirus infection in patients with ulcerative colitis. Inflamm Bowel Dis 2015;21:1580-1586. https://doi.org/10.1097/MIB.0000000000000412

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