Human cytomegalovirus and Epstein-Barr virus infection in inflammatory bowel disease: Need for mucosal viral load measurement

World Journal of Gastroenterology

Volumn 21, Issue 6, 2015, Pages 1915-1926

  Ciccocioppo, Rachele ^a   Racca, Francesca ^a   Paolucci, Stefania ^b   Campanini, Giulia ^b   Pozzi, Lodovica ^b   Betti, Elena ^a   Riboni, Roberta ^b   Vanoli, Alessandro ^b   Baldanti, Fausto ^b   Corazza, Gino Roberto ^a  

^a UNIVERSITY OF PAVIA   (Italy)

^b FONDAZIONE IRCCS POLICLINICO SAN MATTEO   (Italy)

Author keywords

Inflammatory bowel disease; Quantitative real time polymerase chain reaction; Refractory; Steroid therapy; Viral infection

Indexed keywords

GANCICLOVIR; RITUXIMAB; STEROID; VIRUS DNA;

ADOLESCENT; ADULT; AGED; ANTIVIRAL THERAPY; ARTICLE; CLINICAL ARTICLE; COHORT ANALYSIS; COLITIS; CONTROLLED STUDY; CORRELATIONAL STUDY; CROHN DISEASE; DISEASE ACTIVITY; EPSTEIN BARR VIRUS; EPSTEIN BARR VIRUS INFECTION; FEMALE; FOLLOW UP; HUMAN; HUMAN CYTOMEGALOVIRUS; IMMUNOHISTOCHEMISTRY; MALE; PROSPECTIVE STUDY; QUANTITATIVE STUDY; REAL TIME POLYMERASE CHAIN REACTION; RISK FACTOR; TREATMENT DURATION; ULCERATIVE COLITIS; VIRAL COLITIS; VIRUS LOAD; BIOPSY; CASE CONTROL STUDY; COLON; COLONOSCOPY; COMPARATIVE STUDY; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; DIFFERENTIAL DIAGNOSIS; EPSTEIN-BARR VIRUS INFECTIONS; EVALUATION STUDY; GENETICS; INFLAMMATORY BOWEL DISEASES; INTESTINE MUCOSA; ISOLATION AND PURIFICATION; MIDDLE AGED; OPPORTUNISTIC INFECTIONS; PREDICTIVE VALUE; PROGNOSIS; VIROLOGY; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; BIOPSY; CASE-CONTROL STUDIES; COLON; COLONOSCOPY; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; DIAGNOSIS, DIFFERENTIAL; DNA, VIRAL; EPSTEIN-BARR VIRUS INFECTIONS; FEMALE; HERPESVIRUS 4, HUMAN; HUMANS; IMMUNOHISTOCHEMISTRY; INFLAMMATORY BOWEL DISEASES; INTESTINAL MUCOSA; MALE; MIDDLE AGED; OPPORTUNISTIC INFECTIONS; PREDICTIVE VALUE OF TESTS; PROGNOSIS; PROSPECTIVE STUDIES; REAL-TIME POLYMERASE CHAIN REACTION; RISK FACTORS; VIRAL LOAD; YOUNG ADULT;

EID: 84922715882     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v21.i6.1915     Document Type: Article

References (49)

1. Hanauer SB, Kornbluth AA, Messick J, Rubin DT, Sandborn WJ, Sands BE. Clinical scenarios in IBD: optimizing the use of conventional and biologic agents. Inflamm Bowel Dis 2010; 16 Suppl 1: S1-S11 [PMID: 21104734 DOI: 10.1002/ibd.21529]
2. Toruner M, Loftus EV, Harmsen WS, Zinsmeister AR, Orenstein R, Sandborn WJ, Colombel JF, Egan LJ. Risk factors for opportunistic infections in patients with inflammatory bowel disease. Gastroenterology 2008; 134: 929-936 [PMID: 18294633 DOI: 10.1052/j.gastro.2008.01.012]
3. Ford AC, Peyrin-Biroulet L. Opportunistic infections with anti-tumor necrosis factor-α therapy in inflammatory bowel disease: meta-analysis of randomized controlled trials. Am J Gastroenterol 2013; 108: 1268-1276 [PMID: 23649185 DOI: 10.1038/ajg.2013.138]
4. Fishman JA . Overview: cytomegalovirus and the herpesviruses in transplantation. Am J Transplant 2013; 13 Suppl 3: 1-8; quiz 8 [PMID: 23347210 DOI: 10.1111/ajt.12002]
5. Ljungman P, Griffiths P, Paya C. Definitions of cytomegalovirus infection and disease in transplant recipients. Clin Infect Dis 2002; 34: 1094-1097 [PMID: 11914998 DOI: 10.1086/339329]
6. Tashiro Y, Goto M, Takemoto Y, Sato E, Shirahama H, Utsunomiya A, Eizuru Y, Yonezawa S. Epstein-Barr virus-associated enteritis with multiple ulcers after stem cell transplantation: first histologically confirmed case. Pathol Int 2006; 56: 530-537 [PMID: 16930333 DOI: 10.1111/j.1440-1827.2006.02001.x]
7. Beaugerie L, Sokol H, Seksik P. Noncolorectal malignancies in inflammatory bowel disease: more than meets the eye. Dig Dis 2009; 27: 375-381 [PMID: 19786768 DOI: 10.1159/000228577]
8. Green M, Michaels MG. Epstein-Barr virus infection and posttransplant lymphoproliferative disorder. Am J Transplant 2013; 13 Suppl 3: 41-54; quiz 54 [PMID: 23347213 DOI: 10.1111/ajt.12004]
9. Rosado FG, Kim AS. Hemophagocytic lymphohistiocytosis: an update on diagnosis and pathogenesis. Am J Clin Pathol 2013; 139: 713-727 [PMID: 23690113 DOI: 10.1309/AJCP4ZDKJ4ICOUAT]
10. Hommes DW, Sterringa G, van Deventer SJ, Tytgat GN, Weel J. The pathogenicity of cytomegalovirus in inflammatory bowel disease: a systematic review and evidence-based recommendations for future research. Inflamm Bowel Dis 2004; 10: 245-250 [PMID: 15290919 DOI: 10.1097/00054725-200405000-00011]
11. Lawlor G, Moss AC. Cytomegalovirus in inflammatory bowel disease: pathogen or innocent bystander? Inflamm Bowel Dis 2010; 16: 1620-1627 [PMID: 20232408 DOI: 10.1002/ibd.21275]
12. Van Assche G, Dignass A, Panes J, Beaugerie L, Karagiannis J, Allez M, Ochsenkühn T, Orchard T, Rogler G, Louis E, Kupcinskas L, Mantzaris G, Travis S, Stange E. The second European evidence-based Consensus on the diagnosis and management of Crohn's disease: Definitions and diagnosis. J Crohns Colitis 2010; 4: 7-27 [PMID: 21122488 DOI: 10.1016/j.crohns.2009.12.003]
13. Dignass A, Eliakim R, Magro F, Maaser C, Chowers Y, Geboes K, Mantzaris G, Reinisch W, Colombel JF, Vermeire S, Travis S, Lindsay JO, Van Assche G. Second European evidence-based consensus on the diagnosis and management of ulcerative colitis part 1: definitions and diagnosis. J Crohns Colitis 2012; 6: 965-990 [PMID: 23040452 DOI: 10.1016/j.crohns.2012.09.003]
14. Yanai H, Hanauer SB. Assessing response and loss of response to biological therapies in IBD. Am J Gastroenterol 2011; 106: 685-698 [PMID: 21427713 DOI: 10.1038/ajg.2011.103]
15. Bradford K, Shih DQ. Optimizing 6-mercaptopurine and azathioprine therapy in the management of inflammatory bowel disease. World J Gastroenterol 2011; 17: 4166-4173 [PMID: 22072847 DOI: 10.3748/wjg.v17.i37.4166]
16. Satsangi J, Silverberg MS, Vermeire S, Colombel JF. The Montreal classification of inflammatory bowel disease: controversies, consensus, and implications. Gut 2006; 55: 749-753 [PMID: 16698746 DOI: 10.1136/gut.2005.082909]
17. Best WR, Becktel JM, Singleton JW, Kern F. Development of a Crohn's disease activity index. National Cooperative Crohn's Disease Study. Gastroenterology 1976; 70: 439-444 [PMID: 1248701]
18. Rachmilewitz D . Coated mesalazine (5-aminosalicylic acid) versus sulphasalazine in the treatment of active ulcerative colitis: a randomised trial. BMJ 1989; 298: 82-86 [PMID: 2563951 DOI: 10.1136/bmj.298.6666.82]
19. Daperno M, D'Haens G, Van Assche G, Baert F, Bulois P, Maunoury V, Sostegni R, Rocca R, Pera A, Gevers A, Mary JY, Colombel JF, Rutgeerts P. Development and validation of a new, simplified endoscopic activity score for Crohn's disease: the SES-CD. Gastrointest Endosc 2004; 60: 505-512 [PMID: 15472670 DOI: 10.1016/S0016-5107(04)01878-4]
20. Baron JH, Connell AM, Lennard-jones JE. Variation between observers in describing mucosal appearances in proctocolitis. Br Med J 1964; 1: 89-92 [PMID: 14075156 DOI: 10.1136/bmj.1.5375.89]
21. Furione M, Rognoni V, Cabano E, Baldanti F. Kinetics of human cytomegalovirus (HCMV) DNAemia in transplanted patients expressed in international units as determined with the Abbott RealTime CMV assay and an in-house assay. J Clin Virol 2012; 55: 317-322 [PMID: 22989927 DOI: 10.1016/j.jcv.2012.08.017]
22. Watzinger F, Suda M, Preuner S, Baumgartinger R, Ebner K, Baskova L, Niesters HG, Lawitschka A, Lion T. Real-time quantitative PCR assays for detection and monitoring of pathogenic human viruses in immunosuppressed pediatric patients. J Clin Microbiol 2004; 42: 5189-5198 [PMID: 15528714 DOI: 10.1128/JCM.42.11.5189-5198.2004]
23. Maher MM, Nassar MI. Acute cytomegalovirus infection is a risk factor in refractory and complicated inflammatory bowel disease. Dig Dis Sci 2009; 54: 2456-2462 [PMID: 19093204 DOI: 10.1007/is10620-008-0639-6]
24. Lévêque N, Brixi-Benmansour H, Reig T, Renois F, Talmud D, Brodard V, Coste JF, De Champs C, Andréoletti L, Diebold MD. Low frequency of cytomegalovirus infection during exacerbations of inflammatory bowel diseases. J Med Virol 2010; 82: 1694-1700 [PMID: 20827767 DOI: 10.1002/jmv.21877]
25. Kandiel A, Lashner B. Cytomegalovirus colitis complicating inflammatory bowel disease. Am J Gastroenterol 2006; 101: 2857-2865 [PMID: 17026558 DOI: 10.1111/j.1572-0241.2006.00869.x]
26. Cottone M, Pietrosi G, Martorana G, Casà A, Pecoraro G, Oliva L, Orlando A, Rosselli M, Rizzo A, Pagliaro L. Prevalence of cytomegalovirus infection in severe refractory ulcerative and Crohn's colitis. Am J Gastroenterol 2001; 96: 773-775 [PMID: 11280549 DOI: 10.1111/j.1572-0241.2001.03620.x]
27. Bertalot G, Villanacci V, Gramegna M, Orvieto E, Negrini R, Saleri A, Terraroli C, Ravelli P, Cestari R, Viale G. Evidence of Epstein-Barr virus infection in ulcerative colitis. Dig Liver Dis 2001; 33: 551-558 [PMID: 11816543 DOI: 10.1016/S1590-8658(01)80106-7]
28. Yanai H, Shimizu N, Nagasaki S, Mitani N, Okita K. Epstein-Barr virus infection of the colon with inflammatory bowel disease. Am J Gastroenterol 1999; 94: 1582-1586 [PMID: 10364028 DOI: 10.1111/j.1572-0241.1999.01148.x]
29. Vega R, Bertrán X, Menacho M, Domènech E, Moreno de Vega V, Hombrados M, Cabré E, Ojanguren I, Gassull MA. Cytomegalovirus infection in patients with inflammatory bowel disease. Am J Gastroenterol 1999; 94: 1053-1056 [PMID: 10201482 DOI: 10.1111/j.1572-0241.1999.01013.x]
30. 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 [PMID: 20112061 DOI: 10.1007/s10620-010-1126-4]
31. 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 [PMID: 22538204 DOI: 10.1016/j.dld.2012.03.018]
32. McCoy MH, Post K, Sen JD, Chang HY, Zhao Z, Fan R, Chen S, Leland D, Cheng L, Lin J. qPCR increases sensitivity to detect cytomegalovirus in formalin-fixed, paraffin-embedded tissue of gastrointestinal biopsies. Hum Pathol 2014; 45: 48-53 [PMID: 24139212 DOI: 10.1016/j.humpath.2013.07.040]
33. Roblin X, Pillet S, Oussalah A, Berthelot P, Del Tedesco E, Phelip JM, Chambonnière ML, Garraud O, Peyrin-Biroulet L, Pozzetto B. Cytomegalovirus load in inflamed intestinal tissue is predictive of resistance to immunosuppressive therapy in ulcerative colitis. Am J Gastroenterol 2011; 106: 2001-2008 [PMID: 21788989 DOI: 10.1038/ajg.2011.202]
34. Yoshino T, Nakase H, Ueno S, Uza N, Inoue S, Mikami S, Matsuura M, Ohmori K, Sakurai T, Nagayama S, Hasegawa S, Sakai Y, Chiba T. 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 [PMID: 17828781 DOI: 10.1002/ibd.20253]
35. Ganzenmueller T, Henke-Gendo C, Schlué J, Wedemeyer J, Huebner S, Heim A. Quantification of cytomegalovirus DNA levels in intestinal biopsies as a diagnostic tool for CMV intestinal disease. J Clin Virol 2009; 46: 254-258 [PMID: 19748823 DOI: 10.1016/j.jcv.2009.08.008]
36. Folkins AK, Chisholm KM, Guo FP, McDowell M, Aziz N, Pinsky BA. Diagnosis of congenital CMV using PCR performed on formalin-fixed, paraffin-embedded placental tissue. Am J Surg Pathol 2013; 37: 1413-1420 [PMID: 23797721 DOI: 10.1097/PAS.0b013e318290f171]
37. Herfarth HH, Long MD, Rubinas TC, Sandridge M, Miller MB. Evaluation of a non-invasive method to detect cytomegalovirus (CMV)-DNA in stool samples of patients with inflammatory bowel disease (IBD): a pilot study. Dig Dis Sci 2010; 55: 1053-1058 [PMID: 20165976 DOI: 10.1007/s10620-010-1146-0]
38. Rahier JF, Magro F, Abreu C, Armuzzi A, Ben-Horin S, Chowers Y, Cottone M, de Ridder L, Doherty G, Ehehalt R, Esteve M, Katsanos K, Lees CW, Macmahon E, Moreels T, Reinisch W, Tilg H, Tremblay L, Veereman-Wauters G, Viget N, Yazdanpanah Y, Eliakim R, Colombel JF. 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 [PMID: 24613021 DOI: 10.1016/j.crohns.2013.12.013]
39. Dimitroulia E, Pitiriga VC, Piperaki ET, Spanakis NE, Tsakris A. Inflammatory bowel disease exacerbation associated with Epstein-Barr virus infection. Dis Colon Rectum 2013; 56: 322-327 [PMID: 23392146 DOI: 10.1097/DCR.0b013e31827cd02c]
40. Ryan JL, Shen YJ, Morgan DR, Thorne LB, Kenney SC, Dominguez RL, Gulley ML. Epstein-Barr virus infection is common in inflamed gastrointestinal mucosa. Dig Dis Sci 2012; 57: 1887-1898 [PMID: 22410851 DOI: 10.1007/s10620-012-2116-5]
41. Sankaran-Walters S, Ransibrahmanakul K, Grishina I, Hung J, Martinez E, Prindiville T, Dandekar S. Epstein-Barr virus replication linked to B cell proliferation in inflamed areas of colonic mucosa of patients with inflammatory bowel disease. J Clin Virol 2011; 50: 31-36 [PMID: 21035384 DOI: 10.1016/j.jcv.2010.09.011]
42. Iwamoto GK, Monick MM, Clark BD, Auron PE, Stinski MF, Hunninghake GW. Modulation of interleukin 1 beta gene expression by the immediate early genes of human cytomegalovirus. J Clin Invest 1990; 85: 1853-1857 [PMID: 2161430 DOI: 10.1172/JCI114645]
43. Vogl BA, Fagin U, Nerbas L, Schlenke P, Lamprecht P, Jabs WJ. Longitudinal analysis of frequency and reactivity of Epstein-Barr virus-specific T lymphocytes and their association with intermittent viral reactivation. J Med Virol 2012; 84: 119-131 [PMID: 22095540 DOI: 10.1002/jmv.22258]
44. Baroco AL, Oldfield EC. Gastrointestinal cytomegalovirus disease in the immunocompromised patient. Curr Gastroenterol Rep 2008; 10: 409-416 [PMID: 18627655 DOI: 10.1007/s11894-008-0077-9]
45. Lavagna A, Bergallo M, Daperno M, Sostegni R, Costa C, Leto R, Crocellà L, Molinaro G, Rocca R, Cavallo R, Pera A. Infliximab and the risk of latent viruses reactivation in active Crohn's disease. Inflamm Bowel Dis 2007; 13: 896-902 [PMID: 17345605 DOI: 10.1002/ibd.20131]
46. Helbling D, Breitbach TH, Krause M. Disseminated cytomegalovirus infection in Crohn's disease following anti-tumour necrosis factor therapy. Eur J Gastroenterol Hepatol 2002; 14: 1393-1395 [PMID: 12468964 DOI: 10.1097/00042737-200212000-00018]
47. Nebbia G, Mattes FM, Sabin CA, Samonakis D, Rolando N, Burroughs AK, Emery VC. Differential effects of prednisolone and azathioprine on the development of human cytomegalovirus replication post liver transplantation. Transplantation 2007; 84: 605-610 [PMID: 17876273 DOI: 10.1097/01.tp.0000280555.08651.11]
48. Forbes BA, Bonville CA, Dock NL. The effects of a promoter of cell differentiation and selected hormones on human cytomegalovirus infection using an in vitro cell system. J Infect Dis 1990; 162: 39-45 [PMID: 1693943 DOI: 10.1093/infdis/162.1.39]
49. Gerna G, Lilleri D, Furione M, Castiglioni B, Meloni F, Rampino T, Agozzino M, Arbustini E. Human cytomegalovirus endorgan disease is associated with high or low systemic viral load in preemptively treated solid-organ transplant recipients. New Microbiol 2012; 35: 279-287 [PMID: 22842597]