Cytomegalovirus infection and the gastrointestinal tract

Current Gastroenterology Reports

Volumn 14, Issue 4, 2012, Pages 334-342

  You, David M ^a   Johnson, Mark D ^a  

^a NAVAL MEDICAL CENTER SAN DIEGO   (United States)

Author keywords

CMV treatment; Colitis; Cytomegalovirus (CMV); Esophagitis; Ganciclovir resistant CMV; Gastritis; Gastrointestinal; Transplantation CMV

Indexed keywords

BENZIMIDAVIR; CIDOFOVIR; CIDOFOVIR 3 HEXADECYLOXYPROPYL ESTER; FOSCARNET; GANCICLOVIR; PLACEBO; VALGANCICLOVIR;

ANEMIA; ARTICLE; CLINICAL FEATURE; COLITIS; CYTOMEGALOVIRUS INFECTION; CYTOMEGALOVIRUS RETINITIS; DRUG RESPONSE; ESOPHAGITIS; GASTRITIS; GASTROINTESTINAL INFECTION; HISTOPATHOLOGY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HYPERPHOSPHATEMIA; HYPOCALCEMIA; HYPOMAGNESEMIA; HYPOPHOSPHATEMIA; IMMUNOASSAY; INTERMETHOD COMPARISON; INTESTINE INFECTION; NEPHROTOXICITY; NEUTROPENIA; NONHUMAN; POLYMERASE CHAIN REACTION; POSTOPERATIVE INFECTION; THROMBOCYTOPENIA; TREATMENT OUTCOME; ULCERATIVE COLITIS; VIRUS ENCEPHALITIS; VIRUS PATHOGENESIS; VIRUS PNEUMONIA;

AIDS-RELATED OPPORTUNISTIC INFECTIONS; ANTIVIRAL AGENTS; CYTOMEGALOVIRUS INFECTIONS; GANCICLOVIR; GASTROENTERITIS; HUMANS; INFLAMMATORY BOWEL DISEASES; OPPORTUNISTIC INFECTIONS; ORGAN TRANSPLANTATION;

EID: 84865661248     PISSN: 15228037     EISSN: 1534312X     Source Type: Journal    
DOI: 10.1007/s11894-012-0266-4     Document Type: Article

References (91)

1. Staras SA, Dollard SC, Radford KW, et al. Seroprevalence of cytomegalovirus infection in the United States, 1988-1994. Clin Infect Dis. 2006;43:1143-51. (Pubitemid 44632796)
2. Drew WL, Mintz L, Miner RC, et al. Prevalence of cytomegalovirus infection in homosexual men. J Infect Dis. 1981;143:188-92. (Pubitemid 11147842)
3. Klemola E, Von Essen R, Henle G, Henle W. Infectiousmononucleosis-like disease with negative heterophil agglutination test. Clinical features in relation to Epstein-Barr virus and cytomegalovirus antibodies. J Infect Dis. 1970;121:608-14.
4. Adler B, Sinzger C. Endothelial cells in human cytomegalovirus infection: One host cell out of many or a crucial target for virus spread? Thromb Haemost. 2009;102:1057-63.
5. Eddleston M, Peacock S, Juniper M, Warrell DA. Severe cytomegalovirus infection in immunocompetent patients. Clin Infect Dis. 1997;24:52-6. (Pubitemid 27023672)
6. Rafailidis PI, Mourtzoukou EG, Varbobitis IC, Falagas ME. Severe cytomegalovirus infection in apparently immunocompetent patients: A systematic review. Virol J. 2008;5:47.
7. Oku T, Maeda M, Waga E, et al. Cytomegalovirus cholangitis and pancreatitis in an immunocompetent patient. J Gastroenterol. 2005;40:987-92. (Pubitemid 41662523)
8. Cook CH, Trgovcich J, Zimmerman PD, et al. Lipopolysaccharide, tumor necrosis factor alpha, or interleukin-1beta triggers reactivation of latent cytomegalovirus in immunocompetent mice. J Virol. 2006;80:9151-8. (Pubitemid 44359987)
9. Squizzato A, Ageno W, Cattaneo A, Brumana N. A case report and literature review of portal vein thrombosis associated with cytomegalovirus infection in immunocompetent patients. Clin Infect Dis. 2007;44:e13-6.
10. Hommes DW, Sterringa G, van Deventer SJ, et al. The pathogenicity of cytomegalovirus in inflammatory bowel disease: A systematic review and evidence-based recommendations for future research. Inflamm Bowel Dis. 2004;10:245-50. (Pubitemid 38618254)
11. Britt W. Manifestations of human cytomegalovirus infection: Proposed mechanisms of acute and chronic disease. Curr Top Microbiol Immunol. 2008;325:417-70.
12. Baehr PH, McDonald GB. Esophageal infections: Risk factors, presentation, diagnosis, and treatment. Gastroenterology. 1994;106:509-32. (Pubitemid 24041232)
13. Wilcox CM, Straub RF, Schwartz DA. Prospective endoscopic characterization of cytomegalovirus esophagitis in AIDS. Gastrointest Endosc. 1994;40:481-4. (Pubitemid 24235581)
14. Kanda K, Kume K, Yoshikawa I, et al. Cytomegalovirus esophagitis with massive upper-GI hemorrhage. Gastrointest Endosc. 2004;59:741-3. (Pubitemid 38609716)
15. Wilcox CM, Straub RF, Schwartz DA. Cytomegalovirus esophagitis in AIDS: A prospective evaluation of clinical response to ganciclovir therapy, relapse rate, and long-term outcome. Am J Med. 1995;98:169-76.
16. Altman C, Bedossa P, Dussaix E, Buffet C. Cytomegalovirus infection of esophagus in immunocompetent adult. Dig Dis Sci. 1995;40:606-8.
17. Weile J, Streeck B, Muck J, et al. Severe cytomegalovirusassociated esophagitis in an immunocompetent patient after short-term steroid therapy. J Clin Microbiol. 2009;47:3031-3.
18. Laguna F, Garcia-Samaniego J, Alonso MJ, et al. Pseudotumoral appearance of cytomegalovirus esophagitis and gastritis in AIDS patients. Am J Gastroenterol. 1993;88:1108-11. (Pubitemid 23191106)
19. Wilcox CM, Straub RF, Schwartz DA. Prospective evaluation of biopsy number for the diagnosis of viral esophagitis in patients with HIV infection and esophageal ulcer. Gastrointest Endosc. 1996;44:587-93. (Pubitemid 26386906)
20. Moustafellos P, Hadjianastasiou V, Gray D. Postural epigastric pain as a sign of CMV gastritis: A case report. Transplant Proc. 2006;38:1357-8.
21. Giladi M, Lembo A, Johnson Jr BL. Postural epigastric pain: A unique symptom of primary cytomegalovirus gastritis? Infection. 1998;26:234-5. (Pubitemid 28388882)
22. Van Thiel DH, Gavaler JS, Schade RR, et al. Cytomegalovirus infection and gastric emptying. Transplantation. 1992;54:70-3.
23. Reggiani Bonetti L, Losi L, Di Gregorio C, et al. Cytomegalovirus infection of the upper gastrointestinal tract: A clinical and pathological study of 30 cases. Scand J Gastroenterol 2011,46:1228-35. One of the larger case series of upper tract disease, describes the most common endoscopic findings.
24. Kaplan CS, Petersen EA, Icenogle TB, et al. Gastrointestinal cytomegalovirus infection in heart and heart-lung transplant recipients. Arch Intern Med. 1989;149:2095-100. (Pubitemid 19232233)
25. Mong A, Levine MS, Furth EE, Laufer I. Cytomegalovirus duodenitis in an AIDS patient. AJR Am J Roentgenol. 1999;172:939-40. (Pubitemid 29505616)
26. Kelesidis T, Tozzi S, Mitty R, et al. Cytomegalovirus pseudotumor of the duodenum in a patient with AIDS: An unrecognized and potentially treatable clinical entity. Int J Infect Dis. 2010;14: E274-82.
27. Mohan H, Bal A, Garg S, Dalal U. Cytomegalovirus-associated pseudotumor simulating gastric malignancy in acquired immunodeficiency syndrome: A case report with review of literature. Jpn J Infect Dis. 2007;60:134-6. (Pubitemid 47009533)
28. Kram HB, Shoemaker WC. Intestinal perforation due to cytomegalovirus infection in patients with AIDS. Dis Colon Rectum. 1990;33:1037-40.
29. DeRiso 2nd AJ, Kemeny MM, Torres RA, Oliver JM. Multiple jejunal perforations secondary to cytomegalovirus in a patient with acquired immune deficiency syndrome. Case report and review. Dig Dis Sci. 1989;34:623-9.
30. Martinez C, Rosales M, Calvo X, et al. Serial intestinal endoscopic examinations of patients with persistent diarrhea after allo-SCT. Bone Marrow Transplant 2011, epub ahead of print. Describes the impact of treatment decisions that repeated biopsies can have on differentiation between GVHD and GI CMV disease.
31. Ng FH, Chau TN, Cheung TC, et al. Cytomegalovirus colitis in individuals without apparent cause of immunodeficiency. Dig Dis Sci. 1999;44:945-52.
32. Dieterich DT, Rahmin M. Cytomegalovirus colitis in AIDS: Presentation in 44 patients and a review of the literature. J Acquir Immune Defic Syndr. 1991;4 Suppl 1:S29-35.
33. Cheung TW, Teich SA. Cytomegalovirus infection in patients with HIV infection. Mt Sinai J Med. 1999;66:113-24. (Pubitemid 29136438)
34. Lin YH, Yeh CJ, Chen YJ, et al. Recurrent cytomegalovirus colitis with megacolon in an immunocompetent elderly man. J Med Virol. 2010;82:638-41.
35. Studemeister A. Cytomegalovirus proctitis: A rare and disregarded sexually transmitted disease. Sex Transm Dis. 2011;38:876-8.
36. Bhaijee F, Subramony C, Tang SJ, Pepper DJ. Human immunodeficiency virus-associated gastrointestinal disease: Common endoscopic biopsy diagnoses. Patholog Res Int. 2011;2011:247923.
37. Imam SZ, Khan A, Jaso JM, Foringer Jr. Quiz page. CMV colitis presenting as a colonic mass. Am J Kidney Dis. 2010;55:A35-7.
38. Galiatsatos P, Shrier I, Lamoureux E, Szilagyi A. Meta-analysis of outcome of cytomegalovirus colitis in immunocompetent hosts. Dig Dis Sci. 2005;50:609-16. (Pubitemid 40558448)
39. Revello MG, Gerna G. Diagnosis and management of human cytomegalovirus infection in the mother, fetus, and newborn infant. Clin Microbiol Rev. 2002;15:680-715. (Pubitemid 41184084)
40. Weber B, Fall EM, Berger A, Doerr HW. Screening of blood donors for human cytomegalovirus (HCMV) IgG antibody with an enzyme immunoassay using recombinant antigens. J Clin Virol. 1999;14:173-81.
41. Jang EY, Park SY, Lee EJ, et al. Diagnostic performance of the cytomegalovirus (CMV) antigenemia assay in patients with CMV gastrointestinal disease. Clin Infect Dis. 2009;48:e121-4.
42. Nagata N, Kobayakawa M, Shimbo T, et al. Diagnostic value of antigenemia assay for cytomegalovirus gastrointestinal disease in immunocompromised patients.World J Gastroenterol. 2011;17:1185-91.
43. Kandiel A, Lashner B. Cytomegalovirus colitis complicating inflammatory bowel disease. Am J Gastroenterol. 2006;101:2857-65. (Pubitemid 44902661)
44. Kalpoe JS, Kroes AC, de Jong MD, et al. Validation of clinical application of cytomegalovirus plasma DNA load measurement and definition of treatment criteria by analysis of correlation to antigen detection. J Clin Microbiol. 2004;42:1498-504. (Pubitemid 38500787)
45. Martin-Davila P, Fortun J, Gutierrez C, et al. Analysis of a quantitative PCR assay for CMV infection in liver transplant recipients: An intent to find the optimal cut-off value. J Clin Virol. 2005;33:138-44. (Pubitemid 40725308)
46. Caliendo AM, Schuurman R, Yen-Lieberman B, et al. Comparison of quantitative and qualitative PCR assays for cytomegalovirus DNA in plasma. J Clin Microbiol. 2001;39:1334-8. (Pubitemid 32275431)
47. Humar A, Gregson D, Caliendo AM, et al. Clinical utility of quantitative cytomegalovirus viral load determination for predicting cytomegalovirus disease in liver transplant recipients. Transplantation. 1999;68:1305-11.
48. Boeckh M, Gooley TA, Myerson D, et al. Cytomegalovirus pp 65 antigenemia-guided early treatment with ganciclovir versus ganciclovir at engraftment after allogeneic marrow transplantation: A randomized double-blind study. Blood. 1996;88:4063-71. (Pubitemid 26383133)
49. Lawlor G, Moss AC. Cytomegalovirus in inflammatory bowel disease: Pathogen or innocent bystander? Inflamm Bowel Dis 2010,16:1620-7. Thoughtful discussion of the clinical importance of CMV identified in the setting of IBD.
50. Reddy N, Wilcox CM. Diagnosis & management of cytomegalovirus infections in the GI tract. Expert Rev Gastroenterol Hepatol 2007,1:287-94. Although it doesn't discuss the range of clinical manifestations of GI CMV disease in any detail, it provides a thorough review of currently available lab diagnostics and fairly updated review of available antiviral therapy.
51. 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:S1-12. (Pubitemid 35287187)
52. 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;14:1373-9.
53. Cottone M, Pietrosi G, Martorana G, et al. Prevalence of cytomegalovirus infection in severe refractory ulcerative and Crohn's colitis. Am J Gastroenterol. 2001;96:773-5. (Pubitemid 32240729)
54. Kaufman HS, Kahn AC, Iacobuzio-Donahue C, et al. Cytomegaloviral enterocolitis: Clinical associations and outcome. Dis Colon Rectum. 1999;42:24-30. (Pubitemid 29053116)
55. Kornbluth A, Sachar DB. Ulcerative colitis practice guidelines in adults: American College Of Gastroenterology, Practice Parameters Committee. Am J Gastroenterol 2010,105:501-23. Most up to date American College of Gastroenterology Ulcerative Colitis Practice Guidelines, in which the recommendations for management of severe colitis include discussion of diagnosis and management of CMV superinfection.
56. 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;106:2001-8.
57. Fica A, Cervera C, Perez N, et al. Immunohistochemically proven cytomegalovirus end-organ disease in solid organ transplant patients: Clinical features and usefulness of conventional diagnostic tests. Transpl Infect Dis. 2007;9:203-10. (Pubitemid 47231211)
58. Lemonovich TL, Watkins RR. Update on cytomegalovirus infections of the gastrointestinal system in solid organ transplant recipients. Curr Infect Dis Rep 2012,14:33-40. Somewhat narrower scope, focuses on CMV in GI in SOT. Because of this narrower scope, is able to discuss in depth prevention strategies, which were not discussed in any length in by our review.
59. Linares L, Sanclemente G, Cervera C, et al. Influence of cytomegalovirus disease in outcome of solid organ transplant patients. Transplant Proc. 2011;43:2145-8.
60. Eid AJ, Razonable RR. New developments in the management of cytomegalovirus infection after solid organ transplantation. Drugs 2010,70:965-81. Thorough review of newest available therapies for CMV treatment.
61. Arthurs SK, Eid AJ, Pedersen RA, et al. Delayed-onset primary cytomegalovirus disease after liver transplantation. Liver Transpl. 2007;13:1703-9.
62. Eid AJ, Arthurs SK, Deziel PJ, et al. Clinical predictors of relapse after treatment of primary gastrointestinal cytomegalovirus disease in solid organ transplant recipients. Am J Transplant. 2010;10:157-61.
63. Jacobson MA, Mills J. Serious cytomegalovirus disease in the acquired immunodeficiency syndrome (AIDS). Clinical findings, diagnosis, and treatment. Ann Intern Med. 1988;108:585-94.
64. Chui DW, Owen RL. AIDS and the gut. J Gastroenterol Hepatol. 1994;9:291-303. (Pubitemid 24149297)
65. Salzberger B, Hartmann P, Hanses F, et al. Incidence and prognosis of CMV disease in HIV-infected patients before and after introduction of combination antiretroviral therapy. Infection. 2005;33:345-9. (Pubitemid 41552011)
66. El Amari EB, Combescure C, Yerly S, et al. Clinical relevance of cytomegalovirus viraemia. HIV Med 2011,12:394-402.
67. Feasey NA, Healey P, Gordon MA. Review article: The aetiology, investigation and management of diarrhoea in the HIV-positive patient. Aliment Pharmacol Ther. 2011;34:587-603.
68. Bini EJ, Weinshel EH. Endoscopic evaluation of chronic human immunodeficiency virus-related diarrhea: Is colonoscopy superior to flexible sigmoidoscopy? Am J Gastroenterol. 1998;93:56-60. (Pubitemid 29065514)
69. Khater FJ, Myers JW, Moorman JP. A 45-year-old woman with fever and splenic infarcts. Clin Infect Dis. 2003;37(1093):125-6.
70. Serna-Higuera C, Gonzalez-Garcia M, Milicua JM, Munoz V. Acute cholestatic hepatitis by cytomegalovirus in an immunocompetent patient resolved with ganciclovir. J Clin Gastroenterol. 1999;29:276-7. (Pubitemid 29451351)
71. Laing RB, Dykhuizen RS, Smith CC, Molyneaux PJ. Parenteral ganciclovir treatment of acute CMV infection in the immunocompetent host. Infection. 1997;25:44-6. (Pubitemid 27075660)
72. Cvetkovic RS, Wellington K. Valganciclovir: A review of its use in the management of CMV infection and disease in immunocompromised patients. Drugs. 2005;65:859-78. (Pubitemid 40598096)
73. Dieterich DT, PolesMA, Lew EA, et al. Treatment of gastrointestinal cytomegalovirus infection with twice-daily foscarnet: A pilot study of safety, efficacy, and pharmacokinetics in patients with AIDS. Antimicrob Agents Chemother. 1997;41:1226-30. (Pubitemid 27231418)
74. 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;46:51-6.
75. Andrews PA, Emery VC, Newstead C. Summary of the British Transplantation Society Guidelines for the Prevention and Management of CMV Disease After Solid Organ Transplantation. Transplantation 2011,92:1181-7. An update to be compared to Kotton CN et al. International Consensus Guidelines on the Management of Cytomegalovirus in Solid Organ Transplant. Transplantation 2010,89:779-95.
76. Asberg A, Humar A, Rollag H, et al. Oral valganciclovir is noninferior to intravenous ganciclovir for the treatment of cytomegalovirus disease in solid organ transplant recipients. Am J Transplant 2007,7:2106-13. Randomized prospective trial of 321 SOT recipients demonstrating non inferiority of oral valganciclovir compared to standard of care intravenous ganciclovir. This is the first publication of its kind supporting use of a simpler oral antiviral. (Pubitemid 47247057)
77. Len O, Gavalda J, Aguado JM, et al. Valganciclovir as treatment for cytomegalovirus disease in solid organ transplant recipients. Clin Infect Dis. 2008;46:20-7. (Pubitemid 351263554)
78. Whitley RJ, Jacobson MA, Friedberg DN, et al. Guidelines for the treatment of cytomegalovirus diseases in patients with AIDS in the era of potent antiretroviral therapy: Recommendations of an international panel. International AIDS Society-USA. Arch Intern Med 1998,158:957-69. Seminal consensus statement from IASUSA for management of CMV in AIDS, which includes a discussion about GI disease in particular. (Pubitemid 28213573)
79. Blanshard C. Treatment of HIV-related cytomegalovirus disease of the gastrointestinal tract with foscarnet. J Acquir Immune Defic Syndr. 1992;5 Suppl 1:S25-8.
80. Blanshard C, Benhamou Y, Dohin E, et al. Treatment of AIDSassociated gastrointestinal cytomegalovirus infection with foscarnet and ganciclovir: A randomized comparison. J Infect Dis. 1995;172:622-8.
81. Limaye AP, Raghu G, Koelle DM, et al. High incidence of ganciclovir-resistant cytomegalovirus infection among lung transplant recipients receiving preemptive therapy. J Infect Dis. 2002;185:20-7. (Pubitemid 34043012)
82. Limaye AP. Ganciclovir-resistant cytomegalovirus in organ transplant recipients. Clin Infect Dis. 2002;35:866-72.
83. Kaul DR, Stoelben S, Cober E, et al. First report of successful treatment of multidrug-resistant cytomegalovirus disease with the novel anti-CMV compound AIC246. Am J Transplant. 2011;11:1079-84.
84. Arav-Boger R, He R, Chiou CJ, et al. Artemisinin-derived dimers have greatly improved anti-cytomegalovirus activity compared to artemisinin monomers. PLoS One. 2010;5:e10370.
85. Avery RK, Mossad SB, Poggio E, et al. Utility of leflunomide in the treatment of complex cytomegalovirus syndromes. Transplantation. 2010;90:419-26.
86. Avery RK, Marty FM, Strasfeld L, et al. Oral maribavir for treatment of refractory or resistant cytomegalovirus infections in transplant recipients. Transpl Infect Dis. 2010;12:489-96.
87. Trofe J, Pote L, Wade E, et al. Maribavir: A novel antiviral agent with activity against cytomegalovirus. Ann Pharmacother. 2008;42:1447-57.
88. Marty FM, Ljungman P, Papanicolaou GA, et al. Maribavir prophylaxis for prevention of cytomegalovirus disease in recipients of allogeneic stem-cell transplants: A phase 3, double-blind, placebocontrolled, randomised trial. Lancet Infect Dis. 2011;11:284-92.
89. Bravo FJ, Bernstein DI, Beadle JR, et al. Oral hexadecyloxypropylcidofovir therapy in pregnant guinea pigs improves outcome in the congenital model of cytomegalovirus infection. Antimicrob Agents Chemother. 2011;55:35-41.
90. Quenelle DC, Lampert B, Collins DJ, et al. Efficacy of CMX001 against herpes simplex virus infections in mice and correlations with drug distribution studies. J Infect Dis. 2010;202:1492-9.
91. Price NB, Prichard MN. Progress in the Development of New Therapies for Herpesvirus Infections. Curr Opin Virol 2011,1:548-54. Thorough review of newest available therapies for CMV treatment.