Diarrhea in liver transplant recipients: Etiology and management

Liver Transplantation

Volumn 11, Issue 8, 2005, Pages 881-890

  Ginsburg, Philip M ^a   Thuluvath, Paul J ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; ANTIINFECTIVE AGENT; ANTIPARASITIC AGENT; ANTIVIRUS AGENT; AZATHIOPRINE; CORTICOSTEROID; CYCLOSPORIN A; GANCICLOVIR; IMMUNOMODULATING AGENT; IMMUNOSUPPRESSIVE AGENT; METRONIDAZOLE; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; RAPAMYCIN; TACROLIMUS;

CLOSTRIDIUM DIFFICILE; COLON CANCER; CYTOMEGALOVIRUS; DIARRHEA; DISEASE EXACERBATION; DRUG MECHANISM; ENTERITIS; GRAFT VERSUS HOST REACTION; HUMAN; INTESTINE INFECTION; LIVER TRANSPLANTATION; LYMPHOPROLIFERATIVE DISEASE; POSTOPERATIVE COMPLICATION; PRIORITY JOURNAL; REVIEW; SYMPTOMATOLOGY;

COLONIC NEOPLASMS; DIARRHEA; GRAFT VS HOST DISEASE; HUMANS; IMMUNOSUPPRESSIVE AGENTS; INFECTION; INFLAMMATORY BOWEL DISEASES; LIVER TRANSPLANTATION; LYMPHOPROLIFERATIVE DISORDERS;

EID: 23744452277     PISSN: 15276465     EISSN: None     Source Type: Journal    
DOI: 10.1002/lt.20500     Document Type: Review

References (93)

1. Cox GJ, Matsui SM, Lo RS, Hinds M, Bowden RA, Hackman RC, et al. Etiology and outcome of diarrhea after marrow transplantation: a prospective study. Gastroenterology 1994;107: 1398-1407.
2. Altiparmak MR, Trablus S, Pamuk ON, Apaydin S, Sariyar M, Ozturk R, et al. Diarrhoea following renal transplantation. Clin Transplant 2002;16:212-216.
3. Framm SR, Soave R. Agents of diarrhea. Med Clin North Am 1997;81:427-447.
4. Wong NA, Bathgate AJ, Bellamy CO. Colorectal disease in liver allograft recipients - a clinicopathological study with follow-up. Eur J Gastroenterol Hepatol 2002;14:231-236.
5. Pescovitz MD, Navarro MT. Immunosuppressive therapy and post-transplantation diarrhea. Clin Transplant 2001;15(Suppl 4):23-28.
6. McFarland LV, Mulligan ME, Kwok RY, Stamm WE. Nosocomial acquisition of Clostridium difficile infection. N Engl J Med 1989;320:204-210.
7. Yassin SF, Young-Fadok TM, Zein NN, Pardi DS. Clostridium difficile-associated diarrhea and colitis. Mayo Clin Proc 2001;76: 725-730.
8. Safdar N, Maki DG. The commonality of risk factors for nosocomial colonization and infection with antimicrobial-resistant Staphylococcus aureus, Enterococcus, gram-negative bacilli, Clostridium difficile, and Candida. Ann Intern Med 2002; 136:834-844.
9. Willingham FF, Ticona CE, Taylor DN, Bowen AB, Crane AR, Gottlieb AL, et al. Diarrhea and Clostridium difficile infection in Latin American patients with AIDS. Working Group on AIDS in Peru. Clin Infect Dis 1998;27:487-493.
10. Dallal RM, Harbrecht BG, Boujoukas AJ, Sirio CA, Farkas LM, Lee KK, et al. Fulminant Clostridium difficile: an underappreciated and increasing cause of death and complications. Ann Surg 2002;235:363-372.
11. Keven K, Basu A, Re L, Tan H, Marcos A, Fung JJ, et al. Clostridium difficile colitis in patients after kidney and pancreas-kidney transplantation. Transpl Infect Dis 2004;6:10-14.
12. Ziring D, Tran R, Edelstein S, McDiarmid SV, Vargas J, Cortina G, et al. Infectious enteritis after intestinal transplantation: incidence, timing, and outcome. Transplant Proc 2004;36:379-380.
13. Chakrabarti S, Lees A, Jones SG, Milligan DW. Clostridium difficile infection in allogeneic stem cell transplant recipients is associated with severe graft-versus-host disease and non-relapse mortality. Bone Marrow Transplant 2000;26:871-876.
14. Dettenkofer M, Ebner W, Bertz H, Babikir R, Finke J, Frank U, et al. Surveillance of nosocomial infections in adult recipients of allogeneic and autologous bone marrow and peripheral blood stem-cell transplantation. Bone Marrow Transplant 2003;31: 795-801.
15. Alexander JA, Cuellar RE, Fadden RJ, Genovese JJ, Gavaler JS, Van Thiel DH. Cytomegalovirus infection of the upper gastrointestinal tract before and after liver transplantation. Transplantation 1988;46:378-382.
16. Van Thiel DH, Gavaler JS, Schade RR, Chien MC, Starzl TE. Cytomegalovirus infection and gastric emptying. Transplantation 1992;54:70-73.
17. Kanj SS, Sharara AI, Clavien PA, Hamilton JD. Cytomegalovirus infection following liver transplantation: review of the literature. Clin Infect Dis 1996;22:537-549.
18. Paya CV, Wilson JA, Espy MJ, Sia IG, DeBernardi MJ, Smith TF, et al. Preemptive use of oral ganciclovir to prevent cytomegalovirus infection in liver transplant patients: a randomized, placebo-controlled trial. J Infect Dis 2002;185:854-860.
19. Rayes N, Oettle H, Schmidt CA, Lohmann R, Steinmuller T, Bechstein WO, et al. Preemptive therapy in CMV-antigen positive patients after liver transplantation - a prospective trial. Ann Transplant 1999;4:12-17.
20. Rayes N, Seehofer D, Schmidt CA, Oettle H, Muller AR, Steinmuller T, et al. Prospective randomized trial to assess the value of preemptive oral therapy for CMV infection following liver transplantation. Transplantation 2001;72:881-885.
21. Singh N, Wannstedt C, Keyes L, Wagener MM, de Vera M, Cacciarelli TV, et al. Impact of evolving trends in recipient and donor characteristics on cytomegalovirus infection in liver transplant recipients. Transplantation 2004;77:106-110.
22. Burak KW, Kremers WK, Batts KP, Wiesner RH, Rosen CB, Razonable RR, et al. Impact of cytomegalovirus infection, year of transplantation, and donor age on outcomes after liver transplantation for hepatitis C. Liver Transpl 2002;8:362-369.
23. Millar AJ, Spearman W, McCulloch M, Goddard E, Raad J, Rode H, et al. Liver transplantation for children - the Red Cross Children's Hospital experience. Pediatr Transplant 2004;8:136-144.
24. Oldakowska-Jedynak U, Niewczas M, Ziolkowski J, Mucha K, Foroncewicz B, Bartlomiejczyk I, et al. Cytomegalovirus infection as a common complication following liver transplantation. Transplant Proc 2003;35:2295-2297.
25. Halme L, Hockerstedt K, Salmela K, Lautenschlager I. Cytomegalovirus detected in the upper gastrointestinal tract parallel with CMV-antigenemia in liver transplant patients. Transplant Proc 1999;31:487.
26. Halme L, Hockerstedt K, Salmela K, Lautenschlager I. CMV infection detected in the upper gastrointestinal tract after liver transplantation. Transpl Int 1998;11(Suppl 1):S242-S244.
27. Halme L, Hockerstedt K, Lautenschlager I. Cytomegalovirus infection and development of biliary complications after liver transplantation. Transplantation 2003;75:1853-1858.
28. Barkholt L, Lewensohn-Fuchs I, Ericzon BG, Tyden G, Andersson J. High-dose acyclovir prophylaxis reduces cytomegalovirus disease in liver transplant patients. Transpl Infect Dis 1999;1:89-97.
29. Gane E, Saliba F, Valdecasas GJ, O'Grady J, Pescovitz MD, Lyman S, et al. Randomised trial of efficacy and safety of oral ganciclovir in the prevention of cytomegalovirus disease in liver-transplant recipients. The Oral Ganciclovir International Transplantation Study Group [Corrected]. Lancet 1997;350:1729-1733.
30. Singh N, Paterson DL, Gayowski T, Wagener MM, Marino IR. Cytomegalovirus antigenemia directed pre-emptive prophylaxis with oral versus I.V. ganciclovir for the prevention of cytomegalovirus disease in liver transplant recipients: a randomized, controlled trial. Transplantation 2000;70:717-722.
31. Trotter JF, Wallack A, Steinberg T. Low incidence of cytomegalovirus disease in liver transplant recipients receiving sirolimus primary immunosuppression with 3-day corticosteroid taper. Transpl Infect Dis 2003;5:174-180.
32. Seu P, Winston DJ, Holt CD, Kaldas F, Busuttil RW. Long-term ganciclovir prophylaxis for successful prevention of primary cytomegalovirus (CMV) disease in CMV-seronegative liver transplant recipients with CMV-seropositive donors. Transplantation 1997;64:1614-1617.
33. Winston DJ, Wirin D, Shaked A, Busuttil RW. Randomised comparison of ganciclovir and high-dose acyclovir for long-term cytomegalovirus prophylaxis in liver-transplant recipients. Lancet 1995;346:69-74.
34. Winston DJ, Busuttil RW. Randomized controlled trial of oral ganciclovir versus oral acyclovir after induction with intravenous ganciclovir for long-term prophylaxis of cytomegalovirus disease in cytomegalovirus-seropositive liver transplant recipients. Transplantation 2003;75:229-233.
35. Winston DJ, Busuttil RW. Randomized controlled trial of sequential intravenous and oral ganciclovir versus prolonged intravenous ganciclovir for long-term prophylaxis of cytomegalovirus disease in high-risk cytomegalovirus-seronegative liver transplant recipients with cytomegalovirus-seropositive donors. Transplantation 2004;77:305-308.
36. van Kraaij MG, Dekker AW, Verdonck LF, van Loon AM, Vinje J, Koopmans MP, et al. Infectious gastro-enteritis: an uncommon cause of diarrhoea in adult allogeneic and autologous stem cell transplant recipients. Bone Marrow Transplant 2000;26: 299-303.
37. Goetz M, Eichenlaub S, Pape GR, Hoffmann RM. Chronic diarrhea as a result of intestinal microsposidiosis in a liver transplant recipient. Transplantation 2001;71:334-337.
38. Gerber DA, Green M, Jaffe R, Greenberg D, Mazariegos G, Reyes J. Cryptosporidial infections after solid organ transplantation in children. Pediatr Transplant 2000;4:50-55.
39. Palau LA, Kemmerly SA. First report of invasive amebiasis in an organ transplant recipient. Transplantation 1997;64:936-937.
40. Mack DR, Dhawan A, Kaufman SS, Langnas AN, Seemayer TA. Small bowel bacterial overgrowth as a cause of chronic diarrhea after liver transplantation in children. Liver Transpl Surg 1998; 4:166-169.
41. Maes BD, Dalle I, Geboes K, Oellerich M, Armstrong VW, Evenepoel P, et al. Erosive enterocolitis in mycophenolate mofetil-treated renal-transplant recipients with persistent afebrile diarrhea. Transplantation 2003;75:665-672.
42. Wiesner R, Rabkin J, Klintmalm G, McDiarmid S, Langnas A, Punch J, et al. A randomized double-blind comparative study of mycophenolate mofetil and azathioprine in combination with cyclosporine and corticosteroids in primary liver transplant recipients. Liver Transpl 2001;7:442-450.
43. Cantarovich M, Tzimas GN, Barkun J, Deschenes M, Alpert E, Tchervenkov J. Efficacy of mycophenolate mofetil combined with very low-dose cyclosporine microemulsion in long-term liver-transplant patients with renal dysfunction. Transplantation 2003;76:98-102.
44. Koch RO, Graziadei IW, Schutz F, Nachbaur K, Konigsrainer A, Margreiter R, et al. Long-term efficacy and safety of mycophenolate mofetil in liver transplant recipients with calcineurin inhibitor-induced renal dysfunction. Transpl Int 2004.
45. Pfitzmann R, Klupp J, Langrehr JM, Uhl M, Neuhaus R, Settmacher U, et al. Mycophenolatemofetil for immunosuppression after liver transplantation: a follow-up study of 191 patients. Transplantation 2003;76:130-136.
46. Fairbanks KD, Thuluvath PJ. Mycophenolate mofetil monotherapy in liver transplant recipients: a single center experience. Liver Transpl 2004;10:1189-1194.
47. Moreno JM, Rubio E, Gomez A, Lopez-Monclus J, Herreros A, Revilla J, et al. Effectiveness and safety of mycophenolate mofetil as monotherapy in liver transplantation. Transplant Proc 2003; 35:1874-1876.
48. Planas JM, Martinez VC, Gonzalez ER, Cruz AG, Lopez-Monclus J, Sanchez-Turrion V, et al. Mycophenolate mofetil can be used as monotherapy late after liver transplantation. Am J Transplant 2004;4:1650-1655.
49. European Mycophenolate Mofetil Cooperative Study Group. Placebo-controlled study of mycophenolate mofetil combined with cyclosporin and corticosteroids for prevention of acute rejection. European Mycophenolate Mofetil Cooperative Study Group. Lancet 1995;345:1321-1325.
50. Tricontinental Mycophenolate Mofetil Renal Transplantation Study Group.A blinded, randomized clinical trial of mycophenolate mofetil for the prevention of acute rejection in cadaveric renal transplantation. Tricontinental Mycophenolate Mofetil Renal Transplantation Study Group. Transplantation 1996;61: 1029-1037.
51. Sollinger HW. Mycophenolate mofetil for the prevention of acute rejection in primary cadaveric renal allograft recipients. U.S. Renal Transplant Mycophenolate Mofetil Study Group. Transplantation 1995;60:225-232.
52. European FK506 Multicentre Liver Study Group. Randomised trial comparing tacrolimus (FK506) and cyclosporin in prevention of liver allograft rejection. European FK506 Multicentre Liver Study Group. Lancet 1994;344:423-428.
53. U.S. Multicenter FK506 Liver Study Group. A comparison of tacrolimus (FK 506) and cyclosporine for immunosuppression in liver transplantation. The U.S. Multicenter FK506 Liver Study Group. N Engl J Med 1994;331:1110-1115.
54. Pirsch JD, Miller J, Deierhoi MH, Vincenti F, Filo RS. A comparison of tacrolimus (FK506) and cyclosporine for immunosuppression after cadaveric renal transplantation. FK506 Kidney Transplant Study Group. Transplantation 1997;63:977-983.
55. Mayer AD, Dmitrewski J, Squifflet JP, Besse T, Grabensee B, Klein B, et al. Multicenter randomized trial comparing tacrolimus (FK506) and cyclosporine in the prevention of renal allograft rejection: a report of the European Tacrolimus Multicenter Renal Study Group. Transplantation 1997;64:436-443.
56. Greig P, Lilly L, Scudamore C, Erb S, Yoshida E, Kneteman N, et al. Early steroid withdrawal after liver transplantation: the Canadian tacrolimus versus microemulsion cyclosporin A trial: 1-year follow-up. Liver Transpl 2003;9:587-595.
57. O'Grady JG, Burroughs A, Hardy P, Elbourne D, Truesdale A. Tacrolimus versus microemulsified ciclosporin in liver transplantation: the TMC randomised controlled trial. Lancet 2002;360: 1119-1125.
58. Otto MG, Mayer AD, Clavien PA, Cavallari A, Gunawardena KA, Mueller EA. Randomized trial of cyclosporine microemulsion (neoral) versus conventional cyclosporine in liver transplantation: MILTON study. Multicentre International Study in Liver Transplantation of Neoral. Transplantation 1998;66: 1632-1640.
59. Levy G, Villamil F, Samuel D, Sanjuan F, Grazi GL, Wu Y, et al. Results of lis2t, a multicenter, randomized study comparing cyclosporine microemulsion with C2 monitoring and tacrolimus with C0 monitoring in de novo liver transplantation. Transplantation 2004;77:1632-1638.
60. Maes BD, Lemahieu W, Kuypers D, Evenepoel P, Coosemans W, Pirenne J, et al. Differential effect of diarrhea on FK506 versus cyclosporine A trough levels and resultant prevention of allograft rejection in renal transplant recipients. Am J Transplant 2002;2:989-992.
61. Teisseyre J, Teisseyre M, Kalicinski P, Ismail H, Drewniak T, Kaminski A, et al. Elevated tacrolimus levels during diarrhea in children after liver transplantation. Transplant Proc 2003;35: 2292-2294.
62. Sehgal SN. Sirolimus: its discovery, biological properties, and mechanism of action. Transplant Proc 2003;35(Suppl 3):7S-14S.
63. Neff GW, Montalbano M, Tzakis AG. Ten years of sirolimus therapy in orthotopic liver transplant recipients. Transplant Proc 2003;35(Suppl 3):209S-216S.
64. Fairbanks KD, Eustace JA, Fine D, Thuluvath PJ. Renal function improves in liver transplant recipients when switched from a calcineurin inhibitor to sirolimus. Liver Transpl 2003;9:1079-1085.
65. Maheshwari A, Thuluvath PJ. Comparative analysis of sirolimus in monotherapy versus sirolimus + prednisone in liver transplant recipients. Hepatology 2004;40:A558.
66. Neff GW, Montalbano M, Slapak-Green G, Berney T, Bejarano PA, Joshi A, et al. A retrospective review of sirolimus (Rapamune) therapy in orthotopic liver transplant recipients diagnosed with chronic rejection. Liver Transpl 2003;9:477-483.
67. MacDonald AS. A worldwide, phase III, randomized, controlled, safety and efficacy study of a sirolimus/cyclosporine regimen for prevention of acute rejection in recipients of primary mismatched renal allografts. Transplantation 2001;71:271-280.
68. Kahan BD. Efficacy of sirolimus compared with azathioprine for reduction of acute renal allograft rejection: a randomised multicentre study. The Rapamune US Study Group. Lancet 2000; 356:194-202.
69. Smith DM, Agura E, Netto G, Collins R, Levy M, Goldstein R, et al. Liver transplant-associated graft-versus-host disease. Transplantation 2003;75:118-126.
70. Jain A, Nalesnik M, Reyes J, Pokharna R, Mazariegos G, Green M, et al. Posttransplant lymphoproliferative disorders in liver transplantation: a 20-year experience. Ann Surg 2002;236:429-436.
71. Younes BS, Ament ME, McDiarmid SV, Martin MG, Vargas JH. The involvement of the gastrointestinal tract in posttransplant lymphoproliferative disease in pediatric liver transplantation. J Pediatr Gastroenterol Nutr 1999;28:380-385.
72. Kocoshis SA. Endoscopic diagnosis of lymphoproliferative disease after solid organ transplantation. J Pediatr Gastroenterol Nutr 1999;28:375-376.
73. Cao S, Cox K, Esquivel CO, Berquist W, Concepcion W, Ojogho O, et al. Posttransplant lymphoproliferative disorders and gastrointestinal manifestations of Epstein-Barr virus infection in children following liver transplantation. Transplantation 1998;66:851-856.
74. Ganne V, Siddiqi N, Kamaplath B, Chang CC, Cohen EP, Bresnahan BA, et al. Humanized anti-CD20 monoclonal antibody (Rituximab) treatment for post-transplant lymphoproliferative disorder. Clin Transplant 2003;17:417-422.
75. Milpied N, Vasseur B, Parquet N, Garnier JL, Antoine C, Quartier P, et al. Humanized anti-CD20 monoclonal antibody (Rituximab) in post transplant B-lymphoproliferative disorder: a retrospective analysis on 32 patients. Ann Oncol 2000;11 Suppl 1:113-116.
76. Serinet MO, Jacquemin E, Habes D, Debray D, Fabre M, Bernard O. Anti-CD20 monoclonal antibody (Rituximab) treatment for Epstein-Barr virus-associated, B-cell lymphoproliferative disease in pediatric liver transplant recipients. J Pediatr Gastroenterol Nutr 2002;34:389-393.
77. Dvorchik I, Subotin M, Demetris AJ, Fung JJ, Starzl TE, Wieand S, et al. Effect of liver transplantation on inflammatory bowel disease in patients with primary sclerosing cholangitis. Hepatology 2002;35:380-384.
78. Miki C, Harrison JD, Gunson BK, Buckels JA, McMaster P, Mayer AD. Inflammatory bowel disease in primary sclerosing cholangitis: an analysis of patients undergoing liver transplantation. Br J Surg 1995;82:1114-1117.
79. Papatheodoridis GV, Hamilton M, Mistry PK, Davidson B, Rolles K, Burroughs AK. Ulcerative colitis has an aggressive course after orthotopic liver transplantation for primary sclerosing cholangitis. Gut 1998;43:639-644.
80. Shaked A, Colonna JO, Goldstein L, Busuttil RW. The interrelation between sclerosing cholangitis and ulcerative colitis in patients undergoing liver transplantation. Ann Surg 1992;215: 598-603.
81. Befeler AS, Lissoos TW, Schiano TD, Conjeevaram H, Dasgupta KA, Millis JM, et al. Clinical course and management of inflammatory bowel disease after liver transplantation. Transplantation 1998;65:393-396.
82. Gavaler JS, Delemos B, Belle SH, Heyl AE, Tarter RE, Starzl TE, et al. Ulcerative colitis disease activity as subjectively assessed by patient-completed questionnaires following orthotopic liver transplantation for sclerosing cholangitis. Dig Dis Sci 1991;36: 321-328.
83. Haagsma EB, van den Berg AP, Kleibeuker JH, Slooff MJ, Dijkstra G. Inflammatory bowel disease after liver transplantation: the effect of different immunosuppressive regimens. Aliment Pharmacol Ther 2003;18:33-44.
84. van de Vrie W, de Man RA, van Buuren HR, Schouten WR, Tilanus HW, Metselaar HJ. Inflammatory bowel disease and liver transplantation for primary sclerosing cholangitis. Eur J Gastroenterol Hepatol 2003;15:657-663.
85. Atassi T, Thuluvath PJ. Risk of colorectal adenoma in liver transplant recipients compared to immunocompetent control population undergoing routine screening colonoscopy. J Clin Gastroenterol 2003;37:72-73.
86. Ekbom A, Helmick C, Zack M, Adami HO. Ulcerative colitis and colorectal cancer. A population-based study. N Engl J Med 1990;323:1228-1233.
87. Bleday R, Lee E, Jessurun J, Heine J, Wong WD. Increased risk of early colorectal neoplasms after hepatic transplant in patients with inflammatory bowel disease. Dis Colon Rectum 1993;36: 908-912.
88. Brentnall TA, Haggitt RC, Rabinovitch PS, Kimmey MB, Bronner MP, Levine DS, et al. Risk and natural history of colonic neoplasia in patients with primary sclerosing cholangitis and ulcerative colitis. Gastroenterology 1996;110:331-338.
89. Higashi H, Yanaga K, Marsh JW, Tzakis A, Kakizoe S, Starzl TE. Development of colon cancer after liver transplantation for primary sclerosing cholangitis associated with ulcerative colitis. Hepatology 1990;11:477-480.
90. Loftus EV Jr, Aguilar HI, Sandborn WJ, Tremaine WJ, Krom RA, Zinsmeister AR, et al. Risk of colorectal neoplasia in patients with primary sclerosing cholangitis aud ulcerative colitis following orthotopic liver transplantation. Hepatology 1998;27:685-690.
91. Narumi S, Roberts JP, Emond JC, Lake J, Ascher NL. Liver transplantation for sclerosing cholangitis. Hepatology 1995;22: 451-457.
92. Vera A, Gunson BK, Ussatoff V, Nightingale P, Candinas D, Radley S, et al. Colorectal cancer in patients With inflammatory bowel disease after liver transplantation for primary sclerosing cholangitis. Transplantation 2003;75:1983-1988.
93. Pardi DS, Loftus EV Jr, Kremers WK, Keach J, Lindor KD. Ursodeoxycholic acid as a chemopreventive agent in patients with ulcerative colitis and primary sclerosing cholangitis. Gastroenterology 2003;124:889-893.