The bacterial pathogenesis and treatment of pouchitis

Therapeutic Advances in Gastroenterology

Volumn 3, Issue 6, 2010, Pages 335-348

  McLaughlin, S D ^a   Clark, S K ^b   Tekkis, P P ^c   Ciclitira, P J ^d  

^a CHELSEA AND WESTMINSTER HOSPITAL   (United Kingdom)

^b ST MARK S HOSPITAL   (United Kingdom)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Dysbiosis; Familial adenomatous polyposis; Ileal pouch anal anastomosis; Inflammatory bowel disease; Pouchitis; Restorative proctocolectomy; Ulcerative colitis

Indexed keywords

ALLOPURINOL; AMOXICILLIN PLUS CLAVULANIC ACID; ANTIBIOTIC AGENT; AZATHIOPRINE; BISMUTH CITRATE; BUDESONIDE; CEFIXIME; CIPROFLOXACIN; CLARITHROMYCIN; COLISTIN; INFLIXIMAB; MESALAZINE; METRONIDAZOLE; NITROFURANTOIN; NONSTEROID ANTIINFLAMMATORY AGENT; PLACEBO; PREDNISOLONE; PROBIOTIC AGENT; RIFAXAMIN; SALAZOSULFAPYRIDINE; TINIDAZOLE; TRIMETHOPRIM; UNCLASSIFIED DRUG;

ANTIBIOTIC THERAPY; BACTERIAL FLORA; BACTERIUM CULTURE; COMBINATION CHEMOTHERAPY; CORTICOSTEROID THERAPY; CROHN DISEASE; CYTOKINE RESPONSE; DRUG DOSE REDUCTION; DRUG EFFICACY; ENTERITIS; FLUORESCENCE IN SITU HYBRIDIZATION; HUMAN; ILEITIS; ILEOSTOMY; INTESTINE FLORA; MAINTENANCE THERAPY; MONOTHERAPY; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; REVIEW; ULCERATIVE COLITIS;

EID: 79551697907     PISSN: 1756283X     EISSN: None     Source Type: Journal    
DOI: 10.1177/1756283X10370611     Document Type: Review

References (96)

1. Andoh, A., Sakata, S., Koizumi, Y., Mitsuyama, K., Fujiyama, Y. and Benno, Y. ( 2007) Terminal restriction fragment length polymorphism analysis of the diversity of fecal microbiota in patients with ulcerative colitis. Inflamm Bowel Dis 13: 955-962.
2. Barton, J.G., Paden, M.A., Lane, M. and Postier, R.G. ( 2001) Comparison of postoperative outcomes in ulcerative colitis and familial polyposis patients after ileoanal pouch operations. Am J Surg 182: 616-620.
3. Bell, A.J., Nicholls, R.J., Forbes, A., Ellis, H.J. and Ciclitira, P.J. ( 2004) Human lymphocyte stimulation with pouchitis flora is greater than with flora from a healthy pouch but is suppressed by metronidazole. Gut 53: 1801-1805.
4. Bell, A.J., Price, A.B., Forbes, A., Ciclitira, P.J., Groves, C. and Nicholls, R.J. ( 2006) Pre-pouch ileitis: a disease of the ileum in ulcerative colitis after restorative proctocolectomy. Colorectal Dis 8: 402-410.
5. Belluzzi, A., Serrani, M., Roda, G., Bianchi, M.L., Castellani, L., Grazia, M. et al. (2010) Pilot study: the use of sulfasalazine for the treatment of acute pouchitis. Aliment Pharmacol Ther 31 (2): 228-232.
6. Calabrese, C., Fabbri, A., Gionchetti, P., Rizzello, F., Morselli, C., Liguori, G. et al. (2007) Controlled study using wireless capsule endoscopy for the evaluation of the small intestine in chronic refractory pouchitis. Aliment Pharmacol Ther 25: 1311-1316.
7. Calabrese, C., Gionchetti, P., Rizzello, F., Liguori, G., Gabusi, V., Tambasco, R. et al. (2008) Short-term treatment with infliximab in chronic refractory pouchitis and ileitis. Aliment Pharmacol Ther 27: 759-764.
8. Carter, M.J., Lobo, A.J. and Travis, S.P. ( 2004) Guidelines for the management of inflammatory bowel disease in adults. Gut 53(Suppl 5): V1-V16.
9. Casadesus, D., Tani, T., Wakai, T., Maruyama, S., Iiai, T., Okamoto, H. et al. (2007) Possible role of human cytomegalovirus in pouchitis after proctocolectomy with ileal pouch-anal anastomosis in patients with ulcerative colitis. World J Gastroenterol 13: 1085-1089.
10. de Silva, H.J., Ireland, A., Kettlewell, M., Mortensen, N. and Jewell, D.P. (1989) Short-chain fatty acid irrigation in severe pouchitis. N Engl J Med 321: 1416-1417.
11. Dozois, R.R., Kelly, K.A., Welling, D.R., Gordon, H., Beart Jr, R.W., Wolff, B.G. et al. (1989) Ileal pouch-anal anastomosis: comparison of results in familial adenomatous polyposis and chronic ulcerative colitis. Ann Surg 210: 268-271.
12. Duffy, M., O'Mahony, L., Coffey, J.C., Collins, J.K., Shanahan, F., Redmond, H.P. et al. (2002) Sulfate-reducing bacteria colonize pouches formed for ulcerative colitis but not for familial adenomatous polyposis. Dis Colon Rectum 45: 384-388.
13. Elewaut, D., de Keyser, F., Cuvelier, C., Lazarovits, A.I., Mielants, H., Verbruggen, G. et al. (1998) Distinctive activated cellular subsets in colon from patients with Crohn's disease and ulcerative colitis. Scand J Gastroenterol 33: 743-748.
14. Falk, A., Olsson, C., Ahrne, S., Molin, G., Adawi, D. and Jeppsson, B. ( 2007) Ileal pelvic pouch microbiota from two former ulcerative colitis patients, analysed by DNA-based methods, were unstable over time and showed the presence of Clostridium perfringens. Scand J Gastroenterol 42: 973-985.
15. Fazio, V.W., Ziv, Y., Church, J.M., Oakley, J.R., Lavery, I.C., Milsom, J.W. et al. (1995) Ileal pouch-anal anastomoses complications and function in 1005 patients. Ann Surg 222: 120-127.
16. Ferrante, M., D'Haens, G., Dewit, O., Baert, F., Holvoet, J., Geboes, K. et al. (2010) Efficacy of infliximab in refractory pouchitis and Crohn's disease-related complications of the pouch: a Belgian case series. Inflamm Bowel Dis 16 (2): 243-249.
17. Fiocchi, C. ( 1998) Inflammatory bowel disease: etiology and pathogenesis. Gastroenterology 115: 182-205.
18. Frank, D.N., St Amand, A.L., Feldman, R.A., Boedeker, E.C., Harpaz, N. and Pace, N.R. ( 2007) Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A 104: 13780-13785.
19. Fukushima, K., Fujii, H., Yamamura, T., Sugita, A., Kameoka, S., Nagawa, H. et al. (2007) Pouchitis atlas for objective endoscopic diagnosis. J Gastroenterol 42: 799-806.
20. Gately, M.K., Renzetti, L.M., Magram, J., Stern, A.S., Adorini, L., Gubler, U. et al. (1998) The interleukin-12/interleukin-12-receptor system: role in normal and pathologic immune responses. Annu Rev Immunol 16: 495-521.
21. Giacomelli, R., Passacantando, A., Parzanese, I., Vernia, P., Klidara, N., Cucinelli, F. et al. (1998) Serum levels of soluble CD 30 are increased in ulcerative colitis (UC) but not in Crohn's disease (CD). Clin Exp Immunol 111: 532-535.
22. Gionchetti, P., Rizzello, F., Morselli, C., Poggioli, G., Tambasco, R., Calabrese, C. et al. (2007 a) High-dose probiotics for the treatment of active pouchitis. Dis Colon Rectum 50: 2075-2082.
23. Gionchetti, P., Rizzello, F., Poggioli, G., Morselli, C., Lammers, K.M. and Campieri, M. ( 2005) Probiotic therapy to prevent pouchitis onset. Dis Colon Rectum 48: 1493-1494.
24. Gionchetti, P., Rizzello, F., Poggioli, G., Pierangeli, F., Laureti, S., Morselli, C. et al. (2007 b) Oral budesonide in the treatment of chronic refractory pouchitis. Aliment Pharmacol Ther 25: 1231-1236.
25. Gionchetti, P., Rizzello, F., Venturi, A., Brigidi, P., Matteuzzi, D., Bazzocchi, G. et al. (2000) Oral bacteriotherapy as maintenance treatment in patients with chronic pouchitis: a double-blind, placebo-controlled trial. Gastroenterology 119: 305-309.
26. Gionchetti, P., Rizzello, F., Venturi, A., Ferretti, M., Brignola, C., Peruzzo, S. et al. (1997) Long-term efficacy of bismuth carbomer enemas in patients with treatment-resistant chronic pouchitis. Aliment Pharmacol Ther 11: 673-678.
27. Gophna, U., Sommerfeld, K., Gophna, S., Doolittle, W.F. and Veldhuyzen van Zanten, S.J. ( 2006) Differences between tissue-associated intestinal microfloras of patients with Crohn's disease and ulcerative colitis. J Clin Microbiol 44: 4136-4141.
28. Gosselink, M.P., Schouten, W.R., van Lieshout, L.M., Hop, W.C., Laman, J.D. and Ruseler-van Embden, J.G. ( 2004) Eradication of pathogenic bacteria and restoration of normal pouch flora: comparison of metronidazole and ciprofloxacin in the treatment of pouchitis. Dis Colon Rectum 47: 1519-1525.
29. Hahnloser, D., Pemberton, J.H., Wolff, B.G., Larson, D.R., Crownhart, B.S. and Dozois, R.R. ( 2007) Results at up to 20 years after ileal pouch-anal anastomosis for chronic ulcerative colitis. Br J Surg 94: 333-340.
30. Hayashi, H., Sakamoto, M. and Benno, Y. ( 2002) Phylogenetic analysis of the human gut microbiota using 16S rDNA clone libraries and strictly anaerobic culture-based methods. Microbiol Immunol 46: 535-548.
31. Hurst, R.D., Chung, T.P., Rubin, M. and Michelassi, F. ( 1998) The implications of acute pouchitis on the long-term functional results after restorative proctocolectomy. Inflamm Bowel Dis 4: 280-284.
32. Isaacs, K.L., Sandler, R.S., Abreu, M., Picco, M.F., Hanauer, S.B., Bickston, S.J. et al. (2007) Rifaximin for the treatment of active pouchitis: a randomized, double-blind, placebo-controlled pilot study. Inflamm Bowel Dis 13: 1250-1255.
33. Iwata, T., Yamamoto, T., Umegae, S. and Matsumoto, K. ( 2007) Pouchitis and pre-pouch ileitis developed after restorative proctocolectomy for ulcerative colitis: a case report. World J Gastroenterol 13: 643-646.
34. Iwaya, A., Iiai, T., Okamoto, H., Ajioka, Y., Yamamoto, T., Asahara, T. et al. (2006) Change in the bacterial flora of pouchitis. Hepatogastroenterology 53: 55-59.
35. Joelsson, M., Andersson, M., Bark, T., Gullberg, K., Hallgren, T., Jiborn, H. et al. (2001) Allopurinol as prophylaxis against pouchitis following ileal pouch-anal anastomosis for ulcerative colitis. A randomized placebo-controlled double-blind study. Scand J Gastroenterol 36: 1179-1184.
36. Johnson, E., Carlsen, E., Nazir, M. and Nygaard, K. ( 2001) Morbidity and functional outcome after restorative proctocolectomy for ulcerative colitis. Eur J Surg 167: 40-45.
37. Johnson, M.W., Rogers, G.B., Bruce, K.D., Lilley, A.K., von Herbay, A., Forbes, A. et al. (2009) Bacterial community diversity in cultures derived from healthy and inflamed ileal pouches after restorative proctocolectomy. Inflamm Bowel Dis 15 (12): 1803-1811.
38. Kartheuser, A.H., Parc, R., Penna, C.P., Tiret, E., Frileux, P., Hannoun, L. et al. (1996) Ileal pouch-anal anastomosis as the first choice operation in patients with familial adenomatous polyposis: a ten-year experience. Surgery 119: 615-623.
39. Kmiot, W.A., Youngs, D., Tudor, R., Thompson, H. and Keighley, M.R. ( 1993) Mucosal morphology, cell proliferation and faecal bacteriology in acute pouchitis. Br J Surg 80: 1445-1449.
40. Kobayashi, M., Fitz, L., Ryan, M., Hewick, R.M., Clark, S.C., Chan, S., Loudon, R. et al. (1989) Identification and purification of natural killer cell stimulatory factor (NKSF), a cytokine with multiple biologic effects on human lymphocytes. J Exp Med 170: 827-845.
41. Komanduri, S., Gillevet, P.M., Sikaroodi, M., Mutlu, E. and Keshavarzian, A. ( 2007) Dysbiosis in pouchitis: evidence of unique microfloral patterns in pouch inflammation. Clin Gastroenterol Hepatol 5: 352-360.
42. Kuhbacher, T., Ott, S.J., Helwig, U., Mimura, T., Rizzello, F., Kleessen, B. et al. (2006) Bacterial and fungal microbiota in relation to probiotic therapy (VSL#3) in pouchitis. Gut 55: 833-841.
43. Kuisma, J., Jarvinen, H., Kahri, A. and Farkkila, M. ( 2004) Factors associated with disease activity of pouchitis after surgery for ulcerative colitis. Scand J Gastroenterol 39: 544-548.
44. Kuisma, J., Mentula, S., Luukkonen, P., Jarvinen, H., Kahri, A. and Farkkila, M. ( 2003) Factors associated with ileal mucosal morphology and inflammation in patients with ileal pouch-anal anastomosis for ulcerative colitis. Dis Colon Rectum 46: 1476-1483.
45. Lim, M., Adams, J.D., Wilcox, M., Finan, P., Sagar, P. and Burke, D. (2009) An assessment of bacterial dysbiosis in pouchitis using terminal restriction fragment length polymorphisms of 16S ribosomal DNA from pouch effluent microbiota. Dis Colon Rectum 52: 1492-1500.
46. Lim, M., Sagar, P., Finan, P., Burke, D. and Schuster, H. ( 2006) Dysbiosis and pouchitis. Br J Surg 93: 1325-1334.
47. Lohmuller, J.L., Pemberton, J.H., Dozois, R.R., Ilstrup, D. and van, H.J. ( 1990) Pouchitis and extra-intestinal manifestations of inflammatory bowel disease after ileal pouch-anal anastomosis. Ann Surg 211: 622-627.
48. Madden, M.V., McIntyre, A.S. and Nicholls, R.J. ( 1994) Double-blind crossover trial of metronidazole versus placebo in chronic unremitting pouchitis. Dig Dis Sci 39: 1193-1196.
49. Madiba, T.E. and Bartolo, D.C. ( 2001) Pouchitis following restorative proctocolectomy for ulcerative colitis: incidence and therapeutic outcome. J R Coll Surg Edinb 46: 334-337.
50. McLaughlin, S.D., Clark, S.K., Bell, A.J., Tekkis, P.P., Ciclitira, P.J. and Nicholls, R.J. ( 2008 a) An open study of antibiotics for the treatment of pre-pouch ileitis following restorative proctocolectomy with ileal pouch-anal anastomosis. Aliment Pharmacol Ther 27 (10): 895-909 [Epub 2008 Feb 9. Review].
51. McLaughlin, S.D., Clark, S.K., Shafi, S., Petrovksa, L., Tekkis, P.P., Ciclitira, P.J. et al. (2009 a) Fecal coliform testing to identify effective antibiotic therapies for patients with antibiotic-resistant pouchitis. Clin Gastroenterol Hepatol 7: 545-548.
52. McLaughlin, S.D., Clark, S.K., Tekkis, P.P., Ciclitira, P.J. and Nicholls, R.J. ( 2008b) Review article: restorative proctocolectomy, indications, management of complications and follow-up-a guide for gastroenterologists. Aliment Pharmacol Ther 27: 895-909.
53. McLaughlin, S.D., Clark, S.K., Tekkis, P.P., Ciclitira, P.J. and Nicholls, R.J. (2009 b) An open study of maintenance antibiotic therapy for chronic antibiotic dependent pouchitis; efficacy, complications and outcome. Clin Gastroenterol Hepatol 7 (5): 545-548.
54. McLaughlin, S.D., Walker, A.W., Churcher, C., Clark, S.K., Tekkis, P.P., Johnson, M.W. et al. (2010) The bacteriology of pouchitis: a molecular phylogenetic analysis using 16srRNA gene cloning and sequencing. Ann Surg, in press.
55. Mimura, T., Rizzello, F., Helwig, U., Poggioli, G., Schreiber, S., Talbot, I.C. et al. (2004) Once daily high dose probiotic therapy (VSL#3) for maintaining remission in recurrent or refractory pouchitis. Gut 53: 108-114.
56. Moskowitz, R.L., Shepherd, N.A. and Nicholls, R.J. ( 1986) An assessment of inflammation in the reservoir after restorative proctocolectomy with ileoanal ileal reservoir. Int J Colorectal Dis 1: 167-174.
57. Mowschenson, P.M., Critchlow, J.F. and Peppercorn, M.A. ( 2000) Ileoanal pouch operation: long-term outcome with or without diverting ileostomy. Arch Surg 135: 463-465.
58. Nicholls, R.J., Belliveau, P., Neill, M., Wilks, M. and Tabaqchali, S. ( 1981) Restorative proctocolectomy with ileal reservoir: a pathophysiological assessment. Gut 22: 462-468.
59. Nyam, D.C., Brillant, P.T., Dozois, R.R., Kelly, K.A., Pemberton, J.H. and Wolff, B.G. ( 1997) Ileal pouch-anal canal anastomosis for familial adenomatous polyposis: early and late results. Ann Surg 226: 514-519.
60. O'Connell, P.R., Rankin, D.R., Weiland, L.H. and Kelly, K.A. ( 1986) Enteric bacteriology, absorption, morphology and emptying after ileal pouch-anal anastomosis. Br J Surg 73: 909-914.
61. Ohge, H., Furne, J.K., Springfield, J., Rothenberger, D.A., Madoff, R.D. and Levitt, M.D. ( 2005) Association between fecal hydrogen sulfide production and pouchitis. Dis Colon Rectum 48: 469-475.
62. Ott, S.J., Musfeldt, M., Wenderoth, D.F., Hampe, J., Brant, O., Folsch, U.R. et al. (2004) Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory bowel disease. Gut 53: 685-693.
63. Pardi, D.S. and Sandborn, W.J. ( 2006) Systematic review: the management of pouchitis. Aliment Pharmacol Ther 23: 1087-1096.
64. Pfau, P.R. and Lichtenstein, G.R. ( 2000) Cytomegalovirus infection as a cause of ileoanal pouchitis. Dis Colon Rectum 43: 113-114.
65. Romanos, J., Samarasekera, D.N., Stebbing, J.F., Jewell, D.P., Kettlewell, M.G. and Mortensen, N.J. ( 1997) Outcome of 200 restorative proctocolectomy operations: the John Radcliffe Hospital experience. Br J Surg 84: 814-818.
66. Rowley, S., Candinas, D., Mayer, A.D., Buckels, J.A., McMaster, P. and Keighley, M.R. ( 1995) Restorative proctocolectomy and pouch anal anastomosis for ulcerative colitis following orthotopic liver transplantation. Gut 37: 845-847.
67. Ruseler-van Embden, J.G., Schouten, W.R. and van Lieshout, L.M. ( 1994) Pouchitis: result of microbial imbalance? Gut 35: 658-664.
68. Sambuelli, A., Boerr, L., Negreira, S., Gil, A., Camartino, G., Huernos, S. et al. (2002) Budesonide enema in pouchitis-a double-blind, double-dummy, controlled trial. Aliment Pharmacol Ther 16: 27-34.
69. Sandborn, W.J. and Pardi, D.S. ( 2004) Clinical management of pouchitis. Gastroenterology 127: 1809-1814.
70. Sandborn, W.J., Tremaine, W.J., Batts, K.P., Pemberton, J.H. and Phillips, S.F. ( 1994) Pouchitis after ileal pouch-anal anastomosis: a Pouchitis Disease Activity Index. Mayo Clin Proc 69: 409-415.
71. Sandborn, W.J., Tremaine, W.J., Batts, K.P., Pemberton, J.H., Rossi, S.S., Hofmann, A.F. et al. (1995) Fecal bile acids, short-chain fatty acids, and bacteria after ileal pouch-anal anastomosis do not differ in patients with pouchitis. Dig Dis Sci 40: 1474-1483.
72. Santavirta, J., Mattila, J., Kokki, M. and Matikainen, M. ( 1991) Mucosal morphology and faecal bacteriology after ileoanal anastomosis. Int J Colorectal Dis 6: 38-41.
73. Sartor, R.B. ( 1991) Pathogenetic and clinical relevance of cytokines in inflammatory bowel disease. Immunol Res 10: 465-471.
74. Sartor, R.B. ( 2008) Microbial influences in inflammatory bowel diseases. Gastroenterology 134: 577-594.
75. Seksik, P., Rigottier-Gois, L., Gramet, G., Sutren, M., Pochart, P., Marteau, P. et al. (2003) Alterations of the dominant faecal bacterial groups in patients with Crohn's disease of the colon. Gut 52: 237-242.
76. Shen, B., Achkar, J.P., Connor, J.T., Ormsby, A.H., Remzi, F.H., Bevins, C.L. et al. (2003) Modified pouchitis disease activity index: a simplified approach to the diagnosis of pouchitis. Dis Colon Rectum 46: 748-753.
77. Shen, B., Achkar, J.P., Lashner, B.A., Ormsby, A.H., Remzi, F.H., Brzezinski, A. et al. (2001) A randomized clinical trial of ciprofloxacin and metronidazole to treat acute pouchitis. Inflamm Bowel Dis 7: 301-305.
78. Shen, B., Brzezinski, A., Fazio, V.W., Remzi, F.H., Achkar, J.P., Bennett, A.E. et al. (2005) Maintenance therapy with a probiotic in antibiotic-dependent pouchitis: experience in clinical practice. Aliment Pharmacol Ther 22: 721-728.
79. Shen, B., Fazio, V.W., Remzi, F.H., Bennett, A.E., Brzezinski, A., Lopez, R. et al. (2006) Risk factors for clinical phenotypes of Crohn's disease of the ileal pouch. Am J Gastroenterol 101: 2760-2768.
80. Shen, B., Fazio, V.W., Remzi, F.H., Bennett, A.E., Lopez, R., Brzezinski, A. et al. (2007 a) Combined ciprofloxacin and tinidazole therapy in the treatment of chronic refractory pouchitis. Dis Colon Rectum 50 (4): 498-508.
81. Shen, B., Fazio, V.W., Remzi, F.H., Bennett, A.E., Lopez, R., Lavery, I.C. et al. (2007 b) Effect of withdrawal of nonsteroidal anti-inflammatory drug use on ileal pouch disorders. Dig Dis Sci 52 (12): 3321-3328 [Epub 2007 Apr 5].
82. Shen, B., Remzi, F.H., Lopez, A.R. and Queener, E. ( 2008) Rifaximin for maintenance therapy in antibiotic-dependent pouchitis. BMC Gastroenterol 8: 26.
83. Slatter, C., Girgis, S., Huynh, H. and El Matary, W. ( 2008) Pre-pouch ileitis after colectomy in paediatric ulcerative colitis. Acta Paediatr 97: 381-383.
84. Sokol, H., Lepage, P., Seksik, P., Dore, J. and Marteau, P. ( 2006) Temperature gradient gel electrophoresis of fecal 16S rRNA reveals active Escherichia coli in the microbiota of patients with ulcerative colitis. J Clin Microbiol 44: 3172-3177.
85. Sokol, H., Pigneur, B., Watterlot, L., Lakhdari, O., Bermudez-Humaran, L.G., Gratadoux, J.J. et al. (2008) Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci U S A 105: 16731-16736.
86. Sokol, H., Seksik, P., Furet, J.P., Firmesse, O., Nion-Larmurier, I., Beaugerie, L. et al. (2009) Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm Bowel Dis 15: 1183-1189.
87. Stahlberg, D., Gullberg, K., Liljeqvist, L., Hellers, G. and Lofberg, R. ( 1996) Pouchitis following pelvic pouch operation for ulcerative colitis. Incidence, cumulative risk, and risk factors. Dis Colon Rectum 39: 1012-1018.
88. Stallmach, A., Schafer, F., Hoffmann, S., Weber, S., Muller-Molaian, I., Schneider, T. et al. (1998) Increased state of activation of CD 4 positive T cells and elevated interferon gamma production in pouchitis. Gut 43: 499-505.
89. Suau, A., Bonnet, R., Sutren, M., Godon, J.J., Gibson, G.R., Collins, M.D. et al. (1999) Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Appl Environ Microbiol 65: 4799-4807.
90. Thomas, P.D., Forbes, A., Nicholls, R.J. and Ciclitira, P.J. ( 2001) Altered expression of the lymphocyte activation markers CD 30 and CD 27 in patients with pouchitis. Scand J Gastroenterol 36: 258-264.
91. Thomas, P.D., Forbes, A., Price, A.B., Nicholls, R.J. and Ciclitira, P.J. ( 2002) Differential expression of cell adhesion molecules within inflamed ileal pouch mucosa: relationship to recruited cell subtypes. Eur J Gastroenterol Hepatol 14: 137-144.
92. Tremaine, W.J., Sandborn, W.J., Wolff, B.G., Carpenter, H.A., Zinsmeister, A.R. et al. (1997) Bismuth carbomer foam enemas for active chronic pouchitis: a randomized, double-blind, placebo-controlled trial. Aliment Pharmacol Ther 11: 1041-1046.
93. Wolf, J.M., Achkar, J.P., Lashner, B.A., Delaney, C.P., Petras, R.E., Goldblum, J.R. et al. (2004) Afferent limb ulcers predict Crohn's disease in patients with ileal pouch-anal anastomosis. Gastroenterology 126: 1686-1691.
94. Wolf, S.F., Temple, P.A., Kobayashi, M., Young, D., Dicig, M., Lowe, L. et al. (1991) Cloning of cDNA for natural killer cell stimulatory factor, a heterodimeric cytokine with multiple biologic effects on T and natural killer cells. J Immunol 146: 3074-3081.
95. Zins, B.J., Sandborn, W.J., Penna, C.R., Landers, C.J., Targan, S.R., Tremaine, W.J. et al. (1995) Pouchitis disease course after orthotopic liver transplantation in patients with primary sclerosing cholangitis and an ileal pouch-anal anastomosis. Am J Gastroenterol 90: 2177-2181.
96. Zoetendal, E.G., Rajilic-Stojanovic, M. and de Vos, W.M. ( 2008) High-throughput diversity and functionality analysis of the gastrointestinal tract microbiota. Gut 57: 1605-1615.