Digestive Diseases and Sciences

, Volume 40, Issue 7, pp 1474–1483 | Cite as

Fecal bile acids, short-chain fatty acids, and bacteria after ileal pouch-anal anastomosis do not differ in patients with pouchitis

  • William J. Sandborn
  • William J. Tremaine
  • Kenneth P. Batts
  • John H. Pemberton
  • Steven S. Rossi
  • Alan F. Hofmann
  • Gregory J. Gores
  • Sidney F. Phillips
Intestinal Disorders, Inflammatory Bowel Disease, Immunology, and Microbiology

Abstract

Construction of an ileal reservoir changes the fecal bacterial flora and the fecal composition of bile acids and short-chain fatty acids. We examined the relationships between pouch inflammation (pouchitis) and pouch content, as assessed by analysis of fecal bacteria, bile acids, and short chain fatty acids. Four groups were studied: ileal pouch-anal anastomosis (IPAA) for ulcerative colitis with pouchitis (N=10), IPAA without pouchitis (N=5), IPAA for familial adenomatous polyposis without pouchitis (N=5); and Brooke ileostomy for ulcerative colitis, which served as controls (N=5). Pouchitis was defined as ≥7 points on an 18-point pouchitis disease activity index. Aerobic and anaerobic bacteria were quantitatively cultured. Total aqueous-phase bile acids were measured by thin-layer chromatography and an enzymatic 3α-OH hydroxysteroid dehydrogenase method. Fecal short chain fatty acids were measured by gas liquid chromatography. All patients with an IPAA had higher ratios of anaerobes/aerobes and concentrations of anaerobic gram-negative rods than did patients with an ileostomy. There were no other differences between patient groups with respect to bacteria, aqueous-phase total bile acids, or fecal short-chain fatty acids. Fecal concentrations of bacteria, bile acids, and short-chain fatty acids were similar in patients with and without pouchitis, indicating that these factors can not be the sole cause of pouchitis.

Key Words

ileal pouch-anal anastomosis pouchitis ulcerative colitis familial adenomatous polyposis shortchain fatty acids bile acids 

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References

  1. 1.
    Pemberton JH, Kelly KA, Beart RW, Dozois RR, Wolff BG, Ilstrup DM: Ileal pouch-anal anastomosis for chronic ulcerative colitis. Long-term results. Ann Surg 206:504–513, 1987Google Scholar
  2. 2.
    Sandborn WJ: Pouchitis following ileal pouch-anal anastomosis: Definition, pathogenesis, and treatment. Gastroenterology 107:1856–1860, 1994Google Scholar
  3. 3.
    Phillips SF: Biological effects of a reservoir at the end of the small bowel. World J Surg 11:763–768, 1987Google Scholar
  4. 4.
    Shepherd NA, Hulten L, Tytgat GNJ, Nicholls RJ, Nasmyth DG, Hill MJ, Fernandez F, Gertner DJ, Rampton DS, Owen RW, Kmiot WA, Keighley MRB, O'Connell Kumar D, Williams NS: Workshop: Pouchitis. Int J Colorect Dis 4:205–229, 1989Google Scholar
  5. 5.
    Kelly PG, Phillips SF, Kelly KA, Weinstein WM, Gilchrist MJR: Dysfunction of the continent ileostomy: Clinical features and bacteriology. Gut 24:193–201, 1983Google Scholar
  6. 6.
    Philipson B, Brandberg A, Jagenburg R, Kock NG, Lager I, Ahren C: Mucosal morphology, bacteriology and absorption in intraabdominal ileostomy reservoir. Scand J Gastroenterol 10:145–153, 1975Google Scholar
  7. 7.
    Sagar PM, Holdsworth PJ, Godwin PGR, Quirke P, Smith AN, Johnston D: Comparison of triplicated (S) and quadruplicated (W) pelvic ileal reservoirs. Studies on manovolumetry, fecal bacteriology, fecal volatile fatty acids, mucosal morphology, and functional results. Gastroenterology 102:520–528, 1992Google Scholar
  8. 8.
    Schjonsby H, Halvorsen JF, Hofstad T, Hovenak N: Stagnant loop syndrome in patients with continent ileostomy (intra-abdominal ileal reservoir). Gut 18:795–799, 1977Google Scholar
  9. 9.
    Loeschke K, Bolkert T, Kiefhaber P, Ruckdeschel G, Lohrs U, Bary SV, Schaudig A: Bacterial overgrowth in ileal reservoirs (Kock pouch): Extended functional studies. Hepato-Gastroenterol 27:310–316, 1980Google Scholar
  10. 10.
    O'Connell PR, Rankin DR, Weiland LH, Kelly KA: Enteric bacteriology, absorption, morphology and emptying after ileal pouch-anal anastomosis. Br J Surg 73:909–914, 1986Google Scholar
  11. 11.
    Luukkonen P, Valtonen V, Sivonen A, Sipponen P, Jarvinen H: Fecal bacteriology and reservoir ileitis in patients operated on for ulcerative colitis. Dis Colon Rectum 31:864–867, 1988Google Scholar
  12. 12.
    Nasmyth DG, Godwin PGR, Dixon MF, Williams NS, Johnston D: Ileal ecology after pouch-anal anastomosis or ileostomy. Gastroenterology 96:817–824, 1989Google Scholar
  13. 13.
    Santavirta J, Mattila J, Kokki M, Matikainem M: Mucosal morphology and faecal bacteriology after ileoanal anastomosis. Int J Colorect Dis 6:38–41, 1991Google Scholar
  14. 14.
    Clausen MR, Tvede M, Mortensen PB: Short-chain fatty acids in pouch contents with and without pouchitis after ileal pouchanal anastomosis. Gastroenterology 103:1144–1153, 1992Google Scholar
  15. 15.
    Becker JM, Onderdonk AB: Bacterial dysbiosis in the pathogenesis of ileal pouchitis. Gastroenterology 106:A650, 1994Google Scholar
  16. 16.
    Onderdonk AB, Dvorak AM, Cisneros RL, McLeod RS, Antionoli D, Silen W, Blair JE, Monahan-Earley RA, Cullen J, Cohen Z: Microbiologic assessment of tissue biopsy samples from ileal pouch patients. J Clin Microbiol 30:312–317, 1992Google Scholar
  17. 17.
    Kay RM, Cohen Z, Siu KP, Petrunka CN, Strasberg SM: Ileal excretion and bacterial modification of bile acids and cholesterol in patients with continent ileostomy. Gut 21:128–132, 1979Google Scholar
  18. 18.
    Hylander E, Ladefoged K, Nielsen ML, Nielson OV, Thale M, Jarnum S: excretion, deconjugation, and absorption of bile acids after colectomy for ulcerative colitis. Comparative studies in patients with conventional ileostomy and patients with Kock's reservoir. Scand J Gastroenterol 21:1137–1143, 1986Google Scholar
  19. 19.
    Go PMNYH, Van Diejen-Visser MP, Davies BI, Lens J, Brombacher PJ: Microbial flora and bile acid metabolism in patients with an ileal reservoir. Scand J Gastroenterol 23:229–236, 1988Google Scholar
  20. 20.
    Pederson BH, Simonsen L, Hansen L, Giese B, Justesen T, Tougaard L, Binder V: Bile acid malabsorption in patients with and ileum reservoir with long efferent leg to an anal anastomosis. Scand J Gastroenterol 20:995–1000, 1985Google Scholar
  21. 21.
    Nasmyth DG, Johnston D, Williams NS, King RFGJ, Burkinshaw L, Brooks K: Changes in the absorption of bile acids after total colectomy in patients with an ileostomy or pouch-anal anastomosis. Dis Colon Rectum 32:230–234, 1989Google Scholar
  22. 22.
    Natori H, Utsunomiya J, Yamamaura T, Benno Y, Uchida K: Fecal and stomal bile acid composition after ileostomy or ileoanal anastomosis in patients with chronic ulcerative colitis and adenomatous coll. Gastroenterology 102:1278–1288, 1992Google Scholar
  23. 23.
    Merrett MN, Crotty BJ, Mortensen N, Jewell DP: Ileal pouch dialysate is cytotoxic to I-407 and HT-29 cells: Bile may be the active factor. Gut 32:A1205, 1991Google Scholar
  24. 24.
    Merrett MN, Owen RW, Dalton HR, Mortensen NJ, Jewell DP: Free bile acids are cytotoxic to CaCo-2 cells at levels assayed in ileal pouch dialysate. Gut 33:S51, 1992Google Scholar
  25. 25.
    Whiting JF, Soper NJ, McGrath KM, Becker JM: Pouchitis is unrelated to changes in fecal bile acid or electrolyte composition. Gastroenterology 100:A261, 1991Google Scholar
  26. 26.
    Becker JM, Mou CH, Hocking G: Fecal bile acid composition in patients with pouchitis following colectomy and ileal pouchanal anastomosis. Gastroenterology 106:A650, 1994Google Scholar
  27. 27.
    Ambroze WL, Pemberton JH, Phillips SF, Bell AM, Haddad AC: Fecal short-chain fatty acid concentrations and effect on ileal pouch function. Dis Colon Rectum 36:235–239, 1993Google Scholar
  28. 28.
    Wischmeyer P, Pemberton JH, Phillips SF: Chronic pouchitis after ileal pouch-anal anastomosis: Responses to butyrate and glutamine suppositories in a pilot study. Mayo Clin Proc 68:978–981, 1993Google Scholar
  29. 29.
    Tremaine WJ, Sandborn WJ, Phillips SF, Pemberton JH, Carpenter HA: Short chain fatty acid (SCFA) enema therapy for treatment-resistant pouchitis following ileal-pouch anal anastomosis (IPAA) for ulcerative colitis (UC). Gastroenterology 106:A784, 1994Google Scholar
  30. 30.
    Sandborn WJ, Tremaine WJ, Batts KP, Pemberton JH, Phillips SF: Pouchitis following ileal pouch-anal anastomosis: A pouchitis disease activity index. Mayo Clin Proc 69:409–415, 1994Google Scholar
  31. 31.
    Moskowitz RL, Shepherd NA, Nicholls RJ: An assessment of inflammation in the reservoir after restorative proctocolectomy with ileoanal ileal reservoir. Int J Colorectal Dis 1:167–174, 1986Google Scholar
  32. 32.
    Grundy SM, Ahrens Jr EH, Miettinen TA: Quantitative isolation and gas-liquid chromatographic analysis of total fecal bile acids. J Lipid Res 6:397–410, 1965Google Scholar
  33. 33.
    Setchell KDR, Worthington JA: A rapid method for the quantitative extraction of bile acids and their conjugates from serum using commercially available reverse phase octadecylsilane bonded sila cartridges. Clin Chem Acta 125:135–144, 1982Google Scholar
  34. 34.
    Turley SD, Dietschy JM: Re-evaluation of the 3α-hydroxysteroid dehydrogenase assay for total bile acids in bile. J Lipid Res 19:924–928, 1978Google Scholar
  35. 35.
    Hofmann AF: Thin-layer chromatography of free and conjugated bile acids on silic acid. J Lipid Res 2:127–128, 1962Google Scholar
  36. 36.
    Lake JR, Renner EL, Scharschmidt BF, Cragoe Jr EJ, Hagey LR, Lambert KJ, Gurantz D, Hofmann AF: Inhibition of Na+/H+ exchange in the rat is associated with decreased ursodeoxycholate hypercholeresis, decreased secretion of unconjugated ursodeoxycholate, and increased ursodeoxycholate glucuronidation. Gastroenterology 95:454–463, 1988Google Scholar
  37. 37.
    Collin DP, McCormick, PG, Schmitt MG: Quantitative gaschromatographic determination of short chain fatty acids in aqueous samples. Clin Chem 20:1235–1237, 1974Google Scholar
  38. 38.
    Setchell KDR: Fecal bile acids.In The Bile Acids Methods And Applications. KDR Setchell, D Kritchevsky, PP Nair (eds). New York, Plenum Press, 1988, pp 441–570Google Scholar
  39. 39.
    Macdonald IA, Bokkenheuser VD, Winter J, McLernon AM, Mosbach EH: Degradation of steroids in the human gut: J Lipid Res 24:675–700, 1983Google Scholar
  40. 40.
    Quist RG, Ton-Nu HT, Lillienau J, Hofmann AF, Barrett KE: Activation of mast cells by bile acids. Gastroenterology 101:446–456, 1991Google Scholar
  41. 41.
    Dupas JL, Hofmann AF: Passive jejunal absorption of bile acidsin vivo: Structure-activity relationships. Gastroenterology 86:A1067, 1984Google Scholar
  42. 42.
    Schiff ER, Small NC, Dietschy JM: Characteristics of the kinetics of the passive and active transport mechanisms for bile acid absorption in the small intestine and colon of the rat. J Clin Invest 51:1351–1362, 1972Google Scholar
  43. 43.
    Molino G, Hofmann AF, Cravetto C, Belforte G, Bona B: Simulation of the metabolism and enterohepatic circulation of chenodeoxycholic acid in man using a physiological pharmacokinetic model. Eur J Clin Invest 16:397–414, 1986Google Scholar
  44. 44.
    Casanova S, Roda A, Festi D, Mazzella G, Aldini R, Bazzoli F, Sama C, Morselli Labate A, Barbara L, Roda E: Effect of chenodiol on the small intestine. Unimpaired structure and function during therapy for gallstone dissolution. J Am Med Assoc 246:2597–2601, 1981Google Scholar
  45. 45.
    Schmassmann A, Angellotti MA, Ton-Nu HT, Schteingart CD, Marcus SN, Rossi SS, Hofmann AF: Transport, metabolism, and effect of chronic feeding of cholylsarcosine, a conjugated bile acid resistant to deconjugation and dehydroxylation. Gastroenterology 98:163–174, 1990Google Scholar
  46. 46.
    Kimura M, Hatono S, Une M, Fukuoka C, Kuramoto T, Hoshita T: Synthesis, intestinal absorption and metabolism of sarcosine conjugated ursodeoxycholic acid. Steroids 43:677–687, 1984Google Scholar
  47. 47.
    Scheppach W, Sommer H, Kirchner T, Paganelli GM, Bartram P, Christl S, Richter F, Dusel G, Kasper H: Effect of butyrate enemas on the colonic mucosa in distal ulcerative colitis. Gastroenterology 103:51–56, 1992Google Scholar
  48. 48.
    De Silva HJ, Millard PR, Soper N, Kettlewell M, Mortensen NJ, Jewell DP: Effects of the faecal stream and stasis on the ileal pouch mucosa. Gut 32:1166–1169, 1991Google Scholar
  49. 49.
    Shepherd NA, Healey CJ, Warren BF, Richman PI, Thompson WHF, Wilkinson SP: Distribution of mucosal pathology and an assessment of colonic phenotypic change in the pelvic ileal reservoir. Gut 34:101–105, 1993Google Scholar
  50. 50.
    Lohmuller JL, Pemberton JH, Dozois RR, Ilstrup D, Van Heerden J: Pouchitis and extraintestinal manifestations of inflammatory bowel disease after ileal pouch-anal anastomosis. Ann Surg 211:622–629, 1990Google Scholar
  51. 51.
    Penna C, Dozois RR, LaRusso NF, Tremaine WJ: Pouchitis after ileal pouch anal anastomosis for chronic ulcerative colitis occurs with increased frequency in patients with associated primary sclerosing cholangitis. Gastroenterology 106:A751, 1994Google Scholar
  52. 52.
    Sandborn WJ, Landers CJ, Tremaine WJ, Targan SR: Anti-neutrophil cytoplasmic antibody correlates with chronic pouchitis after ileal pouch-anal anastomosis. Am J Gastroenterol 90:740–747, 1995Google Scholar
  53. 53.
    Merrett MN, Mortensen N, Jewell DP: Smoking may prevent pouchitis in patients with restorative proctocolectomy for ulcerative colitis. Gastroenterology 104:A743, 1993Google Scholar
  54. 54.
    De Silva HJ, Jones M, Prince C, Kettlewell M, Mortensen NJ, Jewell DP: Lymphocyte and macrophage subpopulations in pelvic ileal pouches. Gut 32:1160–1165, 1991Google Scholar

Copyright information

© Plenum Publishing Corporation 1995

Authors and Affiliations

  • William J. Sandborn
    • 1
    • 2
    • 3
    • 4
  • William J. Tremaine
    • 1
    • 2
    • 3
    • 4
  • Kenneth P. Batts
    • 1
    • 2
    • 3
    • 4
  • John H. Pemberton
    • 1
    • 2
    • 3
    • 4
  • Steven S. Rossi
    • 1
    • 2
    • 3
    • 4
  • Alan F. Hofmann
    • 1
    • 2
    • 3
    • 4
  • Gregory J. Gores
    • 1
    • 2
    • 3
    • 4
  • Sidney F. Phillips
    • 1
    • 2
    • 3
    • 4
  1. 1.Inflammatory Bowel Disease Clinic, Division of GastroenterologyMayo ClinicRochester
  2. 2.Department of Laboratory Medicine and PathologyMayo ClinicRochester
  3. 3.Division of Colon and Rectal SurgeryMayo ClinicRochester
  4. 4.Division of Gastroenterology, Department of MedicineUniversity of California San DiegoSan Diego

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