Digestive Diseases and Sciences

, Volume 42, Issue 8, pp 1571–1579 | Cite as

Colonic Sulfide in Pathogenesis and Treatment of Ulcerative Colitis

  • W.E.W. Roediger
  • J. Moore
  • W. Babidge

Abstract

A role for colonic sulfide in the pathogenesisand treatment of ulcerative colitis (UC) has emergedbased on biochemical, microbiological, nutritional,toxicological, epidemiological, and therapeuticevidence. Metabolism of isolated colonic epithelial cellshas indicated that the bacterial short-chain fatty acidn-butyrate maintains the epithelial barrier and thatsulfides can inhibit oxidation of n-butyrate analogous to that observed in active UC. Sulfurfor fermentation in the colon is essential forn-butyrate formation and sulfidogenesis aids disposal ofcolonic hydrogen produced by bacteria. The numbers of sulfate-reducing bacteria and sulfidogenesisis greater in UC than control cases. Sulfide is mainlydetoxified by methylation in colonic epithelial cellsand circulating red blood cells. The enzyme activity of sulfide methylation is higher in red bloodcells of UC patients than control cases. Patients withUC ingest more protein and thereby sulfur amino acidsthan control subjects. Removing foods rich in sulfur amino acids (milk, eggs, cheese) has proventherapeutic benefits in UC. 5-Amino salicylic acidreduces fermentative production of hydrogen sulfide bycolonic bacteria, and aminoglycosides, which inhibit sulfate-reducing bacteria, are of therapeuticbenefit in active UC. Methyl-donating agents are acategory of drugs of potential therapeutic use in UC. Acorrelation between sulfide production and mucosal immune responses in UC needs to be undertaken.Control of sulfidogenesis and sulfide detoxification maybe important in the disease process of UC, althoughwhether their roles is in an initiating or promoting capacity has yet to be determined.

HYDROGEN SULFIDE BUTYRATE OXIDATION AMINO SALICYLIC ACID ULCERATIVE COLITIS 

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REFERENCES

  1. 1.
    Ferry DM, Butt TJ, Broom MF, Hunter J, Chadwick VS: Bacterial chemotactic oligopeptides and the intestinal mucosal barrier. Gastroenterology 97:61–67, 1989Google Scholar
  2. 2.
    Gardiner KR, Halliday MI, Maxwell RJ, Rowlands BJ, Barclay GR, Milne L, Brown D, Stephens S: Significance of systemic endotoxaemia in inflammatory bowel disease. Gut 36:897–901, 1995Google Scholar
  3. 3.
    Roediger WEW, Duncan A, Kapaniris O, Millard S: Reducing sulfur compounds of the colon impair coloncyte nutrition: Implications for ulcerative colitis. Gastroenterology 104:802–809, 1993Google Scholar
  4. 4.
    Pitcher MCL, Cummings JH: Hydrogen sulphide: A bacterial toxin in ulcerative colitis? Gut 39:1–4, 1996Google Scholar
  5. 5.
    Podolsky DK: Inflammatory bowel disease. N Engl J Med 325:928–937, 1008–1016, 1991Google Scholar
  6. 6.
    Roediger WEW: The role of anaerobic bacteria in the metabolic welfare of the colonic mucosa in man. Gut 21:793–798, 1980Google Scholar
  7. 7.
    Ardawi MSM, Newsholme EA: Fuel utilization in colonocytes of the rat. Biochem J 231:713–719, 1985Google Scholar
  8. 8.
    Fleming SE, Fitch D, Devries S, Liu ML, Kight C: Nutrient utilization by cells isolated from rat jejunum, caecum and colon. J Nutr 121:869–878, 1991Google Scholar
  9. 9.
    Cummings JH, Pomare EW, Branch WJ, Naylor CPE, MacFarlane GT: Short chain fatty acids in human large intestine, portal hepatic and venous blood. Gut 28:1221–1227, 1987Google Scholar
  10. 10.
    Miller TL, Wolin MJ: Pathways of acetate, propionate and butyrate formation by the human fecal microbial flora. Appl Environ Microbiol 62:1589–1592, 1996Google Scholar
  11. 11.
    Roediger WEW: The colonic epithelium in ulcerative colitis: An energy-deficiency disease? Lancet 2:712–715, 1980Google Scholar
  12. 12.
    Chapman MAS, Grahn MF, Boyle MA, Hutton M, Rogers J, Williams NS: Butyrate oxidation is impaired in the colonic mucosa of sufferers of quiescent ulcerative colitis. Gut 35:73–76, 1994Google Scholar
  13. 13.
    Roediger WEW, Lawson MJ, Kwok V, Kerr Grant A, Pannall PR: Colonic bicarbonate output as a test of disease activity in ulcerative colitis. J Clin Pathol 37:704–707, 1984Google Scholar
  14. 14.
    Den Hond E, Hiele M, Ghoos Y, Rutgeerts P: In vivo colonic butyrate metabolism in extensive ulcerative colitis. Gastroenterology 110:A797, 1996Google Scholar
  15. 15.
    Finnie IA, Taylor BA, Rhodes JM: Ileal and colonic epithelial metabolism in quiescent ulcerative colitis: Increased glutamine metabolism in distal colon but no defect in butyrate metabolism. Gut 34:1552–1558, 1993Google Scholar
  16. 16.
    Clausen MR, Mortensen PB: Kinetic studies on colonocyte metabolism of short chain fatty acids and glucose in ulcerative colitis. Gut 37:684–689, 1995Google Scholar
  17. 17.
    Duffy MM, Regan MC, Harrington MG, O'Connell PR: Colonic substrate utilisation in Crohn's disease. Gastroenterology 110:A433, 1996Google Scholar
  18. 18.
    Ireland A, Jewell DP: 5-Aminosalicylic acid (5-ASA) has no effect on butyrate metabolism in human colonic epithelial cells. Gastroenterology 98:A176, 1990Google Scholar
  19. 19.
    Roediger WEW, Radcliffe BC: Role of nitrite and nitrate as a redox couple in the rat colon. Gastroenterology 94:915–922, 1988Google Scholar
  20. 20.
    Roediger WEW: Failed redox control as a cause of ulcerative colitis. In Inflammatory Bowel Diseases. E Monteiro, FT Veloso (eds). Dordrecht, Kluwer Academic Publishers, 1995, pp 61–71Google Scholar
  21. 21.
    Roediger WEW, Radcliffe BC, Deakin EJ, Nance SH: Specific metabolic effect of sodium nitrite on fat metabolism by mucosal cells of the colon. Dig Dis Sci 31:535–539, 1986Google Scholar
  22. 22.
    Roediger WEW, Nance S: Selective reduction of fatty acid oxidation in colonocytes: Correlation with ulcerative colitis. Lipids 25:646–652, 1990Google Scholar
  23. 23.
    Lehninger AL: Biochemistry: The Molecular Basis of Cell Structure and Function. New York, Worth Publishers, 1970, pp 365–393Google Scholar
  24. 24.
    Roediger WEW, Duncan A, Kapaniris O, Millard S: Sulphide impairment of substrate oxidation in rat colonocytes: A biochemical basis for ulcerative colitis. Clin Sci 85:623–627, 1993Google Scholar
  25. 25.
    Allan ES, Winter S, Light AM, Allan A: Mucosal enzyme activity for butyrate oxidation; no defect in patients with ulcerative colitis. Gut 38:886–893, 1996Google Scholar
  26. 26.
    Moore JWE, Babidge W, Millard S, Roediger WEW: Effect of sulphide on short chain acyl-CoA metabolism in rat colonocytes. 1997 (in press)Google Scholar
  27. 27.
    Babidge W, Millard S, Roediger WEW: Sulfides impair short chain fatty acid β-oxidation at acyl CoA dehydrogenase level in human colonocytes: implications for ulcerative colitis. 1997 (submitted)Google Scholar
  28. 28.
    Shaw L, Engel PC: CoA persulphide: A possible in vivo inhibitor of mammalian short-chain acyl-CoA dehydrogenase. Biochim Biophys Acta 919:171–174, 1987Google Scholar
  29. 29.
    Roediger WEW, Moore A: Effect of short-chain fatty acid on sodium absorption in isolated human colon perfused through the vascular bed. Dig Dis Sci 26:100–106, 1981Google Scholar
  30. 30.
    Binder HJ, Mehta P: Short chain fatty acids stimulate active Na and Cl absorption in vitro in the rat distal colon. Gastroenterology 96:989–996, 1989Google Scholar
  31. 31.
    Finnie IA, Dwarakanath AD, Taylor BA, Rhodes JM: Colonic mucin synthesis is increased by sodium butyrate. Gut 36:93–99, 1995Google Scholar
  32. 32.
    Roediger WEW, Kapaniris O, Millard S: Lipogenesis from n-butyrate in colonocytes. Action of reducing agent and 5-amino salicylic acid with relevance to ulcerative colitis. Mol Cell Biochem 118:113–118, 1992Google Scholar
  33. 33.
    Ramakrishna BS, Roberts-Thomson IC, Pannall PR, Roediger WEW: Impaired sulphation of phenol by the colonic mucosa in quiescent and active ulcerative colitis. Gut 32:46–49, 1991Google Scholar
  34. 34.
    Weston RH, Lindsay JR, Purser DB, Gordon GLR, Davis P: Feed intake and digestion responses in sheep to the addition of inorganic sulfur to a herbage diet of low sulfur content. Aust J Agric Res 39:1107–1119, 1988Google Scholar
  35. 35.
    Whanger PD, Matrone G: Effect of dietary sulfur upon the fatty acid production in the rumen. Biochim Biophys Acta 98:454–461, 1965Google Scholar
  36. 36.
    Whanger PD, Matrone G: Effects of sulfur deficiency on metabolism in sheep. In Symposium: Sulfur in Nutrition. OH Muth (ed). Westport, Connecticut, AVI Publishing, 1970, pp 153–164Google Scholar
  37. 37.
    Lewis D: The reduction of sulphate in the rumen of the sheep. Biochem J 56:391–399, 1954Google Scholar
  38. 38.
    Gibson GR, MacFarlane GT, Cummings JH: Occurrence of sulphate-reducing bacteria in human faeces and the relationship of dissimilatory sulphate reduction to methanogenesis in the large gut. J Appl Bacteriol 65:103–111, 1988Google Scholar
  39. 39.
    Gibson GR, Cummings JH, MacFarlane GT: Competition for hydrogen between sulphate reducing bacteria and methanogenic bacteria from the human large intestine. J Appl Bacteriol 65:241–247, 1988Google Scholar
  40. 40.
    Whanger PD, Matrone G: Effect of dietary sulfur upon the production and absorption of lactate in sheep. Biochim Biophys Acta 124:273–279, 1966Google Scholar
  41. 41.
    Hume ID, Bird PR: Synthesis of microbial protein in the rumen. IV The influence of the level and form of dietary sulphur. Aust J Agric Res 21:315–322, 1970Google Scholar
  42. 42.
    Levitt MD, Hirsh P, Fetzer CA, Sheahan M, Levine AS: H2 excretion after ingestion of complex carbohydrates. Gastroenterology 92:383–389, 1987Google Scholar
  43. 43.
    Strocchi A, Furne J, Ellis C, Levitt MD: Methanogens outcompete sulphate reducing bacteria for H2 in the human colon. Gut 35:1098–1101, 1994Google Scholar
  44. 44.
    Strocchi A, Levitt MD: Factors affecting hydrogen production and consumption by human fecal flora. J Clin Invest 89:1304–1311, 1992Google Scholar
  45. 45.
    Levitt MD, Berggren T, Hastings J, Bond JH: Hydrogen (H2) catabolism in the colon of the rat. J Lab Clin Med 84:163–167, 1974Google Scholar
  46. 46.
    Miller TL, Weaver GA, Wolin MJ: Methanogens and anaerobes in a colon segment isolated from the normal faecal stream. Appl Environ Microbiol 48:449–450, 1984Google Scholar
  47. 47.
    Gibson GR, Cummings JH, MacFarlane GT, Allison C, Segal I, Vorster HH, Walker ARP: Alternative pathways for hydrogen disposal during fermentation in the human colon. Gut 31:679–683, 1990Google Scholar
  48. 48.
    MacFarlane GT, Gibson GR, Cummings JH: Comparison of fermentation reactions in different regions of the human colon. J Appl Bacteriol 72:57–64, 1992Google Scholar
  49. 49.
    Gibson GR, MacFarlane S, MacFarlane GT: Metabolic interactions involving sulphate-reducing and methanogenic bacteria in the human large intestine. FEMS Microbiol Ecol 12:117–125, 1993Google Scholar
  50. 50.
    Flourie B, Pellier P, Florent C, Marteau P, Pochart P, Rambaud JC: Site and substrates for methane production in human colon. Am J Physiol 260:G752–G757, 1991Google Scholar
  51. 51.
    Pochart P, Dore J, Lemann F, Goderel I, Rambaud J-C: Interrelations between populations of methanogenic archaea and sulfate-reducing bacteria in the human colon. FEMS Microbiol Lett 98:225–228, 1992Google Scholar
  52. 52.
    Bjorneklett A, Jenssen F: Relationship between hydrogen (H2) and methane (CH4) production in man. Scand J Gastroenterol 17:985–992, 1982Google Scholar
  53. 53.
    Lajoie R, Bank S, Miller TL, Wolin MJ: Acetate production from hydrogen and [13C] carbon dioxide by the microflora of human feces. Appl Environ Microbiol 54:2723–2727, 1988Google Scholar
  54. 54.
    Wolin MJ, Miller TL: In Acetogenesis. HL Drake (ed). New York, Chapman and Hall, 1994, p 365Google Scholar
  55. 55.
    Sawyer CN, McCarty PL: Chemistry for Environmental Engineering, 3rd ed. New York, McGraw-Hill, 1978, pp 476–481Google Scholar
  56. 56.
    Hamilton WA: Biocorrosion: The action of sulphate-reducing bacteria. In Biochemistry of Microbial Degradation. C Ratlidge (ed.). Dordrecht, Kluwer Academic Publishers, 1994, 555–570Google Scholar
  57. 57.
    Florin THJ, Gibson GR, Neale G, Cummings JH: A role for sulfate reducing bacteria in ulcerative colitis. Gastroenterology 98:A170, 1990Google Scholar
  58. 58.
    Pitcher MCL, Beatty ER, Cummings JH: Salicylates inhibit bacterial sulphide production within the colonic lumen in ulcerative colitis. Gut 37:A15, 1995Google Scholar
  59. 59.
    Levine J, Ellis CJ, Furne JK, Springfield JR, Levitt MD: Sulfate reducing bacteria and ulcerative colitis. Gastroenterology 110:A959, 1996Google Scholar
  60. 60.
    Gibson GR, Cummings JH, MacFarlane GT: Growth and activities of sulphate reducing bacteria in gut contents of healthy subjects and patients with ulcerative colitis. FEMS Microbiol Ecol 86:103–112, 1991Google Scholar
  61. 61.
    Pitcher MCL, Beatty ER, Gibson GR, Cummings JH: Incidence and activities of sulphate-reducing bacteria in patients with ulcerative colitis. Gut 36:A63, 1995Google Scholar
  62. 62.
    Wright JP: The incidence of inflammatory bowel disease at the tip of Africa. In Inflammatory Bowel Diseases. H Goebell, BM Peskar, H Malchow (eds). Lancaster, MTP Press, 1988, pp 249–250Google Scholar
  63. 63.
    Segal I: Ulcerative colitis in a developing country of Africa: The Baragwanath experience of the first 46 patients. Int J Colorect Dis 3:222–225, 1988Google Scholar
  64. 64.
    Chacko A, Cummings JH: Nitrogen loss from the human bowel: Obligatory losses and the effect of physical form of food. Gut 29:809–815, 1988Google Scholar
  65. 65.
    Florin T, Neale G, Gibson GR, Christl SU, Cummings JH: Metabolism of dietary sulphate: Absorption and excretion in humans. Gut 32:766–773, 1991Google Scholar
  66. 66.
    Garcia RAG, Stipanuk MH: The splanchnic organs liver and kidney have unique roles in the metabolism of sulfur amino acids and their metabolites in rats. J Nutr 122:1693–1701, 1992Google Scholar
  67. 67.
    Sabry ZI, Shadarevian SB, Cowan JW, Campbell JA: Relationship of dietary intake of sulphur amino acids to urinary excretion of inorganic sulphate in man. Nature 206:931–933, 1965Google Scholar
  68. 68.
    Rao AM, Drake MR, Stipanuk MH: Role of the transsulfuration pathway and of γ cystathionase activity in the formation of cysteine and sulfate from methionine in rat hepatocytes. J Nutr 120:837–845, 1990Google Scholar
  69. 69.
    Friedberg F, Tarver H, Greenberg DM: The distribution pattern of sulfur-labeled methionine in the protein and the free amino acid fraction of tissues after intravenous administration. J Biol Chem 173:355–361, 1948Google Scholar
  70. 70.
    Dahm LJ, Jones DP: Secretion of cysteine and glutathione from mucosa to lumen in rat small intestine. Am J Physiol 267:G292–G300, 1994Google Scholar
  71. 71.
    Stephen AM, Millard SH, Babidge WJ, Roediger WEW: Movement of sulphate across the intestinal mucosa. Proc Can Fed Biol Soc June: 1995Google Scholar
  72. 72.
    Tragnone A, Valpiani D, Miglio F, Elmi G, Bazzochi G, Pipitone E, Lanfranchi GA: Dietary habits as risk factors for inflammatory bowel disease. Eur J Gastro-Hepatol 7:47–51, 1995Google Scholar
  73. 73.
    Lutz J, Linkswiler HM: Calcium metabolism in post menopausal and osteoporotic women consuming two levels of dietary protein. Am J Clin Nutr 34:2178–2186, 1981Google Scholar
  74. 74.
    Briggs D, Wahlqvist MD: Food Facts. Ringwood, Australia, Penguin Books, 1984, pp 219–224Google Scholar
  75. 75.
    Scherz H, Senser F: Food Composition and Nutrition Tables 1989/90. Stuttgart, Wissenschaftliche Verlagsgesellschaft, 1989Google Scholar
  76. 76.
    Truelove SC: Ulcerative colitis provoked by milk. Br Med J 1:154–160, 1961Google Scholar
  77. 77.
    Wright R, Truelove SC: A controlled therapeutic trial of various diets in ulcerative colitis. Br Med J 2:138–141, 1965Google Scholar
  78. 78.
    Wright R, Truelove SC: Circulating antibodies to dietary proteins in ulcerative colitis. Br Med J 2:142–144, 1965Google Scholar
  79. 79.
    Knoflach P, Park BH, Cunningham R, Weiser MM, Albini B: Serum antibodies to cow's milk proteins in ulcerative colitis and Crohn's disease. Gastroenterology 92:479–485, 1987Google Scholar
  80. 80.
    Frazer AC, Hood C, Davies AG, Carter PA, Montgomery RD, Schneider R, Goodhart J: Carbohydrate intolerance in ulcerative colitis. Lancet 1:503–505, 1966Google Scholar
  81. 81.
    Cady AB, Rhodes JB, Littman A, Crane RK: Significance of lactase deficit in ulcerative colitis. J Lab Clin Med 70:279–286, 1967Google Scholar
  82. 82.
    Pena AS, Truelove SC: Hypolactasia and ulcerative colitis. Gastroenterology 64:400–404, 1973Google Scholar
  83. 83.
    Kirschner BS, De Favaro MV, Jensen W: Lactose malabsorption in children and adolescents with inflammatory bowel diseases. Gastroenterology 81:829–832, 1981Google Scholar
  84. 84.
    Bernstein CN, Ament M, Artinian L, Ridgeway J, Shanahan F: Milk tolerance in adults with ulcerative colitis. Am J Gastroenterol 89:872–877, 1994Google Scholar
  85. 85.
    Sahi T: Genetics and epidemiology of adult-type hypolactasia. Scand J Gastroenterol 29(suppl 202):7–20, 1994Google Scholar
  86. 86.
    Lash LH, Hagen TM, Jones DP: Exogenous glutathione protects intestinal epithelial cells from oxidative injury. Proc Natl Acad Sci USA 83:4641–4645, 1986Google Scholar
  87. 87.
    Aminlari M, Gilanpour H: Comparative studies on the distribution of rhodanase in different tissues of domestic animals. Comp Biochem Physiol 99B:673–677, 1991Google Scholar
  88. 88.
    Weisiger RA, Pinkus LM, Jakoby WB: Thiol S-methyltransferase: Suggested role in detoxification in intestinal hydrogen sulfide. Biochem Pharmacol 29:2885–2887, 1980Google Scholar
  89. 89.
    Weisiger RA, WB Jakoby: S-Methylation: Thiol S-methyltransferase. In Enzymatic Basis of Detoxification, Vol II. WB Jakoby (ed.). New York, Academic Press, 1980, pp 131–140Google Scholar
  90. 90.
    Pacifici GM, Santerini S, Giuliani L, Rane A: Thiol methyltransferase in humans: Development and tissue distribution. Dev Pharmacol Ther 17:8–15, 1991Google Scholar
  91. 91.
    Pacifici GM, Romiti P, Saneterini S, Giuliani L: S-Methyltransferases in human intestine: Differential distribution of the microsomal thiol methyl-transferase and cytosolic thiopurine methyltransferase along the human bowel. Xenobiotica 23:671–679, 1993Google Scholar
  92. 92.
    Babidge WJ, Millard SH, Roediger WEW: Thiol methyltransferase activity in colonocytes and erythrocyte membranes. J Clin Pathol 48:641–644, 1995Google Scholar
  93. 93.
    Keith RA, Vanloon J, Wussow LF, Weinshilboum RM: Thiol methylation pharmacogen etic heritability of human erythrocyte thiol methyltransferase activity. Clin Pharmacol Ther 34:521–528, 1983Google Scholar
  94. 94.
    Pitcher MCL, Beatty ER, Harris RM, Waring RH, Cummings JH: Detoxification of luminal xenobiotics in ulcerative colititis. Gastroenterology 110:A1740, 1996Google Scholar
  95. 95.
    Claesson R, Granlund-Edstedt M, Persson S, Carlsson J: Activity of polymorphonuclear leukocytes in the presence of sulfide. Infect Immun 57:2776–2781, 1989Google Scholar
  96. 96.
    Granlund-Edstedt M, Johansson E, Claesson R, Carlsson J: Effect of anaerobiosis and sulfide on killing of bacteria by polymorphonuclear leukocytes. J Periodont Res 28:346–353, 1993Google Scholar
  97. 97.
    Persson S, Claesson R, Carlsson J: Chemotaxis and degranulation of polymorphonuclear leukocytes in the presence of sulfide. Oral Microbiol Immunol 8:46–49, 1993Google Scholar
  98. 98.
    Johnston RB, Godzik CA, Cohn ZA: Increased superoxide anion production by immunologically activated and chemically diluted macrophages. J Exp Med 148:115–117, 1978Google Scholar
  99. 99.
    Dutta S, Ali E, Samanta AK: Function of interleukin-8 are mediated through thiol group(s) of IL-8 receptor in human poly-morphonuclear neutrophils. FEBS Lett 325:262–266, 1993Google Scholar
  100. 100.
    Ng W, Tonzetich J: Effect of hydrogen sulfide and methyl mercaptan on the permeability of oral mucosa. J Dent Res 63:994–997, 1984Google Scholar
  101. 101.
    Johnson PW, Yaegaki K, Tonzetich J: Effect of volatile thiol compounds on protein metabolism by human gingival fibroblasts. J Periodont Res 27:553–561, 1992Google Scholar
  102. 102.
    Aslam M, Batten JJ, Florin THJ, Sidebotham RL, Baron JH: Hydrogen sulphide induced damage to the colonic mucosal barrier in the rat. Gut 33:S69, 1992Google Scholar
  103. 103.
    Moore JWE, Roediger WEW, Millard S: Hydrogen sulfide diminishes fatty acid oxidation in the rat colonic mucosa in vivo. Int J Colorec Dis 11:150–151, 1996Google Scholar
  104. 104.
    Travis SPL, Jewell DP: Salicylates for ulcerative colitis—their mode of action. Pharmacol Ther 63:135–161, 1994Google Scholar
  105. 105.
    Roediger WEW, Duncan A: 5-ASA decreases colonic sulfide formation: Implications for ulcerative colitis. Med Sci Res 24:27–29, 1996Google Scholar
  106. 106.
    Saleh AM, MacPherson R, Miller JDA: The effect of inhibitors on sulphate reducing bacteria: A compilation. J Appl Bact 27:281–293, 1964Google Scholar
  107. 107.
    Pitcher MCL, Gibson GR, Neale G, Cummings JH: Gentamicin kills multiple drug-resistant sulfate-reducing bacteria in patients with ulcerative colitis. Gastroenterology 106:A753, 1994Google Scholar
  108. 108.
    Burke DA, Axon ATR, Clayden SA, Dixon MF, Johnston D, Lacey RW: The efficacy of tobramycin in the treatment of ulcerative colitis. Aliment Pharmacol Ther 4:123–129, 1990Google Scholar
  109. 109.
    Lobo AJ, Burke DA, Sobala GM, Axon ATR: Oral tobramycin in ulcerative colitis: Effect on maintenance of remission. Aliment Pharmacol Ther 7:155–158, 1993Google Scholar
  110. 110.
    Turunen U, Färkkilä M, Hakala K, Vuoristo M, Rahm V, Seppala K, Valtonen V, Miettinen TA: A double-blind, placebo controlled six-month ciprofloxacin treatment improves prognosis in ulcerative colitis. Gastroenterology 106:A786, 1994Google Scholar
  111. 111.
    Amdur MO, Doull J, Klaassen CD (eds): Toxicology: The Basic Science of Poisons, 4th Ed. New York, Pergamon Press, 1991Google Scholar
  112. 112.
    Thiede C, Bayerdörffer E, Thiede H-M, Ochsenkühn T, Neubauer A: Quantification of the essential methyl-groups donor S-adenosyl-methionine in human colorectal mucosa of patients with inflammatory bowel disease (IBD) and colorectal adenomas. Gastroentology 108:A546, 1995Google Scholar
  113. 113.
    Di Padova C: Adenosylmethionine in the treatment of osteoarthritis. Review of the clinical studies. Am J Med 83(suppl 5A):60–65, 1987Google Scholar
  114. 114.
    Roediger WEW, Babidge W, Millard S: Methionine derivatives diminish sulphide damage to colonocytes—implications for ulcerative colitis. Gut 39:77–81, 1996Google Scholar
  115. 115.
    Salim AS: Role of sulphydryl-containing agents in the management of recurrent attacks of ulcerative colitis. A new approach. Pharmacology 45:307–318, 1992Google Scholar
  116. 116.
    Yadav VK, Archer DB: Specific inhibition of sulphate-reducing bacteria in methanogenic co-culture. Lett Appl Microbiol 7:165–168, 1988Google Scholar

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© Plenum Publishing Corporation 1997

Authors and Affiliations

  • W.E.W. Roediger
  • J. Moore
  • W. Babidge

There are no affiliations available

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