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Temporal Patterns of Colonic Blood Flow and Tissue Damage in an Animal Model of Colitis

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Abstract

This study tested the hypothesis that alteredcolonic blood flow may contribute to tissue damageduring the development of colitis in the rabbit. Thiswas achieved by using radioactive microspheres tomeasure colonic blood flow at various times aftercolitis induction with trinitrobenzene sulfonic acid.Significant colonic damage occurred 6 hours post colitisinduction and persisted throughout the 5 day study. Blood flow to the muscularis propria andmucosa/muscularis mucosae compartments increasedsignificantly from 5 minutes until one hour postinduction. At 6 and 12 hours post induction colonicblood flow returned to control levels before increasingagain from 24 to 96 hours. This second increase in flowwas, however, predominantly in the mucosa/muscularismucosae compartment. Blood flow in the stomach and non-gastrointestinal tissues did not changesignificantly at any time. These data demonstrate thatincreased colonic blood flow may be disrupted in theearly stages of colitis and that this coincides with the onset of significant damage. It isconcluded that maintenance of elevated colonic bloodflow throughout the development of colitis may help toameliorate subsequent tissue injury.

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REFERENCES

  1. Bolondi L, Gaiani S, Brignola C, Campieri M, Rigamonti A, Zironi G, Gionchetti P, Belloli C, Miglioli M, Barbara L: Changes in splanchnic hemodynamics in inflammatory bowel disease. Scand J Gastroenterol 27:501–507, 1992

    Google Scholar 

  2. Boyd AJ, Sherman IA, Saibil FG: Microcirculation in a trinitrobenzene sulfonic acid-induced chronic ileitis. Gastroenterology 104:A1030, 1993

    Google Scholar 

  3. Sankey EA, Dhillon AP, Anthony A, Wakefield AJ, Sim R, More L, Hudson M, Sawyer AM, Pounder RE: Early mucosal changes in Crohn's disease. Gut 34:375–381, 1993

    Google Scholar 

  4. Hulten L, Lindhagen J, Lundgren O, Fasth S, Ahren C: Regional intestinal blood flow in ulcerative colitis and Crohn's disease. Gastroenterology 72:388–396, 1977

    Google Scholar 

  5. Angerson WJ, Allison MC, Baxter JN, Russell RT: Neoterminal ileal blood flow after ileal resection for Crohn's disease. Gut 34:1531–1534, 1993

    Google Scholar 

  6. Gizzi G, Belcaro G, Cianci M, Villani V, Campieri M, Miglioli M, Barbara L: Evaluation of mucosal and skin flux by laser Doppler flowme try in ulcerative colitis. Gastroenterology 102:A628, 1992

    Google Scholar 

  7. Matsumoto T, Kitano A, Obata A, Suzuki N, Nakamura S, Oshitanai N, Arakawa T, Nagura H, Kobayashi K: Digitalprocessed vascular images correlated to mucosal blood flow and vascular reconstruction in ulcerative colitis. Proc. American Gastroenterological Assoc. Meeting, A588, 1996

  8. Pittilo RM, Wakefield AJ, Cooper P, Dhillon AP, Rowles PM, Hudson M, Pounder RE: Ultrastructural studies of the vascular changes seen in Crohn's disease: Vasculitis, intravascular collagen degradation, and identification of paramyxovirus-like particles. Gastroenterology 104:A763, 1993

    Google Scholar 

  9. Halstensen TS, Mollnes TE, Fausa O, Brandtzaeg P: Deposits of terminal complement complex (TCC) in muscularis mucosae and submucosal vessels in ulcerative colitis and Crohn's disease of the colon. Gut 30:361–366, 1989

    Google Scholar 

  10. Yamada T, Specian RD, Granger DN, Gaginella TS, Grisham MB: Misoprostol attenuates acetic acid-induced increases in mucosal permeability and inflammation: Role of blood flow. Am J Physiol 261:G332–G339, 1991

    Google Scholar 

  11. Brown JA, Zipser RD: Prostaglandin regulation of colonic blood flow in rabbit colitis. Gastroenterology 92:54–59, 1987

    Google Scholar 

  12. Leung FW, Koo A: Mucosal vascular stasis precedes loss of viability of endothelial cells in rat acetic acid colitis. Dig Dis Sci 36:727–732, 1991

    Google Scholar 

  13. Appleyard CB, Wallace JL: Reactivation of hapten-induced colitis and its prevention by antiinflammatory drugs. Am J Physiol 269:G119–G125, 1995

    Google Scholar 

  14. Morris GP, Beck PL, Herridge MS, Depew WT, Szewczuk MR, Wallace JL: Hapten-induced model of chronic inflammation and ulceration in the rat colon. Gastroenterology 96:795–803, 1989

    Google Scholar 

  15. Heymann MA, Payne BD, Hoffman JIE, Rudolph AM: Blood flow measurements with radionuclide-labeled particles. Prog Cardiovasc Dis 20:55–79, 1977

    Google Scholar 

  16. Schalk KA, Williams JL, Heistad DD: Effect of atriopeptin on blood flow to cerebrum and choroid plexus. Am J Physiol 257:R1365–R1369, 1989

    Google Scholar 

  17. Wallace JL, Le T, Carter L, Appleyard CB, Beck PL: Hapteninduced chronic colitis in the rat: Alternatives to trinitrobenzene sulfonic acid. J Pharmacol Toxicol Methods 33:237–239, 1995

    Google Scholar 

  18. Percy WH, Burton MB, Jacobowitz Y, Burakoff R: An investigation in vitro of the properties of the individual muscle layers of the rabbit colon in an induced colitis. In Effects of Immune Cells and Inflammation on Smooth Muscle and Enteric Nerves, WJ Snape, SM Collins (eds). CRC Press, Boca Raton, Florida, 1990, pp 95–108

    Google Scholar 

  19. Percy WH, Burton MB, Rose K, Donovan V, Burakoff R: In vitro changes in the properties of rabbit colonic muscularis mucosae in colitis. Gastroenterology 104:369–376, 1993

    Google Scholar 

  20. Percy WH, Christensen J: Pharmacological characterization of opossum distal colonic muscularis mucosae in vitro. Am J Physiol 250:G98–G102, 1986

    Google Scholar 

  21. Percy WH, Roberts RL, Mason JB, Christensen J: Substrate dependence and oxygen sensitivity of tone and of spontaneous and evoked contractions of the distal colonic muscularis mucosae of the opossum. Gastroenterology 91:570–575, 1986

    Google Scholar 

  22. Percy WH, Rose K, Burton MB: Pharmacologic characterization of the muscularis mucosae in three regions of the rabbit colon. J Pharmacol Exp Ther 261:1136–1142, 1992

    Google Scholar 

  23. Mangino MJ, Anderson CB, Murphy MK, Brunt E, Turk J: Mucosal arachidonate me tabolism and intestinal ischemiareperfusion injury. Am J Physiol 257:G299–G307, 1989

    Google Scholar 

  24. Okada N, Goto H, Hase S, Arisawa T, Niwa Y, Ohmiya N, Histatomi M, Hirose Y, Tachi K, Watanabe T, Tsukamura M, Hisanaga Y, Hayakawa T: Does Nitric oxide synthase inhibitor affect healing of rat experimental colitis? Gastroenterology 110:A984, 1996

    Google Scholar 

  25. Burakoff R, Donovan V, Tolentino T, Zhao L, Percy WH: Changes in motility and arachidonic acid metabolites in a rabbit trinitrobenzene sulfonic acid model of colitis. Gastroenterology 98:A463, 1990

    Google Scholar 

  26. Chou CC, Gallavan RH: Blood flow and intestinal motility. Fed Proc 41:2090–2095, 1982

    Google Scholar 

  27. Parodi J, Grisoni E, Ferrario C, Kramer A, Beven E: Hypertonicity of intestinal smooth muscle as a factor of intestinal ischemia in necrotizing enterocolitis. J Pediatr Surg 22:713–718, 1987

    Google Scholar 

  28. Fabia R, Ar'Rajab A, Willen R, Marklund S, Andersson R: The role of transient mucosal ischemia in acetic acid-induced colitis in the rat. J Surg Res 63:406–412, 1996

    Google Scholar 

  29. Osborne MJ, Hudson M, Piasecki C, Dhillon AP, Lewis A, Pounder RE, Wakefield AJ: Crohn's disease and anastomotic recurrence: Microvascular ischaemia and anastomotic healing in an animal model. Br J Surg 80:226–229, 1993

    Google Scholar 

  30. Dobosz M, Mionskowska L, Dobrowolski S, Dymecki D, Makarewicz W, Hrabowska M, Wajda Z: Is nitric oxide and heparin treatment justified in inflammatory bowel disease? An experimental study. Scand J Clin Lab Invest 56:657–663, 1996

    Google Scholar 

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Authors
  1. Caroline B. Appleyard
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  2. John L. Williams
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  3. Christopher A. Hathaway
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  4. William H. Percy
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Appleyard, C.B., Williams, J.L., Hathaway, C.A. et al. Temporal Patterns of Colonic Blood Flow and Tissue Damage in an Animal Model of Colitis. Dig Dis Sci 44, 431–438 (1999). https://doi.org/10.1023/A:1026687424966

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  • DOI: https://doi.org/10.1023/A:1026687424966

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