Abstract
We intended to characterize the effect of inflammation on the spontaneous colonic motility pattern and the role of iNOS in its disruption in colitis. Colitis was induced by an intracolonic enema of T. spiralis larvae. Animals were studied 2–30 days postinfection (PI). Standard H&E and iNOS staining was performed on colonic sections. Altered stool consistency was found from day 1 to day 21 PI; leukocytosis peaked on days 6–21 PI. Edema and cell infiltration were found in mucosa and submucosa (days 2–14 PI). Contractility displayed a disorganized pattern with decreased high-amplitude, low-frequency (HALF) contractions. A progressive fading of spontaneous activity was observed and was partly restored in strips devoid of submucosa. iNOS immunoreactivity increased in epithelial and infiltrating cells (days 2–14 PI). In this model of colonic inflammation, the decrease in spontaneous contractility, which might be caused by NO generated from mucosal and submucosal iNOS, bears some traits with changes observed in ulcerative colitis and might thus be useful to study the dismotility observed in this human disease.
Similar content being viewed by others
References
Rao SS, Read NW: Gastrointestinal motility in patients with ulcerative colitis. Scand J Gastroenterol Suppl 172:22–28, 1990
Snape WJ, Jr., Williams R, Hyman PE: Defect in colonic smooth muscle contraction in patients with ulcerative colitis. Am J Physiol 261:G987–G991, 1991
Reddy SN, Bazzocchi G, Chan S, Akashi K, Villanueva-Meyer J, Yanni G, Mena I, Snape WJ, Jr: Colonic motility and transit in health and ulcerative colitis. Gastroenterology 101:1289–1297, 1991
Cohen JD, Kao HW, Tan ST, Lechago J, Snape WJ, Jr: Effect of acute experimental colitis on rabbit colonic smooth muscle. Am J Physiol 251:G538–G545, 1986
Grossi L, McHugh K, Collins SM: On the specificity of altered muscle function in experimental colitis in rats. Gastroenterology 104:1049–1056, 1993
Myers BS, Martin JS, Dempsey DT, Parkman HP, Thomas RM, Ryan JP: Acute experimental colitis decreases colonic circular smooth muscle contractility in rats. Am J Physiol 273:G928–G936, 1997
Lu G, Qian X, Berezin I, Telford GL, Huizinga JD, Sarna SK: Inflammation modulates in vitro colonic myoelectric and contractile activity and interstitial cells of Cajal. Am J Physiol 273:G1233–G1245, 1997
Collins SM, Blennerhassett PA, Blennerhassett MG, Vermillion DL: Impaired acetylcholine release from the myenteric plexus of Trichinella-infected rats. Am J Physiol 257:G898–G903, 1989
Hurst SM, Collins SM: Mechanism underlying tumor necrosis factor-alpha suppression of norepinephrine release from rat myenteric plexus. Am J Physiol 266:G1123–G1129, 1994
Main C, Blennerhassett P, Collins SM: Human recombinant interleukin 1 beta suppresses acetylcholine release from rat myenteric plexus. Gastroenterology 104:1648–1654, 1993
Ruhl A, Hurst S, Collins SM: Synergism between interleukins 1 beta and 6 on noradrenergic nerves in rat myenteric plexus. Gastroenterology 107:993–1001, 1994
Khan I, Collins SM: Expression of cytokines in the longitudinal muscle myenteric plexus of the inflamed intestine of rat. Gastroenterology 107:691–700, 1994
Elson CO, Sartor RB, Tennyson GS, Riddell RH: Experimental models of inflammatory bowel disease. Gastroenterology 109:1344–1367, 1995
Jacobson K, McHugh K, Collins SM: Experimental colitis alters myenteric nerve function at inflamed and noninflamed sites in the rat. Gastroenterology 109:718–722, 1995
Mizuta Y, Isomoto H, Takahashi T: Impaired nitrergic innervation in rat colitis induced by dextran sulfate sodium. Gastroenterology 118:714–723, 2000
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
Castro GA, Fairbairn D: Carbohydrates and lipids in Trichinella spiralis larvae and their utilization in vitro. J Parasitol 55:51–58, 1969
Seldenrijk CA, Morson BC, Meuwissen SG, Schipper NW, Lindeman J, Meijer CJ: Histopathological evaluation of colonic mucosal biopsy specimens in chronic inflammatory bowel disease: diagnostic implications. Gut 32:1514–1520, 1991
Sands BE.:From symptom to diagnosis: Clinical distinctions among various forms of intestinal inflammation. Gastroenterology 126:1518–1532, 2004.
Castro GA, Copeland EM, Dudrick SJ, Ramaswamy K: Enteral and parenteral feeding to evaluate malabsorption in intestinal parasitism. Am J Trop Med Hyg 28:500–507, 1979
Faro CJ, Reidelberger RD, Palmer JM: Suppression of food intake is linked to enteric inflammation in nematode-infected rats. Am J Physiol Regul Integr Comp Physiol 278:R118–R124, 2000
Takahashi T, Owyang C: Regional differences in the nitrergic innervation between the proximal and the distal colon in rats. Gastroenterology 115:1504–1512, 1998
Pluja L, Alberti E, Fernandez E, Mikkelsen HB, Thuneberg L, Jimenez M: Evidence supporting presence of two pacemakers in rat colon. Am J Physiol Gastrointest Liver Physiol 281:G255–G266, 2001
Rumessen JJ: Ultrastructure of interstitial cells of Cajal at the colonic submuscular border in patients with ulcerative colitis. Gastroenterology 111:1447–1455, 1996
Wang XY, Berezin I, Mikkelsen HB, Der T, Bercik P, Collins SM, Huizinga JD: Pathology of interstitial cells of Cajal in relation to inflammation revealed by ultrastructure but not immunohistochemistry. Am J Pathol 160:1529–1540, 2002
Xie YN, Gerthoffer WT, Reddy SN, Cominelli F, Eysselein VE, Snape WJ, Jr: An abnormal rate of actin myosin cross-bridge cycling in colonic smooth muscle associated with experimental colitis. Am J Physiol 262:G921–G926, 1992
Liu X, Rusch NJ, Striessnig J, Sarna SK: Down-regulation of L-type calcium channels in inflamed circular smooth muscle cells of the canine colon. Gastroenterology 120:480–489, 2001
McCafferty DM, Miampamba M, Sihota E, Sharkey KA, Kubes P: Role of inducible nitric oxide synthase in trinitrobenzene sulphonic acid induced colitis in mice. Gut 45:864–873, 1999
Miampamba M, Sharkey KA: Temporal distribution of neuronal and inducible nitric oxide synthase and nitrotyrosine during colitis in rats. Neurogastroenterol Motil 11:193–206, 1999
Roberts PJ, Riley GP, Morgan K, Miller R, Hunter JO, Middleton SJ: The physiological expression of inducible nitric oxide synthase (iNOS) in the human colon. J Clin Pathol 54:293–297, 2001
Singer II, Kawka DW, Scott S, Weidner JR, Mumford RA, Riehl TE, Stenson WF: Expression of inducible nitric oxide synthase and nitrotyrosine in colonic epithelium in inflammatory bowel disease. Gastroenterology 111:871–885, 1996
Kimura H, Hokari R, Miura S, Shigematsu T, Hirokawa M, Akiba Y, Kurose I, Higuchi H, Fujimori H, Tsuzuki Y, Serizawa H, Ishii H: Increased expression of an inducible isoform of nitric oxide synthase and the formation of peroxynitrite in colonic mucosa of patients with active ulcerative colitis. Gut 42:180–187, 1998
Bian K, Harari Y, Zhong M, Lai M, Castro G, Weisbrodt N, Murad F: Down-regulation of inducible nitric-oxide synthase (NOS-2) during parasite-induced gut inflammation: a path to identify a selective NOS-2 inhibitor. Mol Pharmacol 59:939–947, 2001
Marzio L, Blennerhassett P, Chiverton S, Vermillion DL, Langer J, Collins SM: Altered smooth muscle function in worm-free gut regions of Trichinella-infected rats. Am J Physiol 259:G306–G313, 1990
Tanovic A, Jimenez M, Fernandez E: Changes in the inhibitory responses to electrical field stimulation of intestinal smooth muscle from Trichinella spiralis infected rats. Life Sci 71:3121–3136, 2002
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Aulí, M., FernóNdez, E. Characterization of Functional and Morphological Changes in a Rat Model of Colitis Induced by Trichinella spiralis. Dig Dis Sci 50, 1432–1443 (2005). https://doi.org/10.1007/s10620-005-2858-4
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s10620-005-2858-4