Abstract
Acute gastrointestinal infections with transient mucosal inflammation frequently precede the onset of functional GI disorders with altered visceral sensory function. We hypothesized that an acute inflammation of the mucosa is linked to long-lasting alterations of afferent visceral pathways. Utilizing abdominal wall electromyography, we tested the visceromotor response to tonic rectal distension (60 mm Hg/3 min) in fasted, conscious, male Lewis rats (n = 40) with a barostat device before and 2, 4, 15, and 17 weeks after rectal instillation of saline or trinitrobenzenesulfonic acid plus ethanol. Tissue samples from paired controls were obtained to assess histologic tissue alterations. Inflammatory changes were present up to 2 weeks after acid/ethanol instillation but not after saline instillation. Compared to baseline measurements, the visceromotor response to colorectal distension increased significantly and reached a maximum 17 weeks (P < 0.001) after induction of colitis, while it decreased in control experiments (P < 0.05). In conclusion, these data suggest that an acute inflammation has long-term effects on somatosensory functioning.
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REFERENCES
Talley NJ, Silverstein F, Agréus L, Nyén O, Sonnenberg A, Holtmann G: American Gastroenterological Association medical position statement: Evaluation of dyspepsia. Gastroenterology 114:579–581, 1998
Thompson WG, Dotevall G, Drossman DA, Heaton KW, Kruis W: Irritable bowel syndrome: Guidelines for the diagnosis. Gastroenterol Int 2:92–95, 1989
Mayer EA, Gebhart GF: Basic and clinical aspects of visceral hyperalgesia. Gastroenterology 107:271–293, 1994
McKendrick MW, Read NW: Irritable bowel syndrome-Post salmonella infection. J Infect 29:1–3, 1994
Neal KR, Hebden J, Spiller R: Prevalence of gastrointestinal symptoms six months after bacterial gastroenteritis and risk factors for development of irritable bowel syndrome: postal survey of patients. Br Med J 314:779–782, 1997
Gschossmann J, Holtmann G, Adam B, Liebregts T, Zeeh JM., Ruwe M, Schmid KW, Mayer EA, Gerken G: Strain differences in the visceromotor response to colorectal distension during trinitrobenzene-sulfonic acid-induced colitis. Gastroenterology 116:A607, 1999
Hoffmann P, Zeeh JM, Lakshmanan J, Wu VS, Procaccino F, Reinshagen M, McRoberts JA, Eysselein VE: Increased expression of transforming growth factor alpha precursors in acute experimental colitis in rats. Gut 41:195–202, 1997
Reinshagen M, Rohm H, Steinkamp M, Lieb K, Geerling I, Von Herbay A, Flamig G, Eysselein VE, Adler G: Protective role of neurotrophins in experimental inflammation of the rat gut. Gastroenterology 119:368–376, 2000
Ness TJ, Gebhart GF: Colorectal distension as a noxious visceral stimulus: physiologic and pharmacologic characterization of pseudaffective reflexes in the rat. Brain Res 450:153–169, 1988
Dieleman LA, Palmen MJ, Akol H, Bloemena E, Pena AS, Meuwissen SG, Van Rees EP: Chronic experimental colitis induced by dextran sulphate sodium (DSS) is characterized by Th1 and Th2 cytokines. Clin Exp Immunol 114:385–391, 1998
Collins SM, Barbara G, Vallance B: Stress, inflammation and the irritable bowel syndrome. Can J Gastroenterol 13 (Suppl A):47A–49A, 1999
Collins SM, McHugh K, Jacobson K, Khan I, Riddell R, Murase K, Weingarten HP: Previous inflammation alters the response of the rat colon to stress. Gastroenterology 111:1509–1515, 1996
Gwee KA, Leong YL, Graham C, McKendrick MW, Collins SM, Walters SJ, Underwood JE, Read NW: The role of psychological and biological factors in postinfective gut dysfunction. Gut 44:400–406, 1999
Holtmann G, Buenger L, Saadat-Gilani K, Gerken G, Pietsch A, Talley NJ: Opioidergic antinociceptive pathways modulate gastric mechanosensory function in healthy subjects. Gastroenterology 120:A81, 2001
Holtmann G, Gschossmann J, Neufang-Hüber J, Gerken G, Talley NJ: Differences in gastric mechanosensory after repeated ramp distension in non-consulters with dyspepsia and healthy. Gut 47:332–336, 2000
Loening Baucke V, Metcalf AM, Shirazi S: Anorectal manometry in active and quiescent ulcerative colitis. Am J Gastroenterol 84:892–897, 1989
Chang L, Munakata J, Mayer EA, Schmulson MJ, Johnson TD, Bernstein CN, Saba L, Naliboff B, Anton PA, Matin K: Perceptual responses in patients with inflammatory and functional bowel disease. Gut 47:497–505, 2000
Laine L, Schoenfeld P, Fennerty MB: Therapy for Helicobacter pylori in patients with nonulcer dyspepsia.Ameta-analysis of randomized, controlled trials. Ann Intern Med 134:361–369, 2001
Miampamba M, Parr EJ, McCafferty DM, Wallace JL, Sharkey KA: Effect of intracolonic benzalkonium chloride on trinitrobenzene sulphonic acid-induced colitis in the rat. Aliment Pharmacol Ther 12:219–228, 1998
Ness TJ, Gebhart GF: Acute inflammation differentially alters the activity of two classes of rat spinal visceral nociceptive neurons. Neurosci Lett 281:131–134, 2000
Miampamba M, Sharkey KA: Distribution of calcitonin gene-related peptide, somatostatin, substance P and vasoactive intestinal polypeptide in experimental colitis in rats. Neurogastroenterol Motil 10:315–329, 1998
Stead RH, Kosecka-Janiszewska U, Oestreicher AB, Dixon MF, Bienenstock J: Remodeling of B-50 (GAP-43)-and NSE-immunoreactive mucosal nerves in the intestines of rats infected with Nippostrongylus brasiliensis. J Neurosci 11:3809–3821, 1991
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Gschossmann, J.M., Liebregts, T., Adam, B. et al. Long-Term Effects of Transient Chemically Induced Colitis on the Visceromotor Response to Mechanical Colorectal Distension. Dig Dis Sci 49, 96–101 (2004). https://doi.org/10.1023/B:DDAS.0000011609.68882.3a
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DOI: https://doi.org/10.1023/B:DDAS.0000011609.68882.3a