Abstract
We investigated the effect of prior acute stress on colonic permeability induced by a chemical irritant known to induce symptoms similar to inflammatory bowel disease in rodents. Adult male rats (n=12) were stressed by a single session of ten unpredictable, uncontrollable foot shocks, and half were home cage controls (n=12). Twenty-nine days later, half of each treatment group was exposed to 4% DSS (dextran sulphate sodium) solution in their drinking water for 48 hours while half received pure water over two periods separated by 17 days. After food deprivation overnight and light isoflurane anaesthesia the following morning, the animals were given a colonic infusion of 2000 nCi (nanocurie)51CrEDTA (51Cr-labelled ethylenediaminetetraacetic acid) and then placed individually in metabolic cages for a six hours continuous urine collection. Radioactivity in urine was measured by a gamma counter and percentage recovery of51CrEDTA calculated as an indicator of colonic mucosal permeability. Results concluded that pre-shocked animals exposed to DSS showed significantly higher mucosal permeability than the pre-shocked animals given water, and the non-shocked animals given either DSS or water. Pre-shock in combination with two exposures to a chemical irritant separated by 17 days had a pronounced effect on colonic permeability, indicating that stress should be considered a possible initiating or contributory factor to increased intestinal permeability related to a mucosal challenge.
Similar content being viewed by others
References
Anic, B., Brkic, T., Banic, M., Heinzl, R., Dohozcky, C., Smud, D., Rotkvic, I., & Buljevac, M. (1997). Histopathologic features of T-cell mediated colonic injury induced with 2,4-dinitrofluorobenzene in BALB/c mice.Acta Medica Croatia, 51(1), 11–14.
Arslan, G., Atasever, T., Cindoruk, M., & Yildirim, I.S. (2001). (51)CrEDTA colonic permeability and therapy response in patients with ulcerative colitis.Nuclear Medicine Communications, 22(9), 997–1001.
Bamias, G., Martin, C. III, Marini, M., Hoang, S., Mishina, M., Ross, W.G., Sachedina, M.A., Friel, C.M., Mize, J., Bickston, S.J., Pizarro, T.T., Wei, P., & Cominelli, F. (2003). Expression, localization, and functional activity of TL1A, a novel Th1-polarizing cytokine in inflammatory bowel disease.Journal of Immunology, 171(9), 4868–4874.
Barreau, F., Ferrier, L., Fioramonti, J., & Bueno, L. (2004). Neonatal maternal deprivation triggers long term alterations in colonic epithelial barrier and mucosal immunity in rats.Gut, 53(4), 501–506.
Berstad, A., Arslan, G., & Folvik, G. (2000). Relationship between intestinal permeability and calprotectin concentration in gut lavage fluid.Scandinavian Journal of Gastroenterology, 35(1), 64–69.
Bjarnason, I., O’Morain, C., Levi, A.J., & Peters, T.J. (1983). Absorption of51chromium-labeled ethylenediaminetetraacetate in inflammatory bowel disease.Gastroenterology, 85(2), 318–322.
Bradesi, S., McRoberts, J.A., Anton, P.A., & Mayer, E.A. (2003). Inflammatory bowel disease and inrritable bowel syndrome: Separate or unified?Current Opinion in Gastroenterology 19(4), 336–342.
Castagliuolo, I., Lamont, J.T., Qiu, B., Fleming, S.M., Bhaskar, K.R., Nikulasson, S.T., Kornetsky, C., & Pothoulakis, C. (1996). Acute stress causes mucin release from rat colon: role of corticotropin releasing factor and mast cells.American Journal of Physiology, 271(5 Pt 1), 884–892.
Cenac, N., Garcia-Villar, R., Ferrier, L., Larauche, M., Vergnolle, N., Bunnet, N.W., Coelho, A.M., Fioramonti, J., & Bueno, L. (2003). Proteinase-activated receptor-2-induced colonic inflammation in mice: possible involvement of afferent neurons, nitric oxide, and paracellular permeability.The Journal of Immunology, 170, 4296–4300.
Chadwick, V.S., Chen, W., Shu, D., Paulus, B., Bethwaite, P., Tie, A., & Wilson, I. (2002). Activation of the mucosal immune system in irritable bowel syndrome.Gastroenterology, 122, 1778–1783.
Collins, S.M., McHugh, K., Jacobson, K., Khan, I., Riddell, R., Murase, K., & Weingarten, H.P. (1996). Previous inflammation alters the response of the rat colon to stress.Gastroenterology, 111(6), 1509–1515.
Cooper, H.S., Murthy, S.N., Shah, R.S., & Sedergran, D.J. (1993). Clinicopathological study of dextran sulfate sodium experimental murine colitis.Laboratory Investigation 69, 238–249.
Den Hond, E., Hiele, M., Peeters, M., Ghoos, Y., & Rutgeerts, P. (1999). Effect of long-term oral glutamine supplements on small intestinal permeability in patients with Crohn’s disease.Journal of Parenteral and Enteral Nutrition, 23(1), 7–11.
Drossman, D.A. (1998). Presidential address: Gastrointestinal illness and the biopsychosocial model.Psychosomatic Medicine, 60(3), 258–267.
Ekström, G.M. & Andersson, S.E. (2000). Plasma exudation, hyperaemia, and epithelial permeability in rats with oxazolone-induced colitis: Modulatory effects of budesonide.Scandinavian Journal of Gastroenterology, 35, 190–197.
Elson, C.O., Sartor, R.B., Tennyson, G.S., & Riddell, R.H. (1995). Experimental models of inflammatory bowel disease.Gastroenterology, 109, 1344–1367.
Fukada, H., Tsuchida, D., Koda, K., Miyazaki, M., Pappas, T.N., & Takahashi, T. Impaired gastric motor activity after abdominal surgery in rats (2004).Neurogastroenterology and Motility, 16, 1–6.
Gaudio, E., Taddei, G., Vetuschi, A., Sferra, R., Frieri, G., & Caprilli, R. (1999). Dextran sulphate sodium (DSS) in rats: Clinical, structural and ultrastructural aspects.Digestive Diseases and Sciences, 44(7), 1458–1475.
Gué, M., Bonbonne, C., Fioramonti, J., More, J., Del Rio-Lacheze, C., Comera, C., & Bueno, L. (1997). Stress-induced enhancement of colitis in rats: CRF and arginine vasorpressin are not involved.American Journal of Physiology, 272(1 Pt 1), 84–91.
Jenkins, R.T., Ramage, J.K., Jones, D.B., Collins, S.M., Goodacre, R.L., & Hunt, R.H. (1988). Small bowel and colonic permeability to 51Cr-EDTA in patients with active inflammatory bowel disease.Clinical and Investigative Medicine, 11(2), 151–155.
Kendall-Tackett, K.A. (2000). Physiological correlates of childhood abuse: chronic hyperarousal in PTSD, depression and irritable bowel syndrome.Child Abuse and Neglect, 24(6), 799–810.
Kullman, F., Messman, H., Alt, M., Gross, V., Bocker, T., Scholmerich, J., & Ruschoff, J. (2001). Clinical and histopathological features of dextran sulfate sodium induced acute and chronic colitis associated with dysplasia in rats.International Journal of Colorectal Disease, 16(4), 238–246.
Levenstein, S., Prantera, C., Varco, V., Scribano, M.L., Andreoli, A., Luzi, C., Arca, M., Berto, E., Milite, G., & Marcheggiano, A. (2000). Stress and exacerbation in ulcerative colitis: A prospective study of patients enrolled in remission.American Journal of Gastroenterology, 95(5), 1213–1220.
Milde, A.M., Sundberg, H., Røseth, A.G., & Murison, R. (2003). Proactive sensitizing effects of acute stress on acoustic startle responses and experimentally induced colitis in adult rats.Stress, 6(1), 49–57.
Milde, A.M., Arslan, G., Røseth, A., Berstad, A., Overmier, J.B., & Murison, R. (2004). Intestinal, permeability and faecal granulocyte marker protein in dextran sulphate sodium-induced colitis in rats.Scandinavian Journal of Laboratory Animal Science, 30(4), 169–175.
Milde, A.M. & Murison, R. (2002). A study of the effects of restraint stress on colitis induced by dextran, sulphate sodium in singly housed rats.Integrative Physiology & Behavioral Science, 37(2), 140–150.
Monnikes, H., Tebbe, J.J., Hildebrandt, M., Arck, P., Osmanoglou, E., Rose, M., Klapp, B., Wiedenmann, B., & Heymann-Monnikes, I. (2001). Role of stress in functional gastrointestinal disorders. Evidence for stress-induced alterations in gastrointestinal motility and sensitivity.Digestive Diseases, 19(3), 201–211.
Muir, W.W. & Mason, D. (1996). InLumb and Jones’ Veterinary Anaesthesia, 3rd edition, eds J.C. Thurmon, W.J. Tranquilli, G.J. Benson, Williams and Wilkins, Baltimore.
Nagura, H., Ohtani, H., Sasano, H., & Matsumoto, T. (2001). The immuno-inflammtory mechanism for tissue injury in inflammatory bowel disease and Helicobacter pylori-infected chronic active gastritis. Roles of the mucosal immune system.Digestion, 63(Suppl. 1), 12–21.
Overmier, J.B. & Murison, R. (2000). Anxiety and helplessness in the face of stress predisposes, precipitates, and sustains gastric ulceration.Behavioural Brain Research 110(1–2), 161–174.
Pfeiffer, C.J., Qiu, B., & Lam, S.K. (2001). Reduction of colonic mucus by repeated short-term stress enhances experimental colitis in rats.Journal of Physiology Paris, 95(1–6), 81–87.
Qiu, B.S., Vallance, B.A., Blennerhasset, P.A., & Collins, S.M. (1999). The role of CD4+ lymphocytes in the susceptibility of mice to stress-induced reactivation of experimental colitis.Nature Medicine, 5(10), 1178–1182.
Røseth, A.G., Aadland, E., Jahnsen, J., & Raknerud, N. (1997). Assessment of disease activity in ulcerative colitis by fecal calprotectin, a novel granulocyte marker protein.Digestion, 58, 176–180.
Saunders, P.R., Kosecka, U., McKay, D.M., & Perdue, M.H. (1994). Acute stressors stimulate ion secretion and increase epithelial permeability in rat intestine.American Journal of Physiology, 267(5 Pt 1), 794–799.
Saunders, P.R., Hanssen, R.P., & Perdue, M.H. (1997). Cholinergic nerves mediate stress-induced intestinal transport abnormalities in Wistar-Kyoto rats.American Journal of Physiology, 273(2 Pt 1), 486–490.
Söderholm, J.D. & Perdue, M.H. (2001). Stress and gastrointestinal tract. II. Stress and intestinal barrier function.American Journal of Gastrointestinal and Liver Physiology, 280(1), 7–13.
Stam, R., Ekkelenkamp, K., Frankuijzen, A.C., Bruijnzeel, A.W., Akkermans, L.M., & Wiegant, V.M. (2002). Long-lasting changes in central nervous system responsivity to colonic distension after stress in rats.Gastroenterology, 123(4), 1216–1225.
Tsukada, F., Nagura, Y., Abe, S., Sato, N., & Ohkubo, N. (2003). Effect of restraint and footshock stress and norepinephrine treatment on gastric emptying in rats.Biological and Pharmaceutical Bulletin, 26(3), 368–370.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Milde, A.M., Arslan, G., Overmier, J.B. et al. An acute stressor enhances sensitivity to a chemical irritant and increases51CrEDTA permeability of the colon in adult rats. Integr. psych. behav. 40, 35–44 (2005). https://doi.org/10.1007/BF02734187
Issue Date:
DOI: https://doi.org/10.1007/BF02734187