View More View Less
  • 1 Department of Clinical Diagnostics, Faculty of Veterinary Medicine, University of Warmia and Mazury in Olsztyn, Oczapowskiego 14, 10-957, Olsztyn, Poland
  • 2 Department of Clinical Physiology, Faculty of Veterinary Medicine, University of Warmia and Mazury in Olsztyn, Olsztyn, Poland
Restricted access

Purchase article

USD  $25.00

1 year subscription (Individual Only)

USD  $836.00

Abstract

Due to its difficult diagnosis and complicated treatment, inflammatory bowel disease (IBD) in dogs is a challenge for the veterinarian. Several aspects connected with pathological changes during IBD still remain unknown. Since one of these aspects is the participation of intestinal innervation in the evolution of the disease, the aim of this study was to demonstrate changes in the number and distribution of intramucosal colonic nerve fibres immunoreactive to substance P (SP) arising as the disease progresses. SP is one of the most important neuronal factors in intestinal innervation which, among other tasks, takes part in the conduction of pain stimuli. Using routine immunofluorescence technique, the density of nerve fibres containing SP was evaluated within mucosal biopsy specimens collected from the descending colon of healthy dogs and animals suffering from IBD of varying severity. The results of the study indicate that during severe IBD the number of nerve fibres containing SP located in the colonic mucosal layer increases in comparison to control animals. The number of SP-positive intramucosal nerves amounted to 10.99 ± 2.11 nerves per observation field in healthy dogs, 14.62 ± 2.86 in dogs with mild IBD, 14.80 ± 0.91 in dogs with moderate IBD and 19.03 ± 6.11 in animals with severe IBD. The observed changes were directly proportional to the intensity of the disease process. These observations may suggest a role of this neuronal substance in pathological processes occurring during IBD. Although the exact mechanism of the observed changes has not been completely explained, the results obtained in this investigation may contribute to improving the diagnosis and treatment of this disease, as well as the staging of canine IBD in veterinary practice.

  • Allenspach, K., Wieland, B., Gröne, A. and Gaschen, F. (2007): Chronic enteropathies in dogs: evaluation of risk factors for negative outcome. J. Vet. Intern. Med. 21, 700708.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Bathia, V. and Tandon, R. K. (2005): Stress and the gastrointestinal tract. J. Gastroenterol. Hepatol. 20, 332339.

  • Bernstein, C. N., Robert, M. E. and Eysselein, V. E. (1993): Rectal substance P concentrations are increased in ulcerative colitis but not in Crohn's disease. Am. J. Gastroenterol. 88, 908913.

    • Search Google Scholar
    • Export Citation
  • Brehmer, A., Croner, R., Dimmler, A., Papadopoulos, T., Schrödl, F. and Neuhuber, W. (2004): Immunohistochemical characterization of putative primary afferent (sensory) myenteric neurons in human small intestine. Auton. Neurosci. 112, 4959.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Brinkman, D. J., Ten Hove, A. S., Vervoordeldonk, M. J., Luyer, M. D. and de Jonge, W. J. (2019): Neuroimmune interactions in the gut and their significance for intestinal immunity. Cells 8, pii: E670.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Brunsson, I., Fahrenkrug, J., Jodal, M., Sjöqvist, A. and Lundgren, O. (1995): Substance P effects on blood flow, fluid transport and vasoactive intestinal polypeptide release in the feline small intestine. J. Physiol. 483, 727734.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • De Fontgalland, D., Wattchow, D. A., Costa, M. and Brookes, S. J. (2008): Immunohistochemical characterization of the innervation of human colonic mesenteric and submucosal blood vessels. Neuro Gastroenterol. Motil. 20, 12121226.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Deguchi, K., Reyes, C., Chakraborty, S., Antalffy, B., Glaze, D. and Armstrong, D. (2001): Substance P immunoreactivity in the enteric nervous system in Rett syndrome. Brain Dev. 23, S127S132.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Gonkowski, S. (2013): Substance P as a neuronal factor in the enteric nervous system of the porcine descending colon in physiological conditions and during selected pathogenic processes. Biofactors 39, 542551.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Gonkowski, S., Rychlik, A. and Calka, J. (2013): Pituitary adenylate cyclase activating peptide-27-like immunoreactive nerve fibers in the mucosal layer of canine gastrointestinal tract in physiology and during inflammatory bowel disease. Bull. Vet. Inst. Pulawy 57, 375380.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Gross, K. J. and Pothoulakis, C. (2007): Role of neuropeptides in inflammatory bowel disease. Inflamm. Bowel Dis. 13, 918932.

  • Holzer, P. (1998): Implications of tachykinins and calcitonin gene-related peptide in inflammatory bowel disease. Digestion 59, 269283.

  • Hwang, D. Y., Kim, S. and Hong, H. S. (2017): Substance-P ameliorates dextran sodium sulfate-induced intestinal damage by preserving tissue barrier function. Tissue Eng. Regen. Med. 15, 6373.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Jergens, A. E., Moore, F. M., March, P. and Miles, K. G. (1992): Idiopathic inflammatory bowel disease associated with gastroduodenal ulceration-erosion: a report of nine cases in the dog and cat. J. Am. Anim. Hosp. Assoc. 28, 2126.

    • Search Google Scholar
    • Export Citation
  • Jergens, A. E., Schreiner, C. A., Frank, D. E., Niyo, Y., Ahrens, F. E., Eckersall, P. D., Benson, T. J. and Evans, R. (2003): A scoring index for disease activity in canine inflammatory bowel disease. J. Vet. Intern. Med. 17, 291297.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Koon, H. W. and Pothoulakis, C. (2006): Immunomodulatory properties of substance P: the gastrointestinal system as a model. Ann. NY Acad. Sci. 1088, 2340.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Koon, H. W., Shih, D., Karagiannides, I., Zhao, D., Fazelbhoy, Z., Hing, T., Xu, H., Lu, B., Gerard, N. and Pothoulakis, C. (2010): Substance P modulates colitis-associated fibrosis. Am. J. Pathol. 177, 23002309.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Lördal, M., Johansson, C. and Hellström, P. M. (1993): Myoelectric pattern and effects on small bowel transit induced by the tachykinins neurokinin A, neurokinin B, substance P and neuropeptide K in the rat. Neurogastroent. Motil. 5, 3340.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Lördal, M., Theodorsson, E. and Hellström, P. M. (1997): Tachykinins influence interdigestive rhythm and contractile strength of human small intestine. Dig. Dis. Sci. 42, 19401949.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Maggi, C. A. (2000): Principles of tachykininergic co-transmission in the peripheral and enteric nervous system. Regul. Pept. 93, 5364.

  • Maggi, C. A., Patacchini, R., Rovero, P. and Giachetti, A. (1993): Tachykinin receptors and receptor antagonists. J. Auton. Pharmacol. 13, 2393.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Makowska, K. and Gonkowski, S. (2018): The influence of inflammation and nerve damage on the neurochemical characterization of calcitonin gene-related peptide-like immunoreactive (CGRP-LI) neurons in the enteric nervous system of the porcine descending colon. Int. J. Mol. Sci. 19, pii: E548.

    • Search Google Scholar
    • Export Citation
  • Mantyh, C. R., Vigna, S. R., Maggio, J. E., Mantyh, P. W., Bollinger, R. R. and Pappas, T. N. (1994): Substance P binding sites on intestinal lymphoid aggregates and blood vessels in inflammatory bowel disease correspond to authentic NK-1 receptors. Neurosci. Lett. 178, 255259.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Mawe, G. M., Collins, S. M. and Shea-Donohue, T. (2004): Changes in enteric neural circuitry and smooth muscle in the inflamed and infected gut. Neuro Gastroenterol. Motil. 16, 133136.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • O'Connor, T. M., O'Connell, J., O'Brien, D. I., Goode, T., Bredin, C. P. and Shanahan, F. (2004): The role of substance P in inflammatory disease. J. Cell. Physiol. 201, 167180.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Okafor, D., Kaye, A. D., Kaye, R. J. and Urman, R. D. (2017): The role of neurokinin-1 (substance P) antagonists in the prevention of postoperative nausea and vomiting. J. Anaesthesiol. Clin. Pharmacol. 33, 441445.

    • Search Google Scholar
    • Export Citation
  • Raithel, M., Schneider, H. T. and Hahn, E. G. (1999): Effect of substance P on histamine secretion from gut mucosa in inflammatory bowel disease. Scand. J. Gastroenterol. 34, 496503.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Rieder, F. and Fiocchi, C. (2008): Intestinal fibrosis in inflammatory bowel disease: progress in basic and clinical science. Curr. Opin. Gastroenterol. 24, 462468.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Riegler, M., Castagliuolo, I., So, P. T., Lotz, M., Wang, C., Wlk, M., Sogukoglu, T., Cosentini, E., Bischof, G., Hamilton, G., Teleky, B., Wenzl, E., Matthews, J. B. and Pothoulakis, C. (1999): Effects of substance P on human colonic mucosa in vitro. Am. J. Physiol. 276, G1473G1483.

    • Search Google Scholar
    • Export Citation
  • Rychlik, A., Gonkowski, S., Nowicki, M. and Calka, J. (2017): Inflammatory bowel disease affects density of nitrergic nerve fibers in the mucosal layer of the canine gastrointestinal tract. Can. J. Vet. Res. 81, 129136.

    • Search Google Scholar
    • Export Citation
  • Rytel, L. and Calka, J. (2016): Acetylsalicylic acid-induced changes in the chemical coding of extrinsic sensory neurons supplying the prepyloric area of the porcine stomach. Neurosci. Lett. 617, 218224.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Sheehan, D., Moran, C. and Shanahan, F. (2015): The microbiota in inflammatory bowel disease. J. Gastroenterol. 50, 495507.

  • Shimizu, Y., Matsuyama, H., Shiina, T., Takewaki, T. and Furness, J. B. (2008): Tachykinins and their functions in the gastrointestinal tract. Cell. Mol. Life Sci. 65, 295311.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Sideri, A., Bakirtzi, K., Shih, D. Q., Koon, H. W., Fleshner, P., Arsenescu, R., Arsenescu, V., Turner, J. R., Karagiannides, I. and Pothoulakis, C. (2015): Substance P mediates pro-inflammatory cytokine release form mesenteric adipocytes in inflammatory bowel disease patients. Cell. Mol. Gastroenterol. Hepatol. 1, 420432.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Simpson, K. W. and Jergens, A. E. (2011): Pitfalls and progress in the diagnosis and management of canine inflammatory bowel disease. Vet. Clin. North Am. Small Anim. Pract. 41, 381398.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Suchodolski, J. S., Xenoulis, P. G., Paddock, C. G., Steiner, J. A. and Jergens, A. E. (2010): Molecular analysis of the bacterial microbiota in duodenal biopsies from dogs with idiopathic inflammatory bowel disease. Vet. Microbiol. 142, 394400.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Szymanska, K., Makowska, K. and Gonkowski S. (2018): The influence of high and low doses of bisphenol A (BPA) on the enteric nervous system of the porcine ileum. Int. J. Mol. Sci. 19, pii: E917.

    • Search Google Scholar
    • Export Citation
  • Taylor, C. T. and Keely, S. J. (2007): The autonomic nervous system and inflammatory bowel disease. Auton. Neurosci. 133, 104114.

  • Vasina, V., Barbara, G., Talamonti, L., Stanghellini, V., Corinaldesi, R., Tonini, M., De Ponti, F. and De Giorgio, R. (2006): Enteric neuroplasticity evoked by inflammation. Auton. Neurosci. 126–127, 264272.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Watson, J. W., Gonsalves, S. F., Fossa, A. A., McClean, S., Seeger, T., Obach, S. and Andrews, P. L. (1995): The anti-emetic effects of CP-99,994 in the ferret and the dog: role of the NK1 receptor. Br. J. Pharmacol. 115, 8494.

    • Crossref
    • Search Google Scholar
    • Export Citation

Monthly Content Usage

Abstract Views Full Text Views PDF Downloads
May 2020 0 0 0
Jun 2020 0 0 0
Jul 2020 0 0 0
Aug 2020 0 0 0
Sep 2020 0 0 0
Oct 2020 86 6 2
Nov 2020 0 0 0