Skip to main content

Lack of an Effect of Gastric Capsaicin on the Rectal Component of the Gastrocolonic Response

Digestive Diseases and Sciences volume 62, pages 3542–3549 (2017)Cite this article

Abstract

Luminal capsaicin induces local and distant reflexes in the upper gastrointestinal tract and stimulates lower gastrointestinal symptoms in susceptible persons. We aimed to evaluate the effect of gastric capsaicin on rectal motor function and sensation.

Methods

Eighteen healthy volunteers participated twice, at least 1 week apart, in this double-blind, placebo-controlled crossover study. Participants swallowed a gastric tube for capsaicin or saline infusion. A barostat tube was placed in the rectum to measure rectal tone before and during gastric capsaicin (40 µg/ml, 2.5 ml/min) or placebo infusion and to conduct distension experiments before and after gastric infusions. Gastric infusions were terminated after 60 min or when epigastric discomfort occurred. Differences in rectal tone, compliance, and sensitivity between gastric placebo and gastric capsaicin were determined.

Results

On both study days, basal rectal volumes, compliance, and sensitivity parameters were comparable (NS) before gastric infusions. Gastric capsaicin infusion induced epigastric discomfort that necessitated termination of infusion after 29.6 ± 12.3 min (saline: 54.7 ± 8.9 min; p < 0.01). Rectal tone, aggregate perception scores, and rectal compliance did not differ between placebo and capsaicin trials (p > 0.05). Rectal tone increased significantly only when capsaicin induced epigastric discomfort (p < 0.05). The reproducibility of the barostat trial was acceptable with significant correlations of volumes, pressures (< 0.05; r 2 from 0.41 to 0.55), rectal compliance (p < 0.01; r 2 = 0.44), and aggregate perception scores (p values all < 0.05; r 2 from 0.44 to 0.0.65) between the two barostat trials.

Conclusion

Gastric perfusion with capsaicin does not directly influence rectal physiology through a reflex arc.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3

References

  1. Snape WJ Jr, Matarazzo SA, Cohen S. Effect of eating and gastrointestinal hormones on human colonic myoelectrical and motor activity. Gastroenterology. 1978;75:373–378.

    CAS  PubMed  Google Scholar 

  2. Steadman CJ, Phillips SF, Camilleri M, Haddad A, Hanson R. Variation of muscle tone in the human colon. Gut. 1992;33:541–546.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  3. Musial F, Crowell MD, Kalveram KT, et al. Nutrient ingestion increases rectal sensitivity in humans. Physiol Behav. 1994;55:953–956.

    CAS  Article  PubMed  Google Scholar 

  4. Simrén M, Abrahamsson H, Björnsson ES. An exaggerated sensory component of the gastrocolonic response in patients with irritable bowel syndrome. Gut.. 2001;48:20–27.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Snape WJ Jr, Wright SH, Battle WM, Cohen S. The gastrocolic response: Evidence for a neural mechanism. Gastroenterology. 1979;77:1235–1240.

    PubMed  Google Scholar 

  6. Christensen J. The response of the colon to eating. Am J Clin Nutr. 1985;42:1025–1032.

    CAS  PubMed  Google Scholar 

  7. Sarna SK. Physiology and pathophysiology of colonic motor activity. Dig Dis Sci. 1991;36:827–862.

    CAS  Article  PubMed  Google Scholar 

  8. Di Stefano M, Miceli E, Missanelli A, et al. Meal-induced rectosigmoid tone modification: A low caloric meal accurately separates functional and organic gastrointestinal disease patients. Gut. 2006;55:1409–1414.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Cannon WB. The movements of the intestines studied by means of the Röntgen rays. Am J Physiol. 1902;6:251–277.

    Google Scholar 

  10. Misiewicz JJ, Connell AM, Pontes FA. Comparison of the effect of meals and prostigmine on the proximal and distal colon in patients with and without diarrhoea. Gut. 1966;7:468–473.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. Renny A, Snape WJ Jr, Sun EA, London R, Cohen S. Role of cholecystokinin in the gastrocolonic response to a fat meal. Gastroenterology. 1983;85:17–21.

    CAS  PubMed  Google Scholar 

  12. Delvaux M, Staumont G, Fioramonti J, Bueno L, Frexinos J. Alterations of colonic motility after oral administration of prostaglandin E1 analogue misoprostol in man. J Gastrointest Motil. 1992;4:33–38.

    Article  Google Scholar 

  13. Sun EA, Snape WJ Jr, Cohen J, Renny A. The role of opiate receptors and cholinergic neurons in the gastrocolonic response. Gastroenterology. 1982;82:689–693.

    CAS  PubMed  Google Scholar 

  14. Gershon MD, Tack J. The serotonin signaling system: From basic understanding to drug development for functional GI disorders. Gastroenterology. 2007;132:397–414.

    CAS  Article  PubMed  Google Scholar 

  15. Von der Ohe MR, Hanson RB, Camilleri M. Serotonergic mediation of postprandial colonic tonic and phasic responses in humans. Gut. 1994;35:536–541.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Arsiè E, Coletta M, Cesana BM, Basilisco G. Symptom-association probability between meal ingestion and abdominal pain in patients with irritable bowel syndrome. Does somatization play a role? Neurogastroenterol Motil. 2015;27:416–422.

    Article  PubMed  Google Scholar 

  17. Ragnarsson G, Bodemar G. Pain is temporally related to eating but not to defaecation in the irritable bowel syndrome (IBS). Patients’ description of diarrhea, constipation and symptom variation during a prospective 6-week study. Eur J Gastroenterol Hepatol. 1998;10:415–421.

    CAS  Article  PubMed  Google Scholar 

  18. Posserud I, Strid H, Stöorsrud S, et al. Symptom pattern following a meal challenge test in patients with irritable bowel syndrome and healthy controls. United Eur Gastroenterol J. 2013;1:358–367.

    Article  Google Scholar 

  19. Connell AM, Jones FA, Rowlands EN. Motility of the pelvic colon. IV. Abdominal pain associated with colonic hypermotility after meals. Gut. 1965;6:105–112.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. Simren M, Agerforz P, Bjornsson ES, Abrahamsson H. Nutrient-dependent enhancement of rectal sensitivity in irritable bowel syndrome (IBS). Neurogastroenterol Motil. 2007;19:20–29.

    CAS  Article  PubMed  Google Scholar 

  21. Ludidi S, Conchillo JM, Keszthelyi D, et al. Does meal ingestion enhance sensitivity of visceroperception assessment in irritable bowel syndrome? Neurogastroenterol Motil. 2012;24:47–53.

    CAS  Article  PubMed  Google Scholar 

  22. Tornblom H, Van Oudenhove L, Tack J, Simren M. Interaction between preprandial and postprandial rectal sensory and motor abnormalities in IBS. Gut. 2014;63:1441–1449.

    Article  PubMed  Google Scholar 

  23. Lembo T, Wright RA, Bagby B, et al. Alosetron controls bowel urgency and provides global symptom improvement in women with diarrhea-predominant irritable bowel syndrome. Am J Gastroenterol. 2001;96:2662–2670.

    CAS  Article  PubMed  Google Scholar 

  24. Fayyaz M, Lackner JM. Serotonin receptor modulators in the treatment of irritable bowel syndrome. Ther Clin Risk Manag. 2008;4:41–48.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. Simren M, Mansson A, Langkilde AM, et al. Food-related gastrointestinal symptoms in the irritable bowel syndrome. Digestion. 2001;63:108–115.

    CAS  Article  PubMed  Google Scholar 

  26. Gonlachanvit S, Mahayosnond A, Kullavanijaya P. Effects of chili on postprandial gastrointestinal symptoms in diarrhoea predominant irritable bowel syndrome: evidence for capsaicin-sensitive visceral nociception hypersensitivity. Neurogastroenterol Motil. 2009;21:23–32.

    CAS  Article  PubMed  Google Scholar 

  27. Gonlachanvit S, Fongkam P, Wittayalertpanya S, Kullavanijaya P. Red chili induces rectal hypersensitivity in healthy humans: possible role of 5HT-3 receptors on capsaicin-sensitive visceral nociceptive pathways. Aliment Pharmacol Ther. 2007;26:617–625.

    CAS  Article  PubMed  Google Scholar 

  28. Hammer J, Führer M. Clinical characteristics of functional dyspepsia depending on chemosensitivity to capsaicin. Neurogastroenterol Motil. 2017;29:1–12.

    CAS  Article  PubMed  Google Scholar 

  29. Aniwan S, Gonlachanvit S. Effects of Chili treatment on gastrointestinal and rectal sensation in diarrhea-predominant irritable bowel syndrome: A randomized, double-blinded, crossover study. J Neurogastroenterol Motil. 2014;20:400–406.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Holzer P. Capsaicin: Cellular targets, mechanisms of action, and selectivity for thin sensory neurons. Pharmacol Rev. 1991;43:143–201.

    CAS  PubMed  Google Scholar 

  31. Caterina MJ, Schumacher MA, Tominaga M, et al. The capsaicin receptor: A heat-activated ion channel in the pain pathway. Nature. 1997;389:816–824.

    CAS  Article  PubMed  Google Scholar 

  32. Ward SM, Bayguinov J, Won KJ, Grundy D, Berthoud HR. Distribution of the vanilloid receptor (VR1) in the gastrointestinal tract. J Comp Neurol. 2003;465:121–135.

    Article  PubMed  Google Scholar 

  33. Holzer P. Transient receptor potential (TRP) channels as drug targets for diseases of the digestive system. Pharmacol Ther. 2011;131:142–170.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. Hammer J, Phillips SF, Talley NJ, Camilleri M. Effect of a 5HT3 antagonist (odansetron) on rectal sensitivity and compliance in health and the irritable bowel syndrome. Aliment Pharmacol Ther. 1993;7:548–551.

    Google Scholar 

  35. Gracely RH. Studies of pain in normal men. In: Wall PD, Melazack R, eds. Textbook of pain. 3rd ed. Edingburgh: Churchill Livingstone; 1994:315–336.

    Google Scholar 

  36. Rohrböck RBK, Hammer J, Vogelsang H, Talley NJ, Hammer HF. Acupuncture has a placebo effect on rectal perception but not on distensibility and spatial summation: A study in health and IBS. Am J Gastroenterol. 2004;99:1990–1997.

    Article  PubMed  Google Scholar 

  37. Führer M, Hammer J. Duodenal chemosensitivity and mechanosensitivity in humans during acid and ethanol perfusion. Eur J Gastroenterol Hepatol. 2008;20:537–544.

    Article  PubMed  Google Scholar 

  38. Hölzer HH, Raybould HE. Vagal and splanchnic sensory pathways mediate inhibition of gastric motility induced by duodenal distension. Am J Physiol. 1992;262:G603–G608.

    PubMed  Google Scholar 

  39. Holzer P. Neural emergency system in the stomach. Gastroenterology. 1998;114:823–839.

    CAS  Article  PubMed  Google Scholar 

  40. Björnsson E, Chey WD, Ladabaum U, et al. Mediation of both the mechano- and chemoreceptor components of the gastrocolonic response but not the colonic peristaltic reflex by serotonergic 5-HT3 pathways in healthy humans. Am J Physiol Gastrointest Liver Physiol. 1998;275:G498–G505.

    Google Scholar 

  41. Wald A. Colonic transit and anorectal manometry in chronic idiopathic constipation. Arch Intern Med. 1986;146:1713–1716.

    CAS  Article  PubMed  Google Scholar 

  42. Hammer J, Führer M, Pipal L, Matiasek J. Chemical hypersensitivity in patients with functional dyspepsia. Neurogastroenterol Motil. 2008;20:125–133.

    CAS  PubMed  Google Scholar 

  43. Hammer J, Führer M. Intestinal chemo- and mechanosensitivity: Selective modification of small intestinal sensitivity by lipids. Aliment Pharmacol Ther. 2007;26:117–124.

    CAS  Article  PubMed  Google Scholar 

  44. Hammer J, Vogelsang H. Characterisation of sensations induced by capsaicin in the upper gastrointestinal tract. Neurogastroenterol Motil. 2007;19:279–287.

    CAS  Article  PubMed  Google Scholar 

  45. Carlstedt A, Nordgren S, Fasth S, Appelgren L, Hultén L. Sympathetic nervous influence on the internal anal sphincter and rectum in man. Int J Colorectal Dis. 1988;3:90–95.

    CAS  Article  PubMed  Google Scholar 

  46. Bharucha AE, Camilleri M, Zinsmeister AR, Hanson RB. Adrenergic modulation of human colonic motor and sensory function. Am J Physiol. 1997;273:G997–G1006.

    CAS  PubMed  Google Scholar 

  47. Cervero F, Laird JM. Visceral pain. Lancet. 1999;353:2145–2148.

    CAS  Article  PubMed  Google Scholar 

  48. Blackshaw LA. Visceral pain readouts in experimental medicine. Neurogastroenterol Motil. 2012;24:891–894.

    CAS  Article  PubMed  Google Scholar 

  49. Sengupta JN. Visceral pain: The neurophysiological mechanism. In: Canning BJ, Spina D, eds. Handbook of Experimental Pharmacology. Berlin: Springer-Verlag; 2009:31–74

    Google Scholar 

  50. Stein RD, Genovesi S, Demarest KT, Weaver LC. Capsaicin treatment attenuates the reflex excitation of sympathetic activity caused by chemical stimulation of intestinal afferent nerves. Brain Res. 1986;397:145–151.

    CAS  Article  PubMed  Google Scholar 

  51. Whitehead WE, Delvaux M, The Working Team of Glaxo-Wellcome Research, UK. Standardization of barostat procedures for testing smooth muscle tone and sensory thresholds in the gastrointestinal tract. Dig Dis Sci. 1997;42:223–241.

    CAS  Article  PubMed  Google Scholar 

  52. Lagier E, Delvaux M, Vellas B, et al. Influence of age on rectal tone and sensitivity to distension in healthy subjects. Neurogastroenterol Motil. 1999;11:101–107.

    CAS  Article  PubMed  Google Scholar 

  53. Sun WM, Read NW. Anorectal function in normal human subjects: Effect of gender. Int J Colorectal Dis. 1989;4:188–196.

    CAS  Article  PubMed  Google Scholar 

  54. Plourde V, Lembo T, Shui Z, et al. Effects of the somatostatin analogue octreotide on rectal afferent nerves in humans. Am J Physiol. 1993;265:G742–G751.

    CAS  PubMed  Google Scholar 

  55. Cremonini F, Houghton LA, Camilleri M, et al. Barostat testing of rectal sensation and compliance in humans: comparison of results across two centres and overall reproducibility. Neurogastroenterol Motil. 2005;17:810–820.

    CAS  Article  PubMed  Google Scholar 

  56. Bouin M, Plourde V, Boivin M, et al. Rectal distention testing in patients with irritable bowel syndrome: Sensitivity, specificity, and predictive values of pain sensory thresholds. Gastroenterology. 2002;122:1771–1777.

    Article  PubMed  Google Scholar 

  57. Hammer HF, Phillips SF, Camilleri M, Hanson RB. Rectal tone, distensibility, and perception: Reproducibility and response to different distensions. Am J Physiol. 1998;274:G584–G590.

    CAS  PubMed  Google Scholar 

  58. Bharucha AE, Seide B, Fox JC, Zinsmeister AR. Day-to-day reproducibility of anorectal sensorimotor assessments in healthy subjects. Neurogastroenterol Motil. 2004;16:241–250.

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgments

Supported by research Grant P 18101-B09 from the Austrian Science Fund (FWF, Fonds zur Förderung der wissenschaftlichen Forschung) to Dr. J. Hammer was gratefully acknowledged.

Author’s contribution

MF contributed with acquisition of the data; analysis and interpretation of the data; statistical analysis; administrative, technical, or material support, revision of the manuscript. JH contributed with study concept and design; funding acquisition; study supervision; analysis and interpretation of the data; drafting of the manuscript and critical revision of the manuscript for important intellectual content.

Author information

Affiliations

  1. Abteilung für Gastroenterologie und Hepatologie, Universitätsklinik für Innere Medizin 3, Medical University of Vienna, Währinger Gürtel 18-20, 1090, Vienna, Austria

    Martina Führer & Johann Hammer

  2. Faculty of Health and Behavioural Sciences, The University of Queensland, Herston, Brisbane, QLD, 4029, Australia

    Johann Hammer

Authors
  1. Martina Führer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Johann Hammer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Johann Hammer.

Ethics declarations

Conflict of interest

No conflict of interest exists.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Führer, M., Hammer, J. Lack of an Effect of Gastric Capsaicin on the Rectal Component of the Gastrocolonic Response. Dig Dis Sci 62, 3542–3549 (2017). https://doi.org/10.1007/s10620-017-4822-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10620-017-4822-5

Keywords

  • Gastrocolonic reflex
  • Rectal barostat
  • Capsaicin
  • Reproducibility