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Published in: International Journal of Colorectal Disease 12/2012

01-12-2012 | Original Article

A clinicopathological study of serotonin of sigmoid colon mucosa in association with chronic symptoms in uncomplicated diverticulosis

Authors: S. Jeyarajah, N. Akbar, J. Moorhead, A. Haji, S. Banerjee, S. Papagrigoriadis

Published in: International Journal of Colorectal Disease | Issue 12/2012

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Abstract

Introduction

Neurotransmitter imbalance is hypothesised as a pathogenetic mechanism in several bowel conditions. We previously reported increased 5-HT in the sigmoid mucosa of colon resected for complicated diverticular disease (DD). We aimed to identify if abnormal 5-HT expression is associated with symptoms of uncomplicated DD.

Methods

This was a prospective, comparative study and follow-up survey of symptoms. We examined the differences in 5-HT between DD patients and controls, as well as the presence of bowel symptoms at time of endoscopy and also 2 years later. Sigmoid biopsies were collected at colonoscopy. Immunohistochemical staining for 5-HT cells was performed.

Results

Eighty-seven patients were recruited, 37 (42.5 %) DD and 50 (57.5 %) controls. No patients underwent surgery. There was no significant difference in total mean number of 5-HT-positive cells in DD compared to controls or between patients and controls with abdominal symptoms. Forty-one patients (47.1 %) responded to questionnaires at median 57.8 months from biopsy. Eighteen (43.9 %) were DD and 23(56.1 %) controls. 5-HT counts showed no significant association to symptom persistence.

Discussion

Although 5-HT expression has previously been found to be increased in complicated DD in whole bowel-resected specimens, the same is not confirmed on colonic mucosal biopsies. This raises the suggestion that 5-HT may be involved in the development of acute complications but may not be involved in the pathogenesis of chronic symptoms.
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Literature
1.
go back to reference Shafik A, Ahmed I, Shafik AA, El Sibai O (2004) Diverticular disease: electrophysiologic study and a new concept of pathogenesis. World J Surg 28(4):411–5PubMedCrossRef Shafik A, Ahmed I, Shafik AA, El Sibai O (2004) Diverticular disease: electrophysiologic study and a new concept of pathogenesis. World J Surg 28(4):411–5PubMedCrossRef
2.
go back to reference Quigley EM, Phillips SF, Dent J, Taylor BM (1983) Myoelectric activity and intraluminal pressure of the canine ileocolonic sphincter. Gastroenterology 85(5):1054–1062PubMed Quigley EM, Phillips SF, Dent J, Taylor BM (1983) Myoelectric activity and intraluminal pressure of the canine ileocolonic sphincter. Gastroenterology 85(5):1054–1062PubMed
3.
go back to reference Durdle NG, Kingma YJ, Bowes KL, Chambers MM (1983) Origin of slow waves in the canine colon. Gastroenterology 84(2):375–382PubMed Durdle NG, Kingma YJ, Bowes KL, Chambers MM (1983) Origin of slow waves in the canine colon. Gastroenterology 84(2):375–382PubMed
4.
go back to reference Bueno L, Fioramonti J, Ruckebusch Y, Frexinos J, Coulom P (1980) Evaluation of colonic myoelectrical activity in health and functional disorders. Gut 21(6):480–485PubMedCrossRef Bueno L, Fioramonti J, Ruckebusch Y, Frexinos J, Coulom P (1980) Evaluation of colonic myoelectrical activity in health and functional disorders. Gut 21(6):480–485PubMedCrossRef
5.
go back to reference Shafik A (1996) Sigmoido-rectal junction reflex: role in the defecation mechanism. Clin Anat 9(6):391–394PubMedCrossRef Shafik A (1996) Sigmoido-rectal junction reflex: role in the defecation mechanism. Clin Anat 9(6):391–394PubMedCrossRef
6.
go back to reference Shafik A (1997) The hypertonic rectosigmoid junction: description of a new clinicopathologic entity causing constipation. Surg Laparosc Endosc 7(2):116–120PubMedCrossRef Shafik A (1997) The hypertonic rectosigmoid junction: description of a new clinicopathologic entity causing constipation. Surg Laparosc Endosc 7(2):116–120PubMedCrossRef
7.
go back to reference Waldron DJ, Gill RC, Bowes KL (1989) Pressure response of human colon to intraluminal distension. Dig Dis Sci 34(8):1163–1167PubMedCrossRef Waldron DJ, Gill RC, Bowes KL (1989) Pressure response of human colon to intraluminal distension. Dig Dis Sci 34(8):1163–1167PubMedCrossRef
8.
go back to reference Ford MJ, Camilleri M, Wiste JA, Hanson RB (1995) Differences in colonic tone and phasic response to a meal in the transverse and sigmoid human colon. Gut 37(2):264–269PubMedCrossRef Ford MJ, Camilleri M, Wiste JA, Hanson RB (1995) Differences in colonic tone and phasic response to a meal in the transverse and sigmoid human colon. Gut 37(2):264–269PubMedCrossRef
9.
go back to reference Painter NS, Truelove SC. The intraluminal pressure patterns in diverticulosis of the colon. I. Resting patterns of pressure. Ii. the effect of morphine. Gut 1964 Jun;5:201–13. Painter NS, Truelove SC. The intraluminal pressure patterns in diverticulosis of the colon. I. Resting patterns of pressure. Ii. the effect of morphine. Gut 1964 Jun;5:201–13.
10.
go back to reference Arfwidsson S, Knock NG, Lehmann L, Winberg T (1964) Pathogenesis of multiple diverticula of the sigmoid colon in diverticular disease. Acta Chir Scand Suppl 63(SUPPL 342):1–68PubMed Arfwidsson S, Knock NG, Lehmann L, Winberg T (1964) Pathogenesis of multiple diverticula of the sigmoid colon in diverticular disease. Acta Chir Scand Suppl 63(SUPPL 342):1–68PubMed
11.
go back to reference Parks TG (1970) Motor responses in unresected and resected diverticular disease of the colon. Proc R Soc Med 63(Suppl):3–6PubMed Parks TG (1970) Motor responses in unresected and resected diverticular disease of the colon. Proc R Soc Med 63(Suppl):3–6PubMed
12.
go back to reference Trotman IF, Misiewicz JJ (1988) Sigmoid motility in diverticular disease and the irritable bowel syndrome. Gut 29(2):218–222PubMedCrossRef Trotman IF, Misiewicz JJ (1988) Sigmoid motility in diverticular disease and the irritable bowel syndrome. Gut 29(2):218–222PubMedCrossRef
13.
go back to reference Cortesini C, Pantalone D (1991) Usefulness of colonic motility study in identifying patients at risk for complicated diverticular disease. Dis Colon Rectum 34(4):339–342PubMedCrossRef Cortesini C, Pantalone D (1991) Usefulness of colonic motility study in identifying patients at risk for complicated diverticular disease. Dis Colon Rectum 34(4):339–342PubMedCrossRef
14.
go back to reference Sugihara K, Muto T, Morioka Y (1983) Motility study in right sided diverticular disease of the colon. Gut 24(12):1130–1134PubMedCrossRef Sugihara K, Muto T, Morioka Y (1983) Motility study in right sided diverticular disease of the colon. Gut 24(12):1130–1134PubMedCrossRef
15.
go back to reference Bassotti G, Battaglia E, Spinozzi F, Pelli MA, Tonini M (2001) Twenty-four hour recordings of colonic motility in patients with diverticular disease: evidence for abnormal motility and propulsive activity. Dis Colon Rectum 44(12):1814–1820PubMedCrossRef Bassotti G, Battaglia E, Spinozzi F, Pelli MA, Tonini M (2001) Twenty-four hour recordings of colonic motility in patients with diverticular disease: evidence for abnormal motility and propulsive activity. Dis Colon Rectum 44(12):1814–1820PubMedCrossRef
16.
go back to reference Bassotti G, Battaglia E, De Roberto G, Morelli A, Tonini M, Villanacci V (2005) Alterations in colonic motility and relationship to pain in colonic diverticulosis. Clin Gastroenterol Hepatol 3(3):248–253PubMedCrossRef Bassotti G, Battaglia E, De Roberto G, Morelli A, Tonini M, Villanacci V (2005) Alterations in colonic motility and relationship to pain in colonic diverticulosis. Clin Gastroenterol Hepatol 3(3):248–253PubMedCrossRef
17.
go back to reference Huizinga JD (1986) Electrophysiology of human colon motility in health and disease. Clin Gastroenterol 15(4):879–901PubMed Huizinga JD (1986) Electrophysiology of human colon motility in health and disease. Clin Gastroenterol 15(4):879–901PubMed
18.
go back to reference Huizinga JD, Waterfall WE, Stern HS (1999) Abnormal response to cholinergic stimulation in the circular muscle layer of the human colon in diverticular disease. Scand J Gastroenterol 34(7):683–688PubMedCrossRef Huizinga JD, Waterfall WE, Stern HS (1999) Abnormal response to cholinergic stimulation in the circular muscle layer of the human colon in diverticular disease. Scand J Gastroenterol 34(7):683–688PubMedCrossRef
19.
go back to reference Sasaki D, Kido A, Yoshida Y (1986) An endoscopic method to study the relationship between bowel habit and motility of the ascending and sigmoid colon. Gastrointest Endosc 32(3):185–189PubMedCrossRef Sasaki D, Kido A, Yoshida Y (1986) An endoscopic method to study the relationship between bowel habit and motility of the ascending and sigmoid colon. Gastrointest Endosc 32(3):185–189PubMedCrossRef
20.
go back to reference Sasaki D, Munakata A, Saitoh Y, Yoshida Y (1981) Anti-spasmodic effect of prifinium bromide on the proximal and distal colon in patients with diverticular disease. Gastroenterol Jpn 16(4):344–349PubMed Sasaki D, Munakata A, Saitoh Y, Yoshida Y (1981) Anti-spasmodic effect of prifinium bromide on the proximal and distal colon in patients with diverticular disease. Gastroenterol Jpn 16(4):344–349PubMed
21.
go back to reference Whiteway J, Morson BC (1985) Pathology of the ageing—diverticular disease. Clin Gastroenterol 14(4):829–846PubMed Whiteway J, Morson BC (1985) Pathology of the ageing—diverticular disease. Clin Gastroenterol 14(4):829–846PubMed
22.
go back to reference Golder M, Burleigh DE, Belai A, Ghali L, Ashby D, Lunniss PJ et al (2003) Smooth muscle cholinergic denervation hypersensitivity in diverticular disease. Lancet 361(9373):1945–1951PubMedCrossRef Golder M, Burleigh DE, Belai A, Ghali L, Ashby D, Lunniss PJ et al (2003) Smooth muscle cholinergic denervation hypersensitivity in diverticular disease. Lancet 361(9373):1945–1951PubMedCrossRef
23.
go back to reference Tam FS (1992) HK. The role of nitric oxide in mediating nonadrenergic non-cholinergic relaxation in longitudinal muscle of human taenia coli. Life Sci 51:1277–1284PubMedCrossRef Tam FS (1992) HK. The role of nitric oxide in mediating nonadrenergic non-cholinergic relaxation in longitudinal muscle of human taenia coli. Life Sci 51:1277–1284PubMedCrossRef
24.
go back to reference Burleigh DE (1992) Ng-nitro-L-arginine reduces nonadrenergic, noncholinergic relaxations of human gut. Gastroenterology 102(2):679–683PubMed Burleigh DE (1992) Ng-nitro-L-arginine reduces nonadrenergic, noncholinergic relaxations of human gut. Gastroenterology 102(2):679–683PubMed
25.
go back to reference Golder M, Burleigh DE, Ghali L, Feakins RM, Lunniss PJ, Williams NS et al (2007) Longitudinal muscle shows abnormal relaxation responses to nitric oxide and contains altered levels of NOS1 and elastin in uncomplicated diverticular disease. Colorectal Dis 9(3):218–228PubMedCrossRef Golder M, Burleigh DE, Ghali L, Feakins RM, Lunniss PJ, Williams NS et al (2007) Longitudinal muscle shows abnormal relaxation responses to nitric oxide and contains altered levels of NOS1 and elastin in uncomplicated diverticular disease. Colorectal Dis 9(3):218–228PubMedCrossRef
26.
go back to reference Gershon MD, Dreyfus CF, Pickel VM, Joh TH, Reis DJ (1977) Serotonergic neurons in the peripheral nervous system: identification in gut by immunohistochemical localization of tryptophan hydroxylase. Proc Natl Acad Sci USA 74(7):3086–3089PubMedCrossRef Gershon MD, Dreyfus CF, Pickel VM, Joh TH, Reis DJ (1977) Serotonergic neurons in the peripheral nervous system: identification in gut by immunohistochemical localization of tryptophan hydroxylase. Proc Natl Acad Sci USA 74(7):3086–3089PubMedCrossRef
27.
go back to reference Bulbring E, Crema A (1959) The release of 5-hydroxytryptamine in relation to pressure exerted on the intestinal mucosa. J Physiol 146(1):18–28PubMed Bulbring E, Crema A (1959) The release of 5-hydroxytryptamine in relation to pressure exerted on the intestinal mucosa. J Physiol 146(1):18–28PubMed
28.
go back to reference Bulbring E, Crema A (1958) Observations concerning the action of 5-hydroxytryptamine on the peristaltic reflex. Br J Pharmacol Chemother 13(4):444–457PubMed Bulbring E, Crema A (1958) Observations concerning the action of 5-hydroxytryptamine on the peristaltic reflex. Br J Pharmacol Chemother 13(4):444–457PubMed
29.
go back to reference Bulbring E, Lin RC (1958) The effect of intraluminal application of 5-hydroxytryptamine and 5-hydroxytryptophan on peristalsis; the local production of 5-HT and its release in relation to intraluminal pressure and propulsive activity. J Physiol 140(3):381–407PubMed Bulbring E, Lin RC (1958) The effect of intraluminal application of 5-hydroxytryptamine and 5-hydroxytryptophan on peristalsis; the local production of 5-HT and its release in relation to intraluminal pressure and propulsive activity. J Physiol 140(3):381–407PubMed
30.
go back to reference Sidhu M, Cooke HJ (1995) Role for 5-HT and ACh in submucosal reflexes mediating colonic secretion. Am J Physiol 269(3 Pt 1):G346–G351PubMed Sidhu M, Cooke HJ (1995) Role for 5-HT and ACh in submucosal reflexes mediating colonic secretion. Am J Physiol 269(3 Pt 1):G346–G351PubMed
31.
go back to reference Kirchgessner AL, Tamir H, Gershon MD (1992) Identification and stimulation by serotonin of intrinsic sensory neurons of the submucosal plexus of the guinea pig gut: activity-induced expression of Fos immunoreactivity. J Neurosci 12(1):235–248PubMed Kirchgessner AL, Tamir H, Gershon MD (1992) Identification and stimulation by serotonin of intrinsic sensory neurons of the submucosal plexus of the guinea pig gut: activity-induced expression of Fos immunoreactivity. J Neurosci 12(1):235–248PubMed
32.
go back to reference Kirchgessner AL, Liu MT, Raymond JR, Gershon MD (1996) Identification of cells that express 5-hydroxytryptamine1A receptors in the nervous systems of the bowel and pancreas. J Comp Neurol 364(3):439–455PubMedCrossRef Kirchgessner AL, Liu MT, Raymond JR, Gershon MD (1996) Identification of cells that express 5-hydroxytryptamine1A receptors in the nervous systems of the bowel and pancreas. J Comp Neurol 364(3):439–455PubMedCrossRef
33.
go back to reference Blackshaw LA, Grundy D (1993) Effects of 5-hydroxytryptamine on discharge of vagal mucosal afferent fibres from the upper gastrointestinal tract of the ferret. J Auton Nerv Syst 45(1):41–50PubMedCrossRef Blackshaw LA, Grundy D (1993) Effects of 5-hydroxytryptamine on discharge of vagal mucosal afferent fibres from the upper gastrointestinal tract of the ferret. J Auton Nerv Syst 45(1):41–50PubMedCrossRef
34.
go back to reference Hillsley K, Kirkup AJ, Grundy D (1998) Direct and indirect actions of 5-hydroxytryptamine on the discharge of mesenteric afferent fibres innervating the rat jejunum. J Physiol 506(Pt 2):551–561PubMedCrossRef Hillsley K, Kirkup AJ, Grundy D (1998) Direct and indirect actions of 5-hydroxytryptamine on the discharge of mesenteric afferent fibres innervating the rat jejunum. J Physiol 506(Pt 2):551–561PubMedCrossRef
35.
go back to reference Chen JX, Pan H, Rothman TP, Wade PR, Gershon MD (1998) Guinea pig 5-HT transporter: cloning, expression, distribution, and function in intestinal sensory reception. Am J Physiol 275(3 Pt 1):G433–G448PubMed Chen JX, Pan H, Rothman TP, Wade PR, Gershon MD (1998) Guinea pig 5-HT transporter: cloning, expression, distribution, and function in intestinal sensory reception. Am J Physiol 275(3 Pt 1):G433–G448PubMed
36.
go back to reference Banerjee S, Akbar N, Moorhead J, Rennie JA, Leather AJ, Cooper D et al (2007) Increased presence of serotonin-producing cells in colons with diverticular disease may indicate involvement in the pathophysiology of the condition. Int J Colorectal Dis 22(6):643–649PubMedCrossRef Banerjee S, Akbar N, Moorhead J, Rennie JA, Leather AJ, Cooper D et al (2007) Increased presence of serotonin-producing cells in colons with diverticular disease may indicate involvement in the pathophysiology of the condition. Int J Colorectal Dis 22(6):643–649PubMedCrossRef
37.
go back to reference Loffeld RJ, Van Der Putten AB (2002) Diverticular disease of the colon and concomitant abnormalities in patients undergoing endoscopic evaluation of the large bowel. Colorectal Dis 4(3):189–192PubMedCrossRef Loffeld RJ, Van Der Putten AB (2002) Diverticular disease of the colon and concomitant abnormalities in patients undergoing endoscopic evaluation of the large bowel. Colorectal Dis 4(3):189–192PubMedCrossRef
38.
go back to reference Zhao RH, Baig MK, Thaler KJ, Mack J, Abramson S, Woodhouse S et al (2003) Reduced expression of serotonin receptor(s) in the left colon of patients with colonic inertia. Dis Colon Rectum 46(1):81–86PubMedCrossRef Zhao RH, Baig MK, Thaler KJ, Mack J, Abramson S, Woodhouse S et al (2003) Reduced expression of serotonin receptor(s) in the left colon of patients with colonic inertia. Dis Colon Rectum 46(1):81–86PubMedCrossRef
39.
go back to reference Zhao R, Baig MK, Wexner SD, Chen W, Singh JJ, Nogueras JJ et al (2000) Enterochromaffin and serotonin cells are abnormal for patients with colonic inertia. Dis Colon Rectum 43(6):858–863PubMedCrossRef Zhao R, Baig MK, Wexner SD, Chen W, Singh JJ, Nogueras JJ et al (2000) Enterochromaffin and serotonin cells are abnormal for patients with colonic inertia. Dis Colon Rectum 43(6):858–863PubMedCrossRef
40.
go back to reference Coates MD, Mahoney CR, Linden DR, Sampson JE, Chen J, Blaszyk H et al (2004) Molecular defects in mucosal serotonin content and decreased serotonin reuptake transporter in ulcerative colitis and irritable bowel syndrome. Gastroenterology 126(7):1657–1664PubMedCrossRef Coates MD, Mahoney CR, Linden DR, Sampson JE, Chen J, Blaszyk H et al (2004) Molecular defects in mucosal serotonin content and decreased serotonin reuptake transporter in ulcerative colitis and irritable bowel syndrome. Gastroenterology 126(7):1657–1664PubMedCrossRef
41.
go back to reference Miwa J, Echizen H, Matsueda K, Umeda N (2001) Patients with constipation-predominant irritable bowel syndrome (IBS) may have elevated serotonin concentrations in colonic mucosa as compared with diarrhea-predominant patients and subjects with normal bowel habits. Digestion 63(3):188–194PubMedCrossRef Miwa J, Echizen H, Matsueda K, Umeda N (2001) Patients with constipation-predominant irritable bowel syndrome (IBS) may have elevated serotonin concentrations in colonic mucosa as compared with diarrhea-predominant patients and subjects with normal bowel habits. Digestion 63(3):188–194PubMedCrossRef
42.
go back to reference Bearcroft CP, Perrett D, Farthing MJ (1998) Postprandial plasma 5-hydroxytryptamine in diarrhoea predominant irritable bowel syndrome: a pilot study. Gut 42(1):42–46PubMedCrossRef Bearcroft CP, Perrett D, Farthing MJ (1998) Postprandial plasma 5-hydroxytryptamine in diarrhoea predominant irritable bowel syndrome: a pilot study. Gut 42(1):42–46PubMedCrossRef
43.
go back to reference Tack J, Fried M, Houghton LA, Spicak J, Fisher G (2006) Systematic review: the efficacy of treatments for irritable bowel syndrome—a European perspective. Aliment Pharmacol Ther 24(2):183–205PubMedCrossRef Tack J, Fried M, Houghton LA, Spicak J, Fisher G (2006) Systematic review: the efficacy of treatments for irritable bowel syndrome—a European perspective. Aliment Pharmacol Ther 24(2):183–205PubMedCrossRef
44.
go back to reference Jung HK, Choung RS, 3rd Locke GR, Schleck CD, Zinsmeister AR, Talley NJ. Diarrhea-predominant irritable bowel syndrome is associated with diverticular disease: a population-based study. Am J Gastroenterol 105(3):652-61 Jung HK, Choung RS, 3rd Locke GR, Schleck CD, Zinsmeister AR, Talley NJ. Diarrhea-predominant irritable bowel syndrome is associated with diverticular disease: a population-based study. Am J Gastroenterol 105(3):652-61
45.
go back to reference Katschinski M, Lederer P, Ellermann A, Ganzleben R, Lux G, Arnold R (1990) Myoelectric and manometric patterns of human rectosigmoid colon in irritable bowel syndrome and diverticulosis. Scand J Gastroenterol 25(7):761–768PubMedCrossRef Katschinski M, Lederer P, Ellermann A, Ganzleben R, Lux G, Arnold R (1990) Myoelectric and manometric patterns of human rectosigmoid colon in irritable bowel syndrome and diverticulosis. Scand J Gastroenterol 25(7):761–768PubMedCrossRef
46.
go back to reference Costedio MM, Coates MD, Danielson AB, Buttolph TR, 3rd, Blaszyk HJ, Mawe GM et al (2008) Serotonin signalling in diverticular disease. J Gastrointest Surg. May 20 Costedio MM, Coates MD, Danielson AB, Buttolph TR, 3rd, Blaszyk HJ, Mawe GM et al (2008) Serotonin signalling in diverticular disease. J Gastrointest Surg. May 20
47.
go back to reference Gershon MD (1982) Serotonergic neurotransmission in the gut. Scand J Gastroenterol Suppl 71:26–41PubMed Gershon MD (1982) Serotonergic neurotransmission in the gut. Scand J Gastroenterol Suppl 71:26–41PubMed
Metadata
Title
A clinicopathological study of serotonin of sigmoid colon mucosa in association with chronic symptoms in uncomplicated diverticulosis
Authors
S. Jeyarajah
N. Akbar
J. Moorhead
A. Haji
S. Banerjee
S. Papagrigoriadis
Publication date
01-12-2012
Publisher
Springer-Verlag
Published in
International Journal of Colorectal Disease / Issue 12/2012
Print ISSN: 0179-1958
Electronic ISSN: 1432-1262
DOI
https://doi.org/10.1007/s00384-012-1515-6

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