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International Journal of Colorectal Disease

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01-02-2013 | Original Article

The role of colonic mast cells and myenteric plexitis in patients with diverticular disease

Authors: Gabrio Bassotti, Vincenzo Villanacci, Riccardo Nascimbeni, Elisabetta Antonelli, Moris Cadei, Stefania Manenti, Luisa Lorenzi, Amin Titi, Bruno Salerni

Published in: International Journal of Colorectal Disease | Issue 2/2013

Abstract

Background

Gut mast cells represent an important cell population involved in intestinal homeostasis and inflammatory processes. However, their possible role has not to date been investigated in colonic diverticular disease.

Aims

This study aims to evaluate colonic mast cells in patients undergoing surgery for diverticular disease.

Methods

Surgical resection samples from 27 patients undergoing surgery for diverticular disease (12 emergency procedures for severe disease and 15 elective procedures) were evaluated. The number of mast cells was assessed in the various layers by means of a specific antibody (tryptase) and compared with those evaluated in ten controls. In patients with mast cells degranulation, double immunohistochemistry, also assessing nerve fibres, was carried out. In addition, the presence of myenteric plexitis was sought.

Results

Compared with controls, the number of mast cells in diverticular patients was significantly increased, both as an overall figure and in the various layers of the large bowel. In patients in whom mast cells degranulation was present, these were always closed to nerve fibres. No differences were found between the two subgroups of patients with respect to the number and distribution of mast cells; however, all patients undergoing emergency surgery (but none of those undergoing elective procedures) had myenteric plexitis, represented by lymphocytic infiltration in 67 % and eosinophilic infiltration in 33 % of cases.

Conclusions

Patients with diverticular disease display an increase of mast cells in the large bowel. The presence of myenteric plexitis in those with complicated, severe disease, suggest that this could represent a histopathologic marker of more aggressive disease.

Mikkelsen HB (2010) Interstitial cells of Cajal, macrophages and mast cells in the gut musculature: morphology, distribution, spatial and possible functional interactions. J Cell Mol Med 14:818–832PubMedCrossRef

The FO, Bennink RJ, Ankum WM, Buist MR, Busch OR, Gouma DJ, van der Heide S, van den Wijngaard RM, de Jonge WJ, Boeckxstaens GE (2008) Intestinal handling-induced mast cell activation and inflammation in human postoperative ileus. Gut 57:33–40PubMedCrossRef

Kraneveld AD, Rijnierse A, Nijkamp FP, Garssen J (2008) Neuro-immune interactions in inflammatory bowel disease and irritable bowel syndrome: future therapeutic targets. Eur J Pharmacol 585:361–374PubMedCrossRef

Lakhan SE, Kirchgessner A (2010) Neuroinflammation in inflammatory bowel disease. J Neuroinflammation 7:37PubMedCrossRef

Guilarte M, Santos J, de Torres I, Alonso C, Vicario M, Ramos L, Martínez C, Casellas F, Saperas E, Malagelada JR (2007) Diarrhoea-predominant IBS patients show mast cell activation and hyperplasia in the jejunum. Gut 56:203–209PubMedCrossRef

Barbara G, Wang B, Stanghellini V, de Giorgio R, Cremon C, Di Nardo G, Trevisani M, Campi B, Geppetti P, Tonini M, Bunnett NW, Grundy D, Corinaldesi R (2007) Mast cell-dependent excitation of visceral-nociceptive sensory neurons in irritable bowel syndrome. Gastroenterology 132:26–37PubMedCrossRef

Bassotti G, Villanacci V, Nascimbeni R, Cadei M, Manenti S, Sabatino G, Maurer CA, Cathomas G, Salerni B (2011) Colonic mast cells in controls and slow transit constipation patients. Aliment Pharmacol Ther 34:92–99PubMedCrossRef

Bassotti G, Villanacci V, Nascimbeni R, Cadei M, Manenti S, Antonelli E, Fanini L, Salerni B (2012) Increase of colonic mast cells in obstructed defecation and their relationship with enteric glia. Dig Dis Sci 57:65–71PubMedCrossRef

Stocchi L (2010) Current indications and role of surgery in the management of sigmoid diverticulitis. World J Gastroenterol 16:804–817PubMed

10.

Hall J, Hammerich K, Roberts P (2010) New paradigms in the management of diverticular disease. Curr Probl Surg 47:680–735PubMedCrossRef

11.

Simpson J, Neal KR, Scholefield JH, Spiller RC (2003) Patterns of pain in diverticular disease and the influence of acute diverticulitis. Eur J Gastroenterol Hepatol 15:1005–1010PubMedCrossRef

12.

Simpson J, Scholefield JH, Spiller RC (2003) Origin of symptoms in diverticular disease. Br J Surg 90:899–908PubMedCrossRef

13.

Bassotti G, Battaglia E, Bellone G, Dughera L, Fisogni S, Zambelli C, Morelli A, Mioli P, Emanuelli G, Villanacci V (2005) Interstitial cells of Cajal, enteric nerves, and glial cells in colonic diverticular disease. J Clin Pathol 58:973–977PubMedCrossRef

14.

Becheanu G, Manuc M, Dumbravă M, Herlea V, Hortopan M, Costache M (2008) The evaluation of interstitial Cajal cells distribution in non-tumoral colon disorders. Rom J Morphol Embryol 9:351–355

15.

Wedel T, Büsing V, Heinrichs G, Nohroudi K, Bruch HP, Roblick UJ, Böttner M (2010) Diverticular disease is associated with an enteric neuropathy as revealed by morphometric analysis. Neurogastroenterol Motil 22:407–414PubMedCrossRef

16.

Simpson J, Sundler F, Humes DJ, Jenkins D, Scholefield JH, Spiller RC (2009) Post inflammatory damage to the enteric nervous system in diverticular disease and its relationship to symptoms. Neurogastroenterol Motil 21:847–e58PubMedCrossRef

17.

Kellow JE (2009) Myenteric plexitis in enteric dysmotility: what are the implications for clinical practice? Gut 58:1042–1043PubMedCrossRef

18.

Hinchey EJ, Schaal PG, Richards GK (1978) Treatment of perforated diverticular disease of the colon. Adv Surg 12:85–109PubMed

19.

Ambrosetti P, Grossholz M, Becker C, Terrier F, Morel P (1997) Computed tomography in acute left colonic diverticulitis. Br J Surg 84:532–534PubMedCrossRef

20.

Richards RJ, Hammitt JK (2002) Timing of prophylactic surgery in prevention of diverticulitis recurrence: a cost-effectiveness analysis. Dig Dis Sci 47:1903–1908PubMedCrossRef

21.

Salem L, Veenstra DL, Sullivan SD, Flum DR (2004) The timing of elective colectomy in diverticulitis: a decision analysis. J Am Coll Surg 199:904–912PubMedCrossRef

22.

Walls AF, Jones DB, Williams JH, Church MK, Holgate ST (1990) Immunohistochemical identification of mast cells in formaldehyde-fixed tissue using monoclonal antibodies specific for tryptase. J Pathol 162:119–126PubMedCrossRef

23.

Villanacci V, Bassotti G, Cathomas G, Maurer CA, Di Fabio F, Fisogni S, Cadei M, Mazzocchi A, Salerni B (2006) Is pseudomelanosis coli a marker of colonic neuropathy in severely constipated patients? Histopathology 49:132–137PubMedCrossRef

24.

Abonia JP, Blanchard C, Butz BB, Rainey HF, Collins MH, Stringer K, Putnam PE, Rothenberg ME (2010) Involvement of mast cells in eosinophilic esophagitis. J Allergy Clin Immunol 126:140–149PubMedCrossRef

25.

Stead RH, Dixon MF, Bramwell NH, Riddell RH, Bienenstock J (1989) Mast cells are closely apposed to nerves in the human gastrointestinal mucosa. Gastroenterology 97:575–585PubMed

26.

Stead RH, Franks AJ, Goldsmith CH, Bienenstock J, Dixon MF (1990) Mast cells, nerves and fibrosis in the appendix: a morphological assessment. J Pathol 161:209–219PubMedCrossRef

27.

Ferrante M, De Hertogh G, Hlavaty T, D’Haens G, Penninckx F, D’Hoore A, Vermeire S, Rutgeerts P, Geboes K, Van Assche G (2006) The value of myenteric plexitis to predict early postoperative Crohn’s disease recurrence. Gastroenterology 130:1595–1606PubMedCrossRef

28.

Villanacci V, Bassotti G, Nascimbeni R, Antonelli E, Cadei M, Fisogni S, Salerni B, Geboes K (2008) Enteric nervous system abnormalities in inflammatory bowel diseases. Neurogastroenterol Motil 20:1009–1016PubMedCrossRef

29.

Buhner S, Schemann M (2012) Mast cell–nerve axis with a focus on the human gut. Biochim Biophys Acta 1822:85–92PubMedCrossRef

30.

De Winter BY, van den Wijngaard RM, de Jonge WJ (2012) BBA review; mechanisms of disease: mast cells; instigators of gut inflammation and motility disturbances. Biochim Biophys Acta 1822:66–73PubMedCrossRef

31.

van Diest SA, Stanisor OI, Boeckxstaens GE, de Jonge WJ, van den Wijngaard RM (2012) Relevance of mast cell–nerve interactions in intestinal nociception. Biochim Biophys Acta 1822:74–84PubMedCrossRef

32.

Raithel M, Winterkamp S, Pacurar A, Ulrich P, Hochberger J, Hahn EG (2001) Release of mast cell tryptase from human colorectal mucosa in inflammatory bowel disease. Scand J Gastroenterol 36:174–179PubMedCrossRef

33.

Andoh A, Deguchi Y, Inatomi O, Yagi Y, Bamba S, Tsujikawa T, Fujiyama Y (2006) Immunohistochemical study of chymase-positive mast cells in inflammatory bowel disease. Oncol Rep 16:103–107PubMed

34.

van Hoboken EA, Thijssen AY, Verhaaren R, van der Veek PP, Prins FA, Verspaget HW, Masclee AA (2011) Symptoms in patients with ulcerative colitis in remission are associated with visceral hypersensitivity and mast cell activity. Scand J Gastroenterol 46:981–987PubMedCrossRef

35.

Piche T, Saint-Paul MC, Dainese R, Marine-Barjoan E, Iannelli A, Montoya ML, Peyron JF, Czerucka D, Cherikh F, Filippi J, Tran A, Hébuterne X (2008) Mast cells and cellularity of the colonic mucosa correlated with fatigue and depression in irritable bowel syndrome. Gut 57:468–473PubMedCrossRef

36.

Lee KJ, Kim YB, Kim JH, Kwon HC, Kim DK, Cho SW (2008) The alteration of enterochromaffin cell, mast cell, and lamina propria T lymphocyte numbers in irritable bowel syndrome and its relationship with psychological factors. J Gastroenterol Hepatol 23:1689–1694PubMedCrossRef

37.

Klooker TK, Braak B, Koopman KE, Welting O, Wouters MM, van der Heide S, Schemann M, Bischoff SC, van den Wijngaard RM, Boeckxstaens GE (2010) The mast cell stabiliser ketotifen decreases visceral hypersensitivity and improves intestinal symptoms in patients with irritable bowel syndrome. Gut 59:1213–1221PubMedCrossRef

38.

Frieling T, Meis K, Kolck UW, Homann J, Hülsdonk A, Haars U, Hertfelder HJ, Oldenburg J, Seidel H, Molderings GJ (2011) Evidence for mast cell activation in patients with therapy-resistant irritable bowel syndrome. Z Gastroenterol 49:191–194PubMedCrossRef

39.

Jones R, Latinovic R, Charlton J, Gulliford M (2006) Physical and psychological co-morbidity in irritable bowel syndrome: a matched cohort study using the General Practice Research Database. Aliment Pharmacol Ther 24:879–886PubMedCrossRef

40.

Harpaz N, Sachar DB (2006) Segmental colitis associated with diverticular disease and other IBD look-alikes. J Clin Gastroenterol 40(Suppl 3):S132–S135PubMedCrossRef

41.

Mulhall AM, Mahid SS, Petras RE, Galandiuk S (2009) Diverticular disease associated with inflammatory bowel disease-like colitis: a systematic review. Dis Colon Rectum 52:1072–1079PubMedCrossRef

42.

Jung HK, Choung RS, Locke GR 3rd, Schleck CD, Zinsmeister AR, Talley NJ (2010) Diarrhea-predominant irritable bowel syndrome is associated with diverticular disease: a population-based study. Am J Gastroenterol 105:652–661PubMedCrossRef

43.

Park JH, Rhee PL, Kim HS, Lee JH, Kim YH, Kim JJ, Rhee JC (2006) Mucosal mast cell counts correlate with visceral hypersensitivity in patients with diarrhea predominant irritable bowel syndrome. J Gastroenterol Hepatol 21:71–78PubMedCrossRef

44.

Cremon C, Gargano L, Morselli-Labate AM, Santini D, Cogliandro RF, De Giorgio R, Stanghellini V, Corinaldesi R, Barbara G (2009) Mucosal immune activation in irritable bowel syndrome: gender-dependence and association with digestive symptoms. Am J Gastroenterol 104:392–400PubMedCrossRef

45.

Cremon C, Carini G, Wang B, Vasina V, Cogliandro RF, De Giorgio R, Stanghellini V, Grundy D, Tonini M, De Ponti F, Corinaldesi R, Barbara G (2011) Intestinal serotonin release, sensory neuron activation, and abdominal pain in irritable bowel syndrome. Am J Gastroenterol 106:1290–1298PubMedCrossRef

46.

Park CH, Joo YE, Choi SK, Rew JS, Kim SJ, Lee MC (2003) Activated mast cells infiltrate in close proximity to enteric nerves in diarrhea-predominant irritable bowel syndrome. J Kor Med Sci 18:204–210

47.

Barbara G, Stanghellini V, De Giorgio R, Cremon C, Cottrell GS, Santini D, Pasquinelli G, Morselli-Labate AM, Grady EF, Bunnett NW, Collins SM, Corinaldesi R (2004) Activated mast cells in proximity to colonic nerves correlate with abdominal pain in irritable bowel syndrome. Gastroenterology 126:693–702PubMedCrossRef

48.

Buhner S, Li Q, Vignali S, Barbara G, De Giorgio R, Stanghellini V, Cremon C, Zeller F, Langer R, Daniel H, Michel K, Schemann M (2009) Activation of human enteric neurons by supernatants of colonic biopsy specimens from patients with irritable bowel syndrome. Gastroenterology 137:1425–1434PubMedCrossRef

49.

De Giorgio R, Barbara G, Stanghellini V, De Ponti F, Salvioli B, Tonini M, Velio P, Bassotti G, Corinaldesi R (2002) Clinical and morphofunctional features of idiopathic myenteric ganglionitis underlying severe intestinal motor dysfunction: a study of three cases. Am J Gastroenterol 97:2454–2459PubMed

50.

Schäppi MG, Smith VV, Milla PJ, Lindley KJ (2003) Eosinophilic myenteric ganglionitis is associated with functional intestinal obstruction. Gut 52:752–755PubMedCrossRef

51.

Veress B, Nyberg B, Törnblom H, Lindberg G (2009) Intestinal lymphocytic epithelioganglionitis: a unique combination of inflammation in bowel dysmotility: a histopathological and immunohistochemical analysis of 28 cases. Histopathology 54:539–549PubMedCrossRef

52.

Ng SC, Lied GA, Kamm MA, Sandhu F, Guenther T, Arebi N (2009) Predictive value and clinical significance of myenteric plexitis in Crohn’s disease. Inflamm Bowel Dis 15:1499–1507PubMedCrossRef

53.

Sokol H, Polin V, Lavergne-Slove A, Panis Y, Treton X, Dray X, Bouhnik Y, Valleur P, Marteau P (2009) Plexitis as a predictive factor of early postoperative clinical recurrence in Crohn’s disease. Gut 58:1218–1225PubMedCrossRef

54.

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 44:1814–1820PubMedCrossRef

55.

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 3:248–253PubMedCrossRef

56.

Floch MH (2006) A hypothesis: is diverticulitis a type of inflammatory bowel disease? J Clin Gastroenterol 40:S121–S125PubMedCrossRef

Title: The role of colonic mast cells and myenteric plexitis in patients with diverticular disease
Authors: Gabrio Bassotti
Vincenzo Villanacci
Riccardo Nascimbeni
Elisabetta Antonelli
Moris Cadei
Stefania Manenti
Luisa Lorenzi
Amin Titi
Bruno Salerni
Publication date: 01-02-2013
Publisher: Springer-Verlag
Published in: International Journal of Colorectal Disease / Issue 2/2013
Print ISSN: 0179-1958
Electronic ISSN: 1432-1262
DOI: https://doi.org/10.1007/s00384-012-1554-z

Keynote webinar | Spotlight on medication adherence

Springer Medicine

The role of colonic mast cells and myenteric plexitis in patients with diverticular disease

Abstract

Background

Aims

Methods

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Aims

Methods

Results

Conclusions

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