Revisiting concepts of visceral nociception in irritable bowel syndrome

European Journal of Pain (United Kingdom)

Volumn 16, Issue 10, 2012, Pages 1444-1454

  Keszthelyi, D ^a,b   Troost, F J ^a,b   Simren M ^c   Ludidi, S ^b   Kruimel, J W ^b   Conchillo, J M ^b   Masclee, A A ^a,b  

^a TOP INSTITUTE FOOD AND NUTRITION   (Netherlands)

^b MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; HUMAN; HYPERSENSITIVITY; IRRITABLE COLON; MUCOSA INFLAMMATION; NEUROANATOMY; NEUROPHYSIOLOGY; NOCICEPTION; PAIN ASSESSMENT; PAIN RECEPTOR; PRIORITY JOURNAL; VISCERAL PAIN;

GASTROINTESTINAL TRACT; HUMANS; IRRITABLE BOWEL SYNDROME; NOCICEPTION; NOCICEPTORS; PAIN THRESHOLD; VISCERAL PAIN;

EID: 84863938386     PISSN: 10903801     EISSN: 15322149     Source Type: Journal    
DOI: 10.1002/j.1532-2149.2012.00147.x     Document Type: Article

References (77)

1. Akbar, A., Yiangou, Y., Facer, P., Walters, J.R., Anand, P., Ghosh, S. (2008). Increased capsaicin receptor TRPV1-expressing sensory fibres in irritable bowel syndrome and their correlation with abdominal pain. Gut 57, 923-929.
2. Al-Khatib, K., Lin, H.C. (2009). Immune activation and gut microbes in irritable bowel syndrome. Gut Liver 3, 14-19.
3. Anand, P., Aziz, Q., Willert, R., van Oudenhove, L. (2007). Peripheral and central mechanisms of visceral sensitization in man. Neurogastroenterol Motil 19, 29-46.
4. Andresen, V. (2009). Visceral sensitivity testing. Best Pract Res Clin Gastroenterol 23, 313-324.
5. Azpiroz, F., Bouin, M., Camilleri, M., Mayer, E.A., Poitras, P., Serra, J., Spiller, R.C. (2007). Mechanisms of hypersensitivity in IBS and functional disorders. Neurogastroenterol Motil 19, 62-88.
6. Barbara, G. (2006). Mucosal barrier defects in irritable bowel syndrome. Who left the door open? Am J Gastroenterol 101, 1295-1298.
7. Bertiaux-Vandaele, N., Youmba, S.B., Belmonte, L., Lecleire, S., Antonietti, M., Gourcerol, G., Leroi, A.M., Dechelotte, P., Menard, J.F., Ducrotte, P., Coeffier, M. (2011). The expression and the cellular distribution of the tight junction proteins are altered in irritable bowel syndrome patients with differences according to the disease subtype. Am J Gastroenterol 106, 2165-2173.
8. Blackshaw, L.A., Brierley, S.M., Hughes, P.A. (2010). TRP channels: New targets for visceral pain. Gut 59, 126-135.
9. Bouin, M., Plourde, V., Boivin, M., Riberdy, M., Lupien, F., Laganiere, M., Verrier, P., Poitras, P. (2002). Rectal distention testing in patients with irritable bowel syndrome: Sensitivity, specificity, and predictive values of pain sensory thresholds. Gastroenterology 122, 1771-1777.
10. Brierley, S.M. (2010). Molecular basis of mechanosensitivity. Auton Neurosci 153, 58-68.
11. Brierley, S.M., Hughes, P.A., Page, A.J., Kwan, K.Y., Martin, C.M., O'Donnell, T.A., Cooper, N.J., Harrington, A.M., Adam, B., Liebregts, T., Holtmann, G., Corey, D.P., Rychkov, G.Y., Blackshaw, L.A. (2009). The ion channel TRPA1 is required for normal mechanosensation and is modulated by algesic stimuli. Gastroenterology 137, 2084-2095. e2083.
12. Brierley, S.M., Jones, R.C. 3rd, Gebhart, G.F., Blackshaw, L.A. (2004). Splanchnic and pelvic mechanosensory afferents signal different qualities of colonic stimuli in mice. Gastroenterology 127, 166-178.
13. Brierley, S.M., Page, A.J., Hughes, P.A., Adam, B., Liebregts, T., Cooper, N.J., Holtmann, G., Liedtke, W., Blackshaw, L.A. (2008). Selective role for TRPV4 ion channels in visceral sensory pathways. Gastroenterology 134, 2059-2069.
14. Brown, P.M., Drossman, D.A., Wood, A.J., Cline, G.A., Frazier, K.S., Jackson, J.I., Bronner, J., Freiman, J., Zambrowicz, B., Sands, A., Gershon, M.D. (2011). The tryptophan hydroxylase inhibitor LX1031 shows clinical benefit in patients with nonconstipating irritable bowel syndrome. Gastroenterology 141, 507-516.
15. Bueno, L., Fioramonti, J., Garcia-Villar, R. (2000). Pathobiology of visceral pain: Molecular mechanisms and therapeutic implications. III. Visceral afferent pathways: A source of new therapeutic targets for abdominal pain. Am J Physiol Gastrointest Liver Physiol 278, G670-G676.
16. 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, 1425-1434.
17. Camilleri, M. (2002). Testing the sensitivity hypothesis in practice: tools and methods, assumptions and pitfalls. Gut 51 (Suppl 1): i34-40.
18. Camilleri, M., McKinzie, S., Busciglio, I., Low, P.A., Sweetser, S., Burton, D., Baxter, K., Ryks, M., Zinsmeister, A.R. (2008). Prospective study of motor, sensory, psychologic, and autonomic functions in patients with irritable bowel syndrome. Clin Gastroenterol Hepatol 6, 772-781.
19. Cattaruzza, F., Spreadbury, I., Miranda-Morales, M., Grady, E.F., Vanner, S., Bunnett, N.W. (2010). Transient receptor potential ankyrin-1 has a major role in mediating visceral pain in mice. Am J Physiol Gastrointest Liver Physiol 298, G81-G91.
20. Cervero, F. (1994). Sensory innervation of the viscera: Peripheral basis of visceral pain. Physiol Rev 74, 95-138.
21. Corsetti, M., Cesana, B., Bhoori, S., Basilisco, G. (2004). Rectal hyperreactivity to distention in patients with irritable bowel syndrome: Role of distention rate. Clin Gastroenterol Hepatol 2, 49-56.
22. Cremon, C., Carini, G., Wang, B., Vasina, V., Cogliandro, R.F., 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, 1290-1298.
23. Cremon, C., Gargano, L., Morselli-Labate, A.M., Santini, D., Cogliandro, R.F., 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, 392-400.
24. Delvaux, M. (2002). Do we need to perform rectal distention tests to diagnose IBS in clinical practice? Gastroenterology 122, 2075-2078.
25. Delvaux, M., Louvel, D., Mamet, J.P., Campos-Oriola, R., Frexinos, J. (1998). Effect of alosetron on responses to colonic distension in patients with irritable bowel syndrome. Aliment Pharmacol Ther 12, 849-855.
26. Dorn, S.D., Palsson, O.S., Thiwan, S.I., Kanazawa, M., Clark, W.C., van Tilburg, M.A., Drossman, D.A., Scarlett, Y., Levy, R.L., Ringel, Y., Crowell, M.D., Olden, K.W., Whitehead, W.E. (2007). Increased colonic pain sensitivity in irritable bowel syndrome is the result of an increased tendency to report pain rather than increased neurosensory sensitivity. Gut 56, 1202-1209.
27. Drossman, D.A., Camilleri, M., Mayer, E.A., Whitehead, W.E. (2002). AGA technical review on irritable bowel syndrome. Gastroenterology 123, 2108-2131.
28. Dunlop, S.P., Hebden, J., Campbell, E., Naesdal, J., Olbe, L., Perkins, A.C., Spiller, R.C. (2006). Abnormal intestinal permeability in subgroups of diarrhea-predominant irritable bowel syndromes. Am J Gastroenterol 101, 1288-1294.
29. Dunlop, S.P., Jenkins, D., Neal, K.R., Spiller, R.C. (2003). Relative importance of enterochromaffin cell hyperplasia, anxiety, and depression in postinfectious IBS. Gastroenterology 125, 1651-1659.
30. Elsenbruch, S., Rosenberger, C., Bingel, U., Forsting, M., Schedlowski, M., Gizewski, E.R. (2010). Patients with irritable bowel syndrome have altered emotional modulation of neural responses to visceral stimuli. Gastroenterology 139, 1310-1319.
31. Feng, B., Gebhart, G.F. (2011). Characterization of silent afferents in the pelvic and splanchnic innervations of the mouse colorectum. Am J Physiol Gastrointest Liver Physiol 300, G170-G180.
32. Ford, A.C., Brandt, L.J., Young, C., Chey, W.D., Foxx-Orenstein, A.E., Moayyedi, P. (2009). Efficacy of 5-HT3 antagonists and 5-HT4 agonists in irritable bowel syndrome: Systematic review and meta-analysis. Am J Gastroenterol 104, 1831-1843. quiz 1844.
33. Gebhart, G.F. (2000). Pathobiology of visceral pain: Molecular mechanisms and therapeutic implications IV. Visceral afferent contributions to the pathobiology of visceral pain. Am J Physiol Gastrointest Liver Physiol 278, G834-G838.
34. Gecse, K., Roka, R., Ferrier, L., Leveque, M., Eutamene, H., Cartier, C., Ait-Belgnaoui, A., Rosztoczy, A., Izbeki, F., Fioramonti, J., Wittmann, T., Bueno, L. (2008). Increased faecal serine protease activity in diarrhoeic IBS patients: A colonic lumenal factor impairing colonic permeability and sensitivity. Gut 57, 591-599.
35. Giamberardino, M.A. (1999). Recent and forgotten aspects of visceral pain. Eur J Pain 3, 77-92.
36. Greenwood-Van Meerveld, B. (2007). Importance of 5-hydroxytryptamine receptors on intestinal afferents in the regulation of visceral sensitivity. Neurogastroenterol Motil 19(Suppl 2), 13-18.
37. Gwee, K.A., Leong, Y.L., Graham, C., McKendrick, M.W., Collins, S.M., Walters, S.J., Underwood, J.E., Read, N.W. (1999). The role of psychological and biological factors in postinfective gut dysfunction. Gut 44, 400-406.
38. Houghton, L.A., Atkinson, W., Whitaker, R.P., Whorwell, P.J., Rimmer, M.J. (2003). Increased platelet depleted plasma 5-hydroxytryptamine concentration following meal ingestion in symptomatic female subjects with diarrhoea predominant irritable bowel syndrome. Gut 52, 663-670.
39. Hughes, P.A., Brierley, S.M., Blackshaw, L.A. (2009a). Postinflammatory modification of colonic afferent mechanosensitivity. Clin Exp Pharmacol Physiol 36, 1034-1040.
40. Hughes, P.A., Brierley, S.M., Martin, C.M., Brookes, S.J., Linden, D.R., Blackshaw, L.A. (2009b). Post-inflammatory colonic afferent sensitisation: Different subtypes, different pathways and different time courses. Gut 58, 1333-1341.
41. Jiang, W., Adam, I.J., Kitsanta, P., Tiernan, J., Hill, C., Shorthouse, A., Grundy, D. (2011). 'First-in-man': Characterising the mechanosensitivity of human colonic afferents. Gut 60, 281-282.
42. Jones, R.C. 3rd, Otsuka, E., Wagstrom, E., Jensen, C.S., Price, M.P., Gebhart, G.F. (2007). Short-term sensitization of colon mechanoreceptors is associated with long-term hypersensitivity to colon distention in the mouse. Gastroenterology 133, 184-194.
43. Knowles, C.H., Aziz, Q. (2009). Basic and clinical aspects of gastrointestinal pain. Pain 141, 191-209.
44. Koltzenburg, M., Lundberg, L.E., Torebjork, H.E. (1992). Dynamic and static components of mechanical hyperalgesia in human hairy skin. Pain 51, 207-219.
45. Kuiken, S.D., Lindeboom, R., Tytgat, G.N., Boeckxstaens, G.E. (2005). Relationship between symptoms and hypersensitivity to rectal distension in patients with irritable bowel syndrome. Aliment Pharmacol Ther 22, 157-164.
46. Kuiken, S.D., Tytgat, G.N., Boeckxstaens, G.E. (2003). The selective serotonin reuptake inhibitor fluoxetine does not change rectal sensitivity and symptoms in patients with irritable bowel syndrome: A double blind, randomized, placebo-controlled study. Clin Gastroenterol Hepatol 1, 219-228.
47. Lembo, T., Munakata, J., Mertz, H., Niazi, N., Kodner, A., Nikas, V., Mayer, E.A. (1994). Evidence for the hypersensitivity of lumbar splanchnic afferents in irritable bowel syndrome. Gastroenterology 107, 1686-1696.
48. Levinthal, D.J., Bielefeldt, K. (2009). Differences in postinflammatory hypersensitivity between splanchnic and pelvic afferents: Mechanisms and implications for human disease. Gut 58, 1317-1318.
49. Marshall, J.K., Thabane, M., Garg, A.X., Clark, W., Meddings, J., Collins, S.M. (2004). Intestinal permeability in patients with irritable bowel syndrome after a waterborne outbreak of acute gastroenteritis in Walkerton, Ontario. Aliment Pharmacol Ther 20, 1317-1322.
50. Mawe, G.M., Coates, M.D., Moses, P.L. (2006). Review article: Intestinal serotonin signalling in irritable bowel syndrome. Aliment Pharmacol Ther 23, 1067-1076.
51. Mayer, E.A., Bradesi, S., Chang, L., Spiegel, B.M., Bueller, J.A., Naliboff, B.D. (2008). Functional GI disorders: From animal models to drug development. Gut 57, 384-404.
52. Mertz, H., Naliboff, B., Munakata, J., Niazi, N., Mayer, E.A. (1995). Altered rectal perception is a biological marker of patients with irritable bowel syndrome. Gastroenterology 109, 40-52.
53. Nozawa, K., Kawabata-Shoda, E., Doihara, H., Kojima, R., Okada, H., Mochizuki, S., Sano, Y., Inamura, K., Matsushime, H., Koizumi, T., Yokoyama, T., Ito, H. (2009). TRPA1 regulates gastrointestinal motility through serotonin release from enterochromaffin cells. Proc Natl Acad Sci U S A 106, 3408-3413.
54. Nozu, T., Kudaira, M. (2009). Altered rectal sensory response induced by balloon distention in patients with functional abdominal pain syndrome. Biopsychosoc Med 3, 13.
55. Ohman, L., Isaksson, S., Lindmark, A.C., Posserud, I., Stotzer, P.O., Strid, H., Sjovall, H., Simren, M. (2009a). T-cell activation in patients with irritable bowel syndrome. Am J Gastroenterol 104, 1205-1212.
56. Ohman, L., Lindmark, A.C., Isaksson, S., Posserud, I., Strid, H., Sjovall, H., Simren, M. (2009b). B-cell activation in patients with irritable bowel syndrome (IBS). Neurogastroenterol Motil 21, 644-650. e627.
57. Park, J.H., Baek, Y.H., Park, D.I., Kim, H.J., Cho, Y.K., Sohn, C.I., Jeon, W.K., Kim, B.I., Rhee, P.L. (2008). Analysis of rectal dynamic and static compliances in patients with irritable bowel syndrome. Int J Colorectal Dis 23, 659-664.
58. Peiris, M., Bulmer, D.C., Baker, M.D., Boundouki, G., Sinha, S., Hobson, A., Lee, K., Aziz, Q., Knowles, C.H. (2011). Human visceral afferent recordings: Preliminary report. Gut 60, 204-208.
59. Piche, M., Arsenault, M., Poitras, P., Rainville, P., Bouin, M. (2010). Widespread hypersensitivity is related to altered pain inhibition processes in irritable bowel syndrome. Pain 148, 49-58.
60. Piche, T., Barbara, G., Aubert, P., Bruley Des Varannes, S., Dainese, R., Nano, J.L., Cremon, C., Stanghellini, V., De Giorgio, R., Galmiche, J.P., Neunlist, M. (2009). Impaired intestinal barrier integrity in the colon of patients with irritable bowel syndrome: Involvement of soluble mediators. Gut 58, 196-201.
61. Posserud, I., Syrous, A., Lindstrom, L., Tack, J., Abrahamsson, H., Simren, M. (2007). Altered rectal perception in irritable bowel syndrome is associated with symptom severity. Gastroenterology 133, 1113-1123.
62. Rapps, N., van Oudenhove, L., Enck, P., Aziz, Q. (2008). Brain imaging of visceral functions in healthy volunteers and IBS patients. J Psychosom Res 64, 599-604.
63. Rescigno, M. (2011). The intestinal epithelial barrier in the control of homeostasis and immunity. Trends Immunol 32, 256-264.
64. Ritchie, J. (1973). Pain from distension of the pelvic colon by inflating a balloon in the irritable colon syndrome. Gut 14, 125-132.
65. Robinson, D.R., Gebhart, G.F. (2008). Inside information: The unique features of visceral sensation. Mol Interv 8, 242-253.
66. Sarna, S.K. (2011). Lessons Learnt from Post-Infectious IBS. Front Physiol 2, 49.
67. Sengupta, J.N. (2009). Visceral pain: The neurophysiological mechanism. Handb Exp Pharmacol 194, 31-74.
68. Spiller, R. (2007). Recent advances in understanding the role of serotonin in gastrointestinal motility in functional bowel disorders: Alterations in 5-HT signalling and metabolism in human disease. Neurogastroenterol Motil 19(Suppl 2), 25-31.
69. Spiller, R.C., Jenkins, D., Thornley, J.P., Hebden, J.M., Wright, T., Skinner, M., Neal, K.R. (2000). Increased rectal mucosal enteroendocrine cells, T lymphocytes, and increased gut permeability following acute Campylobacter enteritis and in postdysenteric irritable bowel syndrome. Gut 47, 804-811.
70. Sun, W.M., Read, N.W., Prior, A., Daly, J.A., Cheah, S.K., Grundy, D. (1990). Sensory and motor responses to rectal distention vary according to rate and pattern of balloon inflation. Gastroenterology 99, 1008-1015.
71. van der Schaar, P.J., Lamers, C.B., Masclee, A.A. (1999). The role of the barostat in human research and clinical practice. Scand J Gastroenterol Suppl 230, 52-63.
72. van der Veek, P.P., Van Rood, Y.R., Masclee, A.A. (2008). Symptom severity but not psychopathology predicts visceral hypersensitivity in irritable bowel syndrome. Clin Gastroenterol Hepatol 6, 321-328.
73. Vandenberghe, J., Vos, R., Persoons, P., Demyttenaere, K., Janssens, J., Tack, J. (2005). Dyspeptic patients with visceral hypersensitivity: Sensitisation of pain specific or multimodal pathways? Gut 54, 914-919.
74. Vergnolle, N. (2010). Visceral afferents: What role in postinflammatory pain? Auton Neurosci 153, 79-83.
75. Wilder-Smith, C.H. (2011). The balancing act: Endogenous modulation of pain in functional gastrointestinal disorders. Gut 60, 1589-1599.
76. Wilder-Smith, C.H., Schindler, D., Lovblad, K., Redmond, S.M., Nirkko, A. (2004). Brain functional magnetic resonance imaging of rectal pain and activation of endogenous inhibitory mechanisms in irritable bowel syndrome patient subgroups and healthy controls. Gut 53, 1595-1601.
77. Zhou, Q., Zhang, B., Verne, G.N. (2009). Intestinal membrane permeability and hypersensitivity in the irritable bowel syndrome. Pain 146, 41-46.