The role of experimental models in developing new treatments for irritable bowel syndrome

Expert Review of Gastroenterology and Hepatology

Volumn 5, Issue 1, 2011, Pages 43-57

  Holschneider, Daniel P ^a,b   Bradesi, Sylvie ^a,c   Mayer, Emeran A ^a,c  

^a VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

^b University of Southern California ^*  (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

functional gastrointestinal disorders; intestinal transit; neuroimaging; visceral pain

Indexed keywords

ALOSETRON; FEDOTOZINE; KAPPA OPIATE RECEPTOR ANTAGONIST; LINACLOTIDE; LUBIPROSTONE; PREGABALIN; SOMATOSTATIN; TEGASEROD;

BRAIN REGION; CLINICAL ASSESSMENT; DISEASE MODEL; DOSE RESPONSE; DRUG DOSE TITRATION; DRUG EFFICACY; DRUG TARGETING; EXPERIMENTAL MODEL; HUMAN; HUMAN VERSUS ANIMAL COMPARISON; IMAGE QUALITY; INTESTINE TRANSIT TIME; IRRITABLE COLON; NEUROIMAGING; NONHUMAN; PHENOTYPE; REVIEW; SENSITIVITY AND SPECIFICITY; SINGLE DRUG DOSE; VISCERAL PAIN;

ABDOMINAL PAIN; ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; ENDOPHENOTYPES; GASTROINTESTINAL AGENTS; GASTROINTESTINAL MOTILITY; HUMANS; IRRITABLE BOWEL SYNDROME; RATS; VISCERA;

EID: 79951622644     PISSN: 17474124     EISSN: None     Source Type: Journal    
DOI: 10.1586/egh.10.88     Document Type: Review

References (137)

1. Mayer EA, Collins SM. Evolving pathophysiologic models of functional gastrointestinal disorders. Gastroenterology 122(7), 2032-2048 (2002). (Pubitemid 34651445)
2. Camilleri M. Is there a SERT-ain association with IBS? Gut 53(10), 1396-1399 (2004). (Pubitemid 39265254)
3. Mayer EA, Naliboff BD, Chang L. Evolving pathophysiological model of functional gastrointestinal disorders: implications for treatment. Eur. J. Surg. Suppl. 168(Suppl. 587), 3-9 (2002). (Pubitemid 36359574)
4. Langley CK, Aziz Q, Bountra C et al. Volunteer studies in pain research - opportunities and challenges to replace animal experiments: the report and recommendations of a Focus on Alternatives workshop. Neuroimage 42(2), 467-473 (2008).
5. Hohoff C. Anxiety in mice and men: a comparison. J. Neural Transm. 116(6), 679-687 (2009).
6. Mogil JS, Simmonds K, Simmonds MJ. Pain research from 1975 to 2007: a categorical and bibliometric meta-trend analysis of every research paper published in the journal, Pain. Pain 142(1-2), 48-58 (2009).
7. Kellow JE, Azpiroz F, Delvaux M et al. Principles of applied neurogastroenterology: Physiology/motility-sensation. In: ROME III: The Functional Gastrointestinal Disorders. Degnon Associates, VA, USA, 89-160 (2006).
8. Camilleri M. Scintigraphic biomarkers for colonic dysmotility. Clin. Pharmacol. Ther. 87(6), 748-753 (2010).
9. Horikawa Y, Mieno H, Inoue M, Kajiyama G. Gastrointestinal motility in patients with irritable bowel syndrome studied by using radioopaque markers. Scand. J. Gastroenterol. 34(12), 1190-1195 (1999). (Pubitemid 30026721)
10. Cann PA, Read NW, Brown C, Hobson N, Holdsworth CD. Irritable bowel syndrome: relationship of disorders in the transit of a single solid meal to symptom patterns. Gut 24(5), 405-411 (1983). (Pubitemid 13089484)
11. Bouchoucha M, Devroede G, Dorval E, Faye A, Arhan P, Arsac M. Different segmental transit times in patients with irritable bowel syndrome and ?normal? colonic transit time: is there a correlation with symptoms? Tech. Coloproctol. 10(4), 287-296 (2006).
12. Camilleri M, Bueno L, De Ponti F, Fioramonti J, Lydiard RB, Tack J. Pharmacological and pharmacokinetic aspects of functional gastrointestinal disorders. Gastroenterology 130(5), 1421-1434 (2006).
13. Mertz H. Review article: visceral hypersensitivity. Aliment. Pharmacol. Ther. 17(5), 623-633 (2003). (Pubitemid 36418885)
14. Lembo T, Naliboff BD, Matin K et al. Irritable bowel syndrome patients show altered sensitivity to exogenous opioids. Pain 87(2), 137-147 (2000). (Pubitemid 30621446)
15. Delvaux M, Louvel D, Lagier E, Scherrer B, Abitbol JL, Frexinos J. The k agonist fedotozine relieves hypersensitivity to colonic distension in patients with irritable bowel syndrome. Gastroenterology 116(1), 38-45 (1999). (Pubitemid 29013491)
16. Dapoigny M, Abitbol JL, Fraitag B. Efficacy of peripheral k-agonist fedotozine versus placebo in treatment of irritable bowel syndrome: a multicenter dose-response study. Dig. Dis. Sci. 40(10), 2244-2249 (1995).
17. Delvaux M, Beck A, Jacob J, Bouzamondo H, Weber FT, Frexinos J. Effect of asimadoline, a k opioid agonist, on pain induced by colonic distension in patients with irritable bowel syndrome. Aliment. Pharmacol. Ther. 20(2), 237-246 (2004). (Pubitemid 38998223)
18. Delvaux M, Louvel D, Mamet JP, Campos-Oriola R, Frexinos J. Effect of alosetron on responses to colonic distension in patients with irritable bowel syndrome. Aliment. Pharmacol. Ther. 12(9), 849-855 (1998). (Pubitemid 28428949)
19. Camilleri M, Mayer EA, Drossman DA et al. Improvement in pain and bowel function in female irritable bowel patients with alosetron, a 5-HT 3 receptor antagonist. Aliment. Pharmacol. Ther. 13(9), 1149-1159 (1999). (Pubitemid 29445893)
20. Thumshirn M, Coulie B, Camilleri M, Zinsmeister AR, Burton DD, Van Dyke C. Effects of alosetron on gastrointestinal transit time and rectal sensation in patients with irritable bowel syndrome. Aliment. Pharmacol. Ther. 14(7), 869-878 (2000). (Pubitemid 30446897)
21. Zighelboim J, Talley NJ, Phillips SF, Harmsen WS, Zinsmeister AR. Visceral perception in irritable bowel syndrome. Dig. Dis. Sci. 40(4), 819-827 (1995).
22. Steadman CJ, Talley NJ, Phillips SF, Zinsmeister AR. Selective 5-hydroxytryptamine type 3 receptor antagonism with ondansetron as treatment for diarrhea-predominant irritable bowel syndrome: a pilot study. Mayo Clinic Proc. 67, 732-738 (1992).
23. Goldberg PA, Kamm MA, Setti-Carraro P, van der Sijp JR, Roth C. Modification of visceral sensitivity and pain in irritable bowel syndrome by 5-HT3 antagonism (ondansetron). Digestion 57(6), 478-483 (1996). (Pubitemid 26385300)
24. Hammer J, Phillips SF, Talley NJ, Camilleri M. Effect of a 5-HT3-antagonist (ondansetron) on rectal sensitivity and compliance in health and the irritable bowel syndrome. Aliment. Pharmacol. Ther. 7(5), 543-551 (1993). (Pubitemid 23317887)
25. Prior A, Read NW. Reduction of rectal sensitivity and post-prandial motility by granisetron, a 5 HT3-receptor antagonist, in patients with irritable bowel syndrome. Aliment. Pharmacol. Ther. 7, 175-180 (1993). (Pubitemid 23109464)
26. Brandt LJ, Prather CM, Quigley EM, Schiller LR, Schoenfeld P, Talley NJ. Systematic review on the management of chronic constipation in North America. Am. J. Gastroenterol. 100(Suppl. 1), S5-S21 (2005).
27. Evans BW, Clark WK, Moore DJ, Whorwell PJ. Tegaserod for the treatment of irritable bowel syndrome. Cochrane Database Syst. Rev. (1), CD003960 (2004).
28. Poitras P, Riberdy Poitras M, Plourde V, Boivin M, Verrier P. Evolution of visceral sensitivity in patients with irritable bowel syndrome. Dig. Dis. Sci. 47(4), 914-920 (2002). (Pubitemid 34286891)
29. Rajagopalan M, Kurian G, John J. Symptom relief with amitriptyline in the irritable bowel syndrome. J. Gastroenterol. Hepatol. 13, 738-741 (1998). (Pubitemid 28407348)
30. Kuiken SD, Tytgat GN, Boeckxstaens GE. The selective serotonin reuptake inhibitor fluoxetine does not change rectal sensistivity and symptoms in patients with irritable bowel syndrome: a double blind, randomized, placebo-controlled study. Clin. Gastroenterol. Hepatol. 1(3), 219-228 (2003). (Pubitemid 37248073)
31. Lee KJ, Kim JH, Cho SW. Gabapentin reduces rectal mechanosensitivity and increases rectal compliance in patients with diarrhoea-predominant irritable bowel syndrome. Aliment. Pharmacol. Ther. 22(10), 981-988 (2005). (Pubitemid 41634880)
32. Houghton LA, Fell C, Whorwell PJ, Jones I, Sudworth DP, Gale JD. Effect of a second-generation a2d ligand (pregabalin) on visceral sensation in hypersensitive patients with irritable bowel syndrome. Gut 56(9), 1218-1225 (2007). (Pubitemid 47300421)
33. Bradette M, Delvaux M, Staumont G, Fioramonti J, Bueno L, Frexinos J. Octreotide increases thresholds of colonic visceral perception in IBS patients without modifying muscle tone. Dig. Dis. Sci. 39(6), 1171-1178 (1994). (Pubitemid 24190252)
34. Klooker TK, Beaumont H, Kuiken SD, Lei A, Boeckxstaens GE. Octreotide as potential treatment for patients with non-constipated irritable bowel syndrome. Gastroenterology 128(4 Suppl. 2), A93-A94 (2005).
35. Hasler WL, Soudah HC, Owyang C. A somatostatin analogue inhibits afferent pathways mediating perception of rectal distention. Gastroenterology 104(5), 1390-1397 (1993). (Pubitemid 23235411)
36. Schwetz I, Naliboff B, Munakata J et al. Anti-hyperalgesic effect of octreotide in patients with irritable bowel syndrome. Aliment. Pharmacol. Ther. 19(1), 123-131 (2004). (Pubitemid 38125645)
37. Dukes GE, Dewit OE, Sanger GJ et al. Lack of effect of the NK3 receptor antagonist, talnetant SB223242 on symptoms of IBS: results of 2 randomized, double-blind, placebo-controlled dose ranging trials. Gastroenterology 132(4 Suppl. 2) (2007).
38. Houghton LA, Atkinson W, Lockhart C, Whorwell PJ, Keevil B. Sigmoid-colonic motility in health and irritable bowel syndrome: a role for 5-hydroxytryptamine. Neurogastroenterol. Motil. 19(9), 724-731 (2007). (Pubitemid 47312399)
39. Gebhart GJ, Sengupta JN, Gaginella TS. Evaluation of visceral pain. In: Handbook of Methods in Gastrointestinal Pharmacology. CRC Press, FL, USA, 359-374 (1996).
40. De Winter BY, Boeckxstaens GE, De Man JG, Moreels TG, Herman AG, Pelckmans PA. Effects of m- and k-opioid receptors on postoperative ileus in rats. Eur. J. Pharmacol. 339(1), 63-67 (1997). (Pubitemid 28015432)
41. Friese N, Chevalier E, Angel F et al. Reversal by k-agonists of peritoneal irritation-induced ileus and visceral pain in rats. Life Sci. 60(9), 625-634 (1997). (Pubitemid 27107380)
42. Langlois A, Diop L, Friese N et al. Fedotozine blocks hypersensitive visceral pain in conscious rats: action at peripheral k-opioid receptors. Eur. J. Pharmacol. 324(2-3), 211-217 (1997). (Pubitemid 27174608)
43. Langlois A, Diop L, Rivi?re PJ, Pascaud X, Junien JL. Effect of fedotozine on the cardiovascular pain reflex induced by distension of the irritated colon in the anesthetized rat. Eur. J. Pharmacol. 271(2-3), 245-251 (1994).
44. Diop L, Riviere PJ, Pascaud X, Junien JL. Peripheral k-opioid receptors mediate the antinociceptive effect of fedotozine (correction of fetodozine) on the duodenal pain reflex in rat. Eur. J. Pharmacol. 271(1), 65-71 (1994). (Pubitemid 24375851)
45. Coffin B, Bouhassira D, Chollet R et al. Effect of the k agonist fedotozine on perception of gastric distension in healthy humans. Aliment. Pharmacol. Ther. 10(6), 919-925 (1996). (Pubitemid 26412920)
46. Pol O, Ferrer I, Puig MM. Diarrhea associated with intestinal inflammation increases the potency of m and d opioids on the inhibition of gastrointestinal transit in mice. J. Pharmacol. Exp. Ther. 270(1), 386-391 (1994). (Pubitemid 24229651)
47. Pol O, Valle L, Sanchez-Blazquez P, Garzon J, Puig MM. Antibodies and antisense oligodeoxynucleotides to m-opioid receptors, selectively block the effects of m-opioid agonists on intestinal transit and permeability in mice. Br. J. Pharmacol. 127(2), 397-404 (1999). (Pubitemid 29245677)
48. Topcu I, Ekici NZ, Isik R, Sakarya M. The effects of tramadol and fentanyl on gastrointestinal motility in septic rats. Anesth. Analg. 102(3), 876-881 (2006).
49. Arvidsson S, Larsson M, Larsson H, Lindstrom E, Martinez V. Assessment of visceral pain-related pseudo-affective responses to colorectal distension in mice by intracolonic manometric recordings. J. Pain 7(2), 108-118 (2006). (Pubitemid 43197619)
50. Larsson M, Arvidsson S, Ekman C, Bayati A. A model for chronic quantitative studies of colorectal sensitivity using balloon distension in conscious mice - effects of opioid receptor agonists. Neurogastroenterol. Motil. 15(4), 371-381 (2003). (Pubitemid 36876252)
51. Fendt M, Mucha RF. Anxiogenic-like effects of opiate withdrawal seen in the fear-potentiated startle test, an interdisciplinary probe for drug-related motivational states. Psychopharmacology 155(3), 242-250 (2001). (Pubitemid 32477280)
52. Narita M, Kaneko C, Miyoshi K et al. Chronic pain induces anxiety with concomitant changes in opioidergic function in the amygdala. Neuropsychopharmacology 31(4), 739-750 (2006).
53. Corazziari E. Role of opioid ligands in the irritable bowel syndrome. Can. J. Gastroenterol. 13(Suppl. A), A71-A75 (1999).
54. Gershon MD. Review article: serotonin receptors and transporters - roles in normal and abnormal gastrointestinal motility. Aliment. Pharmacol. Ther. 20(Suppl. 7), 3-14 (2004). (Pubitemid 39657670)
55. Bradesi S, Lao L, McLean PG et al. Dual role of 5-HT(3) receptors in a rat model of delayed stress-induced visceral hyperalgesia. Pain 130(1), 56-65 (2007). (Pubitemid 46844854)
56. Miranda A, Peles S, McLean PG, Sengupta JN. Effects of the 5-HT3 receptor antagonist, alosetron, in a rat model of somatic and visceral hyperalgesia. Pain 126(1-3), 54-63 (2006). (Pubitemid 44751956)
57. Houghton LA, Foster JM, Whorwell PJ. Alosetron, a 5-HT3 receptor antagonist, delays colonic transit in patients with irritable bowel syndrome and healthy volunteers. Aliment. Pharmacol. Ther. 14(6), 775-782 (2000). (Pubitemid 30352745)
58. Mayer EA, Berman SM, Derbyshire SWG et al. The effect of the 5-HT 3 receptor antagonist alosetron on regional brain activation in IBS patients is not dependent on activation of nociceptive visceral afferents: a H 2 15 O PET study. Gastroenterology 120, A67 (2001).
59. Galligan JJ, Vanner S. Basic and clinical pharmacology of new motility promoting agents. Neurogastroenterol. Motil. 17(5), 643-653 (2005). (Pubitemid 41400712)
60. Jiao HM, Xie PY. Tegaserod inhibits noxious rectal distention induced responses and limbic system c-Fos expression in rats with visceral hypersensitivity. World J. Gastroenterol. 10(19), 2836-2841 (2004).
61. Liang LX, Zhang Q, Qian W, Hou XH. Antinociceptive property of tegaserod in a rat model of chronic visceral hypersensitivity. Chin. J. Dig. Dis. 6(1), 21-25 (2005). (Pubitemid 40467730)
62. Prather CM, Camilleri M, Zinsmeister AR, McKinzie S, Thomforde G. Tegaserod accelerates orocecal transit in patients with constipation-predominant irritable bowel syndrome. Gastroenterology 118, 463-468 (2000). (Pubitemid 30140843)
63. Naliboff BD, Chang L, Crowell MD et al. Tegaserod increases sigmoid accommodation in female irritable bowel syndrome (IBS) patients. Gastroenterology 126(4 Suppl. 2), A101 (2004).
64. Camilleri M. Review article: tegaserod. Aliment. Pharmacol. Ther. 15(3), 277-289 (2001). (Pubitemid 32187551)
65. Kilpatrick L, Labus J, Berman SM et al. A course of tegaserod treatment modulates CNS processing of visceral afferent information. Gastroenterology 130(4 Suppl. 2), A289-A290 (2006).
66. Muller-Lissner SA, Fumagalli I, Bardhan KD et al. Tegaserod, a 5-HT(4) receptor partial agonist, relieves symptoms in irritable bowel syndrome patients with abdominal pain, bloating and constipation. Aliment. Pharmacol. Ther. 15(10), 1655-1666 (2001). (Pubitemid 32912410)
67. Lindstrom E, Ravnefjord A, Brusberg M, Hjorth S, Larsson H, Martinez V. The selective 5-hydroxytryptamine 1A antagonist, AZD7371 [3(R)-(N,N- dicyclobutylamino)-8-fluoro-3,4-dihydro- 2H-1-benzopyran-5-carboxamide (R,R)-tartrate monohydrate] (robalzotan tartrate monohydrate), inhibits visceral pain-related visceromotor, but not autonomic cardiovascular, responses to colorectal distension in rats. J. Pharmacol. Exp. Ther. 329(3), 1048-1055 (2009).
68. Drossman DA, Danilewitz M, Naesdal J, Hwang C, Adler J, Silberg DG. Randomized, double-blind, placebo-controlled trial of the 5-HT1A receptor antagonist AZD7371 tartrate monohydrate (robalzotan tartrate monohydrate) in patients with irritable bowel syndrome. Am. J. Gastroenterol. 103(10), 2562-2569 (2008).
69. Smedh U, Kaplan JM, Bjorkstrand E, Uvnas-Moberg K. Dual effects of somatostatin analog octreotide on gastric emptying during and after intragastric fill. Am. J. Physiol. 277(5 Pt 2), R1291-R1296 (1999).
70. Su X, Burton MB, Gebhart GF. Effects of octreotide on responses to noxious colorectal distension in the rat. Gut 48(5), 676-682 (2001). (Pubitemid 32378590)
71. Meyer BM, Werth BA, Beglinger C et al. Role of cholecystokinin in regulation of gastrointestinal motor functions. Lancet 2(8653), 12-15 (1989). (Pubitemid 19158161)
72. Chey WD, Beydoun A, Roberts DJ, Hasler WL, Owyang C. Octreotide reduces perception of rectal electrical stimulation by spinal afferent pathway inhibition. Am. J. Physiol. Gastrointest. Liver Physiol. 269(6 Pt 1), G821-G826 (1995).
73. Mertz H, Walsh JH, Sytnik B, Mayer EA. The effect of octreotide on human gastric compliance and sensory perception. Neurogastroenterol. Motil. 7, 175-185 (1995).
74. Hasler WL, Soudah HC, Owyang C. Somatostatin analog inhibits afferent response to rectal distension in diarrhea-predominant irritable bowel patients. J. Pharmacol. Exp. Ther. 268(3), 1206-1211 (1994). (Pubitemid 24100334)
75. Klooker TK, Kuiken SD, Lei A, Boeckxstaens GE. Effect of long-term treatment with octreotide on rectal sensitivity in patients with non-constipated irritable bowel syndrome. Aliment. Pharmacol. Ther. 26(4), 605-615 (2007). (Pubitemid 47174283)
76. Varga G, Balint A, Burghardt B, D?Amato M. Involvement of endogenous CCK and CCK1 receptors in colonic motor function. Br. J. Pharmacol. 141(8), 1275-1284 (2004). (Pubitemid 38638816)
77. Bonnafous C, Bueno L, Griffin PH, Schneier H, Rovati LC, D?Amato M. Influence of dexloxiglumide on visceromotor and pain response induced by rectal distension in rats. Gastroenterology 122(4), A527 (2002).
78. Cremonini F, Camilleri M, McKinzie S et al. Effect of CCK-1 antagonist, dexloxiglumide, in female patients with irritable bowel syndrome: a pharmacodynamic and pharmacogenomic study. Am. J. Gastroenterol. 100(3), 652-663 (2005). (Pubitemid 40487566)
79. Sanger GJ. Neurokinin NK1 and NK3 receptors as targets for drugs to treat gastrointestinal motility disorders and pain. Br. J. Pharmacol. 141(8), 1303-1312 (2004). (Pubitemid 38638819)
80. Salome N, Stemmelin J, Cohen C, Griebel G. Selective blockade of NK2 or NK3 receptors produces anxiolytic- and antidepressant-like effects in gerbils. Pharmacol. Biochem. Behav. 83(4), 533-539 (2006). (Pubitemid 43817123)
81. Diop L, Raymond F, Fargeau H, Petoux F, Chovet M, Doherty AM. Pregabalin (CI-1008) inhibits the trinitrobenzene sulfonic acid-induced chronic colonic allodynia in the rat. J. Pharmacol. Exp. Ther. 302(3), 1013-1022 (2002). (Pubitemid 34920221)
82. Ravnefjord A, Brusberg M, Larsson H, Lindstrom E, Martinez V. Effects of pregabalin on visceral pain responses and colonic compliance in rats. Br. J. Pharmacol. 155(3), 407-416 (2008).
83. Mayer EA, Collins SM. Evolving pathophysiologic models of functional gastrointestinal disorders. Gastroenterology 122(7), 2032-2048 (2002). (Pubitemid 34651445)
84. Sabb FW, Bearden CE, Glahn DC, Parker DS, Freimer N, Bilder RM. A collaborative knowledge base for cognitive phenomics. Mol. Psychiatr. 13(4), 350-360 (2008). (Pubitemid 351399821)
85. Saito YA, Mitra N, Mayer EA. Genetic approaches to functional gastrointestinal disorders. Gastroenterology 138(4), 1276-1285 (2010).
86. Diatchenko L, Nackley AG, Tchivileva IE, Shabalina SA, Maixner W. Genetic architecture of human pain perception. Trends Genet. 23(12), 605-613 (2007). (Pubitemid 350186068)
87. North CS, Hong BA, Alpers DH. Relationship of functional gastrointestinal disorders and psychiatric disorders: Implications for treatment. World J. Gastroenterol. 13(14), 2020-2027 (2007). (Pubitemid 46795836)
88. Price DD, Zhou Q, Moshiree B, Robinson ME, Verne GN. Peripheral and central contributions to hyperalgesia in irritable bowel syndrome. J. Pain 7(8), 529-535 (2006). (Pubitemid 44119285)
89. Borsook D, Moulton EA, Schmidt KF, Becerra LR. Neuroimaging revolutionizes therapeutic approaches to chronic pain. Mol. Pain 3, 25 (2007).
90. Borsook D, Bleakman D, Hargreaves R, Upadhyay J, Schmidt KF, Becerra L. A ?BOLD? experiment in defining the utility of fMRI in drug development. Neuroimage 42(2), 461-466 (2008).
91. Mayer EA, Aziz Q, Coen S et al. Brain imaging approaches to the study of functional GI disorders: a Rome working team report. Neurogastroenterol. Motil. 21(6), 579-596 (2009).
92. Traub RJ, Silva E, Gebhart GF, Solodkin A. Noxious colorectal distention induced-c-Fos protein in limbic brain structures in the rat. Neurosci. Lett. 215(3), 165-168 (1996). (Pubitemid 26323452)
93. Stam R, Ekkelenkamp K, Frankhuijzen AC, Bruijnzeel AW, Akkermans LM, Wiegant VM. Long-lasting changes in central nervous system responsivity to colonic distention after stress in rats. Gastroenterology 123(4), 1216-1225 (2002).
94. Monnikes H, Ruter J, Konig M et al. Differential induction of c-Fos expression in brain nuclei by noxious and non-noxious colonic distension: role of afferent C-fibers and 5-HT3 receptors. Brain Res. 966(2), 253-264 (2003). (Pubitemid 36255588)
95. Martinez V, Wang L, Tache Y. Proximal colon distension induces Fos expression in the brain and inhibits gastric emptying through capsaicin-sensitive pathways in conscious rats. Brain Res. 1086(1), 168-180 (2006).
96. Monnikes H, Ruter J, Konig M et al. Differential induction of c-Fos expression in brain nuclei by noxious and non-noxious colonic distension: role of afferent C-fibers and 5-HT3 receptors. Brain Res. 21(966), 253-264 (2003). (Pubitemid 36255588)
97. Lazovic J, Wrzos HF, Yang QX et al. Regional activation in the rat brain during visceral stimulation detected by c-Fos expression and fMRI. Neurogastroenterol. Motil. 17(4), 548-556 (2005). (Pubitemid 41075997)
98. Zhai QZ, Traub RJ. The NMDA receptor antagonist MK-801 attenuates c-Fos expression in the lumbosacral spinal cord following repetitive noxious and non-noxious colorectal distention. Pain 83(2), 321-329 (1999). (Pubitemid 29479292)
99. Traub RJ, Stitt S, Gebhart GF. Attenuation of c-Fos expression in the rat lumbosacral spinal cord by morphine or tramadol following noxious colorectal distention. Brain Res. 701(1-2), 175-182 (1995).
100. Kozlowski CM, Green A, Grundy D, Boissonade FM, Bountra C. The 5-HT 3 receptor antagonist alosetron inhibits the colorectal distention induced depressor response and spinal c-Fos expression in the anaesthetised rat. Gut 46(4), 474-480 (2000). (Pubitemid 30305810)
101. Gao J, Wu X, Owyang C, Li Y. Enhanced responses of the anterior cingulate cortex neurones to colonic distension in viscerally hypersensitive rats. J. Physiol. 570(Pt 1), 169-183 (2006).
102. Al-Chaer ED, Lawand NB, Westlund KN, Willis WD. Visceral nociceptive input into the ventral posterolateral nucleus of the thalamus: a new function for the dorsal column pathway. J. Neurophysiol. 76(4), 2661-2674 (1996). (Pubitemid 26346438)
103. Ohashi K, Ichikawa K, Chen L, Callahan M, Zasadny K, Kurebayashi Y. MicroPET detection of regional brain activation induced by colonic distention in a rat model of visceral hypersensitivity. J. Vet. Med. Sci. 70(1), 43-49 (2008). (Pubitemid 351214399)
104. Wang Z, Bradesi S, Maarek J-MI et al. Regional brain activation in conscious, unrestrained rats in response to visceral pain. Pain 138(1), 233-243 (2008).
105. Wang Z, Guo Y, Bradesi S et al. Sex differences in functional brain activation during noxious visceral stimulation in rats. Pain 145(1-2), 120-128 (2009).
106. Craig AD. A rat is not a monkey is not a human: comment on Mogil (Nature Rev. Neurosci. 10, 283-294 (2009)). Nat. Rev. Neurosci. 10(6), 466 (2009).
107. Bradesi S, Eutamene H, Fioramonti J, Bueno L. Acute restraint stress activates functional NK1 receptor in the colon of female rats: involvement of steroids. Gut 50(3), 349-354 (2002). (Pubitemid 34161050)
108. Bradesi S, Schwetz I, Ennes HS et al. Repeated exposure to water avoidance stress in rats: A new model for sustained visceral hyperalgesia. Am. J. Physiol. Gastrointest. Liver Physiol. 289(1), G42-G53 (2005). (Pubitemid 40944222)
109. LaGraize SC, Borzan J, Peng YB, Fuchs PN. Selective regulation of pain affect following activation of the opioid anterior cingulate cortex system. Exp. Neurol. 197(1), 22-30 (2006). (Pubitemid 41817218)
110. Peyron R, Laurent B, Garcia-Larrea L. Functional imaging of brain responses to pain. A review and meta-analysis (2000). Neurophysiol. Clin. 30(5), 263-288 (2000).
111. Berman SM, Naliboff BD, Suyenobu B et al. Sex differences in regional brain response to aversive pelvic visceral stimuli. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291(2), R268-R276 (2006). (Pubitemid 44035631)
112. Naliboff BD, Berman S, Chang L et al. Sex-related differences in IBS patients: central processing of visceral stimuli. Gastroenterology 124(7), 1738-1747 (2003). (Pubitemid 36666770)
113. Berman S, Munakata J, Naliboff BD et al. Gender differences in regional brain response to visceral pressure in IBS patients. Eur. J. Pain 4(2), 157-172 (2000). (Pubitemid 30470027)
114. Wang Z, Bradesi S, Maarek JM et al. Regional brain activation in conscious, nonrestrained rats in response to noxious visceral stimulation. Pain 138(1), 233-243 (2008).
115. Wang Z BS, Charles J, Pang R et al. Assessment of functional brain activation in expectation of visceral pain in a rat step-down passive avoidance model. Gastroenterology 134(4 Suppl. 1), A-120 (2008).
116. Berman SM, Naliboff BD, Suyenobu B et al. Reduced brainstem inhibition during anticipated pelvic visceral pain correlates with enhanced brain response to the visceral stimulus in women with irritable bowel syndrome. J. Neurosci. 28(2), 349-359 (2008).
117. Sivarao DV, Langdon S, Bernard C, Lodge N. Colorectal distension-induced pseudoaffective changes as indices of nociception in the anesthetized female rat: morphine and strain effects on visceral sensitivity. J. Pharmacol. Toxicol. Methods 56(1), 43-50 (2007). (Pubitemid 46839195)
118. Gibney SM, Gosselin RD, Dinan TG, Cryan JF. Colorectal distension-induced prefrontal cortex activation in the Wistar-Kyoto rat: implications for irritable bowel syndrome. Neuroscience 165(3), 675-683 (2010).
119. Irwin C, Falsetti SA, Lydiard RB, Ballenger JC, Brock CD, Brener W. Comorbidity of posttraumatic stress disorder and irritable bowel syndrome. J. Clin. Psychiatr. 57(12), 576-578 (1996). (Pubitemid 27056899)
120. Levy RL, Cain KC, Jarrett M, Heitkemper MM. The relationship between daily life stress and gastrointestinal symptoms in women with irritable bowel syndrome. J. Behav. Med. 20(2), 177-193 (1997). (Pubitemid 27188127)
121. Ross CA. Childhood sexual abuse and psychosomatic symptoms in irritable bowel syndrome. J. Child. Sex. Abus. 14(1), 27-38 (2005). (Pubitemid 40770340)
122. Walker EA, Katon WJ, Roy-Byrne PP, Jemelka RP, Russo J. Histories of sexual victimization in patients with irritable bowel syndrome or inflammatory bowel disease. Am. J. Psychiatr. 150, 1502-1506 (1993). (Pubitemid 23289307)
123. Walter SA, Aardal-Eriksson E, Thorell LH, Bodemar G, Hallbook O. Pre-experimental stress in patients with irritable bowel syndrome: high cortisol values already before symptom provocation with rectal distensions. Neurogastroenterol. Motil. 18(12), 1069-1077 (2006). (Pubitemid 44748271)
124. Posserud I, Agerforz P, Ekman R, Bjornsson ES, Abrahamsson H, Simren M. Altered visceral perceptual and neuroendocrine response in patients with irritable bowel syndrome during mental stress. Gut 53(8), 1102-1108 (2004). (Pubitemid 38961962)
125. Dickhaus B, Mayer EA, Firooz N et al. Irritable bowel syndrome patients show enhanced modulation of visceral perception by auditory stress. Am. J. Gastroenterol. 98(1), 135-143 (2003). (Pubitemid 36135182)
126. Mayer EA, Naliboff BD, Chang L, Coutinho SV. Stress and the gastrointestinal tract: V. Stress and irritable bowel syndrome. Am. J. Physiol. Gastrointest. Liver Physiol. 280(4), G519-G524 (2001).
127. Murray CD, Flynn J, Ratcliffe L, Jacyna MR, Kamm MA, Emmanuel AV. Effect of acute physical and psychological stress on gut autonomic innervation in irritable bowel syndrome. Gastroenterology 127(6), 1695-1703 (2004). (Pubitemid 39575848)
128. Wang Z, Pang RD, Guo Y, Bradesi S, Mayer EA, Holschneider DP. Functional brain mapping of visceral hypersensitivity induced by chronic water avoidance stress in rats. Presented at: Annual Meeting of the Society for Neuroscience. San Diego, CA, USA, 13-17 November 2010 (Abstract 682.11/UU3).
129. McIntosh AR, Gonzalez-Lima F. Large-scale functional connectivity in associate learning: Interrelations of the rat auditory, visual, and limbic systems. J. Neurophysiol. 80(6), 3148-3162 (1998). (Pubitemid 29029241)
130. Labus JS, Naliboff BN, Fallon J et al. Sex differences in brain activity during aversive visceral stimulation and its expectation in patients with chronic abdominal pain: a network analysis. Neuroimage 41(3), 1032-1043 (2008).
131. Borsook D, Becerra L. Phenotyping central nervous system circuitry in chronic pain using functional MRI: considerations and potential implications in the clinic. Curr. Pain Headache Rep. 11(3), 201-207 (2007). (Pubitemid 46851250)
132. Wise RG, Tracey I. The role of fMRI in drug discovery. J. Magn. Reson. Imaging 23(6), 862-876 (2006). (Pubitemid 43825441)
133. Hess A, Sergejeva M, Budinsky L, Zeilhofer HU, Brune K. Imaging of hyperalgesia in rats by functional MRI. Eur. J. Pain 11(1), 109-119 (2007). (Pubitemid 44636282)
134. Becerra L, Harter K, Gonzalez RG, Borsook D. Functional magnetic resonance imaging measures of the effects of morphine on central nervous system circuitry in opioid-naive healthy volunteers. Anesth. Analg. 103(1), 208-216 (2006). (Pubitemid 44036061)
135. Moylan Governo RJ, Morris PG, Prior MJ, Marsden CA, Chapman V. Capsaicin-evoked brain activation and central sensitization in anaesthetised rats: a functional magnetic resonance imaging study. Pain 126(1-3), 35-45 (2006). (Pubitemid 44751954)
136. Tuor UI, McKenzie E, Tomanek B. Functional magnetic resonance imaging of tonic pain and vasopressor effects in rats. Magn. Reson. Imaging 20(10), 707-712 (2002). (Pubitemid 36245731)
137. Press release. Forest to Discontinue Development in US of Dexloxiglumide for Irritable Bowel Syndrome (IBS). 1 October 2003 www.prnewswire.com/news- releases/ forest-to-discontinue-development-in-us-of-dexloxiglumide-for- irritable-bowel-syndrome-ibs-72334602.html