Journal of Psychosomatic Research
Volume 68, Issue 5 , Pages 475-481 , May 2010

The future of neuroscientific research in functional gastrointestinal disorders: Integration towards multidimensional (visceral) pain endophenotypes?

  • Adam D. Farmer

      Affiliations

    • Neurogastroenterology Group, Wingate Institute of Neurogastroenterology, Centre for Gastroenterology, Blizzard Centre for Cell and Molecular Science, Barts and the London School of Medicine and Dentistry, Queen Mary University of London, London, UK
  • ,
  • Qasim Aziz

      Affiliations

    • Neurogastroenterology Group, Wingate Institute of Neurogastroenterology, Centre for Gastroenterology, Blizzard Centre for Cell and Molecular Science, Barts and the London School of Medicine and Dentistry, Queen Mary University of London, London, UK
  • ,
  • Jan Tack

      Affiliations

    • Department of Pathophysiology, Gastroenterology Section, University of Leuven, Belgium
  • ,
  • Lukas Van Oudenhove

      Affiliations

    • Department of Pathophysiology, Gastroenterology Section, University of Leuven, Belgium
    • Department of Neurosciences, Psychiatry Division, University of Leuven, Belgium
    • Corresponding Author InformationCorresponding author. Center for Gastroenterological Research, University of Leuven, University Hospital Gasthuisberg, O & N I, B-3000 Leuven, Belgium. Tel.: +32 16346387; fax: +32 16345939.

Received 3 November 2009 ,Revised 15 December 2009 ,Accepted 21 December 2009.

References 

  1. Wessely S, Nimnuan C, Sharpe M. Functional somatic syndromes: one or many?. Lancet. 1999;354:936–939
  2. Drossman DA. The functional gastrointestinal disorders and the Rome III process. Gastroenterology. 2006;130:1377–1390
  3. Drossman DA. Rome III: the functional gastrointestinal disorders. McLean, VA: Degnon Associates; 2006;
  4. Drossman DA, Li Z, Andruzzi E, Temple RD, Talley NJ, Thompson WG, et al. U.S. householder survey of functional gastrointestinal disorders. Prevalence, sociodemography, and health impact. Dig Dis Sci. 1993;38:1569–1580
  5. Levy RL, Olden KW, Naliboff BD, Bradley LA, Francisconi C, Drossman DA, et al. Psychosocial aspects of the functional gastrointestinal disorders. Gastroenterology. 2006;130:1447–1458
  6. Locke R, Weaver AL, Joseph Melton L, Talley NJ. Psychosocial factors are linked to functional gastrointestinal disorders: a population based nested case-control study. Am J Gastroenterol. 2004;99:350–357
  7. Leserman J, Drossman DA. Relationship of abuse history to functional gastrointestinal disorders and symptoms: some possible mediating mechanisms. Trauma Violence Abuse. 2007;8:331–343
  8. Henningsen P, Zimmermann T, Sattel H. Medically unexplained physical symptoms, anxiety, and depression: a meta-analytic review. Psychosom Med. 2003;65:528–533
  9. Mussell M, Kroenke K, Spitzer RL, Williams JB, Herzog W, Löwe B. Gastrointestinal symptoms in primary care: prevalence and association with depression and anxiety. J Psychosom Res. 2008;64:605–612
  10. Dorn SD, Palsson OS, Thiwan SI, Kanazawa M, Clark WC, van Tilburg MAL, et al. Increased colonic pain sensitivity in irritable bowel syndrome is the result of an increased tendency to report pain rather than increased neurosensory sensitivity. Gut. 2007;56:1202–1209
  11. Van Oudenhove L, Vandenberghe J, Geeraerts B, Vos R, Persoons P, Demyttenaere K, et al. Determinants of symptoms in functional dyspepsia: gastric sensorimotor function, psychosocial factors or somatization?. Gut. 2008;57:1666–1673
  12. Labus JS, Mayer EA, Chang L, Bolus R, Naliboff BD. The central role of gastrointestinal-specific anxiety in irritable bowel syndrome: further validation of the visceral sensitivity index. Psychosom Med. 2007;69:89–98
  13. Drossman DA, Corazziari E, Talley NJ, Thompson W, Whitehead WE. Rome II: a multinational consensus document on functional gastrointestinal disorders. Gut. 1999;45:1–81
  14. Engel GL. The need for a new medical model: a challenge for biomedicine. Science. 1977;196:129–136
  15. Vandenberghe J, Dupont P, Fischler B, Persoons P, Tack J. Regional brain activation during proximal stomach distention in man: a PET study. Gastroenterology. 2005;128:564–573
  16. Hobson AR, Aziz Q. Brain imaging and functional gastrointestinal disorders: has it helped our understanding?. Gut. 2004;53:1198–1206
  17. Gottesman II, Gould TD. The endophenotype concept in psychiatry: etymology and strategic intentions. Am J Psychiatry. 2003;160:636–645
  18. Barbara G, Stanghellini V, De Giorgio R, Corinaldesi R. Functional gastrointestinal disorders and mast cells: implications for therapy. Neurogastroenterol Motil. 2006;18:6–17
  19. Locke GR, Weaver AL, Melton LJ, Talley NJ. Psychosocial factors are linked to functional gastrointestinal disorders: a population based nested case-control study. Am J Gastroenterol. 2004;99:350–357
  20. Chrousos GP, Gold PW. The concepts of stress and stress system disorders. Overview of physical and behavioral homeostasis. JAMA. 1992;267:1244–1252
  21. Wener J, Morton HS, Polonsky A. The effects of vagotomy on colonic function; observations through a transverse colostomy in a patient with ulcerative colitis. Gastroenterology. 1952;22:250–256
  22. Glazebrook AJ. Functional disorders of small bowel after gastrectomy and vagotomy; correlation of radiographic and kymographic studies. Lancet. 1952;1:895–899
  23. Fukudo S, Suzuki J. Colonic motility, autonomic function, and gastrointestinal hormones under psychological stress on irritable bowel syndrome. Tohoku J Exp Med. 1987;151:373–385
  24. Smart HL, Atkinson M. Abnormal vagal function in irritable bowel syndrome. Lancet. 1987;2:475–478
  25. Paine P, Worthen SF, Gregory LJ, Thompson DG, Aziz Q. Personality differences affect brainstem autonomic responses to visceral pain. Neurogastroenterol Motil. 2009;
  26. Berntson GG, Bigger JT, Eckberg DL, Grossman P, Kaufmann PG, Malik M, et al. Heart rate variability: origins, methods, and interpretive caveats. Psychophysiology. 1997;34:623–648
  27. Julu PO. A linear scale for measuring vagal tone in man. J Auton Pharmacol. 1992;12:109–115
  28. Hamilton RM, McKechnie PS, Macfarlane PW. Can cardiac vagal tone be estimated from the 10-second ECG?. Int J Cardiol. 2004;95:109–115
  29. Tak LM, Riese H, de Bock GH, Manoharan A, Kok IC, Rosmalen JG. As good as it gets? A meta-analysis and systematic review of methodological quality of heart rate variability studies in functional somatic disorders. Biol Psychol. 2009;82:101–110
  30. Julu POO, Monro JA, Yeoh C. Pattern of autonomic disturbance in patients with functional gastrointestinal disorders. Neurogastroenterol Motil. 2009;21:51
  31. Paine P, Kishor J, Worthen SF, Gregory LJ, Aziz Q. Exploring relationships for visceral and somatic pain with autonomic control and personality. Pain. 2009;
  32. Thayer JF, Fischer JE. Heart rate variability, overnight urinary norepinephrine and C-reactive protein: evidence for the cholinergic anti-inflammatory pathway in healthy human adults. J Intern Med. 2009;265:439–447
  33. Sharma A, Paine P, Aziz Q. Autonomic nervous system responses to esophageal acidification predict inter-individual variability in the magnitude of sensitization. Gastroenterology. 2008;134:A556
  34. Phillips M, Gregory L, Cullen S, Coen S, Ng V, Andrew C, et al. The effect of negative emotional context on neural and behavioural responses to oesophageal stimulation. Brain. 2003;126:669–684
  35. Coen SJ, Yágüez L, Aziz Q, Mitterschiffthaler MT, Brammer M, Williams SCR, et al. Negative mood affects brain processing of visceral sensation. Gastroenterology. 2009;137:253–261.e2
  36. Gregory LJ, Yaguez L, Williams SCR, Altmann C, Coen SJ, Ng V, et al. Cognitive modulation of the cerebral processing of human oesophageal sensation using functional magnetic resonance imaging. Gut. 2003;52:1671–1677
  37. Coen SJ, Aziz Q, Yagüez L, Brammer M, Williams SCR, Gregory LJ. Effects of attention on visceral stimulus intensity encoding in the male human brain. Gastroenterology. 2008;135:2065–2074
  38. Labus JS, Naliboff BN, Fallon J, Berman SM, Suyenobu B, Bueller JA, et al. Sex differences in brain activity during aversive visceral stimulation and its expectation in patients with chronic abdominal pain: A network analysis. Neuroimage. 2008;41:1032–1043
  39. Elsenbruch S, Rosenberger C, Enck P, Forsting M, Schedlowski M, Gizewski ER. Affective disturbances modulate the neural processing of visceral pain stimuli in irritable bowel syndrome: an fMRI study. Gut. 2009;
  40. Van Oudenhove L, Psychobiological mechanisms in functional dyspepsia. converging evidence from psychophysiology and functional brain imaging? (doctoral thesis in medical sciences, University of Leuven). Leuven: Peeters, 2008.
  41. Van Oudenhove L, Vandenberghe J, Dupont P, Geeraerts B, Vos R, van Laere K, et al. Cortical deactivations during gastric fundus distension in health: visceral pain-specific response or attenuation of “default mode” brain function? a H215O-PET study. Neurogastroenterol Motil. 2009;21:259–271
  42. Levy RL, Jones KR, Whitehead WE, Feld SI, Talley NJ, Corey LA. Irritable bowel syndrome in twins: heredity and social learning both contribute to etiology. Gastroenterology. 2001;121:799–804
  43. Kalantar JS, Locke GR, Zinsmeister AR, Beighley CM, Talley NJ. Familial aggregation of irritable bowel syndrome: a prospective study. Gut. 2003;52:1703–1707
  44. Bengtson MB, Ronning T, Vatn MH, Harris JR. Irritable bowel syndrome in twins: genes and environment. Gut. 2006;55:1754–1759
  45. Camilleri M. Genetics and irritable bowel syndrome: from genomics to intermediate phenotype and pharmacogenetics. Dig Dis Sci. 2009;54:2318–2324
  46. Camilleri M, Carlson P, McKinzie S, Grudell A, Busciglio I, Burton D, et al. Genetic variation in endocannabinoid metabolism, gastrointestinal motility, and sensation. Am J Physiol Gastrointest Liver Physiol. 2008;294:G13–G19
  47. Fukudo S, Kanazawa M, Mizuno T, Hamaguchi T, Kano M, Watanabe S, et al. Impact of serotonin transporter gene polymorphism on brain activation by colorectal distention. Neuroimage. 2009;47:946–951
  48. D'Amato M, Bruce S, Bresso F, Zucchelli M, Ezer S, Pulkkinen V, et al. Neuropeptide s receptor 1 gene polymorphism is associated with susceptibility to inflammatory bowel disease. Gastroenterology. 2007;133:808–817
  49. Camilleri M, Atanasova E, Carlson PJ, Ahmad U, Kim HJ, Viramontes BE, et al. Serotonin-transporter polymorphism pharmacogenetics in diarrhea-predominant irritable bowel syndrome. Gastroenterology. 2002;123:425–432
  50. Li Y, Nie Y, Xie J, Tang W, Liang P, Sha W, et al. The association of serotonin transporter genetic polymorphisms and irritable bowel syndrome and its influence on tegaserod treatment in Chinese patients. Dig Dis Sci. 2007;52:2942–2949
  51. van Heel DA, Franke L, Hunt KA, Gwilliam R, Zhernakova A, Inouye M, et al. A genome-wide association study for celiac disease identifies risk variants in the region harboring IL2 and IL21. Nat Genet. 2007;39:827–829

PII: S0022-3999(09)00544-3

doi: 10.1016/j.jpsychores.2009.12.006

Journal of Psychosomatic Research
Volume 68, Issue 5 , Pages 475-481 , May 2010