Small bowel homing T cells are associated with symptoms and delayed gastric emptying in functional dyspepsia

American Journal of Gastroenterology

Volumn 106, Issue 6, 2011, Pages 1089-1098

  Liebregts, Tobias ^a,b   Adam, Birgit ^a,b   Bredack, Christoph ^b   Gururatsakul, Montri ^b,c   Pilkington, Katherine R ^d   Brierley, Stuart M ^b   Blackshaw, L Ashley ^b   Gerken, Guido ^a   Talley, Nicholas J ^e   Holtmann, Gerald ^c,f  

^a UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^b HANSON INSTITUTE   (Australia)

^c UNIVERSITY OF ADELAIDE   (Australia)

^d INSTITUTE OF MEDICAL AND VETERINARY SCIENCE   (Australia)

^e UNIVERSITY OF NEWCASTLE   (Australia)

^f UNIVERSITY HOSPITAL ESSEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA4 INTEGRIN; BETA7 INTEGRIN; CHEMOKINE RECEPTOR CCR9; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ABDOMINAL CRAMP; ADULT; ARTICLE; CD4+ T LYMPHOCYTE; CELL CULTURE; CELL ISOLATION; CONTROLLED STUDY; CYTOKINE RELEASE; DENSITY GRADIENT CENTRIFUGATION; DISEASE SEVERITY; DYSPEPSIA; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; IRRITABLE COLON; LYMPHOCYTE HOMING; MAJOR CLINICAL STUDY; MALE; NAUSEA; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; STOMACH EMPTYING; STOMACH PAIN; STOMACH SCINTISCANNING; T LYMPHOCYTE; VOMITING;

ADULT; BIOPSY, NEEDLE; CASE-CONTROL STUDIES; CELLS, CULTURED; CYTOKINES; DYSPEPSIA; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GASTRIC EMPTYING; HUMANS; INTERLEUKIN-10; INTERLEUKIN-1BETA; INTERLEUKIN-6; INTESTINE, SMALL; IRRITABLE BOWEL SYNDROME; LEUKOCYTES, MONONUCLEAR; MALE; MIDDLE AGED; RECEPTORS, LYMPHOCYTE HOMING; REFERENCE VALUES; SENSITIVITY AND SPECIFICITY; SEVERITY OF ILLNESS INDEX; TIME FACTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 79957997895     PISSN: 00029270     EISSN: 15720241     Source Type: Journal    
DOI: 10.1038/ajg.2010.512     Document Type: Article

References (60)

1. Wilson S, Roberts L, Roalfe A et al. Prevalence of irritable bowel syndrome: a community survey. Br J Gen Pract 2004; 54: 495-502. (Pubitemid 38931344)
2. Mitchell CM, Drossman DA. Survey of the AGA membership relating to patients with functional gastrointestinal disorders. Gastroenterology 1987; 92 (5 Part 1): 1282-4.
3. Drossman DA, Li Z, Andruzzi E et al. U.S. householder survey of functional gastrointestinal disorders. Prevalence, sociodemography, and health impact. Dig Dis Sci 1993; 38: 1569-80. (Pubitemid 23271409)
4. Mearin F, Perez-Oliveras M, Perello A et al. Dyspepsia and irritable bowel syndrome aft er a Salmonella gastroenteritis outbreak: one-year follow-up cohort study. Gastroenterology 2005; 129: 98-104. (Pubitemid 41002046)
5. O ' Mahony L, McCarthy J, Kelly P et al. Lactobacillus and bifi dobacterium in irritable bowel syndrome: symptom responses and relationship to cytokine profi les. Gastroenterology 2005; 128: 541-51. (Pubitemid 40585355)
6. Liebregts T, Adam B, Bredack C et al. Immune activation in patients with irritable bowel syndrome. Gastroenterology 2007; 132: 913-20. (Pubitemid 46440872)
7. Spiller RC, Jenkins D, Th ornley JP et al. Increased rectal mucosal enteroendocrine cells, T lymphocytes, and increased gut permeability following acute Campylobacter enteritis and in post-dysenteric irritable bowel syndrome. Gut 2000; 47: 804-11.
8. Gwee KA, Collins SM, Read NW et al. Increased rectal mucosal expression of interleukin 1beta in recently acquired post-infectious irritable bowel syndrome. Gut 2003; 52: 523-6. (Pubitemid 36363405)
9. Meenan J, Spaans J, Grool TA et al. Altered expression of alpha 4 beta 7, a gut homing integrin, by circulating and mucosal T cells in colonic mucosal infl ammation. Gut 1997; 40: 241-6. (Pubitemid 27093101)
10. Mora JR, von Andrian UH. T-cell homing specifi city and plasticity: new concepts and future challenges. Trends Immunol 2006; 27: 235-43. (Pubitemid 44308124)
11. Papadakis KA, Landers C, Prehn J et al. Chemokine receptor 9 expression defi nes a subset of peripheral blood lymphocytes with mucosal T cell phenotype and Th 1 or T-regulatory 1 cytokine profi le. J Immunol 2003; 171: 159-65. (Pubitemid 36745284)
12. Wurbel MA, Malissen M, Guy-Grand D et al. Mice lacking the CCR9 CCchemokine receptor show a mild impairment of early T- and B-cell development and a reduction in T-cell receptor gammadelta(+) gut intraepithelial lymphocytes. Blood 2001; 98: 2626-32.
13. Saruta M, Yu QT, Avanesyan A et al. Phenotype and Effector function of CC chemokine receptor 9-expressing lymphocytes in small intestinal Crohn's disease. J Immunol 2007; 178: 3293-300. (Pubitemid 46333214)
14. Talley NJ, Stanghellini V, Heading RC et al. Functional gastroduodenal disorders. Gut 1999; 45 (Suppl 2): II37-42. (Pubitemid 29434811)
15. Th ompson WG, Longstreth GF, Drossman DA et al. Functional bowel disorders and functional abdominal pain. Gut 1999; 45 (Suppl 2): II43-7. (Pubitemid 29434812)
16. Adam B, Liebregts T, Saadat-Gilani K et al. Validation of the gastrointestinal symptom score for the assessment of symptoms in patients with functional dyspepsia. Aliment Pharmacol Ther 2005; 22: 357-63. (Pubitemid 41207466)
17. Zigmond AS, Snaith RP. The hospital anxiety and depression scale. Acta Psychiatr Scand 1983; 67: 361-70. (Pubitemid 13098606)
18. Collins PJ, Horowitz M, Cook DJ et al. Gastric emptying in normal subjects - a reproducible technique using a single scintillation camera and computer system. Gut 1983; 24: 1117-25. (Pubitemid 14205812)
19. Collins PJ, Horowitz M, Shearman DJ et al. Correction for tissue attenuation in radionuclide gastric emptying studies: a comparison of a lateral image method and a geometric mean method. Br J Radiol 1984; 57: 689-95. (Pubitemid 14053194)
20. Dinan TG, Quigley EM, Ahmed SM et al. Hypothalamic-pituitary-gut axis dysregulation in irritable bowel syndrome: plasma cytokines as a potential biomarker? Gastroenterology 2006; 130: 304-11. (Pubitemid 43202030)
21. Dinan TG, Clarke G, Quigley EM et al. Enhanced cholinergic-mediated increase in the pro-infl ammatory cytokine IL-6 in irritable bowel syndrome: role of muscarinic receptors. Am J Gastroenterol 2008; 103: 2570-6.
22. Van Der Veek PP, Van Den BM, de Kroon YE et al. Role of tumor necrosis factor-alpha and interleukin-10 gene polymorphisms in irritable bowel syndrome. Am J Gastroenterol 2005; 100: 2510-6.
23. Kindt S, Van Oudenhove L, Broekaert D et al. Immune dysfunction in patients with functional gastrointestinal disorders. Neurogastroenterol Motil 2009; 21: 389-98.
24. Scully P, McKernan DP, Keohane J et al. Plasma cytokine profi les in females with irritable bowel syndrome and extra-intestinal co-morbidity. Am J Gastroenterol 2010; 105: 2235-43.
25. Barbara G, Stanghellini V, De Giorgio R et al. Activated mast cells in proximity to colonic nerves correlate with abdominal pain in irritable bowel syndrome. Gastroenterology 2004; 126: 693-702. (Pubitemid 38298317)
26. Holmen N, Isaksson S, Simren M et al. CD4+CD25+ regulatory T cells in irritable bowel syndrome patients. Neurogastroenterol Motil 2007; 19: 119-25. (Pubitemid 46130785)
27. Ohman L, Isaksson S, Lindmark AC et al. T-cell activation in patients with irritable bowel syndrome. Am J Gastroenterol 2009; 104: 1205-12.
28. Hall W, Buckley M, Crotty P et al. Gastric mucosal mast cells are increased in Helicobacter pylori-negative functional dyspepsia. Clin Gastroenterol Hepatol 2003; 1: 363-9. (Pubitemid 37248055)
29. Walker MM, Talley NJ, Prabhakar M et al. Duodenal mastocytosis, eosinophilia and intraepithelial lymphocytosis as possible disease markers in the irritable bowel syndrome and functional dyspepsia. Aliment Pharmacol Ther 2009; 29: 765-73.
30. Talley NJ, Walker MM, Aro P et al. Non-ulcer dyspepsia and duodenal eosinophilia: an adult endoscopic population-based case-control study. Clin Gastroenterol Hepatol 2007; 5: 1175-83. (Pubitemid 47488962)
31. Kindt S, Tertychnyy A, de Hertogh G et al. Intestinal immune activation in presumed post-infectious functional dyspepsia. Neurogastroenterol Motil 2009; 21: 832-e56.
32. Kunkel EJ, Campbell JJ, Haraldsen G et al. Lymphocyte CC chemokine receptor 9 and epithelial thymus-expressed chemokine (TECK) expression distinguish the small intestinal immune compartment: epithelial expression of tissue-specifi c chemokines as an organizing principle in regional immunity . J Exp Med 2000; 192: 761-8.
33. Gotteland M, Lopez M, Munoz C et al. Local and systemic liberation of proinfl ammatory cytokines in ulcerative colitis. Dig Dis Sci 1999; 44: 830-5. (Pubitemid 29186332)
34. Kucharzik T, Stoll R, Lugering N et al. Circulating antiinfl ammatory cytokine IL-10 in patients with infl ammatory bowel disease (IBD). Clin Exp Immunol 1995; 100: 452-6.
35. Gasche C, Bakos S, Dejaco C et al. IL-10 secretion and sensitivity in normal human intestine and infl ammatory bowel disease. J Clin Immunol 2000; 20: 362-70.
36. Windle HJ, Ang YS, Athie-Morales V et al. Human peripheral and gastric lymphocyte responses to Helicobacter pylori NapA and AphC diff er in infected and uninfected individuals. Gut 2005; 54: 25-32. (Pubitemid 40007214)
37. Enarsson K, Brisslert M, Backert S et al. Helicobacter pylori induces transendothelial migration of activated memory T cells. Infect Immun 2005; 73: 761-9. (Pubitemid 40165731)
38. Papadakis KA, Prehn J, Moreno ST et al. CCR9-positive lymphocytes and thymus-expressed chemokine distinguish small bowel from colonic Crohn's disease. Gastroenterology 2001; 121: 246-54. (Pubitemid 32729371)
39. Nakamura M, Saito H, Kasanuki J et al. Cytokine production in patients with infl ammatory bowel disease. Gut 1992; 33: 933-7.
40. Holtkamp W, Stollberg T, Reis HE. Serum interleukin-6 is related to disease activity but not disease specifi city in infl ammatory bowel disease. J Clin Gastroenterol 1995; 20: 123-6.
41. Gross V, Andus T, Caesar I et al. Evidence for continuous stimulation of interleukin- 6 production in Crohn's disease. Gastroenterology 1992; 102: 514-9.
42. Cremon C, Gargano L, Morselli-Labate AM et al. Mucosal immune activation in irritable bowel syndrome: gender-dependence and association with digestive symptoms. Am J Gastroenterol 2009; 104: 392-400.
43. Choung RS, Locke GR III, Zinsmeister AR et al. Psychosocial distress and somatic symptoms in community subjects with irritable bowel syndrome: a psychological component is the rule. Am J Gastroenterol 2009; 104: 1772-9.
44. Van Oudenhove L, Vandenberghe J, Geeraerts B et al. Determinants of symptoms in functional dyspepsia: gastric sensorimotor function, psychosocial factors or somatisation? Gut 2008; 57: 1666-73.
45. Liebregts T, Adam B, Bertel A et al. Psychological stress and the severity of post-infl ammatory visceral hyperalgesia. Eur J Pain 2007; 11: 216-22. (Pubitemid 44820899)
46. Maes M, Song C, Lin A et al. The Effects of psychological stress on humans: increased production of pro-infl ammatory cytokines and a Th 1-like response in stress-induced anxiety. Cytokine 1998; 10: 313-8. (Pubitemid 28227076)
47. Soderholm JD, Yang PC, Ceponis P et al. Chronic stress induces mast celldependent bacterial adherence and initiates mucosal infl ammation in rat intestine. Gastroenterology 2002; 123: 1099-108.
48. Mawdsley JE, Macey MG, Feakins RM et al. The Effect of acute psychologic stress on systemic and rectal mucosal measures of infl ammation in ulcerative colitis. Gastroenterology 2006; 131: 410-9. (Pubitemid 44142453)
49. Lyte M, Li W, Opitz N et al. Induction of anxiety-like behavior in mice during the initial stages of infection with the agent of murine colonic hyperplasia Citrobacter rodentium. Physiol Behav 2006; 89: 350-7. (Pubitemid 44436313)
50. Bercik P, Verdu EF, Foster JA et al. Chronic gastrointestinal infl ammation induces anxiety-like behavior and alters central nervous system biochemistry in mice. Gastroenterology 2010; 139: 2102-12.
51. Chrousos GP. The hypothalamic-pituitary-adrenal axis and immune-mediated infl ammation. N Engl J Med 1995; 332: 1351-62.
52. Chang L, Sundaresh S, Elliott J et al. Dysregulation of the hypothalamic-pituitary- adrenal (HPA) axis in irritable bowel syndrome. Neurogastroenterol Motil 2009; 21: 149-59.
53. Brebner K, Hayley S, Zacharko R et al. Synergistic Effects of interleukin- 1beta, interleukin-6, and tumor necrosis factor-alpha: central monoamine, corticosterone, and behavioral variations. Neuropsychopharmacology 2000; 22: 566-80. (Pubitemid 30219401)
54. Suto G, Kiraly A, Tache Y. Interleukin 1 beta inhibits gastric emptying in rats: mediation through prostaglandin and corticotropin-releasing factor. Gastroenterology 1994; 106: 1568-75.
55. Emch GS, Hermann GE, Rogers RC. TNF-alpha activates solitary nucleus neurons responsive to gastric distension. Am J Physiol Gastrointest Liver Physiol 2000; 279: G582-6.
56. Kindt S, Vanden Berghe P, Boesmans W et al. Prolonged IL-1beta exposure alters neurotransmitter and electrically induced Ca(2+) responses in the myenteric plexus. Neurogastroenterol Motil 2010; 22: 321-e85.
57. Gschossmann JM, Adam B, Liebregts T et al. Effect of transient chemically induced colitis on the visceromotor response to mechanical colorectal distension. Eur J Gastroenterol Hepatol 2002; 14: 1067-72. (Pubitemid 35178766)
58. Liebregts T, Adam B, Bertel A et al. Effect of E. coli Nissle 1917 on postinfl ammatory visceral sensory function in a rat model. Neurogastroenterol Motil 2005; 17: 410-4. (Pubitemid 40768913)
59. Adam B, Liebregts T, Gschossmann JM et al. Severity of mucosal infl ammation as a predictor for alterations of visceral sensory function in a rat model. Pain 2006; 123: 179-86. (Pubitemid 43816772)
60. Hughes PA, Brierley SM, Martin CM et al. TRPV1-expressing sensory fi bres and IBS: links with immune function. Gut 2009; 58: 465-6.