Korean J Gastroenterol.  2022 Jan;79(1):4-11. 10.4166/kjg.2022.001.

Functional Gastrointestinal Disorders in Patients with Inflammatory Bowel Disease

Affiliations
  • 1Department of Internal Medicine, Yeungnam University College of Medicine, Daegu, Korea

Abstract

With emerging more effective drugs, the therapeutic goal of inflammatory bowel disease (IBD) has progressed from clinical remission to mucosal healing. Although the inflammation could be controlled more effectively than before, symptoms such as abdominal pain and bowel habit change is still bothersome to some IBD patients. Recently, these “refractory functional gastrointestinal symptoms” in quiescent IBD patients has been paid more attention. The pathophysiology could be multifactorial with genetics, change in gut motility associated with post inflammatory condition, increased permeability, impaired colorectal function, visceral hypersensitivity and gut microbiota. Because both IBD and functional gastrointestinal disease (FGID) could share similar symptoms and some pathophysiology, it is sometimes challenging to distinguish them exactly. However, to reduce the risk of overtreatment or insufficient control of inflammation, exact diagnosis of functional disease or symptoms in quiescent IBD patients is important. Because there is limited randomized controlled trials or prospective study currently, most of the therapeutic approach in IBD patients are empirical or referred to those of functional gastrointestinal disorders. However, approaches based on pathophysiological mechanisms could give appropriate therapies for both IBD and FGIDs.

Keyword

Inflammatory bowel diseases; Irritable bowel syndrome; Gastrointestinal disorder; functional; Pathogenesis; Abdominal pain

Figure

  • Fig. 1 Potential common pathogenesis in irritable bowel syndrome and inflammatory bowel disease.


Reference

1. Lacy BE, Fermin M, Chang L, et al. 2016; Bowel Disorders. Gastroenterology. 150:1393–1407.e5. DOI: 10.1053/j.gastro.2016.02.031. PMID: 27144627.
Article
2. Kim JM, Cheon JH. 2020; Pathogenesis and clinical perspectives of extraintestinal manifestations in inflammatory bowel diseases. Intest Res. 18:249–264. DOI: 10.5217/ir.2019.00128. PMID: 32295331. PMCID: PMC7385581.
Article
3. Turner D, Ricciuto A, Lewis A, et al. 2021; STRIDE-II: An Update on the Selecting Therapeutic Targets in Inflammatory Bowel Disease (STRIDE) Initiative of the International Organization for the Study of IBD (IOIBD): Determining Therapeutic Goals for Treat-to-Target strategies in IBD. Gastroenterology. 160:1570–1583. DOI: 10.1053/j.gastro.2020.12.031. PMID: 33359090.
Article
4. Ryu KH, Huh KC. 2010; Irritable Bowel Syndrome in Inflammatory Bowel Disease. Intest Res. 8:95–105. DOI: 10.5217/ir.2010.8.2.95.
Article
5. Vasant DH, Ford AC. 2020; Functional gastrointestinal disorders in inflammatory bowel disease: Time for a paradigm shift? World J Gastroenterol. 26:3712–3719. DOI: 10.3748/wjg.v26.i26.3712. PMID: 32774052. PMCID: PMC7383849.
Article
6. Peyrin-Biroulet L, Reinisch W, Colombel JF, et al. 2014; Clinical disease activity, C-reactive protein normalisation and mucosal healing in Crohn's disease in the SONIC trial. Gut. 63:88–95. DOI: 10.1136/gutjnl-2013-304984. PMID: 23974954.
Article
7. Colombel JF, Shin A, Gibson PR. 2019; AGA Clinical Practice Update on Functional Gastrointestinal Symptoms in Patients With Inflammatory Bowel Disease: Expert Review. Clin Gastroenterol Hepatol. 17:380–390.e1. DOI: 10.1016/j.cgh.2018.08.001. PMID: 30099108. PMCID: PMC6581193.
Article
8. Halpin SJ, Ford AC. 2012; Prevalence of symptoms meeting criteria for irritable bowel syndrome in inflammatory bowel disease: systematic review and meta-analysis. Am J Gastroenterol. 107:1474–1482. DOI: 10.1038/ajg.2012.260. PMID: 22929759.
Article
9. Jonefjäll B, Strid H, Ohman L, Svedlund J, Bergstedt A, Simren M. 2013; Characterization of IBS-like symptoms in patients with ulcerative colitis in clinical remission. Neurogastroenterol Motil. 25:756–e578. DOI: 10.1111/nmo.12163. PMID: 23731196.
Article
10. Drossman DA. 2005; Functional GI disorders: what's in a name? Gastroenterology. 128:1771–1772. DOI: 10.1053/j.gastro.2005.04.020. PMID: 15940609.
Article
11. Drossman DA. 2006; Functional versus organic: an inappropriate dichotomy for clinical care. Am J Gastroenterol. 101:1172–1175. DOI: 10.1111/j.1572-0241.2006.00592.x. PMID: 16771931.
Article
12. Quigley EM. 2005; Irritable bowel syndrome and inflammatory bowel disease: interrelated diseases? Chin J Dig Dis. 6:122–132. DOI: 10.1111/j.1443-9573.2005.00202.x. PMID: 16045602.
Article
13. Barbara G, Cremon C, Carini G, et al. 2011; The immune system in irritable bowel syndrome. J Neurogastroenterol Motil. 17:349–359. DOI: 10.5056/jnm.2011.17.4.349. PMID: 22148103. PMCID: PMC3228974.
Article
14. Cenac N, Andrews CN, Holzhausen M, et al. 2007; Role for protease activity in visceral pain in irritable bowel syndrome. J Clin Invest. 117:636–647. DOI: 10.1172/JCI29255. PMID: 17304351. PMCID: PMC1794118.
Article
15. Barbara G, Wang B, Stanghellini V, et al. 2007; Mast cell-dependent excitation of visceral-nociceptive sensory neurons in irritable bowel syndrome. Gastroenterology. 132:26–37. DOI: 10.1053/j.gastro.2006.11.039. PMID: 17241857.
Article
16. Barbara G, Stanghellini V, De Giorgio R, et al. 2004; Activated mast cells in proximity to colonic nerves correlate with abdominal pain in irritable bowel syndrome. Gastroenterology. 126:693–702. DOI: 10.1053/j.gastro.2003.11.055. PMID: 14988823.
Article
17. Matricon J, Meleine M, Gelot A, et al. 2012; Review article: Associations between immune activation, intestinal permeability and the irritable bowel syndrome. Aliment Pharmacol Ther. 36:1009–1031. DOI: 10.1111/apt.12080. PMID: 23066886.
Article
18. Mawdsley JE, Rampton DS. 2006; The role of psychological stress in inflammatory bowel disease. Neuroimmunomodulation. 13:327–336. DOI: 10.1159/000104861. PMID: 17709955.
Article
19. Mulak A, Bonaz B. 2004; Irritable bowel syndrome: a model of the brain-gut interactions. Med Sci Monit. 10:RA55–RA62. PMID: 15260348.
20. Posserud I, Agerforz P, Ekman R, Björnsson ES, Abrahamsson H, Simrén M. 2004; Altered visceral perceptual and neuroendocrine response in patients with irritable bowel syndrome during mental stress. Gut. 53:1102–1108. DOI: 10.1136/gut.2003.017962. PMID: 15247175. PMCID: PMC1774150.
Article
21. Böhmelt AH, Nater UM, Franke S, Hellhammer DH, Ehlert U. 2005; Basal and stimulated hypothalamic-pituitary-adrenal axis activity in patients with functional gastrointestinal disorders and healthy controls. Psychosom Med. 67:288–294. DOI: 10.1097/01.psy.0000157064.72831.ba. PMID: 15784796.
Article
22. Dinan TG, Quigley EM, Ahmed SM, et al. 2006; Hypothalamic-pituitary-gut axis dysregulation in irritable bowel syndrome: plasma cytokines as a potential biomarker? Gastroenterology. 130:304–311. DOI: 10.1053/j.gastro.2005.11.033. PMID: 16472586.
Article
23. Fukudo S, Nomura T, Hongo M. 1998; Impact of corticotropin-releasing hormone on gastrointestinal motility and adrenocorticotropic hormone in normal controls and patients with irritable bowel syndrome. Gut. 42:845–849. DOI: 10.1136/gut.42.6.845. PMID: 9691924. PMCID: PMC1727153.
Article
24. Taché Y, Perdue MH. 2004; Role of peripheral CRF signalling pathways in stress-related alterations of gut motility and mucosal function. Neurogastroenterol Motil. 16(Suppl 1):137–142. DOI: 10.1111/j.1743-3150.2004.00490.x. PMID: 15066020.
Article
25. Vanuytsel T, van Wanrooy S, Vanheel H, et al. 2014; Psychological stress and corticotropin-releasing hormone increase intestinal permeability in humans by a mast cell-dependent mechanism. Gut. 63:1293–1299. DOI: 10.1136/gutjnl-2013-305690. PMID: 24153250.
Article
26. Sagami Y, Shimada Y, Tayama J, et al. 2004; Effect of a corticotropin releasing hormone receptor antagonist on colonic sensory and motor function in patients with irritable bowel syndrome. Gut. 53:958–964. DOI: 10.1136/gut.2003.018911. PMID: 15194643. PMCID: PMC1774093.
Article
27. Welgan P, Meshkinpour H, Beeler M. 1988; Effect of anger on colon motor and myoelectric activity in irritable bowel syndrome. Gastroenterology. 94:1150–1156. DOI: 10.1016/0016-5085(88)90006-6. PMID: 3350284.
Article
28. Evans PR, Bak YT, Shuter B, Hoschl R, Kellow JE. 1997; Gastroparesis and small bowel dysmotility in irritable bowel syndrome. Dig Dis Sci. 42:2087–2093. DOI: 10.1023/A:1018874602790. PMID: 9365140.
29. Camilleri M, Ford MJ. 1994; Functional gastrointestinal disease and the autonomic nervous system: a way ahead? Gastroenterology. 106:1114–1118. DOI: 10.1016/0016-5085(94)90775-7. PMID: 8143980.
Article
30. Jostins L, Ripke S, Weersma RK, et al. 2012; Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature. 491:119–124. DOI: 10.1038/nature11582. PMID: 23128233. PMCID: PMC3491803.
31. Swan C, Duroudier NP, Campbell E, et al. 2013; Identifying and testing candidate genetic polymorphisms in the irritable bowel syndrome (IBS): association with TNFSF15 and TNFα. Gut. 62:985–994. DOI: 10.1136/gutjnl-2011-301213. PMID: 22684480.
Article
32. Labus JS, Dinov ID, Jiang Z, et al. 2014; Irritable bowel syndrome in female patients is associated with alterations in structural brain networks. Pain. 155:137–149. DOI: 10.1016/j.pain.2013.09.020. PMID: 24076048. PMCID: PMC4100785.
Article
33. Srinath AI, Walter C, Newara MC, Szigethy EM. 2012; Pain management in patients with inflammatory bowel disease: insights for the clinician. Therap Adv Gastroenterol. 5:339–357. DOI: 10.1177/1756283X12446158. PMID: 22973418. PMCID: PMC3437534.
Article
34. Major G, Spiller R. 2014; Irritable bowel syndrome, inflammatory bowel disease and the microbiome. Curr Opin Endocrinol Diabetes Obes. 21:15–21. DOI: 10.1097/MED.0000000000000032. PMID: 24296462. PMCID: PMC3871405.
Article
35. Cader MZ, Kaser A. 2013; Recent advances in inflammatory bowel disease: mucosal immune cells in intestinal inflammation. Gut. 62:1653–1664. DOI: 10.1136/gutjnl-2012-303955. PMID: 24104886.
Article
36. Rajilić-Stojanović M, Shanahan F, Guarner F, de Vos WM. 2013; Phylogenetic analysis of dysbiosis in ulcerative colitis during remission. Inflamm Bowel Dis. 19:481–488. DOI: 10.1097/MIB.0b013e31827fec6d. PMID: 23385241.
Article
37. Spiller R, Garsed K. 2009; Postinfectious irritable bowel syndrome. Gastroenterology. 136:1979–1988. DOI: 10.1053/j.gastro.2009.02.074. PMID: 19457422. PMCID: PMC8803069.
Article
38. Porter CK, Tribble DR, Aliaga PA, Halvorson HA, Riddle MS. 2008; Infectious gastroenteritis and risk of developing inflammatory bowel disease. Gastroenterology. 135:781–786. DOI: 10.1053/j.gastro.2008.05.081. PMID: 18640117.
Article
39. Jeffery IB, O'Toole PW, Öhman L, et al. 2012; An irritable bowel syndrome subtype defined by species-specific alterations in faecal microbiota. Gut. 61:997–1006. DOI: 10.1136/gutjnl-2011-301501. PMID: 22180058.
Article
40. Carroll IM, Ringel-Kulka T, Ferrier L, et al. 2013; Fecal protease activity is associated with compositional alterations in the intestinal microbiota. PLoS One. 8:e78017. DOI: 10.1371/journal.pone.0078017. PMID: 24147109. PMCID: PMC3798377.
Article
41. Shutkever O, Gracie DJ, Young C, et al. 2018; No Significant Association Between the Fecal Microbiome and the Presence of Irritable Bowel Syndrome-type Symptoms in Patients with Quiescent Inflammatory Bowel Disease. Inflamm Bowel Dis. 24:1597–1605. DOI: 10.1093/ibd/izy052. PMID: 29668957.
Article
42. Vivinus-Nébot M, Frin-Mathy G, Bzioueche H, et al. 2014; Functional bowel symptoms in quiescent inflammatory bowel diseases: role of epithelial barrier disruption and low-grade inflammation. Gut. 63:744–752. DOI: 10.1136/gutjnl-2012-304066. PMID: 23878165.
Article
43. Salim SY, Söderholm JD. 2011; Importance of disrupted intestinal barrier in inflammatory bowel diseases. Inflamm Bowel Dis. 17:362–381. DOI: 10.1002/ibd.21403. PMID: 20725949.
Article
44. Piche T. 2014; Tight junctions and IBS--the link between epithelial permeability, low-grade inflammation, and symptom generation? Neurogastroenterol Motil. 26:296–302. DOI: 10.1111/nmo.12315. PMID: 24548256.
Article
45. Piche T, Barbara G, Aubert P, et al. 2009; Impaired intestinal barrier integrity in the colon of patients with irritable bowel syndrome: involvement of soluble mediators. Gut. 58:196–201. DOI: 10.1136/gut.2007.140806. PMID: 18824556.
Article
46. Camilleri M. 2012; Peripheral mechanisms in irritable bowel syndrome. N Engl J Med. 367:1626–1635. DOI: 10.1056/NEJMra1207068. PMID: 23094724.
Article
47. Martínez C, Lobo B, Pigrau M, et al. 2013; Diarrhoea-predominant irritable bowel syndrome: an organic disorder with structural abnormalities in the jejunal epithelial barrier. Gut. 62:1160–1168. DOI: 10.1136/gutjnl-2012-302093. PMID: 22637702.
Article
48. Barbara G, Cremon C, Stanghellini V. 2014; Inflammatory bowel disease and irritable bowel syndrome: similarities and differences. Curr Opin Gastroenterol. 30:352–358. DOI: 10.1097/MOG.0000000000000070. PMID: 24811054.
49. Zhou SY, Gillilland M 3rd, Wu X, et al. 2018; FODMAP diet modulates visceral nociception by lipopolysaccharide-mediated intestinal inflammation and barrier dysfunction. J Clin Invest. 128:267–280. DOI: 10.1172/JCI92390. PMID: 29202473. PMCID: PMC5749529.
Article
50. Mawe GM. 2015; Colitis-induced neuroplasticity disrupts motility in the inflamed and post-inflamed colon. J Clin Invest. 125:949–955. DOI: 10.1172/JCI76306. PMID: 25729851. PMCID: PMC4362261.
Article
51. Villanacci V, Bassotti G, Nascimbeni R, et al. 2008; Enteric nervous system abnormalities in inflammatory bowel diseases. Neurogastroenterol Motil. 20:1009–1016. DOI: 10.1111/j.1365-2982.2008.01146.x. PMID: 18492026.
Article
52. Bassotti G, Antonelli E, Villanacci V, Salemme M, Coppola M, Annese V. 2014; Gastrointestinal motility disorders in inflammatory bowel diseases. World J Gastroenterol. 20:37–44. DOI: 10.3748/wjg.v20.i1.37. PMID: 24415856. PMCID: PMC3886030.
Article
53. Annese V, Bassotti G, Napolitano G, Usai P, Andriulli A, Vantrappen G. 1997; Gastrointestinal motility disorders in patients with inactive Crohn's disease. Scand J Gastroenterol. 32:1107–1117. DOI: 10.3109/00365529709002989. PMID: 9399391.
Article
54. Peuhkuri K, Vapaatalo H, Korpela R. 2010; Even low-grade inflammation impacts on small intestinal function. World J Gastroenterol. 16:1057–1062. DOI: 10.3748/wjg.v16.i9.1057. PMID: 20205274. PMCID: PMC2835780.
Article
55. Bassotti G, Villanacci V, Nascimbeni R, et al. 2009; Enteric neuroglial apoptosis in inflammatory bowel diseases. J Crohns Colitis. 3:264–270. DOI: 10.1016/j.crohns.2009.06.004. PMID: 21172285.
Article
56. Chang J, Leong RW, Wasinger VC, Ip M, Yang M, Phan TG. 2017; Impaired Intestinal Permeability Contributes to Ongoing Bowel Symptoms in Patients With Inflammatory Bowel Disease and Mucosal Healing. Gastroenterology. 153:723–731.e1. DOI: 10.1053/j.gastro.2017.05.056. PMID: 28601482.
Article
57. Shivaji UN, Ford AC. 2014; Prevalence of functional gastrointestinal disorders among consecutive new patient referrals to a gastroenterology clinic. Frontline Gastroenterol. 5:266–271. DOI: 10.1136/flgastro-2013-100426. PMID: 28839783. PMCID: PMC5369735.
Article
58. MacDermott RP. 2007; Treatment of irritable bowel syndrome in outpatients with inflammatory bowel disease using a food and beverage intolerance, food and beverage avoidance diet. Inflamm Bowel Dis. 13:91–96. DOI: 10.1002/ibd.20048. PMID: 17206644.
Article
59. Nigam GB, Limdi JK, Vasant DH. 2018; Current perspectives on the diagnosis and management of functional anorectal disorders in patients with inflammatory bowel disease. Therap Adv Gastroenterol. 11:1756284818816956. DOI: 10.1177/1756284818816956. PMID: 30574193. PMCID: PMC6295686.
Article
60. Vasant DH, Solanki K, Radhakrishnan NV. 2017; Rectal Digital Maneuvers May Predict Outcomes and Help Customize Treatment Intensity of Biofeedback in Chronic Constipation and Dyssynergic Defecation. Dis Colon Rectum. 60:e2. DOI: 10.1097/DCR.0000000000000725. PMID: 27926570.
Article
61. Norton C, Dibley LB, Bassett P. 2013; Faecal incontinence in inflammatory bowel disease: associations and effect on quality of life. J Crohns Colitis. 7:e302–e311. DOI: 10.1016/j.crohns.2012.11.004. PMID: 23228710.
Article
62. Barros LL, Farias AQ, Rezaie A. 2019; Gastrointestinal motility and absorptive disorders in patients with inflammatory bowel diseases: Prevalence, diagnosis and treatment. World J Gastroenterol. 25:4414–4426. DOI: 10.3748/wjg.v25.i31.4414. PMID: 31496621. PMCID: PMC6710178.
Article
63. Halmos EP, Christophersen CT, Bird AR, Shepherd SJ, Muir JG, Gibson PR. 2016; Consistent Prebiotic Effect on Gut Microbiota With Altered FODMAP Intake in Patients with Crohn's Disease: A Randomised, Controlled Cross-Over Trial of Well-Defined Diets. Clin Transl Gastroenterol. 7:e164. DOI: 10.1038/ctg.2016.22. PMID: 27077959. PMCID: PMC4855163.
Article
64. Gibson PR. 2017; Use of the low-FODMAP diet in inflammatory bowel disease. J Gastroenterol Hepatol. 32(Suppl 1):40–42. DOI: 10.1111/jgh.13695. PMID: 28244679.
Article
65. Skodje GI, Sarna VK, Minelle IH, et al. 2018; Fructan, Rather Than Gluten, Induces Symptoms in Patients With Self-Reported Non-Celiac Gluten Sensitivity. Gastroenterology. 154:529–539.e2. DOI: 10.1053/j.gastro.2017.10.040. PMID: 29102613.
Article
66. Corinaldesi R, Stanghellini V, Cremon C, et al. 2009; Effect of mesalazine on mucosal immune biomarkers in irritable bowel syndrome: a randomized controlled proof-of-concept study. Aliment Pharmacol Ther. 30:245–252. DOI: 10.1111/j.1365-2036.2009.04041.x. PMID: 19438846.
Article
67. Iskandar HN, Cassell B, Kanuri N, et al. 2014; Tricyclic antidepressants for management of residual symptoms in inflammatory bowel disease. J Clin Gastroenterol. 48:423–429. DOI: 10.1097/MCG.0000000000000049. PMID: 24406434. PMCID: PMC4111227.
Article
68. Camilleri M, Lembo A, Katzka DA. 2017; Opioids in Gastroenterology: Treating Adverse Effects and Creating Therapeutic Benefits. Clin Gastroenterol Hepatol. 15:1338–1349. DOI: 10.1016/j.cgh.2017.05.014. PMID: 28529168. PMCID: PMC5565678.
Article
69. Klooker TK, Braak B, Koopman KE, et al. 2010; The mast cell stabiliser ketotifen decreases visceral hypersensitivity and improves intestinal symptoms in patients with irritable bowel syndrome. Gut. 59:1213–1221. DOI: 10.1136/gut.2010.213108. PMID: 20650926.
Article
70. Han S, Thoresen L, Jung JK, et al. 2017; Discovery of APD371: Identification of a Highly Potent and Selective CB2 Agonist for the Treatment of Chronic Pain. ACS Med Chem Lett. 8:1309–1313. DOI: 10.1021/acsmedchemlett.7b00396. PMID: 29259753. PMCID: PMC5733264.
Article
71. Biancone L, Vernia P, Agostini D, Ferrieri A, Pallone F. 2000; Effect of rifaximin on intestinal bacterial overgrowth in Crohn's disease as assessed by the H2-Glucose Breath Test. Curr Med Res Opin. 16:14–20. DOI: 10.1185/0300799009117003. PMID: 16422030.
Article
72. Khan KJ, Ullman TA, Ford AC, et al. 2011; Antibiotic therapy in inflammatory bowel disease: a systematic review and meta-analysis. Am J Gastroenterol. 106:661–673. DOI: 10.1038/ajg.2011.72. PMID: 21407187.
Article
73. Prantera C, Lochs H, Grimaldi M, et al. 2012; Rifaximin-extended intestinal release induces remission in patients with moderately active Crohn's disease. Gastroenterology. 142:473–481.e4. DOI: 10.1053/j.gastro.2011.11.032. PMID: 22155172.
Article
74. Jigaranu AO, Nedelciuc O, Blaj A, et al. 2014; Is rifaximin effective in maintaining remission in Crohn's disease? Dig Dis. 32:378–383. DOI: 10.1159/000358141. PMID: 24969283.
Article
75. Pimentel M, Lembo A, Chey WD, et al. 2011; Rifaximin therapy for patients with irritable bowel syndrome without constipation. N Engl J Med. 364:22–32. DOI: 10.1056/NEJMoa1004409. PMID: 21208106.
Article
76. Acosta A, Camilleri M, Shin A, et al. 2016; Effects of Rifaximin on Transit, Permeability, Fecal Microbiome, and Organic Acid Excretion in Irritable Bowel Syndrome. Clin Transl Gastroenterol. 7:e173. DOI: 10.1038/ctg.2016.32. PMID: 27228404. PMCID: PMC4893683.
Article
77. Ballou S, Keefer L. 2017; Psychological Interventions for Irritable Bowel Syndrome and Inflammatory Bowel Diseases. Clin Transl Gastroenterol. 8:e214. DOI: 10.1038/ctg.2016.69. PMID: 28102860. PMCID: PMC5288603.
Article
78. Gracie DJ, Irvine AJ, Sood R, Mikocka-Walus A, Hamlin PJ, Ford AC. 2017; Effect of psychological therapy on disease activity, psychological comorbidity, and quality of life in inflammatory bowel disease: a systematic review and meta-analysis. Lancet Gastroenterol Hepatol. 2:189–199. DOI: 10.1016/S2468-1253(16)30206-0. PMID: 28404134.
Article
79. Deter HC, Keller W, von Wietersheim J, et al. 2007; Psychological treatment may reduce the need for healthcare in patients with Crohn's disease. Inflamm Bowel Dis. 13:745–752. DOI: 10.1002/ibd.20068. PMID: 17230495.
Article
80. Gracie DJ, Guthrie EA, Hamlin PJ, Ford AC. 2018; Bi-directionality of Brain-Gut Interactions in Patients With Inflammatory Bowel Disease. Gastroenterology. 154:1635–1646.e3. DOI: 10.1053/j.gastro.2018.01.027. PMID: 29366841.
Article
81. Cheifetz AS, Gianotti R, Luber R, Gibson PR. 2017; Complementary and Alternative Medicines Used by Patients With Inflammatory Bowel Diseases. Gastroenterology. 152:415–429.e15. DOI: 10.1053/j.gastro.2016.10.004. PMID: 27743873.
Article
82. Johannesson E, Simrén M, Strid H, Bajor A, Sadik R. 2011; Physical activity improves symptoms in irritable bowel syndrome: a randomized controlled trial. Am J Gastroenterol. 106:915–922. DOI: 10.1038/ajg.2010.480. PMID: 21206488.
Article
83. Hollander D. 2001; Intestinal permeability in patients with Crohn's disease and their relatives. Dig Liver Dis. 33:649–651. DOI: 10.1016/S1590-8658(01)80038-4.
Article
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