The gut microbiota as a key regulator of visceral pain

Pain

Volumn 158, Issue 4, 2017, Pages S19-S28

  O'Mahony, Siobhain M ^a,b   Dinan, Timothy G ^a,b   Cryan, John F ^a,b  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL MODEL; CENTRAL NERVOUS SYSTEM; COMORBIDITY; FUTUROLOGY; HUMAN; INFANTILE COLIC; INTESTINE FLORA; IRRITABLE COLON; NEUROTRANSMISSION; NONHUMAN; PRECLINICAL STUDY; PRIORITY JOURNAL; REVIEW; STRESS; THERAPY; VISCERAL PAIN; GASTROINTESTINAL TRACT; MICROBIOLOGY; NOCICEPTION; PHYSIOLOGY;

GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; HUMANS; PAIN PERCEPTION; VISCERAL PAIN;

EID: 85021450018     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1097/j.pain.0000000000000779     Document Type: Review

References (169)

1. Adami AJ, Bracken SJ. Breathing better through bugs: asthma and the microbiome. Yale J Biol Med 2016; 89:309-24.
2. Aguilera M, Cerda-Cuellar M, Martinez V. Antibiotic-induced dysbiosis alters host-bacterial interactions and leads to colonic sensory and motor changes in mice. Gut Microbes 2015; 6:10-23.
3. Al-Chaer ED, Kawasaki M, Pasricha PJ. A new model of chronic visceral hypersensitivity in adult rats induced by colon irritation during postnatal development. Gastroenterology 2000; 119:1276-85.
4. Altmann F, Kosma P, O'Callaghan A, Leahy S, Bottacini F, Molloy E, Plattner S, Schiavi E, Gleinser M, Groeger D, Grant R, Rodriguez Perez N, Healy S, Svehla E, Windwarder M, Hofinger A, O'Connell Motherway M, Akdis CA, Xu J, Roper J, van Sinderen D, O'Mahony L. Genome analysis and Characterisation of the Exopolysaccharide produced by bifidobacterium longum subsp. Longum 35624. PLoS One 2016; 11: e0162983.
5. Barbara G, Scaioli E, Barbaro MR, Biagi E, Laghi L, Cremon C, Marasco G, Colecchia A, Picone G, Salfi N, Capozzi F, Brigidi P, Festi D. Gut microbiota, metabolome and immune signatures in patients with uncomplicated diverticular disease. Gut 2016. doi:10.1136/gutjnl-2016-312377. [Epub ahead of print].
6. Barnes D, Yeh AM. Bugs and guts: practical applications of probiotics for gastrointestinal disorders in children. Nutr Clin Pract 2015; 30: 747-59.
7. Benton D, Williams C, Brown A. Impact of consuming a milk drink containing a probiotic on mood and cognition. Eur J Clin Nutr 2007; 61: 355-61.
8. Bercik P, Collins SM, Verdu EF. Microbes and the gut-brain axis. Neurogastroenterol Motil 2012; 24:405-13.
9. Bercik P, Wang L, Verdu EF, Mao YK, Blennerhassett P, Khan WI, Kean I, Tougas G, Collins SM. Visceral hyperalgesia and intestinal dysmotility in a mouse model of postinfective gut dysfunction. Gastroenterology 2004; 127:179-87.
10. Blanchard EB, Lackner JM, Jaccard J, Rowell D, Carosella AM, Powell C, Sanders K, Krasner S, Kuhn E. The role of stress in symptom exacerbation among IBS patients. J Psychosomatic Res 2008; 64: 119-28.
11. Brand S, Furlano R, Sidler M, Schulz J, Holsboer-Trachsler E. "Oh, baby, please don'tcry!": in infants suffering from infantile colic hypothalamic-pituitary-adrenocortical axis activity is related to poor sleep and increased crying intensity. Neuropsychobiology 2011; 64:15-23.
12. Braniste V, Al-Asmakh M, Kowal C, Anuar F, Abbaspour A, Toth M, Korecka A, Bakocevic N, Ng LG, Kundu P, Gulyas B, Halldin C, Hultenby K, Nilsson H, Hebert H, Volpe BT, Diamond B, Pettersson S. The gut microbiota influences blood-brain barrier permeability in mice. Sci Transl Med 2014; 6:263ra158.
13. Braundmeier-Fleming A, Russell NT, Yang W, Nas MY, Yaggie RE, Berry M, Bachrach L, Flury SC, Marko DS, Bushell CB, Welge ME, White BA, Schaeffer AJ, Klumpp DJ. Stool-based biomarkers of interstitial cystitis/bladder pain syndrome. Sci Rep 2016; 6:26083.
14. Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM, Dinan TG, Bienenstock J, Cryan JF. Ingestion of lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci U S A 2011; 108:16050-5.
15. Burke NN, Finn DP, McGuire BE, Roche M. Psychological stress in early life as a predisposing factor for the development of chronic pain: clinical and preclinical evidence and neurobiologicalmechanisms. J Neurosci Res 2016. [Epub ahead of print]. doi:10.1002/jnr.23802.
16. Burokas A, Moloney RD, Dinan TG, Cryan JF. Microbiota regulation of the Mammalian gut-brain axis. Adv Appl Microbiol 2015; 91:1-62.
17. Camilleri M, Park SY, Scarpato E, Staiano A. Exploring hypotheses and rationale for causes of infantile colic. Neurogastroenterol Motil 2016. [Epub ahead of print]. doi:10.1111/nmo.12943.
18. Carroll IM, Ringel-Kulka T, Siddle JP, Ringel Y. Alterations in composition and diversity of the intestinal microbiota in patients with diarrhea-predominant irritable bowel syndrome. Neurogastroenterol Motil 2012; 24:521-30. e248.
19. Cervero F, Laird JM. Visceral pain. Lancet 1999; 353:2145-8.
20. Chau K, Lau E, Greenberg S, Jacobson S, Yazdani-Brojeni P, Verma N, Koren G. Probiotics for infantile colic: a randomized, double-blind, placebo-controlled trial investigating Lactobacillus reuteri DSM 17938. J Pediatr 2015; 166:74-8.
21. Christianson JA, Bielefeldt K, Malin SA, Davis BM. Neonatal colon insult alters growth factor expression and TRPA1 responses in adult mice. PAIN 2010; 151:540-9.
22. Chumpitazi BP, Cope JL, Hollister EB, Tsai CM, McMeans AR, Luna RA, Versalovic J, Shulman RJ. Randomised clinical trial: gut microbiome biomarkers are associated with clinical response to a low FODMAP diet in children with the irritable bowel syndrome. Aliment Pharmacol Ther 2015; 42:418-27.
23. Clarke G, Cryan JF, Dinan TG, Quigley EM. Review article: probiotics for the treatment of irritable bowel syndrome-focus on lactic acid bacteria. Aliment Pharmacol Ther 2012; 35:403-13.
24. Clarke G, Grenham S, Scully P, Fitzgerald P, Moloney R, Shanahan F, Dinan T, Cryan J. The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. Mol Psychiatry 2012; 18:666-73.
25. Clarke G, O'Mahony SM, Dinan TG, Cryan JF. Priming for health: gut microbiota acquired in early life regulates physiology, brain and behaviour. Acta Paediatr 2014; 103:812-19.
26. Coutinho SV, Meller ST, Gebhart GF. Intracolonic zymosan produces visceral hyperalgesia inthe rat that is mediated byspinal NMDA and non-NMDA receptors. Brain Res 1996; 736:7-15.
27. Crouzet L, Gaultier E, Del'Homme C, Cartier C, Delmas E, Dapoigny M, Fioramonti J, Bernalier-Donadille A. The hypersensitivity to colonic distension of IBS patients can be transferred to rats through their fecal microbiota. Neurogastroenterol Motil 2013; 25:e272-82.
28. Cryan JF, O'Mahony SM. The microbiome-gut-brain axis: from bowel to behavior. Neurogastroenterol Motil 2011; 23:187-92.
29. Curro D, Ianiro G, Pecere S, Bibbo S, Cammarota G. Probiotics, fiber and herbal medicinal products for functional and inflammatory bowel disorders. Br J Pharmacol 2016.
30. Dash S, Clarke G, Berk M, Jacka FN. The gut microbiome and diet in psychiatry: focus on depression. Curr Opin Psychiatry 2015; 28:1-6.
31. Davis DJ, Doerr HM, Grzelak AK, Busi SB, Jasarevic E, Ericsson AC, Bryda EC. Lactobacillus plantarum attenuates anxiety-related behavior and protects against stress-induced dysbiosis in adult zebrafish. Scientific Rep 2016; 6:33726.
32. De Palma G, Collins SM, Bercik P. The microbiota-gut-brain axis in functional gastrointestinal disorders. Gut Microbes 2014; 5:419-29.
33. De Palma G, Collins SM, Bercik P, Verdu EF. The microbiota-gut-brain axis in gastrointestinal disorders: stressed bugs, stressed brain or both? J Physiol 2014; 592(pt 14):2989-97.
34. de Weerth C, Fuentes S, de Vos WM. Crying in infants: on the possible role of intestinal microbiota in the development of colic. Gut Microbes 2013; 4:416-21.
35. Desbonnet L, Clarke G, Shanahan F, Dinan TG, Cryan JF. Microbiota is essential for social development in the mouse. Mol Psychiatry 2014; 19:146-8.
36. Desbonnet L, Garrett L, Clarke G, Kiely B, Cryan JF, Dinan TG. Effects of the probiotic Bifidobacterium infantisinthe maternal separation model of depression. Neuroscience 2010; 170:1179-88.
37. Diaz Heijtz R, Wang S, Anuar F, Qian Y, Bjorkholm B, Samuelsson A, Hibberd ML, Forssberg H, Pettersson S. Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci U S A 2011; 108:3047-52.
38. Dinan TG, Cryan JF. Gut instincts: microbiota as a key regulator of brain development, ageing and neurodegeneration. J Physiol 2016. doi:10.1113/JP273106. [Epub ahead of print].
39. Dinan TG, Stilling RM, Stanton C, Cryan JF. Collective unconscious: how gut microbes shape human behavior. J Psychiatr Res 2015; 63:1-9.
40. Donaldson GP, Lee SM, Mazmanian SK. Gut biogeography of the bacterial microbiota. Nat Rev Microbiol 2016; 14:20-32.
41. Eisenberger NI. The pain of social disconnection: examining the shared neural underpinnings of physical and social pain. Nat Rev Neurosci 2012; 13:421-34.
42. El Aidy S, Dinan TG, Cryan JF. Gut microbiota: the conductor in the orchestra of immune-neuroendocrine communication. Clin Ther 2015; 37:954-67.
43. Enck P, Aziz Q, Barbara G, Farmer AD, Fukudo S, Mayer EA, Niesler B, Quigley EM, Rajilic-Stojanovic M, Schemann M, Schwille-Kiuntke J, Simren M, Zipfel S, Spiller RC. Irritable bowel syndrome. Nat Rev Dis Primers 2016; 2:16014.
44. Farzaei MH, Bahramsoltani R, Abdollahi M, Rahimi R. The role of visceral hypersensitivity in irritable bowel syndrome: pharmacological targets and Novel treatments. J Neurogastroenterol Motil 2016; 22: 558-74.
45. Felice VD, Moloney RD, Cryan JF, Dinan TG, O'Mahony SM. Visceral Pain and Psychiatric Disorders. Mod Trends Pharmacopsychiatri 2015; 30:103-19.
46. Fraher MH, O'Toole PW, Quigley EM. Techniques used to characterize the gut microbiota: a guide for the clinician. Nat Rev Gastroenterol Hepatol 2012; 9:312-22.
47. Galipeau HJ, Verdu EF. Gut microbes and adverse food reactions: focus on gluten related disorders. Gut Microbes 2014; 5:594-605.
48. Galley JD, Parry NM, Ahmer BM, Fox JG, Bailey MT. The commensal microbiota exacerbate infectious colitis in stressor-exposed mice. Brain Behav Immun 2016.
49. Giannetti E, Maglione M, Alessandrella A, Strisciuglio C, De Giovanni D, Campanozzi A, Miele E, Staiano A. A mixture of 3 Bifidobacteria decreases abdominal pain and improves the quality of life in children with irritable bowel syndrome: a multicenter, randomized, double-blind, placebo-controlled, crossover trial. J Clin Gastroenterol 2016. [Epub ahead of print].
50. Gulden E, Wong FS, Wen L. The gut microbiota and type 1 diabetes. Clin Immunol 2015; 159:143-53.
51. Hartstra AV, Bouter KE, Backhed F, Nieuwdorp M. Insights into the role of the microbiome in obesity and type 2 diabetes. Diabetes Care 2015; 38:159-65.
52. Hong JY, Kilpatrick LA, Labus J, Gupta A, Jiang Z, Ashe-McNalley C, Stains J, Heendeniya N, Ebrat B, Smith S, Tillisch K, Naliboff B, Mayer EA. Patients with chronic visceral pain show sex-related alterations in intrinsic oscillations of the resting brain. J Neurosci 2013; 33: 11994-2002.
53. Horvath A, Dziechciarz P, Szajewska H. Meta-analysis: lactobacillus rhamnosus GG for abdominal pain-related functional gastrointestinal disorders in childhood. Aliment Pharmacol Ther 2011; 33:1302-10.
54. Hungin AP, Mulligan C, Pot B, Whorwell P, Agreus L, Fracasso P, Lionis C, Mendive J, Philippart de Foy JM, Rubin G, Winchester C, de Wit N. Systematic review: probiotics in the management of lower gastrointestinal symptoms in clinical practice-an evidence-based international guide. Aliment Pharmacol Ther 2013; 38:864-86.
55. Hungin AP, Whorwell PJ, Tack J, Mearin F. The prevalence, patterns and impact of irritable bowel syndrome: an international survey of 40,000 subjects. Aliment Pharmacol Ther 2003; 17:643-50.
56. Hyland NP, Quigley EM, Brint E. Microbiota-host interactions in irritable bowel syndrome: epithelial barrier, immune regulation and brain-gut interactions. World J Gastroenterol 2014; 20:8859-66.
57. Inoue R, Sakaue Y, Sawai C, Sawai T, Ozeki M, Romero-Perez GA, Tsukahara T. A preliminary investigation on the relationship between gut microbiota and gene expressions in peripheral mononuclear cells of infants with autism spectrum disorders. Biosci Biotechnol Biochem 2016; 80:2450-8.
58. Jalanka-Tuovinen J, Salojarvi J, Salonen A, Immonen O, Garsed K, Kelly FM, Zaitoun A, Palva A, Spiller RC, de Vos WM. Faecal microbiota composition and host-microbe cross-talk following gastroenteritis and in postinfectious irritable bowel syndrome. Gut 2014; 63:1737-45.
59. Jeffery IB, Lynch DB, O'Toole PW. Composition and temporal stability of the gut microbiota in older persons. ISME J 2016; 10:170-82.
60. Jeffery IB, O'Toole PW, Ohman L, Claesson MJ, Deane J, Quigley EM, Simren M. An irritable bowel syndrome subtype defined by species-specific alterations in faecal microbiota. Gut 2012; 61:997-1006.
61. Jennings EM, Okine BN, Roche M, Finn DP. Stress-induced hyperalgesia. Prog Neurobiol 2014; 121:1-18.
62. Jiang Z, Dinov ID, Labus J, Shi Y, Zamanyan A, Gupta A, Ashe-McNalley C, Hong JY, Tillisch K, Toga AW, Mayer EA. Sex-related differences of cortical thickness in patients with chronic abdominal pain. PLoS One 2013; 8:e73932.
63. Kannampalli P, Pochiraju S, Chichlowski M, Berg BM, Rudolph C, Bruckert M, Miranda A, Sengupta JN. Probiotic lactobacillus rhamnosus GG (LGG) and prebiotic prevent neonatal inflammation-induced visceral hypersensitivity in adult rats. Neurogastroenterol Motil 2014; 26:1694-704.
64. Kelly JR, Borre Y, C OB, Patterson E, El Aidy S, Deane J, Kennedy PJ, Beers S, Scott K, Moloney G, Hoban AE, Scott L, Fitzgerald P, Ross P, Stanton C, Clarke G, Cryan JF, Dinan TG. Transferring the blues: depression-associated gut microbiota induces neurobehavioural changes in the rat. J Psychiatr Res 2016; 82:109-18.
65. King TS, Elia M, Hunter JO. Abnormal colonic fermentation in irritable bowel syndrome. Lancet 1998; 352:1187-9.
66. Koh A, De Vadder F, Kovatcheva-Datchary P, Backhed F. From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell 2016; 165:1332-45.
67. Krieger JN, Lee SW, Jeon J, Cheah PY, Liong ML, Riley DE. Epidemiology of prostatitis. Int J Antimicrob Agents 2008; 31:85-90.
68. Larauche M, Mulak A, Tache Y. Stress-related alterations of visceral sensation: animal models for irritable bowel syndrome study. J Neurogastroenterol Motil 2011; 17:213-34.
69. Larauche M, Mulak A, Tache Y. Stress and visceral pain: from animal models to clinical therapies. Exp Neurol 2012; 233:49-67.
70. Lehtonen L, Korvenranta H, Eerola E. Intestinal microflora in colicky and noncolicky infants: bacterial cultures and gas-liquid chromatography. J Pediatr Gastroenterol Nutr 1994; 19:310-14.
71. Li D, Wang P, Hu X, Chen F. The gut microbiota: a treasure for human health. Biotechnol Adv 2016; 34:1210-24.
72. Lin C, Al-Chaer ED. Long-term sensitization of primary afferents in adult rats exposed to neonatal colon pain. Brain Res 2003; 971:73-82.
73. Long YQ, Tong JJ, Qian W, Hou XH. Altered expression of intestinal cytokines in development of postinfectious irritable bowel syndrome mouse model [in Chinese]. Zhonghua Yi Xue Za Zhi 2010; 90:2415-19.
74. Lopez-Cepero AA, Palacios C. Association of the intestinal microbiota and obesity. P R Health Sci J 2015; 34:60-4.
75. Lovell RM, Ford AC. Global prevalence of and risk factors for irritable bowel syndrome: a meta-analysis. Clin Gastroenterol Hepatol 2012; 10: 712-21 e714.
76. Lyte M. Microbial endocrinology in the microbiome-gut-brain axis: how bacterial production and utilization of neurochemicals influence behavior. PLoS Pathog 2013; 9:e1003726.
77. Lyte M. Microbial endocrinology: host-microbiota neuroendocrine interactions influencing brain and behavior. Gut Microbes 2014; 5: 381-9.
78. Malinen E, Krogius-Kurikka L, Lyra A, Nikkila J, Jaaskelainen A, Rinttila T, Vilpponen-Salmela T, von Wright AJ, Palva A. Association of symptoms with gastrointestinal microbiota in irritable bowel syndrome. World J Gastroenterol 2010; 16:4532-40.
79. Marchesi J, Shanahan F. The normal intestinal microbiota. Curr Opin Infect Dis 2007; 20:508-13.
80. Martin LJ, Tuttle AH, Mogil JS. The interaction between pain and social behavior in humans and rodents. Curr Top Behav Neurosci 2014; 20: 233-50.
81. Matsunami M, Tarui T, Mitani K, Nagasawa K, Fukushima O, Okubo K, Yoshida S, Takemura M, Kawabata A. Luminal hydrogen sulfide plays a pronociceptive role in mouse colon. Gut 2009; 58:751-61.
82. Mayer EA, Knight R, Mazmanian SK, Cryan JF, Tillisch K. Gut microbes and the brain: paradigm shift in neuroscience. J Neurosci 2014; 34:15490-6.
83. Mayer EA, Labus JS, Tillisch K, Cole SW, Baldi P. Towards a systems view of IBS. Nat Rev Gastroenterol Hepatol 2015; 12:592-605.
84. Mayer EA, Naliboff BD, Chang L, Coutinho SVV Stress and irritable bowel syndrome. Am J Physiol Gastrointest Liver Physiol 2001; 280: G519-524.
85. Mayer EA, Savidge T, Shulman RJ. Brain-gut microbiome interactions and functional bowel disorders. Gastroenterology 2014; 146:1500-12.
86. McIntosh K, Reed DE, Schneider T, Dang F, Keshteli AH, De Palma G, Madsen K, Bercik P, Vanner S. FODMAPs alter symptoms and the metabolome of patients with IBS: a randomised controlled trial. Gut 2016. [Epub ahead of print]. doi:10.1136/gutjnl-2015-311339.
87. McKernan DP, Fitzgerald P, Dinan TG, Cryan JF. The probiotic Bifidobacterium infantis 35624 displays visceral antinociceptive effects in the rat. Neurogastroenterol Motil 2010; 22:1029-35. e1268.
88. McVey Neufeld KA, Luczynski P, Seira Oriach C, Dinan TG, Cryan JF. What's bugging your teen?-The microbiota and adolescent mental health. Neurosci Biobehav Rev 2016; 70:300-12.
89. McVey Neufeld KA, Mao YK, Bienenstock J, Foster JA, Kunze WA. The microbiome is essential for normal gut intrinsic primary afferent neuron excitability in the mouse. Neurogastroenterol Motil 2013; 25: 183-e188.
90. Melli LC, do Carmo-Rodrigues MS, Araujo-Filho HB, Sole D, de Morais MB. Intestinal microbiota and allergic diseases: a systematic review. Allergol Immunopathol (Madr) 2016; 44:177-88.
91. Messaoudi M, Lalonde R, Violle N, Javelot H, Desor D, Nejdi A, Bisson JF, Rougeot C, Pichelin M, Cazaubiel M, Cazaubiel JM. Assessment of psychotropic-like properties of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in rats and human subjects. Br J Nutr 2011; 105:755-64.
92. Milidou I, Sondergaard C, Jensen MS, Olsen J, Henriksen TB. Gestational age, small for gestational age, and infantile colic. Paediatr Perinat Epidemiol 2014; 28:138-45.
93. Miquel S, Martin R, Lashermes A, Gillet M, Meleine M, Gelot A, Eschalier A, Ardid D, Bermudez-Humaran LG, Sokol H, Thomas M, Theodorou V, Langella P, Carvalho FA. Anti-nociceptive effect of Faecalibacterium prausnitzii in non-inflammatory IBS-like models. Sci Rep 2016; 6:19399.
94. Mohammadi AA, Jazayeri S, Khosravi-Darani K, Solati Z, Mohammadpour N, Asemi Z, Adab Z, Djalali M, Tehrani-Doost M, Hosseini M, Eghtesadi S. The effects of probiotics on mental health and hypothalamic-pituitary-adrenal axis: a randomized, double-blind, placebo-controlled trial in petrochemical workers. Nutr Neurosci 2016; 19:387-95.
95. Moloney RD, Dinan TG, Cryan JF. Strain-dependent variations in visceral sensitivity: relationship to stress, anxiety and spinal glutamate transporter expression. Genes Brain Behav 2015; 14:319-29.
96. Moloney RD, Golubeva AV, O'Connor RM, Kalinichev M, Dinan TG, Cryan JF. Negative allosteric modulation of the mGlu7 receptor reduces visceral hypersensitivity in a stress-sensitive rat strain. Neurobiol Stress 2015; 2:28-33.
97. Moloney RD, Johnson AC, O'Mahony SM, Dinan TG, Greenwood-Van Meerveld B, Cryan JF. Stress and the microbiota-gut-brain axis in visceral pain: relevance to irritable bowel syndrome. CNS Neurosci Ther 2016; 22:102-17.
98. Moloney RD, O'Mahony SM, Dinan TG, Cryan JF. Stress-induced visceral pain: toward animal models of irritable-bowel syndrome and associated comorbidities. Front Psychiatry 2015; 6:15.
99. Nagel R, Traub RJ, Allcock RJ, Kwan MM, Bielefeldt-Ohmann H. Comparison of faecal microbiota in Blastocystis-positive and Blastocystis-negative irritable bowel syndrome patients. Microbiome 2016; 4:47.
100. Napthali K, Koloski N, Talley NJ. Abdominal migraine. Cephalalgia 2015.
101. Ness TJ, Gebhart GF. Colorectal distension as a noxious visceral stimulus: physiologic and pharmacologic characterization of pseudaffective reflexes in the rat. Brain Res 1988; 450:153-69.
102. Neufeld K, Kang N, Bienenstock J, Foster J. Reduced anxiety-like behavior and central neurochemical change in germ-free mice. Neurogastroenterol Motil 2011; 23:255. e119.
103. O'Mahony L, McCarthy J, Kelly P, Hurley G, Luo F, Chen K, O'Sullivan GC, Kiely B, Collins JK, Shanahan F, Quigley EM. Lactobacillus and bifidobacterium in irritable bowel syndrome: symptom responses and relationship to cytokine profiles. Gastroenterology 2005; 128:541-51.
104. O'Mahony SM, Bulmer DC, Coelho AM, Fitzgerald P, Bongiovanni C, Lee K, Winchester W, Dinan TG, Cryan JF. 5-HT(2B) receptors modulate visceral hypersensitivity in a stress-sensitive animal model of brain-gut axis dysfunction. Neurogastroenterology Motil 2010; 22: 573-8. e124.
105. O'Mahony SM, Clarke G, Borre YE, Dinan TG, Cryan JF. Serotonin, tryptophan metabolism and the brain-gut-microbiome axis. Behav Brain Res 2015; 277:32-48.
106. O'Mahony SM, Felice VD, Nally K, Savignac HM, Claesson MJ, Scully P, Woznicki J, Hyland NP, Shanahan F, Quigley EM, Marchesi JR, O'Toole PW, Dinan TG, Cryan JF. Disturbance of the gut microbiota in early-life selectively affects visceral pain in adulthood without impacting cognitive or anxiety-related behaviors in male rats. Neuroscience 2014; 277:885-901.
107. O'Mahony SM, Marchesi JR, Scully P, Codling C, Ceolho AM, Quigley EM, Cryan JF, Dinan TG. Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol Psychiatry 2009; 65:263-7.
108. O'Mahony SM, Stilling R, Dinan TG, Cryan JF. The microbiome and childhood diseases: focus on brain-gut axis. Birth Defects Res C Embryo Today 2015; 105:296-313.
109. O'Mahony SM, Tramullas M, Fitzgerald P, Cryan JF. Rodent models of colorectal distension. Curr Protoc Neurosci 2012; 9. Unit 9.40.
110. O'Malley D, Julio-Pieper M, O'Mahony SM, Dinan TG, Cryan JF. Differential visceral pain sensitivity and colonic morphology in four common laboratory rat strains. Exp Physiol 2014; 99:359-67.
111. Olango WM, Finn DP. Neurobiology of stress-induced hyperalgesia. Curr Top Behav Neurosci 2014; 20:251-80.
112. Palecek J, Willis WD. The dorsal column pathway facilitates visceromotor responses to colorectal distention after colon inflammation in rats. PAIN 2003; 104:501-7.
113. Palsson OS, Whitehead WE, van Tilburg MA, Chang L, Chey W, Crowell MD, Keefer L, Lembo AJ, Parkman HP, Rao SS, Sperber A, Spiegel B, Tack J, Vanner S, Walker LS, Whorwell P, Yang Y. Rome IV Diagnostic Questionnaires and Tables for Investigators and Clinicians. Gastroenterology 2016. [Epub ahead of print]. doi:10.1053/j.gastro.2016.02.014.
114. Partty A, Luoto R, Kalliomaki M, Salminen S, Isolauri E. Effects of early prebiotic and probiotic supplementation on development of gut microbiota and fussing and crying in preterm infants: a randomized, double-blind, placebo-controlled trial. J Pediatr 2013; 163:1272-7. e1271-1272.
115. Perez-Burgos A, Wang L, McVey Neufeld KA, Mao YK, Ahmadzai M, Janssen LJ, Stanisz AM, Bienenstock J, Kunze WA. The TRPV1 channel in rodents is a major target for antinociceptive effect of the probiotic Lactobacillus reuteri DSM 17938. J Physiol 2015; 593:3943-57.
116. Pimentel M, Lembo A, Chey WD, Zakko S, Ringel Y, Yu J, Mareya SM, Shaw AL, Bortey E, Forbes WP. Rifaximin therapy for patients with irritable bowel syndrome without constipation. New Engl J Med 2011; 364:22-32.
117. Pimentel M, Morales W, Chua K, Barlow G, Weitsman S, Kim G, Amichai MM, Pokkunuri V, Rook E, Mathur R, Marsh Z. Effects of rifaximin treatment and retreatment in nonconstipated IBS subjects. Dig Dis Sci 2011; 56:2067-72.
118. Pirbaglou M, Katz J, de Souza RJ, Stearns JC, Motamed M, Ritvo P. Probiotic supplementation can positively affect anxiety and depressive symptoms: a systematic review of randomized controlled trials. Nutr Res 2016; 36:889-98.
119. Pistollato F, Sumalla Cano S, Elio I, Masias Vergara M, Giampieri F, Battino M. Role of gut microbiota and nutrients in amyloid formation and pathogenesis of Alzheimer disease. Nutr Rev 2016; 74:624-34.
120. Prusator DK, Greenwood-Van Meerveld B. Sex differences in stress-induced visceral hypersensitivity following early life adversity: a two hit model. Neurogastroenterol Motil 2016; 28:1876-89.
121. Rajilic-Stojanovic M, Biagi E, Heilig HG, Kajander K, Kekkonen RA, Tims S, de Vos WM Global and deep molecular analysis of microbiota signatures in fecal samples from patients with irritable bowel syndrome. Gastroenterology 2011; 141:1792-801.
122. Rajilic-Stojanovic M, Jonkers DM, Salonen A, Hanevik K, Raes J, Jalanka J, de Vos WM, Manichanh C, Golic N, Enck P, Philippou E, Iraqi FA, Clarke G, Spiller RC, Penders J. Intestinal microbiota and diet in IBS: causes, consequences, or epiphenomena? Am J Gastroenterol 2015; 110:278-87.
123. Rasquin A, Di Lorenzo C, Forbes D, Guiraldes E, Hyams JS, Staiano A, Walker LS. Childhood functional gastrointestinal disorders: child/adolescent. Gastroenterology 2006; 130:1527-37.
124. Rijkers GT, de Vos WM, Brummer RJ, Morelli L, Corthier G, Marteau P. Health benefits and health claims of probiotics: bridging science and marketing. Br J Nutr 2011; 106:1291-6.
125. Ringel-Kulka T, Benson AK, Carroll IM, Kim J, Legge RM, Ringel Y. Molecular characterization of the intestinal microbiota in patients with and without abdominal bloating. Am J Physiol Gastrointest Liver Physiol 2016; 310:G417-426.
126. Ringel-Kulka T, Goldsmith JR, Carroll IM, Barros SP, Palsson O, Jobin C, Ringel Y. Lactobacillus acidophilus NCFM affects colonic mucosal opioid receptor expression in patients with functional abdominal pain- a randomised clinical study. Aliment Pharmacol Ther 2014; 40:200-7.
127. Rousseaux C, Thuru X, Gelot A, Barnich N, Neut C, Dubuquoy L, Dubuquoy C, Merour E, Geboes K, Chamaillard M, Ouwehand A, Leyer G, Carcano D, Colombel JF, Ardid D, Desreumaux P. Lactobacillus acidophilus modulates intestinal pain and induces opioid and cannabinoid receptors. Nat Med 2007; 13:35-7.
128. Sagami Y, Shimada Y, Tayama J, Nomura T, Satake M, Endo Y, Shoji T, Karahashi K, Hongo M, Fukudo S. Effect of a corticotropin releasing hormone receptor antagonist on colonic sensory and motor function in patients with irritable bowel syndrome. Gut 2004; 53:958-64.
129. Sandhu KV, Sherwin E, Schellekens H, Stanton C, Dinan TG, Cryan JF. Feeding the microbiota-gut-brain axis: diet, microbiome and neuropsychiatry. Translational Res 2016 In press.
130. Saulnier DM, Riehle K, Mistretta TA, Diaz MA, Mandal D, Raza S, Weidler EM, Qin X, Coarfa C, Milosavljevic A, Petrosino JF, Highlander S, Gibbs R, Lynch SV, Shulman RJ, Versalovic J. Gastrointestinal microbiome signatures of pediatric patients with irritable bowel syndrome. Gastroenterology 2011; 141:1782-91.
131. Savignac HM, Kiely B, Dinan TG, Cryan JF. Bifidobacteria exert strain-specific effects on stress-related behavior and physiology in BALB/c mice. Neurogastroenterol Motil 2014; 26:1615-27.
132. Savino F, Bailo E, Oggero R, Tullio V, Roana J, Carlone N, Cuffini AM, Silvestro L. Bacterial counts of intestinal Lactobacillus species in infants with colic. Pediatr Allergy Immunol 2005; 16:72-5.
133. Savino F, Castagno E, Bretto R, Brondello C, Palumeri E, Oggero R. A prospective 10-year study on children who had severe infantile colic. Acta Paediatr Suppl 2005; 94:129-32.
134. Savino F, Cordisco L, Tarasco V, Locatelli E, Di Gioia D, Oggero R, Matteuzzi D. Antagonistic effect of Lactobacillus strains against gas-producing coliforms isolated from colicky infants. BMC Microbiol 2011; 11:157.
135. Savino F, Cresi F, Pautasso S, Palumeri E, Tullio V, Roana J, Silvestro L, Oggero R. Intestinal microflora in breastfed colicky and non-colicky infants. Acta Paediatr 2004; 93:825-9.
136. Savino F, Pelle E, Palumeri E, Oggero R, Miniero R. Lactobacillus reuteri (American Type Culture Collection Strain 55730) versus simethicone in the treatment of infantile colic: a prospective randomized study. Pediatrics 2007; 119:e124-130.
137. Scheperjans F. Gut microbiota, 10(1)(3) new pieces in the Parkinson's disease puzzle. Curr Opin Neurol 2016; 29:773-80.
138. Schmidt K, Cowen PJ, Harmer CJ, Tzortzis G, Errington S, Burnet PW. Prebiotic intake reduces the waking cortisol response and alters emotional bias in healthy volunteers. Psychopharmacology (Berl) 2015; 232:1793-801.
139. Sender R, Fuchs S, Milo R. Revised Estimates for the number of human and bacteria cells in the body. PloS Biol 2016; 14:e1002533.
140. Sengupta JN. Visceral pain: the neurophysiological mechanism. Handb Exp Pharmacol 2009; 194:31-74.
141. Sharon G, Garg N, Debelius J, Knight R, Dorrestein PC, Mazmanian SK. Specialized metabolites from the microbiome in health and disease. Cell Metab 2014; 20:719-30.
142. Sheehan D, Moran C, Shanahan F. The microbiota in inflammatory bowel disease. J Gastroenterol 2015; 50:495-507.
143. Sibelli A, Chalder T, Everitt H, Workman P, Windgassen S, MossMorris R. A systematic review with meta-analysis of the role of anxiety and depression in irritable bowel syndrome onset. Psychol Med 2016; 46:3065-80.
144. Simren M, Barbara G, Flint HJ, Spiegel BM, Spiller RC, Vanner S, Verdu EF, Whorwell PJ, Zoetendal EG. Intestinal microbiota in functional bowel disorders: a Rome foundation report. Gut 2013; 62:159-76.
145. Simren M, Ringstrom G, Bjornsson ES, Abrahamsson H. Treatment with hypnotherapy reduces the sensory and motor component of the gastrocolonic response in irritable bowel syndrome. Psychosom Med 2004; 66:233-8.
146. Slavin J. Fiber and prebiotics: mechanisms and health benefits. Nutrients 2013; 5:1417-35.
147. Sommer F, Backhed F. The gut microbiota-masters of host development and physiology. Nat Rev Microbiol 2013; 11:227-38.
148. Srebro D, Vuckovic S, Prostran M. Inhibition of neuronal and inducible nitric oxide synthase does not affect the analgesic effects of NMDA antagonists in visceral inflammatory pain. Acta Neurobiol Exp (Wars) 2016; 76:110-16.
149. Staudacher HM, Whelan K. Altered gastrointestinal microbiota in irritable bowel syndrome and its modification by diet: probiotics, prebiotics and the low FODMAP diet. Proc Nutr Soc 2016; 75:306-18.
150. Stilling RM, Bordenstein SR, Dinan TG, Cryan JF. Friends with social benefits: host-microbe interactions as a driver of brain evolution and development? Front Cell Infect Microbiol 2014; 4:147.
151. Stilling RM, van de Wouw M, Clarke G, Stanton C, Dinan TG, Cryan JF. The neuropharmacology of butyrate: the bread and butter of the microbiota-gut-brain axis? Neurochem Int 2016; 99:110-32.
152. Sudo N, Chida Y, Aiba Y, Sonoda J, Oyama N, Yu XN, Kubo C, Koga Y. Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J Physiol 2004; 558:263-75.
153. Sung V, Cabana MD, D'Amico F, Deshpande G, Dupont C, Indrio F, Mentula S, Partty A, Savino F, Szajewska H, Tancredi D. Lactobacillus reuteri DSM 17938 for managing infant colic: protocol for an individual participant data meta-analysis. BMJ open 2014; 4:e006475.
154. Sung V, Hiscock H, Tang ML, Mensah FK, Nation ML, Satzke C, Heine RG, Stock A, Barr RG, Wake M. Treating infant colic with the probiotic Lactobacillus reuteri: double blind, placebo controlled randomised trial. BMJ 2014; 348:g2107.
155. Thabane M, Kottachchi DT, Marshall JK. Systematic review and meta-analysis: the incidence and prognosis of post-infectious irritable bowel syndrome. Aliment Pharmacol Ther 2007; 26:535-44.
156. Thé odorou V. Susceptibility to stress-induced visceral sensitivity: a bad legacy for next generations. Neurogastroenterol Motil 2013; 25:927-30.
157. Theodorou V, Belgnaoui AA, Agostini S, Eutamene H. Effect of commensals and probiotics on visceral sensitivity and pain in irritable bowel syndrome. Gut Microbes 2014; 5:430-6.
158. Tillisch K, Labus J, Kilpatrick L, Jiang Z, Stains J, Ebrat B, Guyonnet D, Legrain-Raspaud S, Trotin B, Naliboff B, Mayer EA. Consumption of fermented milk product with probiotic modulates brain activity. Gastroenterology 2013; 144:1394-401. 1401.e1391-1394.
159. Verdu EF, Bercik P, Verma-Gandhu M, Huang XX, Blennerhassett P, Jackson W, Mao Y, Wang L, Rochat F, Collins SM. Specific probiotic therapy attenuates antibiotic induced visceral hypersensitivity in mice. Gut 2006; 55:182-90.
160. Walker LS, Guite JW, Duke M, Barnard JA, Greene JW. Recurrent abdominal pain: a potential precursor of irritable bowel syndrome in adolescents and young adults. J Pediatr 1998; 132:1010-15.
161. Wall R, Cryan JF, Ross RP, Fitzgerald GF, Dinan TG, Stanton C. Bacterial neuroactive compounds produced by psychobiotics. Adv Exp Med Biol 2014; 817:221-39.
162. Wang EM, Li WT, Yan XJ, Chen X, Liu Q, Feng CC, Cao ZJ, Fang JY, Chen SL. Vagal afferent-dependent cholecystokinin modulation of visceral pain requires central amygdala NMDA-NR2B receptors in rats. Neurogastroenterol Motil 2015; 27:1333-43.
163. Wang J, Gu C, Al-Chaer ED. Altered behavior and digestive outcomes in adult male rats primed with minimal colon pain as neonates. Behav Brain Funct 2008; 4:28.
164. Wessel MA, Cobb JC, Jackson EB, Harris GS Jr, Detwiler AC. Paroxysmal fussing in infancy, sometimes called colic. Pediatrics 1954; 14:421-35.
165. Winek K, Dirnagl U, Meisel A. The gut microbiome as therapeutic target in central nervous system diseases: implications for stroke. Neurotherapeutics 2016; 13:762-74.
166. Wu J, Zhou Z, Hu Y, Dong S. Butyrate-induced GPR41 activation inhibits histone acetylation and cell growth. J Genet Genomics 2012; 39:375-84.
167. Yano JM, Yu K, Donaldson GP, Shastri GG, Ann P, Ma L, Nagler CR, Ismagilov RF, Mazmanian SK, Hsiao EY. Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell 2015; 161:264-76.
168. Zeber-Lubecka N, Kulecka M, Ambrozkiewicz F, Paziewska A, Goryca K, Karczmarski J, Rubel T, Wojtowicz W, Mlynarz P, Marczak L, Tomecki R, Mikula M, Ostrowski J. Limited prolonged effects of rifaximin treatment on irritable bowel syndrome-related differences in the fecal microbiome and metabolome. Gut Microbes 2016; 7:397-413.
169. Zhou XY, Li M, Li X, Long X, Zuo XL, Hou XH, Cong YZ, Li YQ. Visceral hypersensitive rats share common dysbiosis features with irritable bowel syndrome patients. World J Gastroenterol 2016; 22:5211-27.