The hypersensitivity to colonic distension of IBS patients can be transferred to rats through their fecal microbiota
Open accessAbstract
Background: Alterations of intestinal microbiota and hypersensitivity to colonic distension are two features of the irritable bowel syndrome (IBS). However, the role of intestinal microbiota in visceral hypersensitivity of IBS patients is far to be established. The aim of our study was to determine whether the intestinal microbiota is involved in the visceral hypersensitivity in IBS. Methods: The painful response to colorectal distension and colonic mucosal parameters were assessed in gnotobiotic rats. Germfree (GF) rats were inoculated with the fecal microbiota from IBS patients characterized by hypersensitivity to colorectal distension (IBS HMA rats) or from non‐hypersensitive healthy volunteers (Healthy HMA rats). Conventional rats were studied as normosensitivity control. Fecal microbial analyses were carried out in human and HMA rats fecal samples using cultural and molecular approaches. Key Results: The microbial dysbiosis of the IBS gut microbiota (more sulfate‐reducing bacteria and Enterobacteriaceae and less bifidobacteria) could be maintained in gnotobiotic rats. The number of abdominal contractions in response to colorectal distensions was significantly higher in IBS HMA rats than in healthy HMA rats. No difference was observed between healthy HMA and conventional rats. Colorectal compliance, epithelial paracellular permeability, and density of colonic mucosal mast cells were similar in the three groups of rats. Conclusions & Inferences: We herein showed that sensitivity to colonic distension of IBS patients can be transferred to rats by the fecal microbiota. Mucosal alterations associated with microbiota transfer are not involved in this hypersensitivity. The altered IBS microbiota may have important role in the hypersensitivity characterizing IBS patients through specific bacterial metabolites.
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Evidence for a role of the gut microbiome in regulating GI sensation comes from gnotobiotic studies showing transfer of the visceral hypersensitivity phenotype after transplantation of gut microbiota from IBS patients into germ-free mice.
“Evidence for a role of the gut microbiome in regulating GI sensation (Figure 3) comes from gnotobiotic studies showing transfer of the visceral hypersensitivity phenotype following transplantation of gut microbiota from patients with IBS into germ-free (GF) mice 66.”
From The gut Microbiome in adult and pediatric functional gastrointestinal disorders (2019) · cites this paper as [66]
Reports describe microbiota-induced hypersensitivity to colonic distension in germ-free rats inoculated with fecal microbiota from IBS patients.
“Study of specific IBS pathways include reports describing microbiota-induced hypersensitivity to colonic distension in GF rats inoculated with the fecal microbiota from IBS patients66.”
From The gut Microbiome in adult and pediatric functional gastrointestinal disorders (2019) · cites this paper as [66]
Microbiota composition changes in IBS are inconsistent across studies, possibly due to heterogeneous populations and differing sample preparation and analysis methods.
“However, changes in microbiota composition are not consistent across studies, possibly due to heterogeneous study populations and differing methodologies for sample preparation and analysis.”
From Update on Fecal Microbiota Transplantation 2015: Indications, Methodologies, Mechanisms, and Outlook (2015) · cites this paper as [89]
Several currently used IBS therapies, including prebiotics, probiotics, dietary restrictions, and antibiotics, modulate gut microbiota.
“several currently used therapies, such as pre and probiotics, dietary restrictions and antibiotics, modulate the gut microbiota.89”
From Update on Fecal Microbiota Transplantation 2015: Indications, Methodologies, Mechanisms, and Outlook (2015) · cites this paper as [89]
Gut microbiota is an important target for study in treating functional disorders such as IBS.
“Thus, gut microbiota is an important target for study in the treatment of functional disorders such as IBS”
From Update on Fecal Microbiota Transplantation 2015: Indications, Methodologies, Mechanisms, and Outlook (2015) · cites this paper as [89]
Several studies have found alterations in the gut microbiome in IBS patients.
“Several studies have found alterations in the gut microbiome in patients with IBS.86–89”
From Update on Fecal Microbiota Transplantation 2015: Indications, Methodologies, Mechanisms, and Outlook (2015) · cites this paper as [89]
Sensitivity to colonic distension of IBS patients can be transferred to rats by fecal microbiota transplant.
“sensitivity to colonic distension of IBS patients can be transferred to rats by the fecal microbiota transplant [303]”
From Gut microbiota role in irritable bowel syndrome: New therapeutic strategies (2016) · cites this paper as [303]
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The Gut Microbial Bile Acid Modulation and Its Relevance to Digestive Health and Diseases
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Pathogenic role of the gut microbiota in gastrointestinal diseases
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“human microbiota-associated (HMA) rats were compared with healthy HMA rats.(81) An investigation of whether changes in gut flora and gut inflammatory cell”
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“demonstrated that germ free rats inoculated with the fecal microbiota from IBS patients developed visceral hypersensitivity [14].”
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Microbiota regulates visceral pain in the mouse
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“Intriguingly, visceral hyper-sensitivity can be transferred via the microbiota of IBS patients to animals previously lacking microbes ( Crouzet et al., 2013 ).”
The gut Microbiome in adult and pediatric functional gastrointestinal disorders
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Self-citationGut Microbiota as Potential Orchestrators of Irritable Bowel Syndrome
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“Although not fully understood, studies in rats have suggested that fecal bacteria, through specific bacterial metabolites such as sulphides, induce visceral hypersensitivity, which is often demonstrated in IBS patients.(189) In conclusion, although gut microbiota might explain symptom generation in only a subgroup of…”
BackgroundAit-Belgnaoui, A., Payard, I., Rolland, C., Harkat, C., Braniste, V., Théodorou, V., & Tompkins, T. A. (2018) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm16167 · Cited by 139 · see citing works
“Fecal microbiota transplanted from these patients into germ-free rats led to visceral hypersensitivity.(15) Therefore, restoring the balance of gut microbiota by using the probiotics combination could be an interesting alternative in the management of IBS symptoms.”
BackgroundFukui, H., Xu, X., & Miwa, H. (2018) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm18071 · Cited by 128 · see citing works
“This is supported by experimental evidence that germ-free (GF) animals given microbiota transplants from IBS patients show visceral hypersensitivity and GI dysmotility.(131,132) On the other hand, although stress events in early life are closely associated with IBS development, the gut microbiota profile may be possib…”
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AGA Technical Review on the Role of Probiotics in the Management of Gastrointestinal Disorders
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“Responders (n=37) Non responder (n=9) Responders (n=31) Non responder (n=18) Age (years) 38 (12) 35(11) 36 (12) 32 (12) 37 (13) 32 (12) 38 (13) 35 (11) Female 17 (65) 16 (80) 15 (65) 15 (63) 26 (70) 7 (78) 21 (68) 11 (61) Symptom duration (m) 106 (133) 64 (84) 76 (99) 49 (53) 82 (107) 111 (149) 89 (116) 97 (125) IBS s…”
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“Firstly, germfree mice models provide direct evidence that the GI microbiota can induce local GI dysfunction with transplantation of dysbiotic stool from individuals with IBS leading to altered microbiota along with features of IBS such as visceral hypersensitivity in the mice at 4 weeks((53)).”
Impact of stressor exposure on the interplay between commensal microbiota and host inflammation
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Prevalence of Functional Gastrointestinal Disorders in Colombian School Children
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“Moreover, microbiota transfer from IBS patients into rodents has been reported to confer alterations in intestinal transit and visceral sensitivity to recipient animals [4, 5].”
BackgroundSu, T., Liu, R., Lee, A., Long, Y., Du, L., Lai, S., Chen, X., Wang, L., Si, J., Owyang, C., et al. (2018) · Gastroenterology Research and Practice · doi:10.1155/2018/6961783 · Cited by 117 · see citing works
“transplants from IBS patients to germ-free mice leads to physiologic changes seen in IBS, including rapid GI transit, impaired gut barrier function, and visceral hypersensitivity [14].”
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Gutsy Moves: The Amygdala as a Critical Node in Microbiota to Brain Signaling
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Mast cell mediation of visceral sensation and permeability in irritable bowel syndrome
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Anti-nociceptive effect of Faecalibacterium prausnitzii in non-inflammatory IBS-like models
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Visceral pain: gut microbiota, a new hope?
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Self-citationThe microbiota–microglia axis in central nervous system disorders
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“Furthermore, GF rats, which received an FMT from irritable bowel syndrome (IBS) patients characterized by hypersensitivity to colorectal distension, showed an enhanced visceral pain response (198).”
BackgroundThe gut microbiota as a key regulator of visceral pain
O’Mahony, S. M., Dinan, T. G., & Cryan, J. F. (2016) · Pain · doi:10.1097/j.pain.0000000000000779 · Cited by 98 · see citing works
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“conditions associated with gut–brain axis dysfunction 43,80,81 , including visceral pain 82 , comorbid gastrointestinal dysmotility and anxiety in individuals with irritable bowel syndrome (IBS) 83,84 , and Parkinson disease 85 .”
Meynier, M., Baudu, E., Rolhion, N., Defaye, M., Straube, M., Daugey, V., Modoux, M., Wawrzyniak, I., Delbac, F., Villéger, R., et al. (2022) · Gut Microbes · doi:10.1080/19490976.2021.2022997 · Cited by 90 · see citing works
“Proliferation of specific bacterial species is even associated with IBS symptoms as illustrated by an increase of sulfate-reducing bacteria in patients with CHS and microbiota transfer to germ-free rats enhances sensitivity to colorectal distension suggesting a contribution of microbiota alterations in pain processing…”
BackgroundPanic Disorder Comorbidity with Medical Conditions and Treatment Implications
Meuret, A. E., Kroll, J. L., & Ritz, T. (2017) · Annual Review of Clinical Psychology · doi:10.1146/annurev-clinpsy-021815-093044 · Cited by 88 · see citing works
“…negatively impacting gastrointestinal physiology (Ringel & Ringel-Kulka 2015), visceral sensitivity (Enck et al. 2016), and elevating risk for IBS (Crouzet et al. 2013) Loss of mucosal barrier by IL-6 and other proinflammatory cytokines possibly altering visceral pain perception and colonic…”
BackgroundMolecular Mechanisms of Microbiota-Mediated Pathology in Irritable Bowel Syndrome
Mishima, Y., & Ishihara, S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21228664 · Cited by 89 · see citing works
“The former is supported by evidence presented in several reports showing the features of human IBS, such as visceral colonic hypersensitivity can be transferred to a germ-free animal by fecal transplantation [50], development of post-infectious IBS (PI-IBS) after severe colitis with dysbiosis [51,52], and improved IBS…”
BackgroundEffect of commensals and probiotics on visceral sensitivity and pain in irritable bowel syndrome
Theodorou, V., Ait-Belgnaoui, A., Agostini, S., & Eutamene, H. (2014) · Gut Microbes · doi:10.4161/gmic.29796 · Cited by 83 · see citing works
“It has been recently shown that visceral hypersensitivity characterizing IBS-C patients can be transferred to rats by the fecal microbiota.(52) Accordingly, germ free rats inoculated with IBS-C fecal suspension exhibited increased visceral sensitivity in response to colorectal distension compared with germ free rats i…”
BackgroundInfluentialThe Influence of Nutrition on Intestinal Permeability and the Microbiome in Health and Disease
Inczefi, O., Bacsúr, P., Resál, T., Keresztes, C., & Molnár, T. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.718710 · Cited by 85 · see citing works
Gut dysbiosis and irritable bowel syndrome: The potential role of probiotics
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“42 62 – 64 Despite being highly successful in the treatment of RCDI, the use of FMT as a treatment modality in IBS has only recently been explored.”
BackgroundChronic Visceral Pain: New Peripheral Mechanistic Insights and Resulting Treatments
Ford, A. C., Vanner, S. J., Kashyap, P., & Nasser, Y. (2024) · Gastroenterology · doi:10.1053/j.gastro.2024.01.045 · Cited by 79 · see citing works
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Microbiota: a novel regulator of pain
Defaye, M., Gervason, S., Altier, C., Berthon, J., Ardid, D., Filaire, E., & Carvalho, F. A. (2019) · Journal of Neural Transmission · doi:10.1007/s00702-019-02083-z · Cited by 79 · see citing works
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Enteric Microbiota-Mediated Serotonergic Signaling in Pathogenesis of Irritable Bowel Syndrome
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The Role of Bacteria, Probiotics and Diet in Irritable Bowel Syndrome
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Gnotobiotics: Past, present and future
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The Role of the Human Microbiome in the Pathogenesis of Pain
Ustianowska, K., Ustianowski, Ł., Machaj, F., Gorący, A., Rosik, J., Szostak, B., Szostak, J., & Pawlik, A. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232113267 · Cited by 75 · see citing works
“With fecal microbiota transplant in rats, visceral hypersensitivity increased when compared to gnotobiotic rats receiving a healthy microbiota, suggesting a link between IBS-associated hypersensitivity and the intestinal microbiota [87,88].”
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“They were kept in sterile isolators with positive pressure over the entire trial period as described previously((40,43)).”
BackgroundMethodSelf-citationIrritable bowel syndrome, inflammatory bowel disease and the microbiome
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Markers for visceral hypersensitivity in patients with irritable bowel syndrome
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Varjú, P., Gede, N., Szakács, Z., Hegyi, P., Cazacu, I. M., Pécsi, D., Fábián, A., Szepes, Z., Vincze, Á., Tenk, J., et al. (2018) · Neurogastroenterology & Motility · doi:10.1111/nmo.13527 · Cited by 66 · see citing works
The microbiota-gut-brain axis: An emerging role for the epigenome
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“Transfer of the fecal microbiota from patients with IBS or MDD to germ-free (GF) animals also transferred IBS-like visceral pain and depressive-like behavior to these animals.(15,16) These studies showed the importance of the microbiota to induce behavioral alterations, but also indicated that the transient nature of…”
BackgroundMicrobiota Is Involved in Post-resection Adaptation in Humans with Short Bowel Syndrome
Gillard, L., Mayeur, C., Robert, V., Pingenot, I., Beyec, J. L., Bado, A., Lepage, P., Thomas, M., & Joly, F. (2017) · Frontiers in Physiology · doi:10.3389/fphys.2017.00224 · Cited by 65 · see citing works
“Data are expressed as the mean ± SEM, *p < 0.05, **p < 0.01, ***p < 0.001 based on the Kruskal-Wallis test followed. studies (Chung et al., 2012; Crouzet et al., 2013).”
MethodInfluentialVisceral Pain and Gastrointestinal Microbiome
Chichlowski, M., & Rudolph, C. (2015) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm15025 · Cited by 65 · see citing works
“study, GF rats inoculated with IBS microbiota showed abnormal gut fermentation with increased hydrogen excretion and sulfides production vs controls.(98) This led the authors to hypothesize that”
Long, X., Li, M.-X., Li, L. ‐., Sun, Y., Zhang, W. ‐., Zhao, D. ‐., & Li, Y. (2017) · Neurogastroenterology & Motility · doi:10.1111/nmo.13227 · Cited by 64 · see citing works
Functional abdominal pain disorders in children
Rajindrajith, S., Zeevenhooven, J., Devanarayana, N. M., Perera, B. J. C., & Benninga, M. A. (2018) · Expert Review of Gastroenterology & Hepatology · doi:10.1080/17474124.2018.1438188 · Cited by 64 · see citing works
“Experimental studies using germ free animals receiving gut microbiota of patients with IBS reported increasing visceral sensitivity, altered gastrointestinal transit and increase permeability of the intestine indicating potential pathogenic mechanisms [130].”
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Neuropsychiatric Disorders: Influence of Gut Microbe to Brain Signalling
Scriven, M., Wall, M., Cryan, J. F., & Dinan, T. G. (2018) · Diseases · doi:10.3390/diseases6030078 · Cited by 62 · see citing works
Zhou, J., Shrestha, P., Qiu, Z. G., Harman, D. G., Teoh, W.-C., Al‐Sohaily, S., Liem, H., Turner, I. B., & Ho, V. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9072162 · Cited by 61 · see citing works
The microbiome and disorders of the central nervous system
Felice, V. D., & O'Mahony, S. M. (2017) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.06.016 · Cited by 60 · see citing works
“This effect, however, is not associated with changes in epithelial permeability, colonic compliance and density of mast cells in the mucosa (Crouzet et al., 2013).”
The Role of the Gastrointestinal Microbiota in Visceral Pain
Rea, K., O’Mahony, S. M., Dinan, T. G., & Cryan, J. F. (2016) · Handbook of experimental pharmacology · doi:10.1007/164_2016_115 · Cited by 62 · see citing works
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Microbiota dysbiosis and its pathophysiological significance in bowel obstruction
Hegde, S., Lin, Y.-M., Golovko, G., Khanipov, K., Cong, Y., Savidge, T., Fofanov, Y., & Shi, X.-Z. P. (2018) · Scientific Reports · doi:10.1038/s41598-018-31033-0 · Cited by 61 · see citing works
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“This hypothesis is supported by the notion that IBS-like traits can be observed in rats following fecal transplant from IBS patients.(4) Both diet regimens (low intake of fermentable oligo-, di-, and monosaccharides and polyols”
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“Visceral hypersensitivity characterizing constipation-predominant IBS patients can be transferred to rats by fecal microbiota.(33) In IBS patients, alteration of intestinal microbiota has been linked to immune dysfunction and altered neurological functions, such as reduced pain threshold and increased anxiety, suggest…”
BackgroundIrritable bowel syndrome and endometriosis: New insights for old diseases
Viganò, D., Zara, F., & Usai, P. (2017) · Digestive and Liver Disease · doi:10.1016/j.dld.2017.12.017 · Cited by 57 · see citing works
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“Several facts support this tendency: some pre-/probiotics can relieve IBS symptoms [58]; visceral colonic hypersensitivity that is a critical feature of the IBS can be transferred to germfree mice by fecal transplantation [59]; randomized controlled trails with rifaximin, a no-absorbable antibiotic, revealed benefit f…”
BackgroundGut microbiota in chronic pain: Novel insights into mechanisms and promising therapeutic strategies
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The Intestinal Microbiota and Irritable Bowel Syndrome
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Early‐life adversity, epigenetics, and visceral hypersensitivity
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Mars, R. A. T., Frith, M., & Kashyap, P. (2020) · Gastroenterology · doi:10.1053/j.gastro.2020.10.058 · Cited by 54 · see citing works
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Gu, X., Song, L., Li, L., Liu, T., Zhang, M.-M., Li, Z., Wang, P., Li, M., & Zuo, X. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.01281 · Cited by 52 · see citing works
Can Gut Microbiota Composition Predict Response to Dietary Treatments?
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- Authors
- Crouzet, L., Gaultier, E., Del'Homme, C., Cartier, C., Delmas, E., Dapoigny, M., Fioramonti, J., & Bernalier‐Donadille, A.
- Affiliations
- Institut National de la Recherche Agronomique (FR)
- Toxicologie Alimentaire (FR)
- INRA, UR 454 Microbiology Unit Clermont‐Ferrand Research Centre Saint Genès‐Champanelle France
- Centre Hospitalier Universitaire de Clermont-Ferrand (FR)
- Corresponding author
- Bernalier‐Donadille, A.
- Venue
- Neurogastroenterology & Motility
- Publisher
- Wiley
- Published
- 2013-02-25
- Volume
- 25
- Issue
- 4
- Pages
- e272-82
- ISSN
- 1350-1925 (ISSN-L)
- 1365-2982
- OpenAlex
- W2088256169
- Cited by
- 280
- References
- 54
- Citations by year
- 2026: 5 · 2025: 14 · 2024: 20 · 2023: 25 · 2022: 28 · 2021: 24 · 2020: 25 · 2019: 24 · 2018: 27 · 2017: 30 · 2016: 20 · 2015: 15 · 2014: 15 · 2013: 8
- FWCI
- 18.15
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Neurogastroenterology & Motility (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Topics
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Health Professions › Pharmacy › Infant Health and Development
- Keywords
- irritable bowel syndrome, visceral hypersensitivity, colorectal distension, fecal microbiota transplantation, gut microbiota, gnotobiotic rats, germ-free rats, dysbiosis, sulfate-reducing bacteria, Enterobacteriaceae, Bifidobacterium, abdominal contractions, paracellular permeability
- MeSH terms
- Adult, Animals, Colon, Feces, Female, Gastrointestinal Motility, Humans, Hypersensitivity, Intestinal Mucosa, Male, Middle Aged, Rats, Inbred F344, Species Specificity, Irritable Bowel Syndrome, Rats, Microbiota
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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