Intestinal membrane permeability and hypersensitivity in the irritable bowel syndrome
Open accessAbstract
Irritable bowel syndrome (IBS) is a common gastrointestinal disorder in which the underlying pathophysiology is poorly understood; however, increased intestinal permeability in diarrhea-predominant IBS patients has been reported. Here we demonstrate that diarrhea-predominant IBS (D-IBS) patients display increased intestinal permeability. We have also found that increased intestinal membrane permeability is associated with visceral and thermal hypersensitivity in this subset of D-IBS patients. We evaluated 54 D-IBS patients and 22 controls for intestinal membrane permeability using the lactulose/mannitol method. All subjects ingested 5g of lactulose and 2g of mannitol in 100ml of water after which their urine was collected. We also evaluated the mean mechanical visual analogue scale (M-VAS) pain rating to nociceptive thermal and visceral stimulation in all subjects. All study participants also completed the FBDSI scale. Approximately 39% of diarrhea-predominant IBS patients had increased intestinal membrane permeability as measured by the lactulose/mannitol ratio. These IBS patients also demonstrated higher M-VAS pain intensity reading scale. Interestingly, the IBS patients with hypersensitivity and increased intestinal permeability had a higher FBDSI score (100.8 + or - 5.4) than IBS patients with normal membrane permeability and sensitivity (51.6 + or - 12.7) and controls (6.1 + or - 5.6) (p<0.001). A subset of D-IBS patients had increased intestinal membrane permeability that was associated with an increased FBDSI score and increased hypersensitivity to visceral and thermal nociceptive pain stimuli. Thus, increased intestinal membrane permeability in D-IBS patients may lead to more severe IBS symptoms and hypersensitivity to somatic and visceral stimuli.
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Cites
Longstreth, G. F., Thompson, W. G., Chey, W. D., Houghton, L. A., Mearin, F., & Spiller, R. C. (2006) · Gastroenterology · doi:10.1053/j.gastro.2005.11.061 · Cited by 4,856 · see citing works
Price, D. D., Bush, F. M., Long, S., & Harkins, S. W. (1994) · Pain · doi:10.1016/0304-3959(94)90097-3 · Cited by 1,174 · see citing works
Spiller, R. C., Jenkins, D., Thornley, J. P., Hebden, J. M., Wright, T., Skinner, M., & Neal, K. R. (2000) · Gut · doi:10.1136/gut.47.6.804 · Cited by 1,155 · see citing works
Immunity, Inflammation, and Allergy in the Gut
MacDonald, T. T., & Monteleone, G. (2005) · Science · doi:10.1126/science.1106442 · Cited by 1,035 · see citing works
Postinfectious Irritable Bowel Syndrome
Spiller, R., & Garsed, K. (2009) · Gastroenterology · doi:10.1053/j.gastro.2009.02.074 · Cited by 1,024 · see citing works
Intestinal permeability: an overview
Bjarnason, I., Macpherson, A., & Hollander, D. (1995) · Gastroenterology · doi:10.1016/0016-5085(95)90708-4 · Cited by 927 · see citing works
Basic and clinical aspects of visceral hyperalgesia
Mayer, E. A., & Gebhart, G. F. (1994) · Gastroenterology · doi:10.1016/0016-5085(94)90086-8 · Cited by 920 · see citing works
Al–Chaer, E. D., Kawasaki, M., & Pasricha, P. J. (2000) · Gastroenterology · doi:10.1053/gast.2000.19576 · Cited by 727 · see citing works
Tolerance for Rectosigmoid Distention in Irritable Bowel Syndrome
Whitehead, W. E., Holtkötter, B., Enck, P., Hoelzl, R., Holmes, K. D., Anthony, J. C., Shabsin, H. S., & Schuster, M. M. (1990) · Gastroenterology · doi:10.1016/0016-5085(90)90332-u · Cited by 592 · see citing works
Sex-related hormonal influences on pain and analgesic responses
Fillingim, R. B., & Ness, T. J. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(00)00017-8 · Cited by 554 · see citing works
Abnormal Intestinal Permeability in Subgroups of Diarrhea-Predominant Irritable Bowel Syndromes
Dunlop, S. P., Hebden, J., Campbell, E., Naesdal, J., Olbe, L., Perkins, A. C., & Spiller, R. C. (2006) · The American Journal of Gastroenterology · doi:10.1111/j.1572-0241.2006.00672.x · Cited by 476 · see citing works
Psychometric scores and persistence of irritable bowel after infectious diarrhoea
Gwee, K., Read, N. W., Graham, J. C., McKendrick, M. W., Collins, S. M., Marshall, J. S., & Walters, S. J. (1996) · The Lancet · doi:10.1016/s0140-6736(96)90341-4 · Cited by 466 · see citing works
Psychometric scores and persistence of irritable bowel after infectious diarrhoea
Ka, G., Graham, J. C., McKendrick, M. W., Collins, S. M., Marshall, J. S., Walters, S., & Read, N. W. (1996) · African journal of medical practice · Cited by 429 · see citing works
Mearin, F., Pérez-Oliveras, M., Juan, A. P., Vinyet, J., Ibañez, A., Coderch, J., & Perona, M. C. (2005) · Gastroenterology · doi:10.1053/j.gastro.2005.04.012 · Cited by 406 · see citing works
Leaky Gut in Alcoholic Cirrhosis: A Possible Mechanism for Alcohol-Induced Liver Damage
Keshavarzian, A., HOLMES, E. W., Patel, M., Iber, F. L., Fields, J. Z., & Pethkar, S. (1999) · The American Journal of Gastroenterology · doi:10.1111/j.1572-0241.1999.00797.x · Cited by 381 · see citing works
Evidence for two distinct perceptual alterations in irritable bowel syndrome
Naliboff, B. D., Munakata, J., Fullerton, S. C., Gracely, R. H., Kodner, A., Harraf, F., & Mayer, E. A. (1997) · Gut · doi:10.1136/gut.41.4.505 · Cited by 364 · see citing works
Spiller, R. E. (2003) · Gastroenterology · doi:10.1016/s0016-5085(03)00324-x · Cited by 353 · see citing works
Evolving pathophysiologic models of functional gastrointestinal disorders
Mayer, E. A., & Collins, S. M. (2002) · Gastroenterology · doi:10.1053/gast.2002.33584 · Cited by 326 · see citing works
Irritable bowel syndrome—post salmonella infection
McKendrick, M. W., & Read, N. W. (1994) · Journal of Infection · doi:10.1016/s0163-4453(94)94871-2 · Cited by 320 · see citing works
Hypersensitivity to visceral and cutaneous pain in the irritable bowel syndrome
Verne, N. G., Robinson, M. E., & Price, D. D. (2001) · Pain · doi:10.1016/s0304-3959(01)00285-8 · Cited by 291 · see citing works
Self-citationSelective dysfunction of mechanosensitive intestinal afferents in irritable bowel syndrome
Accarino, A. M., Azpiroz, F., & Malagelada, J. (1995) · Gastroenterology · doi:10.1016/0016-5085(95)90434-4 · Cited by 282 · see citing works
Central representation of visceral and cutaneous hypersensitivity in the irritable bowel syndrome
Verne, N. G., Himes, N. C., Robinson, M. E., Gopinath, K., Briggs, R. W., Crosson, B., & Price, D. D. (2003) · Pain · doi:10.1016/s0304-3959(02)00416-5 · Cited by 255 · see citing works
Self-citationAltered Rectal Perception in Irritable Bowel Syndrome Is Associated With Symptom Severity
Posserud, I., Syrous, A., Lindström, L., Tack, J., Abrahamsson, H., & Simrén, M. (2007) · Gastroenterology · doi:10.1053/j.gastro.2007.07.024 · Cited by 248 · see citing works
Patients with irritable bowel syndrome have greater pain tolerance than normal subjects
Cook, I. J., van Eeden, A., & Collins, S. M. (1987) · Gastroenterology · doi:10.1016/0016-5085(87)90434-3 · Cited by 233 · see citing works
IV. Visceral afferent contributions to the pathobiology of visceral pain
Gebhart, G. F. (2000) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.2000.278.6.g834 · Cited by 201 · see citing works
Chang, L., Mayer, E. A., Johnson, T. D., FitzGerald, L., & Naliboff, B. D. (2000) · Pain · doi:10.1016/s0304-3959(99)00215-8 · Cited by 195 · see citing works
Role of infection in irritable bowel syndrome
Spiller, R. C. (2007) · Journal of Gastroenterology · doi:10.1007/s00535-006-1925-8 · Cited by 187 · see citing works
The differing effects of acute and chronic alcohol on gastric and intestinal permeability.
Keshavarzian, A., Fields, J. Z., Vaeth, J., & HOLMES, E. W. (1994) · PubMed · Cited by 165 · see citing works
Functional GI disorders: from animal models to drug development
Mayer, E. A., Bradesi, S., Chang, L., Spiegel, B. M. R., Bueller, J. A., & Naliboff, B. D. (2007) · Gut · doi:10.1136/gut.2006.101675 · Cited by 162 · see citing works
Wilder‐Smith, C. H. (2007) · World Journal of Gastroenterology · doi:10.3748/wjg.v13.i27.3699 · Cited by 156 · see citing works
Visceral perception in irritable bowel syndrome
Zighelboim, J., Talley, N. J., Phillips, S. F., Harmsen, W. S., & Zinsmeister, A. R. (1995) · Digestive Diseases and Sciences · doi:10.1007/bf02064986 · Cited by 152 · see citing works
Evidence for generalized hyperalgesia in temporomandibular disorders patients
Sarlani, E., & Greenspan, J. D. (2003) · Pain · doi:10.1016/s0304-3959(03)00095-2 · Cited by 150 · see citing works
Intestinal permeability and irritable bowel syndrome
Camilleri, M., & Gorman, H. (2007) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2007.00925.x · Cited by 144 · see citing works
Pattern of gastrointestinal and somatic symptoms across the menstrual cycle
Heitkemper, M. M., & Jarrett, M. (1992) · Gastroenterology · doi:10.1016/0016-5085(92)90097-i · Cited by 123 · see citing works
van der Veek, P. P. J., van Rood, Y. R., & Masclee, A. (2008) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2007.12.005 · Cited by 119 · see citing works
Gastric Rupture and Necrosis in Prader‐Willi Syndrome
Stevenson, D. A., Heinemann, J., Angulo, M., Butler, M. G., Loker, J., Rupe, N., Kendell, P., Cassidy, S. B., & Scheimann, A. O. (2007) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0b013e31805b82b5 · Cited by 115 · see citing works
Bouin, M., Meunier, P., Riberdy, M., & Poitras, P. (2001) · Digestive Diseases and Sciences · doi:10.1023/a:1012356827026 · Cited by 111 · see citing works
Kuiken, S., Lindeboom, R., Tytgat, G. N. J., & Boeckxstaens, G. E. (2005) · Alimentary Pharmacology & Therapeutics · doi:10.1111/j.1365-2036.2005.02524.x · Cited by 101 · see citing works
Geisser, M. E., Robinson, M. E., & Pickren, W. E. (1992) · Behavior Therapy · doi:10.1016/s0005-7894(05)80306-5 · Cited by 92 · see citing works
Sperber, A. D., Carmel, S., Atzmon, Y., Weisberg, I., Shalit, Y., Neumann, L., Fich, A., Friger, M., & Buskila, D. (2000) · The American Journal of Gastroenterology · doi:10.1111/j.1572-0241.2000.01977.x · Cited by 88 · see citing works
Irritable bowel syndrome as a common precipitant of central sensitization
Verne, G. N., & Price, D. D. (2002) · Current Rheumatology Reports · doi:10.1007/s11926-002-0041-x · Cited by 82 · see citing works
Dunphy, R. C., Bridgewater, L., Price, D. D., Robinson, M. E., Zeilman, C. J., & Verne, N. G. (2003) · Pain · doi:10.1016/s0304-3959(02)00342-1 · Cited by 81 · see citing works
Self-citationPorras, M., Martín, M. T., Yang, P., Jury, J., Perdue, M. H., & Vergara, P. (2006) · Inflammatory Bowel Diseases · doi:10.1097/01.mib.0000231571.88806.62 · Cited by 76 · see citing works
Visceral and somatic hypersensitivity in a subset of rats following TNBS-induced colitis
Zhou, Q., Price, D. D., Caudle, R. M., & Verne, N. G. (2007) · Pain · doi:10.1016/j.pain.2007.03.029 · Cited by 71 · see citing works
Self-citationSabaté, J. M., Veyrac, M., Mion, F., Siproudhis, L., Ducrotte, P. R., Zerbib, F., Grimaud, J., Dapoigny, M. C., Dyard, F., & Coffin, B. (2008) · Alimentary Pharmacology & Therapeutics · doi:10.1111/j.1365-2036.2008.03759.x · Cited by 54 · see citing works
The fibromyalgia syndrome: Musculoskeletal pathophysiology
Geel, S. E. (1994) · Seminars in Arthritis and Rheumatism · doi:10.1016/0049-0172(94)90030-2 · Cited by 48 · see citing works
Castilloux, J., Noble, A. J., & Faure, C. C. (2008) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0b013e31814b91e7 · Cited by 46 · see citing works
Verne, G. N., & Cerda, J. J. (1997) · Postgraduate Medicine · doi:10.3810/pgm.1997.09.322 · Cited by 13 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Chey, W. D., Kurlander, J. E., & Eswaran, S. L. (2015) · JAMA · doi:10.1001/jama.2015.0954 · Cited by 1,086 · see citing works
Intestinal barrier function in health and gastrointestinal disease
Camilleri, M., Madsen, K., Spiller, R., Van Meerveld, B. G., & Verne, G. N. (2012) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2012.01921.x · Cited by 908 · see citing works
Human Intestinal Barrier Function in Health and Disease
König, J., Wells, J. M., Cani, P. D., García‐Ródenas, C. L., MacDonald, T. T., Mercenier, A., Whyte, J., Troost, F. J., & Brummer, R. J. (2016) · Clinical and Translational Gastroenterology · doi:10.1038/ctg.2016.54 · Cited by 787 · see citing works
Homeostasis of the gut barrier and potential biomarkers
Wells, J. M., Brummer, R. J., Derrien, M., MacDonald, T. T., Troost, F. J., Cani, P. D., Théodorou, V., Dekker, J. P., Méheust, A., de Vos, W. M., et al. (2016) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00048.2015 · Cited by 616 · see citing works
Ait-Belgnaoui, A., Durand, H., Cartier, C., Chaumaz, G., Eutamene, H., Ferrier, L., Houdeau, E., Fioramonti, J., Bueno, L., & Theodorou, V. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.03.024 · Cited by 612 · see citing works
British Society of Gastroenterology guidelines on the management of irritable bowel syndrome
Vasant, D. H., Paine, P. A., Black, C. J., Houghton, L. A., Everitt, H. A., Corsetti, M., Agrawal, A., Aziz, I., Farmer, A. D., Eugenicos, M. P., et al. (2021) · Gut · doi:10.1136/gutjnl-2021-324598 · Cited by 547 · see citing works
Impaired duodenal mucosal integrity and low-grade inflammation in functional dyspepsia
Vanheel, H., Vicario, M., Vanuytsel, T., Van Oudenhove, L., Martinez, C., Keita, Å. V., Pardon, N., Santos, J., Söderholm, J. D., Tack, J., et al. (2014) · Gut · doi:10.1136/gutjnl-2012-303857 · Cited by 424 · see citing works
Camilleri, M., Lasch, K. L., & Zhou, W. (2012) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00155.2012 · Cited by 397 · see citing works
Vivinus-Nébot, M., Frin-Mathy, G., Bzioueche, H., Dainese, R., Bernard, G., Anty, R., Filippi, J., Saint‐Paul, M., Tulić, M. K., Verhasselt, V., et al. (2013) · Gut · doi:10.1136/gutjnl-2012-304066 · Cited by 365 · see citing works
Jalanka-Tuovinen, J., Salojärvi, J., Salonen, A., Immonen, O., Garsed, K., Kelly, F. M., Zaitoun, A., Palva, A., Spiller, R. C., & de Vos, W. M. (2014) · Gut · doi:10.1136/gutjnl-2013-305994 · Cited by 340 · see citing works
The role of mast cells in functional GI disorders
Wouters, M. M., Vicario, M., & Santos, J. (2016) · Gut · doi:10.1136/gutjnl-2015-309151 · Cited by 308 · see citing works
Irritable bowel syndrome: a gut microbiota-related disorder?
Bhattarai, Y., Muniz Pedrogo, D. A., & Kashyap, P. C. (2017) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00338.2016 · Cited by 294 · see citing works
Bertiaux-Vandaële, N., Beutheu, S., Belmonte, L., Lecleire, S., Antonietti, M., Gourcerol, G., Leroi, A., Déchelotte, P., Ménard, J.-F., Ducrotte, P. R., et al. (2011) · The American Journal of Gastroenterology · doi:10.1038/ajg.2011.257 · Cited by 296 · see citing works
Martínez, C., Lobo, B., Pigrau, M., Ramos, L., González-Castro, A. M., Alonso, C., Guilarte, M., Guilá, M., de Torres, I., Azpiroz, F., et al. (2013) · Gut · doi:10.1136/gutjnl-2012-302093 · Cited by 283 · see citing works
Crouzet, L., Gaultier, E., Del'Homme, C., Cartier, C., Delmas, E., Dapoigny, M., Fioramonti, J., & Bernalier‐Donadille, A. (2013) · Neurogastroenterology & Motility · doi:10.1111/nmo.12103 · Cited by 280 · see citing works
Slyepchenko, A., Maes, M., Jacka, F. N., Köhler, C. A., Barichello, T., McIntyre, R. S., Berk, M., Grande, I., Foster, J. A., Vieta, E., et al. (2017) · Psychotherapy and Psychosomatics · doi:10.1159/000448957 · Cited by 278 · see citing works
MicroRNA-29a regulates intestinal membrane permeability in patients with irritable bowel syndrome
Zhou, Q., Souba, W. W., Croce, C. M., & Verne, G. N. (2009) · Gut · doi:10.1136/gut.2009.181834 · Cited by 277 · see citing works
Self-citationXu, D., Gao, J., Gillilland, M., Wu, X., Song, I., Kao, J. Y., & Owyang, C. (2014) · Gastroenterology · doi:10.1053/j.gastro.2013.10.026 · Cited by 271 · see citing works
The Role of Stress on Physiologic Responses and Clinical Symptoms in Irritable Bowel Syndrome
Chang, L. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.01.032 · Cited by 268 · see citing works
Layer, P., Andresen, V., Pehl, C., Allescher, H. ‐., Bischoff, S., Claßen, M., Enck, P., Frieling, T., Haag, S., Holtmann, G., et al. (2011) · Zeitschrift für Gastroenterologie · doi:10.1055/s-0029-1245976 · Cited by 231 · see citing works
Gender-related differences in irritable bowel syndrome: Potential mechanisms of sex hormones
Méleine, M. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i22.6725 · Cited by 220 · see citing works
Matricon, J., Méleine, M., Gelot, A., Piche, T., Dapoigny, M. C., Muller, E., & Ardid, D. (2012) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.12080 · Cited by 216 · see citing works
Simon, E., Călinoiu, L. F., Mitrea, L., & Vodnar, D. C. (2021) · Nutrients · doi:10.3390/nu13062112 · Cited by 224 · see citing works
Martínez, C., Vicario, M., Ramos, L., Lobo, B., Mosquera, J. L., Alonso, C., Sánchez, A., Guilarte, M., Antolín, M., de Torres, I., et al. (2012) · American Journal of Gastroenterology · doi:10.1038/ajg.2011.472 · Cited by 214 · see citing works
Stress and visceral pain: From animal models to clinical therapies
Larauche, M. H., Mulak, A., & Taché, Y. (2011) · Experimental Neurology · doi:10.1016/j.expneurol.2011.04.020 · Cited by 212 · see citing works
The immune system in irritable bowel syndrome
Barbara, G., Cremon, C., Carini, G., Bellacosa, L., Zecchi, L., Giorgio, R. D., Corinaldesi, R., & Stanghellini, V. (2011) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm.2011.17.4.349 · Cited by 211 · see citing works
Zhou, S.-Y., Gillilland, M. G., Wu, X., Leelasinjaroen, P., Zhang, G., Zhou, H. R., Ye, B., Lu, Y., & Owyang, C. (2017) · Journal of Clinical Investigation · doi:10.1172/jci92390 · Cited by 204 · see citing works
Intestinal Barrier Dysfunction in Irritable Bowel Syndrome: A Systematic Review
Hanning, N., Edwinson, A. L., Ceuleers, H., Peters, S. A., De Man, J. G., Hassett, L. C., De Winter, B. Y., & Grover, M. (2021) · Therapeutic Advances in Gastroenterology · doi:10.1177/1756284821993586 · Cited by 197 · see citing works
Zhou, Q., Verne, M. L., Fields, J. Z., Lefante, J. J., Basra, S., Salameh, H., & Verne, G. N. (2019) · Gut · doi:10.1136/gutjnl-2017-315136 · Cited by 195 · see citing works
Self-citationCrosstalk at the mucosal border: importance of the gut microenvironment in IBS
Öhman, L., Törnblom, H., & Simrén, M. (2014) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2014.200 · Cited by 181 · see citing works
Irritable bowel syndrome: towards biomarker identification
Clarke, G. A., Quigley, E. M. M., Cryan, J. F., & Dinan, T. G. (2009) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2009.08.001 · Cited by 180 · see citing works
Zhou, Q., Costinean, S., Croce, C. M., Brasier, A. R., Merwat, S. N., Larson, S. A., Basra, S. S., & Verne, G. N. (2014) · Gastroenterology · doi:10.1053/j.gastro.2014.09.037 · Cited by 178 · see citing works
Self-citationThe epithelial barrier theory and its associated diseases
Sun, N., Öğülür, İ., Mitamura, Y., Yazıcı, D., Pat, Y., Bu, X., Li, M., Zhu, X., Babayev, H., Ardıçlı, S., et al. (2024) · Allergy · doi:10.1111/all.16318 · Cited by 188 · see citing works
Understanding the Gut–Brain Axis and Its Therapeutic Implications for Neurodegenerative Disorders
Zheng, Y., Bonfili, L., Wei, T., & Eleuteri, A. M. (2023) · Nutrients · doi:10.3390/nu15214631 · Cited by 175 · see citing works
Schnabel, L., Buscail, C., Sabate, J.-M., Bouchoucha, M., Kesse-Guyot, E., Allès, B., Touvier, M., Monteiro, C. A., Hercberg, S., Benamouzig, R., et al. (2018) · American Journal of Gastroenterology · doi:10.1038/s41395-018-0137-1 · Cited by 173 · see citing works
New insights into visceral hypersensitivity—clinical implications in IBS
Zhou, Q., & Verne, G. N. (2011) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2011.83 · Cited by 161 · see citing works
Self-citationHan, X., Lee, A. A., Huang, S., Gao, J., Spence, J. R., & Owyang, C. (2018) · Gut Microbes · doi:10.1080/19490976.2018.1479625 · Cited by 159 · see citing works
Lenhart, A., & Chey, W. D. (2017) · Advances in Nutrition · doi:10.3945/an.117.015560 · Cited by 160 · see citing works
Mast Cell-Mediated Mechanisms of Nociception
Aich, A., Afrin, L. B., & Gupta, K. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms161226151 · Cited by 156 · see citing works
Piche, T. (2014) · Neurogastroenterology & Motility · doi:10.1111/nmo.12315 · Cited by 154 · see citing works
van Hemert, S., Breedveld, A. C., Rovers, J. M. P., Vermeiden, J. P. W., Witteman, B. J. M., Smits, M. G., & de Roos, N. M. (2014) · Frontiers in Neurology · doi:10.3389/fneur.2014.00241 · Cited by 150 · see citing works
Irritable bowel syndrome: the clinical approach
Adriani, A., Ribaldone, D. G., Astegiano, M., Durazzo, M., Saracco, G. M., & Pellicano, R. (2018) · Panminerva Medica · doi:10.23736/s0031-0808.18.03541-3 · Cited by 149 · see citing works
Silva, S. D., Masselot, C. R., Ait-Belgnaoui, A., Mancuso, A., Mercade, M., Salvador–Cartier, C., Gillet, M., Ferrier, L., Loubière, P., Dague, É., et al. (2014) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00290.2013 · Cited by 147 · see citing works
Immune Activation in Irritable Bowel Syndrome: Can Neuroimmune Interactions Explain Symptoms?
Hughes, P. A., Zola, H., Penttila, I., Blackshaw, L. A., Andrews, J. M., & Krumbiegel, D. (2013) · The American Journal of Gastroenterology · doi:10.1038/ajg.2013.120 · Cited by 147 · see citing works
Rao, A. S., Camilleri, M., Eckert, D. J., Busciglio, I. A., Burton, D. D., Ryks, M. D., Wong, B. S., Lamsam, J. L., Singh, R., & Zinsmeister, A. R. (2011) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00168.2011 · Cited by 145 · see citing works
Gut inflammation in chronic fatigue syndrome
Lakhan, S. E., & Kirchgessner, A. (2010) · Nutrition & Metabolism · doi:10.1186/1743-7075-7-79 · Cited by 143 · see citing works
Vivinus-Nébot, M., Dainese, R., Anty, R., Saint‐Paul, M., Nano, J. L., Gonthier, N., Marjoux, S., Frin-Mathy, G., Bernard, G., Hébuterne, X., et al. (2011) · The American Journal of Gastroenterology · doi:10.1038/ajg.2011.315 · Cited by 141 · see citing works
O’Malley, D., Quigley, E. M. M., Dinan, T. G., & Cryan, J. F. (2011) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2011.04.009 · Cited by 139 · see citing works
Wilcz‐Villega, E., McClean, S., & OʼSullivan, M. (2013) · The American Journal of Gastroenterology · doi:10.1038/ajg.2013.92 · Cited by 135 · see citing works
Bednarska, O., Walter, S. A., Casado‐Bedmar, M., Ström, M., Salvo‐Romero, E., Vicario, M., Mayer, E. A., & Keita, Å. V. (2017) · Gastroenterology · doi:10.1053/j.gastro.2017.06.051 · Cited by 133 · see citing works
New Perspectives on the Potential Role of Aquaporins (AQPs) in the Physiology of Inflammation
Meli, R., Pirozzi, C., & Pelagalli, A. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00101 · Cited by 133 · see citing works
Moussaoui, N., Jacobs, J. P., Larauche, M. H., Biraud, M., Million, M., Mayer, E. A., & Taché, Y. (2016) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm16105 · Cited by 133 · see citing works
Ruan, Z., Liu, S., Zhou, Y., Mi, S., Liu, G., Wu, X., Kang, Y., Assaad, H., Deng, Z., Hou, Y., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0097815 · Cited by 122 · see citing works
Central and peripheral hypersensitivity in the irritable bowel syndrome
Zhou, Q., Fillingim, R. B., Riley, J. L., Malarkey, W. B., & Verne, N. G. (2010) · Pain · doi:10.1016/j.pain.2009.12.005 · Cited by 121 · see citing works
Self-citationLee, H., Park, J. H., Park, D. I., Kim, H. J., Cho, Y. K., Sohn, C. I., Jeon, W. K., Kim, B. I., & Chae, S. W. (2013) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm.2013.19.2.244 · Cited by 119 · see citing works
Claudin-related intestinal diseases
Barmeyer, C., Schulzke, J. D., & Fromm, M. (2015) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2015.05.006 · Cited by 120 · see citing works
Midenfjord, I., Polster, A. V., Sjövall, H., Törnblom, H., & Simrén, M. (2019) · Neurogastroenterology & Motility · doi:10.1111/nmo.13619 · Cited by 115 · see citing works
Cellular and Molecular Basis of Intestinal Barrier Dysfunction in the Irritable Bowel Syndrome
Martínez, C., González-Castro, A. M., Vicario, M., & Santos, J. (2012) · Gut and Liver · doi:10.5009/gnl.2012.6.3.305 · Cited by 115 · see citing works
Alteration of intestinal barrier function during activity-based anorexia in mice
Jésus, P., Ouelaa, W., François, M., Riachy, L., Guérin, C., Aziz, M., Do Rego, J.-C., Déchelotte, P., Fetissov, S. O., & Coëffier, M. (2014) · Clinical Nutrition · doi:10.1016/j.clnu.2013.11.006 · Cited by 114 · see citing works
Shulman, R. J., Hollister, E. B., Cain, K., Czyzewski, D. I., Self, M. M., Weidler, E. M., Devaraj, S., Luna, R. A., Versalovic, J., & Heitkemper, M. (2017) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2016.03.045 · Cited by 113 · see citing works
Camilleri, M., Lyle, B. J., Madsen, K. L., Sonnenburg, J. L., Verbeke, K., & Wu, G. D. (2019) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00063.2019 · Cited by 111 · see citing works
Mechanisms of Stress-induced Visceral Pain
Meerveld, B. G., & Johnson, A. C. (2018) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm17137 · Cited by 109 · see citing works
Mujagic, Z., Ludidi, S., Keszthelyi, D., Hesselink, M., Kruimel, J. W., Lenaerts, K., Hanssen, N. M. J., Conchillo, J. M., Jonkers, D. M. A. E., & Masclee, A. (2014) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.12829 · Cited by 108 · see citing works
Intestinal microbiota in pathophysiology and management of irritable bowel syndrome.
(2014) · PubMed Central · doi:10.3748/wjg.v20.i27.8886 · Cited by 106 · see citing works
Anti-nociceptive effect of Faecalibacterium prausnitzii in non-inflammatory IBS-like models
Miquel, S., Martín, R., Lashermes, A., Gillet, M., Meleine, M., Gelot, A., Eschalier, A., Ardid, D., Bermúdez-Humarán, L. G., Sokol, H., et al. (2016) · Scientific Reports · doi:10.1038/srep19399 · Cited by 105 · see citing works
Mast cell mediation of visceral sensation and permeability in irritable bowel syndrome
Hasler, W. L., Grabauskas, G., Singh, P., & Owyang, C. (2022) · Neurogastroenterology & Motility · doi:10.1111/nmo.14339 · Cited by 105 · see citing works
Agostini, S., Goubern, M., Tondereau, V., Salvador–Cartier, C., Bézirard, V., Lévèque, M., Keränen, H., Théodorou, V., Bourdu-Naturel, S., Goupil-Feuillerat, N., et al. (2012) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2011.01865.x · Cited by 106 · see citing works
Inflammation in irritable bowel syndrome: Myth or new treatment target?
Sinagra, E., Pompei, G., Tomasello, G., Cappello, F., Morreale, G. C., Amvrosiadis, G., Rossi, F., Monte, A. I. L., Rizzo, A. G., & Raimondo, D. (2016) · World Journal of Gastroenterology · doi:10.3748/wjg.v22.i7.2242 · Cited by 102 · see citing works
Carco, C., Young, W., Gearry, R. B., Talley, N. J., McNabb, W. C., & Roy, N. C. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.00468 · Cited by 97 · see citing works
Linsalata, M., Riezzo, G., D’Attoma, B., Clemente, C., Orlando, A., & Russo, F. (2018) · BMC Gastroenterology · doi:10.1186/s12876-018-0888-6 · Cited by 97 · see citing works
Annaházi, A., Ferrier, L., Bézirard, V., Lévêque, M., Eutamène, H., Ait-Belgnaoui, A., Coëffier, M., Ducrotté, P., Róka, R., Inczefi, O., et al. (2013) · American Journal of Gastroenterology · doi:10.1038/ajg.2013.152 · Cited by 96 · see citing works
Giardia spp. and the Gut Microbiota: Dangerous Liaisons
Fekete, E., Allain, T., Siddiq, A., Sosnowski, O., & Buret, A. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.618106 · Cited by 82 · see citing works
Gecse, K. B., Róka, R., Séra, T., Rosztoczy, A. I., Annaházi, A., Izbéki, F., Nagy, F. T., Molnár, T., Szepes, Z., Pávics, L., et al. (2011) · Digestion · doi:10.1159/000333083 · Cited by 93 · see citing works
Stress-Related Alterations of Visceral Sensation: Animal Models for Irritable Bowel Syndrome Study
Larauche, M. H., Mulak, A., & Taché, Y. (2011) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm.2011.17.3.213 · Cited by 92 · see citing works
Tooth, D., Garsed, K., Singh, G., Marciani, L., Lam, C., Fordham, I., Fields, A., Banwait, R., Lingaya, M., Layfield, R., et al. (2013) · Gut · doi:10.1136/gutjnl-2012-304042 · Cited by 87 · see citing works
Benson, S., Kattoor, J., Wegner, A., Hammes, F., Reidick, D., Grigoleit, J.-S., Engler, H., Oberbeck, R., Schedlowski, M., & Elsenbruch, S. (2012) · Pain · doi:10.1016/j.pain.2011.12.001 · Cited by 89 · see citing works
Molecular 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
Low-level inflammation, immunity, and brain-gut axis in IBS: unraveling the complex relationships
Yuan, Y., Wang, X., Huang, S., Wang, H., & Shen, G.-M. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2263209 · Cited by 92 · see citing works
Serum zonulin and its diagnostic performance in non-coeliac gluten sensitivity
Barbaro, M. R., Cremon, C., Morselli‐Labate, A. M., Sabatino, A. D., Giuffrida, P., Corazza, G. R., Stefano, M. D., Caio, G., Latella, G., Ciacci, C., et al. (2020) · Gut · doi:10.1136/gutjnl-2019-319281 · Cited by 88 · see citing works
Li, X., Kan, E. M., Lu, J., Cao, Y., Wong, R. K. M., Keshavarzian, A., & Wilder‐Smith, C. H. (2013) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.12269 · Cited by 87 · see citing works
Impact of diet on symptoms of the irritable bowel syndrome
Spiller, R. (2021) · Nutrients · doi:10.3390/nu13020575 · Cited by 86 · see citing works
Shulman, R. J., Jarrett, M. E., Cain, K. C., Broussard, E. K., & Heitkemper, M. M. (2014) · Journal of Gastroenterology · doi:10.1007/s00535-013-0919-6 · Cited by 85 · see citing works
Fodor, A. A., Pimentel, M., Chey, W. D., Lembo, A. J., Golden, P. L., Israel, R. J., & Carroll, I. M. (2018) · Gut Microbes · doi:10.1080/19490976.2018.1460013 · Cited by 84 · see citing works
Effect 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
Fukui, H., Oshima, T., Tanaka, Y., Oikawa, Y., Makizaki, Y., Ohno, H., Tomita, T., Watari, J., & Miwa, H. (2018) · Scientific Reports · doi:10.1038/s41598-018-30943-3 · Cited by 81 · see citing works
Pigrau, M., Rodiño‐Janeiro, B. K., Casado‐Bedmar, M., Lobo, B., Vicario, M., Santos, J., & Alonso, C. (2015) · Neurogastroenterology & Motility · doi:10.1111/nmo.12717 · Cited by 79 · see citing works
Barbara, G., Zecchi, L., Barbaro, M. R., Cremon, C., Bellacosa, L., Marcellini, M. M., GIORGIO, R. D., Corinaldesi, R., & Stanghellini, V. (2012) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0b013e318264e918 · Cited by 79 · see citing works
Layer, P., Andresen, V., Allescher, H. ‐., Bischoff, S. C., Claßen, M., Elsenbruch, S., Freitag, M., Frieling, T., Gebhard, M., Goebel‐Stengel, M., et al. (2021) · Zeitschrift für Gastroenterologie · doi:10.1055/a-1591-4794 · Cited by 78 · see citing works
Chen, Q., Ren, Y., Lu, J., Bartlett, M., Chen, L., Zhang, Y., Guo, X., & Liu, C. (2017) · Nutrients · doi:10.3390/nu9121341 · Cited by 75 · see citing works
The Role of Bacteria, Probiotics and Diet in Irritable Bowel Syndrome
Harper, A. J., Naghibi, M., & Garcha, D. S. (2018) · Foods · doi:10.3390/foods7020013 · Cited by 77 · see citing works
Aboushanab, S. A., Khedr, S. M., Гетте, И. Ф., Danilova, I. G., Кольберг, Н. А., Ravishankar, G. A., Rao, A. R., & Kovaleva, E. G. (2021) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2021.1946006 · Cited by 75 · see citing works
Camilleri, M., & Lorenzo, C. D. (2011) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0b013e31823d34c3 · Cited by 74 · see citing works
Risk factors associated with intestinal permeability in an adult population: A systematic review
Leech, B., McIntyre, E., Steel, A., & Sibbritt, D. W. (2019) · International Journal of Clinical Practice · doi:10.1111/ijcp.13385 · Cited by 72 · see citing works
Multispecies probiotic protects gut barrier function in experimental models
Vivinus-Nébot, M. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i22.6832 · Cited by 72 · see citing works
Øines, E., Murison, R., Mrdalj, J., Grønli, J., & Milde, A. M. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.11.024 · Cited by 66 · see citing works
Food Additives, Gut Microbiota, and Irritable Bowel Syndrome: A Hidden Track
Rinninella, E., Cintoni, M., Raoul, P. C., Gasbarrini, A., & Mele, M. C. (2020) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph17238816 · Cited by 70 · see citing works
Serum zonulin is elevated in IBS and correlates with stool frequency in IBS‐D
Singh, P., Silvester, J. A., Chen, X., Xu, H. J., Sawhney, V., Rangan, V., Iturrino, J., Nee, J. W., Duerksen, D. R., & Lembo, A. J. (2019) · United European Gastroenterology Journal · doi:10.1177/2050640619826419 · Cited by 67 · see citing works
Zong, Y., Zhu, S., Zhang, S., Zheng, G., Wiley, J. W., & Hong, S. (2018) · Neurogastroenterology & Motility · doi:10.1111/nmo.13477 · Cited by 69 · see citing works
Markers for visceral hypersensitivity in patients with irritable bowel syndrome
Ludidi, S., Mujagic, Z., Jonkers, D. M. A. E., Keszthelyi, D., Hesselink, M., Kruimel, J. W., Conchillo, J. M., & Masclee, A. (2014) · Neurogastroenterology & Motility · doi:10.1111/nmo.12365 · Cited by 66 · see citing works
Ko, S., Han, G., Kim, S.-K., Seo, J., Chung, W., Ryu, B., Kim, J., Yeo, I., Lee, B., Lee, J., et al. (2013) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2013/824605 · Cited by 62 · see citing works
- Authors
- Zhou, Q., Zhang, B., & Verne, N. G.
- Affiliations
- The Ohio State University (US)
- Cincinnati VA Medical Center (US)
- Corresponding author
- Verne, Nicholas G.
- Venue
- Pain
- Published
- 2009-11
- Volume
- 146
- Issue
- 1
- Pages
- 41-46
- ISSN
- 0304-3959 (ISSN-L)
- PMC
- PMC2763174
- OpenAlex
- W1967139826
- Cited by
- 373
- References
- 48
- Citations by year
- 2026: 15 · 2025: 12 · 2024: 18 · 2023: 15 · 2022: 20 · 2021: 36 · 2020: 26 · 2019: 25 · 2018: 29 · 2017: 25 · 2016: 22 · 2015: 18 · 2014: 29 · 2013: 25 · 2012: 21
- FWCI
- 20.54
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Pain (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (R01NS053090)
- National Center for Research Resources (M01RR000082)
- Topics
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
- Keywords
- irritable bowel syndrome, diarrhea-predominant irritable bowel syndrome, intestinal permeability, visceral hypersensitivity, thermal hypersensitivity, lactulose/mannitol test, visceral pain, IBS symptom severity, gut-brain axis
- MeSH terms
- Adult, Catheterization, Cell Membrane Permeability, Diarrhea, Female, Hot Temperature, Humans, Hypersensitivity, Intestinal Mucosa, Male, Pain, Pain Measurement, Physical Stimulation, Severity of Illness Index, Irritable Bowel Syndrome
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