Leaky gut: mechanisms, measurement and clinical implications in humans
Open accessAbstract
The objectives of this review on 'leaky gut' for clinicians are to discuss the components of the intestinal barrier, the diverse measurements of intestinal permeability, their perturbation in non-inflammatory 'stressed states' and the impact of treatment with dietary factors. Information on 'healthy' or 'leaky' gut in the public domain requires confirmation before endorsing dietary exclusions, replacement with non-irritating foods (such as fermented foods) or use of supplements to repair the damage. The intestinal barrier includes surface mucus, epithelial layer and immune defences. Epithelial permeability results from increased paracellular transport, apoptosis or transcellular permeability. Barrier function can be tested in vivo using orally administered probe molecules or in vitro using mucosal biopsies from humans, exposing the colonic mucosa from rats or mice or cell layers to extracts of colonic mucosa or stool from human patients. Assessment of intestinal barrier requires measurements beyond the epithelial layer. 'Stress' disorders such as endurance exercise, non-steroidal anti-inflammatory drugs administration, pregnancy and surfactants (such as bile acids and dietary factors such as emulsifiers) increase permeability. Dietary factors can reverse intestinal leakiness and mucosal damage in the 'stress' disorders. Whereas inflammatory or ulcerating intestinal diseases result in leaky gut, no such disease can be cured by simply normalising intestinal barrier function. It is still unproven that restoring barrier function can ameliorate clinical manifestations in GI or systemic diseases. Clinicians should be aware of the potential of barrier dysfunction in GI diseases and of the barrier as a target for future therapy.
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Dietary habits and a healthy lifestyle are of the foremost importance in maintaining healthy intestinal barrier functions.
“Last, but definitely not the least, dietary habits and a healthy lifestyle are of the foremost importance in maintaining healthy intestinal barrier functions.207”
From Regulation of Intestinal Barrier Function by Microbial Metabolites (2021) · cites this paper as [207]
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Intestinal mucosal barrier function in health and disease
Turner, J. R. (2009) · Nature reviews. Immunology · doi:10.1038/nri2653 · Cited by 3,952 · see citing works
Cytokines sing the blues: inflammation and the pathogenesis of depression
Raison, C. L., Capuron, L., & Miller, A. H. (2006) · Trends in Immunology · doi:10.1016/j.it.2005.11.006 · Cited by 3,009 · see citing works
Peng, L., Li, Z.-R., Green, R. S., Holzmanr, I. R., & Lin, J. (2009) · The Journal of Nutrition · doi:10.3945/jn.109.104638 · Cited by 2,130 · see citing works
Dietary emulsifiers impact the mouse gut microbiota promoting colitis and metabolic syndrome
Chassaing, B., Koren, O., Goodrich, J. K., Poole, A. C., Srinivasan, S., Ley, R. E., & Gewirtz, A. T. (2015) · Nature · doi:10.1038/nature14232 · Cited by 2,055 · see citing works
Gut microbiota are related to Parkinson's disease and clinical phenotype
Scheperjans, F., Aho, V., Pereira, P. A. B., Koskinen, K., Paulin, L., Pekkonen, E., Haapaniemi, E., Kaakkola, S., Eerola‐Rautio, J., Pohja, M., et al. (2015) · Movement Disorders · doi:10.1002/mds.26069 · Cited by 1,968 · see citing works
Intestinal permeability – a new target for disease prevention and therapy
Bischoff, S. C., Barbara, G., Buurman, W., Ockhuizen, T., Schulzke, J.-D., Serino, M., Tilg, H., Watson, A., & Wells, J. M. (2014) · BMC Gastroenterology · doi:10.1186/s12876-014-0189-7 · Cited by 1,755 · see citing works
Zhu, L., Baker, S. S., Gill, C., Liu, W., Alkhouri, R., Baker, R. D., & Gill, S. R. (2013) · Hepatology · doi:10.1002/hep.26093 · Cited by 1,708 · see citing works
Van der Sluis, M., De Koning, B. A. E., De Bruijn, A. C. J. M., Velcich, A., Meijerink, J. P. P., Van Goudoever, J. B., Büller, H. A., Dekker, J., Van Seuningen, I., Renes, I. B., et al. (2006) · Gastroenterology · doi:10.1053/j.gastro.2006.04.020 · Cited by 1,684 · see citing works
Control of pathogens and pathobionts by the gut microbiota
Kamada, N., Chen, G. Y., Inohara, N., & Núñez, G. (2013) · Nature Immunology · doi:10.1038/ni.2608 · Cited by 1,625 · see citing works
Pelaseyed, T., Bergström, J. H., Gustafsson, J. K., Ermund, A., Birchenough, G. M. H., Schütte, A., van der Post, S., Svensson, F., Rodríguez‐Piñeiro, A. M., Nyström, E. E. L., et al. (2014) · Immunological Reviews · doi:10.1111/imr.12182 · Cited by 1,363 · see citing works
The intestinal epithelial barrier: a therapeutic target?
Odenwald, M. A., & Turner, J. R. (2017) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2016.169 · Cited by 1,288 · see citing works
Colonic bacterial composition in Parkinson's disease
Keshavarzian, A., Green, S. J., Engen, P. A., Voigt, R. M., Naqib, A., Forsyth, C. B., Mutlu, E., & Shannon, K. M. (2015) · Movement Disorders · doi:10.1002/mds.26307 · Cited by 1,281 · see citing works
Kelly, J. R., Kennedy, P. J., Cryan, J. F., Dinan, T. G., Clarke, G., & Hyland, N. P. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00392 · Cited by 1,110 · see citing works
Immunological aspects of intestinal mucus and mucins
Johansson, M. E. V., & Hansson, G. C. (2016) · Nature Reviews Immunology · doi:10.1038/nri.2016.88 · Cited by 1,007 · see citing works
Forsyth, C. B., Shannon, K. M., Kordower, J. H., Voigt, R. M., Shaikh, M., Jaglin, J. A., Estes, J. D., Dodiya, H. B., & Keshavarzian, A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028032 · Cited by 974 · see citing works
Hyperglycemia drives intestinal barrier dysfunction and risk for enteric infection
Thaiss, C. A., Levy, M., Grosheva, I., Zheng, D., Soffer, E., Blacher, E., Braverman, S., Tengeler, A. C., Barak, O., Elazar, M., et al. (2018) · Science · doi:10.1126/science.aar3318 · Cited by 942 · see citing works
Chelakkot, C., Choi, Y., Kim, D., Park, H. T., Ghim, J., Kwon, Y., Jeon, J., Kim, M.-S., Jee, Y., Gho, Y. S., et al. (2018) · Experimental & Molecular Medicine · doi:10.1038/emm.2017.282 · Cited by 859 · see citing works
Increased Intestinal Permeability in Patients with Crohn's Disease and Their Relatives
Hollander, D., Vadheim, C. M., Brettholz, E., Petersen, G. M., Delahunty, T., & Rotter, J. I. (1986) · Annals of Internal Medicine · doi:10.7326/0003-4819-105-6-883 · Cited by 762 · see citing works
Bile Salts and Glycine as Cogerminants for <i>Clostridium difficile</i> Spores
Sorg, J. A., & Sonenshein, A. L. (2008) · Journal of Bacteriology · doi:10.1128/jb.01765-07 · Cited by 711 · see citing works
Michielan, A., & D’Incà, R. (2015) · Mediators of Inflammation · doi:10.1155/2015/628157 · Cited by 709 · see citing works
The composition of the gut microbiota shapes the colon mucus barrier
Jakobsson, H. E., Rodríguez‐Piñeiro, A. M., Schütte, A., Ermund, A., Boysen, P., Bemark, M., Sommer, F., Bäckhed, F., Hansson, G. C., & Johansson, M. E. (2015) · The EMBO Reports · doi:10.15252/embr.201439263 · Cited by 700 · see citing works
Alterations in intestinal permeability
Arrieta, M., Bistritz, L., & Meddings, J. B. (2006) · Gut · doi:10.1136/gut.2005.085373 · Cited by 634 · see citing works
Vanuytsel, T., van Wanrooy, S., Vanheel, H., Vanormelingen, C., Verschueren, S., Houben, E., Salim Rasoel, S., Tόth, J., Holvoet, L., Farré, R., et al. (2014) · Gut · doi:10.1136/gutjnl-2013-305690 · Cited by 615 · see citing works
Hiippala, K., Jouhten, H., Ronkainen, A., Hartikainen, A., Kainulainen, V., Jalanka, J., & Satokari, R. M. (2018) · Nutrients · doi:10.3390/nu10080988 · Cited by 605 · see citing works
Mechanisms of Damage to the Gastrointestinal Tract From Nonsteroidal Anti-Inflammatory Drugs
Bjarnason, I., Scarpignato, C., Holmgren, E., Olszewski, M., Rainsford, K. D., & Lanas, Á. (2017) · Gastroenterology · doi:10.1053/j.gastro.2017.10.049 · Cited by 550 · see citing works
Role of Inflammation in Muscle Homeostasis and Myogenesis
Costamagna, D., Costelli, P., Sampaolesi, M., & Penna, F. (2015) · Mediators of Inflammation · doi:10.1155/2015/805172 · Cited by 532 · see citing works
Stevens, B. R., Goel, R., Seungbum, K., Richards, E. M., Holbert, R. C., Pepine, C. J., & Raizada, M. K. (2018) · Gut · doi:10.1136/gutjnl-2017-314759 · Cited by 508 · see citing works
Verdile, G., Keane, K. N., Cruzat, V. F., Medic, S., Sabale, M., Rowles, J., Wijesekara, N., Martins, R. N., Fraser, P. E., & Newsholme, P. (2015) · Mediators of Inflammation · doi:10.1155/2015/105828 · Cited by 501 · see citing works
Probiotic Escherichia coli Nissle 1917 inhibits leaky gut by enhancing mucosal integrity
Ukena, S. N., Singh, A., Dringenberg, U., Engelhardt, R., Seidler, U., Hansen, W., Bleich, A., Bruder, D., Franzke, A., Rogler, G., et al. (2007) · PLoS ONE · doi:10.1371/journal.pone.0001308 · Cited by 482 · see citing works
The Human Microbiome and Obesity: Moving beyond Associations
Maruvada, P., Leone, V., Kaplan, L. M., & Chang, E. B. (2017) · Cell Host & Microbe · doi:10.1016/j.chom.2017.10.005 · Cited by 468 · see citing works
Gut microbiota: A player in aging and a target for anti-aging intervention
Vaiserman, A. M., Koliada, A. K., & Marotta, F. (2017) · Ageing Research Reviews · doi:10.1016/j.arr.2017.01.001 · Cited by 465 · see citing works
Vázquez‐Roque, M. I., Camilleri, M., Smyrk, T. C., Murray, J. A., Marietta, E. V., O’Neill, J., Carlson, P., Lamsam, J. L., Janzow, D., Eckert, D. J., et al. (2013) · Gastroenterology · doi:10.1053/j.gastro.2013.01.049 · Cited by 454 · see citing works
Self-citationMaes, M., Kubera, M., Leunis, J.-C., & Berk, M. (2012) · Journal of Affective Disorders · doi:10.1016/j.jad.2012.02.023 · Cited by 446 · see citing works
Yu, L. C. (2018) · Journal of Biomedical Science · doi:10.1186/s12929-018-0483-8 · Cited by 404 · 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
Self-citationKarl, J. P., Margolis, L. M., Madslien, E. H., Murphy, N. E., Castellani, J. W., Gundersen, Y., Hoke, A. V., Levangie, M. W., Kumar, R., Chakraborty, N., et al. (2017) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00066.2017 · Cited by 373 · see citing works
Intestinal Permeability Defects: Is It Time to Treat?
Odenwald, M. A., & Turner, J. R. (2013) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2013.07.001 · Cited by 366 · see citing works
Bühner, S., Büning, C., Genschel, J., Kling, K., Herrmann, D., Dignass, A., Kuechler, I., Krueger, S., Schmidt, H. H.-J., & Lochs, H. (2005) · Gut · doi:10.1136/gut.2005.065557 · Cited by 366 · see citing works
Krumbeck, J. A., Rasmussen, H. E., Hutkins, R. W., Clarke, J., Shawron, K., Keshavarzian, A., & Walter, J. (2018) · Microbiome · doi:10.1186/s40168-018-0494-4 · Cited by 342 · see citing works
Fritscher-Ravens, A., Schuppan, D., Ellrichmann, M., Schoch, S., Röcken, C., Brasch, J., Bethge, J., Böttner, M., Klose, J., & Milla, P. J. (2014) · Gastroenterology · doi:10.1053/j.gastro.2014.07.046 · Cited by 329 · see citing works
Zhang, R., Miller, R. G., Gascon, R., Champion, S., Katz, J., Lancero, M., Narvaez, A., Honrada, R., Ruvalcaba, D., & McGrath, M. S. (2009) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2008.09.017 · Cited by 319 · see citing works
Gut microbiota as a source of novel antimicrobials
García-Gutiérrez, E., Mayer, M. J., Cotter, P. D., & Narbad, A. (2018) · Gut Microbes · doi:10.1080/19490976.2018.1455790 · Cited by 298 · see citing works
Structural alterations of the intestinal epithelial barrier in Parkinson’s disease
Clairembault, T., Leclair‐Visonneau, L., Coron, E., Bourreille, A., Dily, S. L., Vavasseur, F., Heymann, M., Neunlist, M., & Derkinderen, P. (2015) · Acta Neuropathologica Communications · doi:10.1186/s40478-015-0196-0 · Cited by 292 · see citing works
Keita, Å. V., & Söderholm, J. D. (2010) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2010.01498.x · Cited by 286 · see citing works
Hepatic Injury in Nonalcoholic Steatohepatitis Contributes to Altered Intestinal Permeability
Luther, J., Garber, J. J., Khalili, H., Dave, M., Bale, S. S., Jindal, R., Motola, D. L., Luther, S., Bohr, S., Jeoung, S. W., et al. (2015) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2015.01.001 · Cited by 286 · see citing works
Roberts, C. L., Keita, Å. V., Duncan, S. H., O’Kennedy, N., Söderholm, J. D., Rhodes, J. M., & Campbell, B. J. (2010) · Gut · doi:10.1136/gut.2009.195370 · Cited by 285 · see citing works
Bjarnason, I., Peters, T. B., & Veall, N. (1983) · The Lancet · doi:10.1016/s0140-6736(83)91628-8 · Cited by 268 · see citing works
Bergmann, K. R., Liu, S. X. L., Tian, R., Kushnir, A., Turner, J. R., Li, H.-L., Chou, P. M., Weber, C. R., & Plaen, I. G. D. (2013) · American Journal Of Pathology · doi:10.1016/j.ajpath.2013.01.013 · Cited by 268 · see citing works
Summa, K. C., Voigt, R. M., Forsyth, C. B., Shaikh, M. W., Cavanaugh, K. E., Tang, Y., Vitaterna, M. H., Song, S., Turek, F. W., & Keshavarzian, A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0067102 · Cited by 254 · see citing works
Measurements of Intestinal Permeability Using Low Molecular Weight Polyethylene Glycols (PEG 400)
CHADWICK, V. S., Phillips, S. F., & Hofmann, A. F. (1977) · Gastroenterology · doi:10.1016/s0016-5085(19)32197-3 · Cited by 251 · see citing works
Gut inflammation and dysbiosis in human motor neuron disease
Rowin, J., Xia, Y., Jung, B., & Sun, J. (2017) · Physiological Reports · doi:10.14814/phy2.13443 · Cited by 224 · see citing works
Intra-Articular Cytokine Levels in Adolescent Patients after Anterior Cruciate Ligament Tear
Bigoni, M., Turati, M., Zatti, G., Gandolla, M., Sacerdote, P., Piatti, M., Castelnuovo, A., Rigamonti, L., Munegato, D., Franchi, S., et al. (2018) · Mediators of Inflammation · doi:10.1155/2018/4210593 · Cited by 220 · see citing works
Intestinal Permeability Test As A Predictor of Clinical Course in Crohn's Disease
Renata D'Incà, Leo, V. D., Corrao, G., Martines, D., D’Odorico, A., Mestriner, C., Venturi, C., Longo, G., & Sturniolo, G. C. (1999) · The American Journal of Gastroenterology · doi:10.1111/j.1572-0241.1999.01444.x · Cited by 218 · see citing works
Overview and systematic review of studies of microbiome in schizophrenia and bipolar disorder
Nguyen, T. T., Kościółek, T., Eyler, L. T., Knight, R. D., & Jeste, D. V. (2018) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2018.01.013 · Cited by 210 · see citing works
Fang, X., Wang, X., Yang, S., Meng, F., Wang, X., Wei, H., & Chen, T. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01479 · Cited by 206 · see citing works
Zhou, Y., Jiang, Z., Sun, Y., Wang, X., Ma, E. L., & Wilmore, D. W. (2003) · Journal of Parenteral and Enteral Nutrition · doi:10.1177/0148607103027004241 · Cited by 205 · see citing works
Gut permeability and food allergies
Perrier, C., & Corthésy, B. (2010) · Clinical & Experimental Allergy · doi:10.1111/j.1365-2222.2010.03639.x · Cited by 203 · 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
Intestinal permeability and inflammation in patients on NSAIDs
Sigthorsson, G., Tibble, J. A., Hayllar, J. S., Menzies, I. S., Macpherson, A. J., Moots, R. J., Scott, D. L., Gumpel, M., & Bjarnason, I. (1998) · Gut · doi:10.1136/gut.43.4.506 · Cited by 190 · see citing works
Man, A., Bertelli, E., Rentini, S., Regoli, M., Briars, G., Marini, M., Watson, A., & Nicoletti, C. (2015) · Clinical science · doi:10.1042/cs20150046 · Cited by 189 · see citing works
Esophageal Microbiome in Eosinophilic Esophagitis
Harris, J. K., Fang, R., Wagner, B. D., Choe, H. N., Kelly, C. J., Schroeder, S. R., Moore, W. R., Stevens, M. J., Yeckes, A. R., Amsden, K., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0128346 · Cited by 172 · see citing works
Kapil, S., Duseja, A. K., Sharma, B. K., Singla, B., Chakraborti, A., Das, A., Ray, P., Dhiman, R. K., & Chawla, Y. K. (2015) · Journal of Gastroenterology and Hepatology · doi:10.1111/jgh.13058 · Cited by 172 · see citing works
Peng, X., Yan, H., You, Z., Wang, P., & Wang, S. (2004) · Burns · doi:10.1016/j.burns.2003.09.032 · Cited by 166 · see citing works
Intestinal Permeability Biomarker Zonulin is Elevated in Healthy Aging
Qi, Y., Goel, R., Kim, S., Richards, E. M., Carter, C. S., Pepine, C. J., Raizada, M. K., & Buford, T. W. (2017) · Journal of the American Medical Directors Association · doi:10.1016/j.jamda.2017.05.018 · Cited by 165 · see citing works
Marchbank, T., Davison, G., Oakes, J. R., Ghatei, M. A., Patterson, M., Moyer, M. P., & Playford, R. J. (2011) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00281.2010 · Cited by 163 · see citing works
Inflammation-associated microbiota in pediatric eosinophilic esophagitis
Benitez, A., Hoffmann, C., Muir, A. B., Dods, K. K., Spergel, J. M., Bushman, F. D., & Wang, M. (2015) · Microbiome · doi:10.1186/s40168-015-0085-6 · Cited by 162 · 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
Self-citationMokkala, K., Röytiö, H., Munukka, E., Pietilä, S., Ekblad, U., Rönnemaa, T., Eerola, E., Laiho, A., & Laitinen, K. (2016) · Journal of Nutrition · doi:10.3945/jn.116.235358 · Cited by 145 · see citing works
Intestinal permeability in patients with adverse reactions to food
Ventura, M. T., Polimeno, L., Amoruso, A., Gatti, F. L., Annoscia, E., Marinaro, M., Leo, E. D., Matino, M., Buquicchio, R., Bonini, S., et al. (2006) · Digestive and Liver Disease · doi:10.1016/j.dld.2006.06.012 · Cited by 144 · see citing works
Association Between Exercise-Induced Hyperthermia and Intestinal Permeability: A Systematic Review
Pires, W., Veneroso, C. E., Wanner, S. P., Pacheco, D. A. S., Vaz, G. C., Amorim, F. T., Tonoli, C., Soares, D. D., & Coimbra, C. C. (2016) · Sports Medicine · doi:10.1007/s40279-016-0654-2 · Cited by 141 · see citing works
Leaky gut – concept or clinical entity?
Quigley, E. M. M. (2016) · Current Opinion in Gastroenterology · doi:10.1097/mog.0000000000000243 · Cited by 139 · see citing works
Ponziani, F. R., Zocco, M. A., Cerrito, L., Gasbarrini, A., & Pompili, M. (2018) · Expert Review of Gastroenterology & Hepatology · doi:10.1080/17474124.2018.1481747 · Cited by 139 · see citing works
Synthetic surfactant food additives can cause intestinal barrier dysfunction
Csáki, K. F. (2011) · Medical Hypotheses · doi:10.1016/j.mehy.2011.01.030 · Cited by 126 · see citing works
Russo, F., Linsalata, M., Clemente, C., Chiloiro, M., Orlando, A., Marconi, E., Chimienti, G., & Riezzo, G. (2012) · Nutrition Research · doi:10.1016/j.nutres.2012.09.010 · Cited by 126 · see citing works
Mahmood, A., FitzGerald, A. J., Marchbank, T., Ntatsaki, E., Murray, D., Ghosh, S., & Playford, R. J. (2007) · Gut · doi:10.1136/gut.2006.099929 · Cited by 119 · see citing works
Meng, X., Li, S., Li, Y., Gan, R., & Li, H. (2018) · Nutrients · doi:10.3390/nu10101457 · Cited by 117 · 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
Plaisancié, P., Barcelo, A., Moro, F., Claustre, J., Chayvialle, J., & Cuber, J.-C. (1998) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1998.275.5.g1073 · Cited by 111 · see citing works
Lock, J. Y., Carlson, T. L., Wang, C.-M., Chen, A., & Carrier, R. L. (2018) · Scientific Reports · doi:10.1038/s41598-018-27957-2 · Cited by 105 · see citing works
Demehri, F. R., Barrett, M., Ralls, M. W., Miyasaka, E. A., Feng, Y., & Teitelbaum, D. H. (2013) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2013.00105 · Cited by 102 · see citing works
Krawczyk, M. J., Maciejewska, D., Ryterská, K., Czerwińska-Rogowska, M., Jamioł-Milc, D., Skonieczna‐Żydecka, K., Milkiewicz, P., Raszeja‐Wyszomirska, J., & Stachowska, E. (2018) · Nutrients · doi:10.3390/nu10111793 · Cited by 98 · see citing works
Karhu, E., Forsgård, R. A., Alanko, L., Alfthan, H. V., Pussinen, P. J., Hämäläinen, E. K., & Korpela, R. (2017) · European Journal of Applied Physiology · doi:10.1007/s00421-017-3739-1 · Cited by 96 · see citing works
The Gut-Brain Axis in Alzheimer’s Disease and Omega-3. A Critical Overview of Clinical Trials
Rosa, F. L., Clerici, M., Ratto, D., Occhinegro, A., Licito, A., Romeo, M., Iorio, C. D., & Rossi, P. (2018) · Nutrients · doi:10.3390/nu10091267 · Cited by 93 · see citing works
Intestinal permeability in children with food allergy on specific elimination diets
Järvinen, K. M., Konstantinou, G. Ν., Pilapil, M., et al. (2013) · Pediatric Allergy and Immunology · doi:10.1111/pai.12106 · Cited by 89 · see citing works
The microbiome as a novel paradigm in studying stress and mental health.
Liu, R. T. (2017) · American Psychologist · doi:10.1037/amp0000058 · Cited by 89 · see citing works
Gut Microbiota as a Driver of Inflammation in Nonalcoholic Fatty Liver Disease
Bibbò, S., Ianiro, G., Dore, M. P., Simonelli, C., Newton, E. E., & Cammarota, G. (2018) · Mediators of Inflammation · doi:10.1155/2018/9321643 · Cited by 87 · see citing works
Mokkala, K., Pellonperä, O., Röytiö, H., Pussinen, P. J., Rönnemaa, T., & Laitinen, K. (2017) · Metabolism · doi:10.1016/j.metabol.2016.12.015 · Cited by 86 · see citing works
Benjamin, J., Makharia, G. K., Ahuja, V., Rajan, A., Kalaivani, M., Gupta, S. D., & Joshi, Y. K. (2011) · Digestive Diseases and Sciences · doi:10.1007/s10620-011-1947-9 · Cited by 85 · see citing works
Enteral nutrient deprivation in patients leads to a loss of intestinal epithelial barrier function
Ralls, M. W., Demehri, F. R., Feng, Y., Ignatoski, K. M. W., & Teitelbaum, D. H. (2015) · Surgery · doi:10.1016/j.surg.2014.12.004 · Cited by 84 · see citing works
L-Citrulline Improves Splanchnic Perfusion and Reduces Gut Injury during Exercise
van Wijck, K., Wijnands, K. A. P., Meesters, D. M., Boonen, B., van Loon, L. J. C., Buurman, W. A., Dejong, C. H. C., Lenaerts, K., & Poeze, M. (2014) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000000332 · Cited by 83 · see citing works
Terciolo, C., Dapoigny, M. C., & André, F. (2019) · Clinical and Experimental Gastroenterology · doi:10.2147/ceg.s181590 · Cited by 81 · see citing works
Meaney, C., & O’Driscoll, C. M. (1999) · European Journal of Pharmaceutical Sciences · doi:10.1016/s0928-0987(99)00007-x · Cited by 75 · see citing works
Bjornsson, E. S., Cederborg, A., Åkvist, A., Simrén, M., Stotzer, P., & Bjarnason, I. (2005) · Scandinavian Journal of Gastroenterology · doi:10.1080/00365520510023288 · Cited by 71 · see citing works
Intestinal Microbial Diversity and Perioperative Complications
Ralls, M. W., Miyasaka, E. A., & Teitelbaum, D. H. (2013) · Journal of Parenteral and Enteral Nutrition · doi:10.1177/0148607113486482 · Cited by 69 · see citing works
Zareie, M., Riff, J. D., Donato, K. A., et al. (2005) · Cellular Microbiology · doi:10.1111/j.1462-5822.2005.00595.x · Cited by 67 · see citing works
Potential Role of the Gut Microbiome in ALS: A Systematic Review
Wright, M. L., Fournier, C. N., Houser, M. C., Tansey, M. G., Glass, J. D., & Hertzberg, V. (2018) · Biological Research For Nursing · doi:10.1177/1099800418784202 · Cited by 67 · see citing works
Intestinal Microbiota, Lipids, and the Pathogenesis of Intestinal Failure–Associated Liver Disease
Lee, W. S., & Sokol, R. J. (2015) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2015.05.048 · Cited by 66 · see citing works
Groh, K. J., Geueke, B., & Muncke, J. (2017) · Food and Chemical Toxicology · doi:10.1016/j.fct.2017.08.023 · Cited by 66 · see citing works
Dose-related effects of chenodeoxycholic acid in the rabbit colon
Camilleri, M., Murphy, R., & CHADWICK, V. S. (1980) · Digestive Diseases and Sciences · doi:10.1007/bf01395507 · Cited by 65 · see citing works
Self-citationEndotoxemia unrequired in the pathogenesis of pediatric nonalcoholic steatohepatitis
Yuan, J., Baker, S. S., Liu, W., Alkhouri, R. H., Baker, R. D., Xie, J., Ji, G., & Zhu, L. (2013) · Journal of Gastroenterology and Hepatology · doi:10.1111/jgh.12510 · Cited by 64 · see citing works
Phillips, T. E., Phillips, T., & Neutra, M. R. (1987) · Cell and Tissue Research · doi:10.1007/bf00215748 · Cited by 62 · see citing works
Breuer, N. F., Rampton, D. S., Tammar, A., Murphy, G. M., & Dowling, R. H. (1983) · Gastroenterology · doi:10.1016/0016-5085(83)90199-3 · Cited by 61 · see citing works
13C mannitol as a novel biomarker for measurement of intestinal permeability
Grover, M., Camilleri, M., Hines, J., Burton, D. D., Ryks, M. D., Wadhwa, A., Sundt, W. J., Dyer, R. B., & Singh, R. J. (2016) · Neurogastroenterology & Motility · doi:10.1111/nmo.12802 · Cited by 59 · see citing works
Self-citationYin, M., Yan, X., Weng, W., Yang, Y., Gao, R., Liu, M., Pan, C., Zhu, Q., Li, H., Wei, Q., et al. (2018) · Cellular Physiology and Biochemistry · doi:10.1159/000487027 · Cited by 58 · see citing works
Wu, R. L., Vázquez‐Roque, M. I., Carlson, P., Burton, D. D., Grover, M., Camilleri, M., & Turner, J. R. (2016) · Laboratory Investigation · doi:10.1038/labinvest.2016.118 · Cited by 54 · see citing works
Self-citationFaubion, W. A., Camilleri, M., Murray, J. A., et al. (2016) · BMJ Global Health · doi:10.1136/bmjgh-2016-000066 · Cited by 50 · see citing works
Self-citationRole of Prostaglandins in Bile Salt-Induced Changes in Rat Colonic Structure and Function
Rampton, D. S., Breuer, N. F., Vaja, S., Sladen, G. E., & Dowling, R. H. (1981) · Clinical Science · doi:10.1042/cs0610641 · Cited by 49 · see citing works
Warners, M. J., Vlieg‐Boerstra, B., Verheij, J., van Hamersveld, P. H. P., van Rhijn, B. D., van Ampting, M. T. J., Harthoorn, L. F., de Jonge, W. J., Smout, A. J. P. M., & Bredenoord, A. J. (2017) · The American Journal of Gastroenterology · doi:10.1038/ajg.2017.107 · Cited by 49 · see citing works
Willumsen, J. F., Darling, J. C., Kitundu, J. A., et al. (1997) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/00005176-199703000-00001 · Cited by 48 · see citing works
Peters, S. A., Edogawa, S., Sundt, W. J., Dyer, R. B., Dalenberg, D. A., Mazzone, A., Singh, R. J., Moses, N., Smyrk, T. C., Weber, C., et al. (2017) · American Journal of Gastroenterology · doi:10.1038/ajg.2017.48 · Cited by 48 · see citing works
Self-citationTornai, T., Pályu, E., Vitális, Z., Tornai, I., Tornai, D., Antal‐Szalmás, P., Norman, G. L., Shums, Z., Veres, G., Dezsőfi, A., et al. (2017) · World Journal of Gastroenterology · doi:10.3748/wjg.v23.i29.5412 · Cited by 47 · see citing works
Mayeur, C., Gillard, L., Beyec, J. L., Bado, A., Joly, F., & Thomas, M. (2016) · Microorganisms · doi:10.3390/microorganisms4010016 · Cited by 44 · see citing works
Arias, Á., Vicario, M., Bernardo, D., et al. (2018) · Clinical and Translational Gastroenterology · doi:10.1038/s41424-018-0017-4 · Cited by 44 · see citing works
Hayden, U. L., & Carey, H. V. (2000) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2000.278.6.r1589 · Cited by 43 · see citing works
Agapova, S. E., Stephenson, K. B., Divala, O., Kaimila, Y., Maleta, K. M., Thakwalakwa, C. M., Ordiz, M. I., Trehan, I., & MANARY, M. J. (2018) · Journal of Nutrition · doi:10.1093/jn/nxx013 · Cited by 39 · see citing works
Moore, A., Bjarnason, I., Cryer, B., et al. (2009) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2009.03.032 · Cited by 38 · see citing works
Clinical impact of microbiome in patients with decompensated cirrhosis
Oikonomou, T., Papatheodoridis, G., Samarkos, M., Goulis, I., & Cholongitas, Ε. (2018) · World Journal of Gastroenterology · doi:10.3748/wjg.v24.i34.3813 · Cited by 37 · see citing works
Sucrose but Not Nitrate Ingestion Reduces Strenuous Cycling–induced Intestinal Injury
Jonvik, K. L., Lenaerts, K., Smeets, J. S. J., Kolkman, J. J., van Loon, L. J. C., & Verdijk, L. B. (2018) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000001800 · Cited by 36 · see citing works
Hulsewé, K. W. E. (2004) · Clinical Nutrition · doi:10.1016/j.clnu.2004.04.002 · Cited by 32 · see citing works
Effect of Bile Salts on Colonic Mucus Secretion in Isolated Vascularly Perfused Rat Colon
Barcelo, A., Claustre, J., Toumi, F., et al. (2001) · Digestive Diseases and Sciences · doi:10.1023/a:1010607127822 · Cited by 30 · see citing works
Aguas, M., Garrigues, V., Bastida, G., Nos, P., Ortiz, V., Fernández, A., & Ponce, J. D. C. (2011) · Journal of Crohn s and Colitis · doi:10.1016/j.crohns.2011.01.008 · Cited by 29 · see citing works
A glance at … dietary emulsifiers, the human intestinal mucus and microbiome, and dietary fiber
Glade, M. J., & Meguid, M. M. (2015) · Nutrition · doi:10.1016/j.nut.2015.12.036 · Cited by 28 · see citing works
Piano, M. D., Balzarini, M., Carmagnola, S., Pagliarulo, M., Tari, R., Nicola, S., Deidda, F., & Pane, M. (2014) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0000000000000254 · Cited by 27 · see citing works
Mokkala, K., Pussinen, P. J., Houttu, N., Koivuniemi, E., Vahlberg, T. J., & Laitinen, K. (2018) · Beneficial Microbes · doi:10.3920/bm2017.0072 · Cited by 27 · see citing works
Camilleri, M., Murphy, R., & CHADWICK, V. S. (1982) · Digestive Diseases and Sciences · doi:10.1007/bf01316567 · Cited by 25 · see citing works
Self-citationBulik‐Sullivan, E. C., Roy, S., Elliott, R. J., Kassam, Z., Lichtman, S. N., Carroll, I. M., & Gulati, A. (2018) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000002043 · Cited by 25 · see citing works
Effects of Bile Acids on Mucus Secretion in the Dog Colon
Lewin, M. R., Masri, S. H. E., & Clark, C. G. (2008) · European Surgical Research · doi:10.1159/000128089 · Cited by 22 · see citing works
Plaisancié, P., Bosshard, A., Meslin, J.-C., et al. (2009) · Digestion · doi:10.1159/000201440 · Cited by 20 · see citing works
Takeuchi, K. (2014) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2014.07.005 · Cited by 17 · see citing works
Katzka, D. A., Geno, D. M., Blair, H. E., et al. (2014) · Gut · doi:10.1136/gutjnl-2013-305882 · Cited by 17 · see citing works
Intestinal and Gastric Permeability in Children With Eosinophilic Esophagitis and Reflux Esophagitis
Leung, A. J.-T., Persad, S., Slae, M., Abdelradi, A., Kluthe, C., Shirton, L., Danchuk, R., Persad, R., Meddings, J. B., & Huynh, H. Q. (2014) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000000590 · Cited by 17 · see citing works
Mullen, A., Gosset, L., Larke, N. L., et al. (2011) · British Journal Of Nutrition · doi:10.1017/s0007114511003734 · Cited by 15 · see citing works
Intravenous Leiomyomatosis with Cardiac Extension
Saitoh, M., Hayasaka, T., Nakahara, K., et al. (2004) · Gynecologic and Obstetric Investigation · doi:10.1159/000079658 · Cited by 14 · see citing works
Ascorbic Acid may Exacerbate Aspirin‐Induced Increase in Intestinal Permeability
Sequeira, I. R., Kruger, M. C., Hurst, R. D., & Lentle, R. G. (2015) · Basic & Clinical Pharmacology & Toxicology · doi:10.1111/bcpt.12388 · Cited by 12 · see citing works
Meng, Y., Lei, J., Hao, Z.-M., et al. (2011) · PubMed · Cited by 8 · see citing works
Microbiome: In Search of Mechanistic Information and Relevance
Camilleri, M., & Vakil, N. B. (2019) · The American Journal of Gastroenterology · doi:10.14309/ajg.0000000000000306 · Cited by 3 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 2
- [89]Katzka DA, Geno DM, Blair HE, Small intestinal permeability in patients with eosinophilic oesophagitis during active phase and remission. Gut 2015; 64: 538– 43. 24957264
- [90]Warners MJ, Vlieg-Boerstra BJ, Verheij J, Esophageal and small intestinal mucosal integrity in eosinophilic esophagitis and response to an elemental diet. Am J Gastroenterol 2017; 112: 1061– 71. 28417991 PMC5527277
Cited by
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Ghosh, S., Whitley, C. S., Haribabu, B., & Jala, V. R. (2021) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2021.02.007 · Cited by 835 · see citing works
Microplastics detected in cirrhotic liver tissue
Horvatits, T., Tamminga, M., Liu, B., Sebode, M., Carambia, A., Fischer, L., Püschel, K., Huber, S., & Fischer, E. K. (2022) · eBioMedicine · doi:10.1016/j.ebiom.2022.104147 · Cited by 778 · see citing works
Liang, B., Zhong, Y., Huang, Y., Lin, X., Liu, J., Lin, L., Hu, M., Jiang, J., Dai, M., Wang, B., et al. (2021) · Particle and Fibre Toxicology · doi:10.1186/s12989-021-00414-1 · Cited by 508 · see citing works
López-Otín, C., & Kroemer, G. (2021) · Cell · doi:10.1016/j.cell.2020.11.034 · Cited by 499 · see citing works
Gut barrier disruption and chronic disease
Martel, J., Chang, S.-H., Ko, Y.-F., Hwang, T.-L., Young, J. D., & Ojcius, D. M. (2022) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2022.01.002 · Cited by 514 · see citing works
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Wolter, M., Grant, E. T., Boudaud, M., Steimle, A., Pereira, G. V., Martens, E. C., & Desai, M. S. (2021) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-021-00512-7 · Cited by 211 · see citing works
Seethaler, B., Nguyen, N. K., Basrai, M., Kiechle, M., Walter, J., Delzenne, N. M., & Bischoff, S. C. (2022) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqac175 · Cited by 179 · see citing works
De Munck, T. J. I., Xu, P., Verwijs, H. J. A., Masclee, A. A. M., Jonkers, D., Verbeek, J., & Koek, G. H. (2020) · Liver International · doi:10.1111/liv.14696 · Cited by 145 · see citing works
How bile acids and the microbiota interact to shape host immunity
Lee, M. H., Nuccio, S.-P., Mohanty, I., Hagey, L. R., Dorrestein, P. C., Chu, H., & Raffatellu, M. (2024) · Nature Reviews Immunology · doi:10.1038/s41577-024-01057-x · Cited by 143 · see citing works
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Wang, J.-K., & Yao, S.-K. (2021) · Evidence-Based Complementary and Alternative Medicine · doi:10.1155/2021/5560310 · Cited by 98 · see citing works
Al-Sadi, R., Engers, J., Haque, M., King, S., Al-Omari, D., & Ma, T. Y. (2021) · PLOS ONE · doi:10.1371/journal.pone.0249544 · Cited by 93 · see citing works
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Arrona Cardoza, P., Spillane, M. B., & Morales Marroquin, E. (2022) · Nutrition Reviews · doi:10.1093/nutrit/nuab022 · Cited by 53 · see citing works
Weber, L., Kuck, K., Jürgenliemk, G., Heilmann, J., Lipowicz, B., & Vissiennon, C. (2020) · Biomolecules · doi:10.3390/biom10071033 · Cited by 51 · see citing works
Wasiak, J., & Gawlik-Kotelnicka, O. (2023) · Behavioural Brain Research · doi:10.1016/j.bbr.2023.114459 · Cited by 47 · see citing works
Wauters, L., Van Oudenhove, L., Accarie, A., Geboers, K., Geysen, H., Toth, J., Luypaerts, A., Verbeke, K., Smokvina, T., Raes, J., et al. (2022) · Gut Microbes · doi:10.1080/19490976.2022.2031695 · Cited by 34 · see citing works
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Agarwal, S., Goswami, P., Poudel, S., Gunjan, D., Singh, N., Yadav, R., Kumar, U., Pandey, G., & Saraya, A. (2023) · Pancreatology · doi:10.1016/j.pan.2022.11.011 · Cited by 36 · see citing works
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Qin, C., Hu, J., Wan, Y., Cai, M., Wang, Z., Peng, Z., Liao, Y., Li, D., Yao, P., Liu, L., et al. (2021) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.110093 · Cited by 32 · see citing works
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Marino, M., Mignozzi, S., Michels, K. B., Cintolo, M., Penagini, R., Gargari, G., Ciafardini, C., Ferraroni, M., Patel, L., Del Bo’, C., et al. (2024) · Scientific Reports · doi:10.1038/s41598-024-76697-z · Cited by 10 · see citing works
Dumitru, C. N., Dumitru, A. O., Popa, G. V., Marcu, T., Ursu, M., Nechita, A., & Matei, N. M. (2026) · Dentistry Journal · doi:10.3390/dj14050289 · Cited by 6 · see citing works
Hajihashemi, P., Haghighatdoost, F., Kassaian, N., Hoveida, L., Tamizifar, B., Nili, H., Rahim Khorasani, M., & Adibi, P. (2024) · Digestive Diseases and Sciences · doi:10.1007/s10620-023-08219-2 · Cited by 4 · see citing works
- Authors
- Camilleri, M.
- Affiliations
- Mayo Clinic (US)
- Corresponding author
- Camilleri, Michael
- ORCID
- Camilleri, Michael
- Venue
- Gut
- Publisher
- BMJ
- Published
- 2019-05-10
- Volume
- 68
- Issue
- 8
- Pages
- 1516-1526
- ISSN
- 0017-5749 (ISSN-L)
- 1468-3288
- PMC
- PMC6790068
- OpenAlex
- W2944348781
- Cited by
- 1,081
- References
- 136
- Citations by year
- 2026: 159 · 2025: 193 · 2024: 178 · 2023: 175 · 2022: 169 · 2021: 124 · 2020: 69 · 2019: 14
- FWCI
- 17.13
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Gut (publishedVersion, public-domain)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- HighWire Press Open Archive (submittedVersion)
- Funders
- National Institutes of Health
- 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
- leaky gut, intestinal barrier, intestinal permeability, epithelial permeability, mucus layer, paracellular transport, transcellular permeability, epithelial apoptosis, colonic mucosa, stress disorders, endurance exercise, nonsteroidal anti-inflammatory drugs, pregnancy, bile acids, food emulsifiers, fermented foods, dietary supplementation, inflammatory bowel disease, ulcerative colitis, intestinal barrier dysfunction
- MeSH terms
- Gastrointestinal Diseases, Humans, Intestinal Mucosa, Permeability, Disease Management
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