Mechanisms of probiotic action: Implications for therapeutic applications in inflammatory bowel diseases
Abstract
Probiotics are defined as nonpathogenic living microorganisms, including some commensal bacterial flora, which have beneficial effects on host health and disease prevention and/or treatment. Clinical trials have shown beneficial effects of probiotics on several human diseases, such as inflammatory bowel diseases (IBDs), which are among the most-studied diseases testing probiotics as a potential therapy. However, a significant question regarding clinical use of probiotics is the mechanism underlying the wide range of actions. Studies discussed in this review suggest 3 distinct cellular and molecular mechanisms for probiotic regulation in IBD therapy: 1) Probiotics block pathogenic bacterial effects by producing bactericidal substances and competing with pathogens and toxins for adherence to the intestinal epithelium; 2) Probiotics regulate immune responses by enhancing the innate immunity and modulating pathogen-induced inflammation via toll-like receptor-regulated signaling pathways; and 3) Probiotics regulate intestinal epithelial homeostasis by promoting intestinal epithelial cell survival, enhancing barrier function, and stimulating protective responses. Probiotics modulate host cell signaling pathways, including Akt, mitogen-activated protein kinases, and nuclear factor-kappaB to mediate these intestinal epithelial functions. It is hoped that developing a mechanistic understanding of probiotic action will provide the rationale to support the development of new hypothesis-driven studies to define the clinical efficacy in preventive, adjunctive, or alternative treatments for IBD.
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Evidence for mutual interaction between the nervous system and the commensal enteric microbiota has been demonstrated in gut inflammation, visceral pain, certain symptoms of IBS, and in obesity.
“Evidence for such mutual interaction has been demonstrated in gut inflammation,14 visceral pain,77 certain symptoms of IBS,12 and in obesity.78”
From Principles and clinical implications of the brain-gut-enteric microbiota axis (2009) · cites this paper as [14]
Modification of the enteric microbiota by administration of antibiotics, probiotic bacteria or prebiotic substances (for example, certain fibers or lactulose) are beneficial in the treatment of IBD and improve some symptoms of IBS.
“Evidence suggests that modification of the enteric microbiota by administration of antibiotics, probiotic bacteria or prebiotic substances (for example, certain fibers or lactulose) are beneficial in the treatment of IBD14 and improve some symptoms of IBS.12”
From Principles and clinical implications of the brain-gut-enteric microbiota axis (2009) · cites this paper as [14]
Cites
Unravelling the pathogenesis of inflammatory bowel disease
Xavier, R. J., & Podolsky, D. K. (2007) · Nature · doi:10.1038/nature06005 · Cited by 4,364 · see citing works
Recognition of Commensal Microflora by Toll-Like Receptors Is Required for Intestinal Homeostasis
Rakoff-Nahoum, S., Paglino, J., Eslami-Varzaneh, F., Edberg, S., & Medzhitov, R. (2004) · Cell · doi:10.1016/j.cell.2004.07.002 · Cited by 4,251 · see citing works
An Immunomodulatory Molecule of Symbiotic Bacteria Directs Maturation of the Host Immune System
Mazmanian, S. K., Liu, C. H., Tzianabos, A. O., & Kasper, D. L. (2005) · Cell · doi:10.1016/j.cell.2005.05.007 · Cited by 2,910 · see citing works
Bacteriocins: Developing innate immunity for food
Cotter, P. D., Hill, C., & Ross, R. P. (2005) · Nature Reviews Microbiology · doi:10.1038/nrmicro1273 · Cited by 2,380 · see citing works
Induction of Protective IgA by Intestinal Dendritic Cells Carrying Commensal Bacteria
Macpherson, A. J., & Uhr, T. (2004) · Science · doi:10.1126/science.1091334 · Cited by 1,584 · see citing works
Comparative genomics of the lactic acid bacteria.
Makarova, K., Slesarev, A., Wolf, Y., Sorokin, A., Mirkin, B., Koonin, E., Pavlov, A., Pavlova, N., Karamychev, V., Polouchine, N., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0607117103 · Cited by 1,391 · see citing works
Besselink, M. G., van Santvoort, H. C., Buskens, E., Boermeester, M. A., van Goor, H., Timmerman, H. M., Nieuwenhuijs, V. B., Bollen, T. L., van Ramshorst, B., Witteman, B. J., et al. (2008) · The Lancet · doi:10.1016/s0140-6736(08)60207-x · Cited by 1,367 · see citing works
Ott, S. J., Musfeldt, M., Wenderoth, D. F., Hampe, J., Brant, O., Fölsch, U. R., Timmis, K. N., & Schreiber, S. (2004) · Gut · doi:10.1136/gut.2003.025403 · Cited by 1,311 · see citing works
The fundamental basis of inflammatory bowel disease
Strober, W., Fuss, I. J., & Mannon, P. (2007) · Journal of Clinical Investigation · doi:10.1172/jci30587 · Cited by 1,310 · see citing works
Kruis, W., Frič, P., Pokrotnieks, J., Lukáš, M., Fixa, B., Kaščák, M., Kamm, M. A., Weismueller, J., Beglinger, C., Stolte, M., et al. (2004) · Gut · doi:10.1136/gut.2003.037747 · Cited by 1,285 · see citing works
Probiotics: Growth-Promoting Factors Produced by Microorganisms
Lilly, D. M., & Stillwell, R. H. (1965) · Science · doi:10.1126/science.147.3659.747 · Cited by 1,247 · see citing works
Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens
Servin, A. L. (2004) · FEMS Microbiology Reviews · doi:10.1016/j.femsre.2004.01.003 · Cited by 1,234 · see citing works
Prophylaxis of pouchitis onset with probiotic therapy: a double-blind, placebo-controlled trial
Gionchetti, P., Rizzello, F., Helwig, U., Venturi, A., Lammers, K. M., Brigidi, P., Vitali, B., Poggioli, G., Miglioli, M., & Campieri, M. (2003) · Gastroenterology · doi:10.1016/s0016-5085(03)00171-9 · Cited by 1,147 · see citing works
Rembacken, B., Snelling, A. M., Hawkey, P. M., Chalmers, D. M., & Axon, A. (1999) · The Lancet · doi:10.1016/s0140-6736(98)06343-0 · Cited by 1,100 · see citing works
Epithelial NEMO links innate immunity to chronic intestinal inflammation
Nenci, A., Becker, C., Wullaert, A., Gareus, R., Loo, G., Danese, S., Huth, M., Nikolaev, A., Neufert, C. F., Madison, B., et al. (2007) · Nature · doi:10.1038/nature05698 · Cited by 1,077 · see citing works
Kelly, D., Campbell, J. I., King, T. P., Grant, G., Jansson, E. Å., Coutts, A., Pettersson, S., & Conway, S. (2003) · Nature Immunology · doi:10.1038/ni1018 · Cited by 997 · see citing works
Angiogenins: a new class of microbicidal proteins involved in innate immunity
Hooper, L. V., Stappenbeck, T. S., Hong, C. V., & Gordon, J. I. (2003) · Nature Immunology · doi:10.1038/ni888 · Cited by 929 · see citing works
Mimura, T., Rizzello, F., Helwig, U., Poggioli, G., Schreiber, S., Talbot, I. C., Nicholls, R. J., Gionchetti, P., Campieri, M., & Kamm, M. A. (2003) · Gut · doi:10.1136/gut.53.1.108 · Cited by 912 · see citing works
Rachmilewitz, D., Katakura, K., Karmeli, F., Hayashi, T., Reinus, C., Rudensky, B., Akira, S., Takeda, K., Lee, J., Takabayashi, K., et al. (2004) · Gastroenterology · doi:10.1053/j.gastro.2003.11.019 · Cited by 859 · see citing works
Yan, F., Cao, H., Cover, T. L., Whitehead, R. H., Washington, M. K., & Polk, D. B. (2006) · Gastroenterology · doi:10.1053/j.gastro.2006.11.022 · Cited by 828 · see citing works
Self-citationSmits, H. H., Engering, A. J., van der Kleij, D., de Jong, E. C., Schipper, K., van Capel, T. M. M., Zaat, B. A. J., Yazdanbakhsh, M., Wierenga, E. A., & van Kooyk, Y. (2005) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2005.03.036 · Cited by 765 · see citing works
VSL#3 Probiotic-Mixture Induces Remission in Patients with Active Ulcerative Colitis
Bibiloni, R., Fedorak, R. N., Tannock, G. W., Madsen, K. L., Gionchetti, P., Campieri, M., Simone, C. D., & Sartor, R. B. (2005) · The American Journal of Gastroenterology · doi:10.1111/j.1572-0241.2005.41794.x · Cited by 743 · see citing works
Lee, J., Mo, J., Katakura, K., Alkalay, I., Rucker, A. N., Liu, Y., Lee, H., Shen, C., Cojocaru, G., Shenouda, S., et al. (2006) · Nature Cell Biology · doi:10.1038/ncb1500 · Cited by 621 · see citing works
Probiotic Bacterium Prevents Cytokine-induced Apoptosis in Intestinal Epithelial Cells*
Yan, F., & Polk, D. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m207050200 · Cited by 599 · see citing works
Self-citationComplete genome sequence of the probiotic lactic acid bacterium Lactobacillus acidophilus NCFM
Altermann, E., Russell, W. M., Azcárate-Peril, M. A., Barrangou, R., Buck, B. L., McAuliffe, O. E., Souther, N. E., Dobson, A., Duong, T., Callanan, M. J., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0409188102 · Cited by 594 · see citing works
Human Toll-like receptor 4 recognizes host-specific LPS modifications
Hajjar, A. M., Ernst, R. K., Tsai, J. H., Wilson, C. B., & Miller, S. I. (2002) · Nature Immunology · doi:10.1038/ni777 · Cited by 579 · see citing works
Modulation of human dendritic cell phenotype and function by probiotic bacteria
Hart, A. L., Lammers, K., Brigidi, P., Vitali, B., Rizzello, F., Gionchetti, P., Campieri, M., Kamm, M. A., Knight, S. C., & Stagg, A. J. (2004) · Gut · doi:10.1136/gut.2003.037325 · Cited by 555 · see citing works
Epithelial-cell-intrinsic IKK-β expression regulates intestinal immune homeostasis
Zaph, C., Troy, A. E., Taylor, B. C., Berman-Booty, L. D., Guild, K. J., Du, Y., Yost, E. A., Gruber, A. D., May, M. J., Greten, F. R., et al. (2007) · Nature · doi:10.1038/nature05590 · Cited by 496 · see citing works
The genome sequence of the probiotic intestinal bacterium Lactobacillus johnsonii NCC 533
Pridmore, R. D., Berger, B. W., Desiere, F., Vilanova, D., Barretto, C., Pittet, A.-C., Zwahlen, M.-C., Rouvet, M., Altermann, E., Barrangou, R., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0307327101 · Cited by 485 · see citing works
Efficacy of Lactobacillus GG in maintaining remission of ulcerative colitis
Zocco, M. A., Verme, L. Z. D., Cremonini, F., Piscaglia, A. C., Nista, E. C., Candelli, M., Novi, M., Rigante, D., Cazzato, I. A., Ojetti, V., et al. (2006) · Alimentary Pharmacology & Therapeutics · doi:10.1111/j.1365-2036.2006.02927.x · Cited by 472 · see citing works
Wehkamp, J., Harder, J., Wehkamp, K., Meissner, B. W.-V., Schlee, M., Enders, C., Sonnenborn, U., Nuding, S., Bengmark, S., Fellermann, K., et al. (2004) · Infection and Immunity · doi:10.1128/iai.72.10.5750-5758.2004 · Cited by 471 · see citing works
Lactobacilli activate human dendritic cells that skew T cells toward T helper 1 polarization
Mohamadzadeh, M., Olson, S. D., Kalina, W. V., Ruthel, G. T., Demmin, G. L., Warfield, K. L., Bavari, S., & Klaenhammer, T. R. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0500098102 · Cited by 465 · see citing works
Zyrek, A. A., Cichon, C., Helms, S., Enders, C., Sonnenborn, U., & Schmidt, M. A. (2006) · Cellular Microbiology · doi:10.1111/j.1462-5822.2006.00836.x · Cited by 427 · see citing works
Marteau, P. R., Lémann, M., Seksik, P., Laharie, D., Colombel, J. F., Bouhnik, Y., Cadiot, G., Soulé, J. C., Bourreille, A., Metman, E.-H., et al. (2005) · Gut · doi:10.1136/gut.2005.076604 · Cited by 412 · see citing works
Seth, A., Yan, F., Polk, D. B., & Rao, R. K. (2008) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00202.2007 · Cited by 404 · see citing works
Self-citationFunctional modulation of enterocytes by gram-positive and gram-negative microorganisms
Otte, J., & Podolsky, D. K. (2004) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00341.2003 · Cited by 403 · see citing works
Kato, K., Mizuno, S., Umesaki, Y., Ishii, Y., Sugitani, M., Imaoka, A., Otsuka, M., Hasunuma, O., Kurihara, R., Iwasaki, A., et al. (2004) · Alimentary Pharmacology & Therapeutics · doi:10.1111/j.1365-2036.2004.02268.x · Cited by 397 · see citing works
Probiotic lactobacilli and VSL#3 induce enterocyte β‐defensin 2
Schlee, M., Harder, J., Köten, B., Stange, E., Wehkamp, J., & Fellermann, K. (2008) · Clinical and Experimental Immunology · doi:10.1111/j.1365-2249.2007.03587.x · Cited by 393 · see citing works
The complete genome sequence of the meat-borne lactic acid bacterium Lactobacillus sakei 23K
Chaillou, S., Champomier‐Vergès, M., Cornet, M., Coq, A.-M. C.-L., Dudez, A.-M., Martin, V., Beaufils, S., Darbon, E., Bossy, R., Loux, V., et al. (2005) · Nature Biotechnology · doi:10.1038/nbt1160 · Cited by 390 · see citing works
Gut-associated bacterial microbiota in paediatric patients with inflammatory bowel disease
Conte, M. P., Schippa, S., Zamboni, I., Penta, M., Chiarini, F., Seganti, L., Osborn, J., Falconieri, P., Borrelli, O., & Cucchiara, S. (2006) · Gut · doi:10.1136/gut.2005.078824 · Cited by 383 · see citing works
Bousvaros, A., Guandalini, S., Baldassano, R. N., Botelho, C. A., Evans, J., Ferry, G. D., Goldin, B. R., Parker‐Hartigan, L., Kugathasan, S., Levy, J. F., et al. (2005) · Inflammatory Bowel Diseases · doi:10.1097/01.mib.0000175905.00212.2c · Cited by 363 · see citing works
Lactobacillus GG in inducing and maintaining remission of Crohn's disease
Schultz, M., Timmer, A., Herfarth, H. H., Sartor, R. B., Vanderhoof, J. A., & Rath, H. C. (2004) · BMC Gastroenterology · doi:10.1186/1471-230x-4-5 · Cited by 349 · see citing works
Tien, M.-T., Girardin, S. E., Regnault, B., Bourhis, L. L., Dillies, M., Coppée, J., Bourdet‐Sicard, R., Sansonetti, P. J., & Pédron, T. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.176.2.1228 · Cited by 323 · see citing works
DNA from probiotic bacteria modulates murine and human epithelial and immune function
Jijon, H. B., Backer, J., Díaz, H., Yeung, H. P., Thiel, D., McKaigney, C. J., Simone, C. D., & Madsen, K. L. (2004) · Gastroenterology · doi:10.1053/j.gastro.2004.02.003 · Cited by 318 · see citing works
Keersmaecker, S. C. J. D., Verhoeven, T. L. A., Desair, J., Kathleen Marchal, D., Vanderleyden, J., & Nagy, I. (2006) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2006.00250.x · Cited by 316 · see citing works
Schlee, M., Wehkamp, J., Altenhoefer, A., Oelschlaeger, T. A., Stange, E. F., & Fellermann, K. (2007) · Infection and Immunity · doi:10.1128/iai.01563-06 · Cited by 315 · see citing works
Resta‐Lenert, S. C., & Barrett, K. E. (2006) · Gastroenterology · doi:10.1053/j.gastro.2005.12.015 · Cited by 308 · see citing works
Role of commercial probiotic strains against human pathogen adhesion to intestinal mucus
Collado, M. C., Meriluoto, J., & Salminen, S. (2007) · Letters in Applied Microbiology · doi:10.1111/j.1472-765x.2007.02212.x · Cited by 303 · see citing works
Cario, E., Brown, D., McKee, M. L., Lynch–Devaney, K., Gerken, G., & Podolsky, D. K. (2002) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)64360-x · Cited by 301 · see citing works
Tao, Y., Drabik, K., Waypa, T. S., Musch, M. W., Alverdy, J. C., Schneewind, O., Chang, E. B., & Petrof, E. O. (2005) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00131.2005 · Cited by 301 · see citing works
Zhang, L., Li, N., Caicedo, R. A., & Neu, J. (2005) · Journal of Nutrition · doi:10.1093/jn/135.7.1752 · Cited by 294 · see citing works
Ma, D., Forsythe, P., & Bienenstock, J. (2004) · Infection and Immunity · doi:10.1128/iai.72.9.5308-5314.2004 · Cited by 289 · see citing works
O’Hara, A. M., O'Regan, P., Fanning, A., O’Mahony, C., MacSharry, J. A., Lyons, A., Bienenstock, J., O’Mahony, L., & Shanahan, F. (2006) · Immunology · doi:10.1111/j.1365-2567.2006.02358.x · Cited by 284 · see citing works
Effect of Lactobacillus rhamnosus GG on ileal pouch inflammation and microbial flora
Kuisma, J., Mentula, S., Järvinen, H., Kahri, A., Saxelin, M., & Färkkilä, M. A. (2003) · Alimentary Pharmacology & Therapeutics · doi:10.1046/j.1365-2036.2003.01465.x · Cited by 282 · see citing works
CpG motifs: the active ingredient in bacterial extracts?
Krieg, A. Μ. (2003) · Nature Medicine · doi:10.1038/nm0703-831 · Cited by 269 · see citing works
Molecular Characterization of Rectal Mucosa-Associated Bacterial Flora in Inflammatory Bowel Disease
Mylonaki, M., Rayment, N. B., Rampton, D. S., Hudspith, B. N., & Brostoff, J. (2005) · Inflammatory Bowel Diseases · doi:10.1097/01.mib.0000159663.62651.4f · Cited by 250 · see citing works
Sherman, P. M., Johnson-Henry, K. C., Yeung, H. P., Ngo, P. S. C., Goulet, J., & Tompkins, T. A. (2005) · Infection and Immunity · doi:10.1128/iai.73.8.5183-5188.2005 · Cited by 246 · see citing works
Makras, L., Triantafyllou, V., Fayol-Messaoudi, D., Adriany, T., Ζουμποπούλου, Γ., Tsakalidou, E., Servin, A. L., & Vuyst, L. D. (2005) · Research in Microbiology · doi:10.1016/j.resmic.2005.09.002 · Cited by 238 · see citing works
Matsumoto, S., Hara, T., Hori, T., Mitsuyama, K., Nagaoka, M., Tomiyasu, N., Suzuki, A., & Sata, M. (2005) · Clinical & Experimental Immunology · doi:10.1111/j.1365-2249.2005.02790.x · Cited by 224 · see citing works
Bacterial Probiotic Modulation of Dendritic Cells
Drakes, M. L., Blanchard, T. G., & Czinn, S. J. (2004) · Infection and Immunity · doi:10.1128/iai.72.6.3299-3309.2004 · Cited by 218 · see citing works
Pronio, A., Montesani, C., Butteroni, C., Vecchione, S., Mumolo, G. M., Vestri, A., Vitolo, D., & Boirivant, M. (2008) · Inflammatory Bowel Diseases · doi:10.1002/ibd.20369 · Cited by 212 · see citing works
Faecal SIgA secretion in infants fed on pre‐ or probiotic infant formula
Bakker‐Zierikzee, A. M., van Tol, E. A. F., Kroes, H., Alles, M., Kok, F. J., & BINDELS, J. G. (2006) · Pediatric Allergy and Immunology · doi:10.1111/j.1399-3038.2005.00370.x · Cited by 199 · see citing works
Grabig, A., Paclik, D., Guzy, C., Dankof, A., Baumgart, D. C., Erckenbrecht, J. F., Raupach, B., Sonnenborn, U., Eckert, J., Schumann, R. R., et al. (2006) · Infection and Immunity · doi:10.1128/iai.01449-05 · Cited by 198 · see citing works
Peña, J. A., & Versalovic, J. A. (2003) · Cellular Microbiology · doi:10.1046/j.1462-5822.2003.t01-1-00275.x · Cited by 194 · see citing works
Veckman, V., Miettinen, M., Pirhonen, J., Sirén, J., Matikainen, S., & Julkunen, I. (2004) · Journal of Leukocyte Biology · doi:10.1189/jlb.1003461 · Cited by 185 · see citing works
Roselli, M., Finamore, A., Britti, M. S., & Mengheri, E. (2006) · British Journal Of Nutrition · doi:10.1079/bjn20051681 · Cited by 183 · see citing works
Peña, J. A., Rogers, A. B., Ge, Z., Ng, V., Li, S. Y., Fox, J. G., & Versalovic, J. A. (2005) · Infection and Immunity · doi:10.1128/iai.73.2.912-920.2005 · Cited by 160 · see citing works
Molecular and Cellular Basis of Microflora-Host Interactions1,
Winkler, P., Ghadimi, D., Schrezenmeir, J., & Kraehenbühl, J.-P. (2007) · Journal of Nutrition · doi:10.1093/jn/137.3.756s · Cited by 157 · see citing works
Synergistic enhancement of Toll-like receptor responses by NOD1 activation
van Heel, D. A., Ghosh, S. K., Butler, M., Hunt, K. A., Foxwell, B. M. J., Mengin‐Lecreulx, D., & Playford, R. J. (2005) · European Journal of Immunology · doi:10.1002/eji.200526296 · Cited by 153 · see citing works
Parassol, N., Freitas, M., Thoreux, K., Dalmasso, G., Bourdet‐Sicard, R., & Rampal, P. (2004) · Research in Microbiology · doi:10.1016/j.resmic.2004.09.013 · Cited by 146 · see citing works
Sturm, A., Rilling, K., Baumgart, D. C., Gargas, K., Abou-Ghazalé, T., Raupach, B., Eckert, J., Schumann, R. R., Enders, C., Sonnenborn, U., et al. (2005) · Infection and Immunity · doi:10.1128/iai.73.3.1452-1465.2005 · Cited by 145 · see citing works
Are, A., Aronsson, L., Wang, S., Greicius, G., Lee, Y. K., Gustafsson, J.-Α., Pettersson, S., & Arulampalam, V. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0711734105 · Cited by 142 · see citing works
Kim, S. O., Sheikh, H. I., Ha, S.-D., Martins, A. J., & Reid, G. (2006) · Cellular Microbiology · doi:10.1111/j.1462-5822.2006.00763.x · Cited by 141 · see citing works
Commensal bacteria in the gut: learning who our friends are
Yan, F., & Polk, D. B. (2004) · Current Opinion in Gastroenterology · doi:10.1097/00001574-200411000-00011 · Cited by 139 · see citing works
Self-citationTallon, R., Arias, S., Bressollier, P., & Urdaci, M. C. (2006) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2006.03086.x · Cited by 138 · see citing works
Cotter, P. D., Deegan, L. H., Lawton, E. M., et al. (2006) · Molecular Microbiology · doi:10.1111/j.1365-2958.2006.05398.x · Cited by 133 · see citing works
Morgan, S. M., O’Connor, P. M., Cotter, P. D., et al. (2005) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.49.7.2606-2611.2005 · Cited by 121 · see citing works
Recombinant Probiotics for Treatment and Prevention of Enterotoxigenic Escherichia coli Diarrhea
Paton, A. W., Jennings, M. P., Morona, R., Wang, H., Focareta, A., Roddam, L. F., & Paton, J. C. (2005) · Gastroenterology · doi:10.1053/j.gastro.2005.01.050 · Cited by 107 · see citing works
Production of Bacteriocin-Like Inhibitory Compounds by Human Fecal Bifidobacterium Strains
Collado, M. C., Hernández, M., & Sanz, Y. (2005) · Journal of Food Protection · doi:10.4315/0362-028x-68.5.1034 · Cited by 102 · see citing works
Two-Peptide Lantibiotics: A Medical Perspective
Lawton, E. M., Ross, R. P., Hill, C., & Cotter, P. D. (2007) · Mini-Reviews in Medicinal Chemistry · doi:10.2174/138955707782795638 · Cited by 102 · see citing works
A Recombinant Probiotic for Treatment and Prevention of Cholera
Focareta, A., Paton, J. C., Morona, R., Cook, J., & Paton, A. W. (2006) · Gastroenterology · doi:10.1053/j.gastro.2006.02.005 · Cited by 101 · see citing works
Keeping the Gut Microflora at Bay
Kraehenbühl, J.-P., & Corbett, M. (2004) · Science · doi:10.1126/science.1096222 · Cited by 85 · see citing works
Candela, M., Seibold, G. M., Vitali, B., Lachenmaier, S., Eikmanns, B. J., & Brigidi, P. (2005) · Research in Microbiology · doi:10.1016/j.resmic.2005.04.006 · Cited by 84 · see citing works
Probiotics as functional food in the treatment of diarrhea
Yan, F., & Polk, D. B. (2006) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/01.mco.0000247477.02650.51 · Cited by 80 · see citing works
Self-citationBraat, H., de Jong, E. C., van den Brande, J. M. H., Kapsenberg, M. L., Peppelenbosch, M. P., van Tol, E. A. F., & van Deventer, S. J. H. (2003) · Journal of Molecular Medicine · doi:10.1007/s00109-003-0509-9 · Cited by 77 · see citing works
Lammers, K. M., Vergopoulos, A., Babel, N., Gionchetti, P., Rizzello, F., Morselli, C., Caramelli, E., Fiorentino, M., D’Errico, A., Volk, H., et al. (2005) · Inflammatory Bowel Diseases · doi:10.1097/01.mpa.0000160302.40931.7b · Cited by 73 · see citing works
Factors involved in binding of Lactobacillus plantarum Lp6 to rat small intestinal mucus
Sun, J., Le, G.-W., Shi, Y.-H., & Su, G.-W. (2007) · Letters in Applied Microbiology · doi:10.1111/j.1472-765x.2006.02031.x · Cited by 70 · see citing works
Sheil, B., MacSharry, J. A., O'Callaghan, L., O'Riordan, A., Waters, A., Morgan, J. G., Collins, J. K., O’Mahony, L., & Shanahan, F. (2006) · Clinical & Experimental Immunology · doi:10.1111/j.1365-2249.2006.03051.x · Cited by 70 · see citing works
Prophylaxis of pouchitis onset with probiotic therapy
Gionchetti, P., Rizzello, F., Helwig, U., Venturi, A., Lammers, K. M., Brigidi, P., Vitali, B., Poggioli, G., Miglioli, M., & Campieri, M. (2003) · European Journal of Gastroenterology & Hepatology · doi:10.1097/00042737-200307000-00020 · Cited by 64 · see citing works
Mukai, T., Kaneko, S., Matsumoto, M., & Ohori, H. (2003) · International Journal of Food Microbiology · doi:10.1016/s0168-1605(03)00317-9 · Cited by 63 · see citing works
Walker, W. A., Goulet, O., Morelli, L., & Antoine, J. (2006) · European Journal of Nutrition · doi:10.1007/s00394-006-1101-1 · Cited by 57 · see citing works
Ridwan, B. U., Koning, C. J. M., Besselink, M. G., Timmerman, H. M., Brouwer, E. C., Verhoef, J., Gooszen, H. G., & Akkermans, L. M. A. (2007) · Letters in Applied Microbiology · doi:10.1111/j.1472-765x.2007.02260.x · Cited by 56 · see citing works
Effect of Orally Administered Non‐Viable Lactobacillus Cells on Murine Humoral Immune Responses
He, F., Morita, H., Kubota, A., Ouwehand, A. C., Hosoda, M., Hiramatsu, M., & Kurisaki, J. (2005) · Microbiology and Immunology · doi:10.1111/j.1348-0421.2005.tb03695.x · Cited by 53 · see citing works
Toll‐Like Receptor Signaling and its Relevance to Intestinal Inflammation
Cario, E., & Podolsky, D. K. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1326.006 · Cited by 38 · see citing works
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Principles and clinical implications of the brain-gut-enteric microbiota axis
Rhee, S. H., Pothoulakis, C., & Mayer, E. A. (2009) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2009.35 · Cited by 1,342 · see citing works
Yan, F., & Polk, D. B. (2011) · Current Opinion in Gastroenterology · doi:10.1097/mog.0b013e32834baa4d · Cited by 447 · see citing works
Self-citationGut-Lung Axis: The Microbial Contributions and Clinical Implications
He, Y., Wen, Q., Yao, F., Xu, D., Huang, Y., & Wang, J. (2017) · Critical Reviews in Microbiology · doi:10.1080/1040841x.2016.1176988 · Cited by 301 · see citing works
Mileti, E., Matteoli, G., Iliev, I. D., & Rescigno, M. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007056 · Cited by 272 · see citing works
The Potential Role of Gut Microbiota in Alzheimer’s Disease: From Diagnosis to Treatment
Varesi, A., Pierella, E., Romeo, M., Piccini, G. B., Alfano, C., Bjørklund, G., Oppong, A., Ricevuti, G., Esposito, C., Chirumbolo, S., et al. (2022) · Nutrients · doi:10.3390/nu14030668 · Cited by 225 · see citing works
Vahabnezhad, E., Mochon, A. B., Wozniak, L. J., & Ziring, D. A. (2013) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0b013e318279abf0 · Cited by 156 · see citing works
Immune-stimulating effects of lactic acid bacteria <i>in vivo</i> and <i>in vitro</i>
Elmadfa, I., Klein, P., & Meyer, A. L. (2010) · Proceedings of the Nutrition Society · doi:10.1017/s0029665110001710 · Cited by 89 · see citing works
Toumi, R., Abdelouhab, K., Rafa, H., Soufli, I., Raissi-Kerboua, D., Djeraba, Z., & Touil-Boukoffa, C. (2013) · Immunopharmacology and Immunotoxicology · doi:10.3109/08923973.2013.790413 · Cited by 68 · see citing works
Bilal, M., Ashraf, S., & Zhao, X. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.931458 · Cited by 58 · see citing works
Immunological Effects of Probiotics and their Significance to Human Health
Gill, H. S., Grover, S., Batish, V. K., & Gill, P. (2009) · Prebiotics and Probiotics Science and Technology · doi:10.1007/978-0-387-79058-9_23 · Cited by 13 · see citing works
- Authors
- Vanderpool, C., Yan, F., & Polk, B. D.
- Affiliations
- Vanderbilt University (US)
- Venue
- Inflammatory Bowel Diseases
- Publisher
- Oxford University Press (OUP)
- Published
- 2008-11
- Volume
- 14
- Issue
- 11
- Pages
- 1585-1596
- ISSN
- 1078-0998 (ISSN-L)
- OpenAlex
- W1993805426
- Cited by
- 340
- References
- 95
- Citations by year
- 2026: 6 · 2025: 13 · 2024: 9 · 2023: 13 · 2022: 33 · 2021: 24 · 2020: 17 · 2019: 15 · 2018: 20 · 2017: 11 · 2016: 12 · 2015: 13 · 2014: 25 · 2013: 20 · 2012: 26
- FWCI
- 3.68
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Inflammatory Bowel Diseases (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Keywords
- probiotics, probiotic mechanisms of action
- MeSH terms
- Animals, Bacterial Infections, Epithelial Cells, Female, Humans, Intestinal Mucosa, Intestines, Male, Risk Factors, Sensitivity and Specificity, Inflammatory Bowel Diseases, Treatment Outcome, Immunity, Mucosal, Probiotics
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.
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