Probiotic Bifidobacterium strains and galactooligosaccharides improve intestinal barrier function in obese adults but show no synergism when used together as synbiotics
Open accessAbstract
BACKGROUND: One way to improve both the ecological performance and functionality of probiotic bacteria is by combining them with a prebiotic in the form of a synbiotic. However, the degree to which such synbiotic formulations improve probiotic strain functionality in humans has not been tested systematically. Our goal was to use a randomized, double-blind, placebo-controlled, parallel-arm clinical trial in obese humans to compare the ecological and physiological impact of the prebiotic galactooligosaccharides (GOS) and the probiotic strains Bifidobacterium adolescentis IVS-1 (autochthonous and selected via in vivo selection) and Bifidobacterium lactis BB-12 (commercial probiotic allochthonous to the human gut) when used on their own or as synbiotic combinations. After 3 weeks of consumption, strain-specific quantitative real-time PCR and 16S rRNA gene sequencing were performed on fecal samples to assess changes in the microbiota. Intestinal permeability was determined by measuring sugar recovery in urine by GC after consumption of a sugar mixture. Serum-based endotoxin exposure was also assessed. RESULTS: IVS-1 reached significantly higher cell numbers in fecal samples than BB-12 (P < 0.01) and, remarkably, its administration induced an increase in total bifidobacteria that was comparable to that of GOS. Although GOS showed a clear bifidogenic effect on the resident gut microbiota, both probiotic strains showed only a non-significant trend of higher fecal cell numbers when administered with GOS. Post-aspirin sucralose:lactulose ratios were reduced in groups IVS-1 (P = 0.050), IVS-1 + GOS (P = 0.022), and GOS (P = 0.010), while sucralose excretion was reduced with BB-12 (P = 0.002) and GOS (P = 0.020), indicating improvements in colonic permeability but no synergistic effects. No changes in markers of endotoxemia were observed. CONCLUSION: This study demonstrated that "autochthony" of the probiotic strain has a larger effect on ecological performance than the provision of a prebiotic substrate, likely due to competitive interactions with members of the resident microbiota. Although the synbiotic combinations tested in this study did not demonstrate functional synergism, our findings clearly showed that the pro- and prebiotic components by themselves improved markers of colonic permeability, providing a rational for their use in pathologies with an underlying leakiness of the gut.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The structure of the intestinal microbial community is principally modulated by synbiotic intake.
“This is in line with the majority of the literature data [48,50], in which the structure of the intestinal microbial community is principally modulated by the synbiotic intake [22].”
Few probiotic/prebiotic synbiotic approaches have been reported considering the positive effect under competitive conditions of the gastrointestinal tract.
“In addition, few probiotic/prebiotic synbiotic approaches have been reported considering the positive effect under the competitive conditions of the gastrointestinal tract [22].”
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Metabolic Endotoxemia Initiates Obesity and Insulin Resistance
Cani, P. D., Amar, J., Iglesias, M. A., Poggi, M., Knauf, C., Bastelica, D., Neyrinck, A. M., Fava, F., Tuohy, K. M., Chabo, C., et al. (2007) · Diabetes · doi:10.2337/db06-1491 · Cited by 6,638 · see citing works
Linking long-term dietary patterns with gut microbial enterotypes
Wu, G. D., Chen, J., Hoffmann, C., Bittinger, K., Chen, Y.-Y., Keilbaugh, S. A., Bewtra, M., Knights, D., Walters, W. A., Knight, R., et al. (2011) · Science · doi:10.1126/science.1208344 · Cited by 6,513 · see citing works
Cani, P. D., Bibiloni, R., Knauf, C., Waget, A., Neyrinck, A. M., Delzenne, N. M., & Burcelin, R. (2008) · Diabetes · doi:10.2337/db07-1403 · Cited by 4,819 · see citing works
Richness of human gut microbiome correlates with metabolic markers
Le Chatelier, E., Nielsen, T., Qin, J., Prifti, E., Hildebrand, F., Falony, G., Almeida, M., Arumugam, M., Batto, J.-M., Kennedy, S., et al. (2013) · Nature · doi:10.1038/nature12506 · Cited by 4,662 · see citing works
The impact of the gut microbiota on human health: an integrative view
Clemente, J. C., Ursell, L. K., Parfrey, L. W., & Knight, R. (2012) · Cell · doi:10.1016/j.cell.2012.01.035 · Cited by 3,710 · see citing works
The gut microbiota--masters of host development and physiology
Sommer, F., & Bäckhed, F. (2013) · Nature Reviews Microbiology · doi:10.1038/nrmicro2974 · Cited by 3,681 · see citing works
The gut microbiota and host health: a new clinical frontier
Marchesi, J. R., Adams, D. H., Fava, F., Hermes, G. D. A., Hirschfield, G. M., Hold, G., Quraishi, M. N., Kinross, J., Smidt, H., Tuohy, K. M., et al. (2016) · Gut · doi:10.1136/gutjnl-2015-309990 · Cited by 2,302 · see citing works
The role of the gut microbiota in nutrition and health
Flint, H. J., Scott, K. P., Louis, P., & Duncan, S. H. (2012) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2012.156 · Cited by 2,203 · see citing works
Normalization and microbial differential abundance strategies depend upon data characteristics
Weiss, S. J., Xu, Z. Z., Peddada, S. D., Amir, A., Bittinger, K. L., González, A., Lozupone, C., Zaneveld, J., Vázquez‐Baeza, Y., Birmingham, A., et al. (2017) · Microbiome · doi:10.1186/s40168-017-0237-y · Cited by 2,123 · see citing works
Inflammation as a link between obesity, metabolic syndrome and type 2 diabetes
Esser, N., Legrand-Poels, S., Piette, J., Scheen, A. J., & Paquot, N. (2014) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2014.04.006 · Cited by 1,981 · see citing works
Cani, P. D., Neyrinck, A. M., Fava, F., Knauf, C., Burcelin, R., Tuohy, K. M., Gibson, G. R., & Delzenne, N. M. (2007) · Diabetologia · doi:10.1007/s00125-007-0791-0 · Cited by 1,770 · see citing works
Kovatcheva-Datchary, P., Nilsson, A., Akrami, R., Lee, Y. S., De Vadder, F., Arora, T., Hallen, A., Martens, E., Björck, I., & Bäckhed, F. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.10.001 · Cited by 1,731 · see citing works
Convergent adaptation of human lactase persistence in Africa and Europe
Tishkoff, S. A., Reed, F. A., Ranciaro, A., Voight, B. F., Babbitt, C. C., Silverman, J. S., Powell, K., Mortensen, H. M., Hirbo, J. B., Osman, M., et al. (2007) · Nature Genetics · doi:10.1038/ng1946 · Cited by 1,615 · see citing works
Delannoy, S., Chaves, B. D., Ison, S. A., Webb, H. E., Beutin, L., Delaval, J., Billet, I., & Fach, P. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00001 · Cited by 1,186 · see citing works
Probiotic bacteria enhance murine and human intestinal epithelial barrier function
Madsen, K., Cornish, A. S., Soper, P., McKaigney, C. J., Jijon, H. B., Yachimec, C., Doyle, J. S. G., Jewell, L. D., & Simone, C. D. (2001) · Gastroenterology · doi:10.1053/gast.2001.27224 · Cited by 1,096 · 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
Self-citationCani, P. D., Osto, M., Geurts, L., & Everard, A. (2012) · Gut Microbes · doi:10.4161/gmic.19625 · Cited by 864 · see citing works
Carbohydrate metabolism in Bifidobacteria
Pokusaeva, K., Fitzgerald, G. F., & van Sinderen, D. (2011) · Genes & Nutrition · doi:10.1007/s12263-010-0206-6 · Cited by 855 · see citing works
Ramirez-Farias, C., Slezak, K., Fuller, Z., Duncan, A., Holtrop, G., & Louis, P. (2008) · British Journal of Nutrition · doi:10.1017/s0007114508019880 · Cited by 822 · see citing works
Host genetic variation impacts microbiome composition across human body sites
Blekhman, R., Goodrich, J. K., Huang, K., Sun, Q., Bukowski, R., Bell, J. T., Spector, T. D., Keinan, A., Ley, R. E., Gevers, D., et al. (2015) · Genome Biology · doi:10.1186/s13059-015-0759-1 · Cited by 745 · see citing works
Schroeder, B. O., Birchenough, G. M. H., Ståhlman, M., Arike, L., Johansson, M. E. V., Hansson, G. C., & Bäckhed, F. (2018) · Cell Host & Microbe · doi:10.1016/j.chom.2017.11.004 · Cited by 713 · see citing works
Martínez, I., Kim, J., Duffy, P. R., Schlegel, V. L., & Walter, J. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015046 · Cited by 645 · see citing works
Self-citationSalonen, A., Lahti, L., Salojärvi, J., Holtrop, G., Korpela, K., Duncan, S. H., Date, P., Farquharson, F., Johnstone, A. M., Lobley, G. E., et al. (2014) · The ISME Journal · doi:10.1038/ismej.2014.63 · Cited by 626 · see citing works
Ewaschuk, J. B., Diaz, H., Meddings, L., Diederichs, B., Dmytrash, A., Backer, J., Looijer-van Langen, M., & Madsen, K. L. (2008) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.90227.2008 · Cited by 590 · see citing works
Intestinal barrier: An interface between health and disease
Farhadi, A., Banan, A., Fields, J. Z., & Keshavarzian, A. (2003) · Journal of Gastroenterology and Hepatology · doi:10.1046/j.1440-1746.2003.03032.x · Cited by 532 · see citing works
Self-citationA randomized synbiotic trial to prevent sepsis among infants in rural India
Panigrahi, P., Parida, S., Nanda, N. C., Satpathy, R., Pradhan, L., Chandel, D. S., Baccaglini, L., Mohapatra, A., Mohapatra, S. S., Misra, P. R., et al. (2017) · Nature · doi:10.1038/nature23480 · Cited by 526 · see citing works
Maldonado-Gómez, M. X., Martínez, I., Bottacini, F., O’Callaghan, A., Ventura, M., van Sinderen, D., Hillmann, B., Vangay, P., Knights, D., Hutkins, R. W., et al. (2016) · Cell Host & Microbe · doi:10.1016/j.chom.2016.09.001 · Cited by 517 · see citing works
Self-citationMicrobial Invasions: The Process, Patterns, and Mechanisms
Mallon, C. A., van Elsas, J. D., & Salles, J. F. (2015) · Trends in Microbiology · doi:10.1016/j.tim.2015.07.013 · Cited by 488 · see citing works
Vulevic, J., Drakoularakou, A., Yaqoob, P., Tzortzis, G., & Gibson, G. R. (2008) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.2008.26242 · Cited by 451 · see citing works
Intestinal barrier in inflammatory bowel disease
Antoni, L. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i5.1165 · Cited by 416 · see citing works
Variable responses of human microbiomes to dietary supplementation with resistant starch
Venkataraman, A., Sieber, J. R., Schmidt, A. W., Waldron, C., Theis, K. R., & Schmidt, T. M. (2016) · Microbiome · doi:10.1186/s40168-016-0178-x · Cited by 384 · see citing works
Synbiotics Easing Renal Failure by Improving Gut Microbiology (SYNERGY)
Rossi, M., Johnson, D. W., Morrison, M., Pascoe, E. M., Coombes, J. S., Forbes, J. M., Szeto, C., McWhinney, B. C., Ungerer, J. P. J., & Campbell, K. L. (2016) · Clinical Journal of the American Society of Nephrology · doi:10.2215/cjn.05240515 · Cited by 379 · see citing works
Interplay between obesity and associated metabolic disorders: New insights into the gut microbiota
Cani, P. D., & Delzenne, N. M. (2009) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2009.06.016 · Cited by 377 · see citing works
Obesity, Inflammation, and Insulin Resistance – A Mini-Review
Zeyda, M., & Stulnig, T. M. (2009) · Gerontology · doi:10.1159/000212758 · Cited by 364 · see citing works
Martínez, I., Wallace, G., Zhang, C., Legge, R. M., Benson, A. K., Carr, T. P., Moriyama, E. N., & Walter, J. (2009) · Applied and Environmental Microbiology · doi:10.1128/aem.00380-09 · Cited by 355 · see citing works
Self-citationVulevic, J., Juric, A., Tzortzis, G., & Gibson, G. R. (2013) · The Journal of Nutrition · doi:10.3945/jn.112.166132 · Cited by 349 · see citing works
Agans, R., Rigsbee, L., Kenche, H., Michail, S., Khamis, H. J., & Paliy, O. (2011) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2011.01120.x · Cited by 343 · see citing works
Femia, A. P. (2002) · Carcinogenesis · doi:10.1093/carcin/23.11.1953 · Cited by 330 · see citing works
Davis, L. M. G., Martínez, I., Walter, J., Goin, C., & Hutkins, R. W. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025200 · Cited by 321 · see citing works
Self-citationHaarman, M., & Knol, J. (2006) · Applied and Environmental Microbiology · doi:10.1128/aem.72.4.2359-2365.2006 · Cited by 321 · see citing works
Synbiotics in Health and Disease
Kolida, S., & Gibson, G. R. (2011) · Annual Review of Food Science and Technology · doi:10.1146/annurev-food-022510-133739 · Cited by 309 · 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
Azcárate-Peril, M. A., Ritter, A. J., Savaiano, D. A., Monteagudo-Mera, A., Anderson, C., Magness, S. T., & Klaenhammer, T. R. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1606722113 · Cited by 246 · see citing works
Effects of Administration of TOS and Bifidobacterium breve 4006 on the Human Fecal Flora
Tanaka, R., Takayama, H., Morotomi, M., Kuroshima, T., Ueyama, S., Matsumoto, K. T., Kuroda, A., & Mutai, M. (1983) · Bifidobacteria and Microflora · doi:10.12938/bifidus1982.2.1_17 · Cited by 238 · see citing works
Ringel-Kulka, T., Cheng, J., Ringel, Y., Salojärvi, J., Carroll, I., Palva, A., de Vos, W. M., & Satokari, R. (2013) · PLoS ONE · doi:10.1371/journal.pone.0064315 · Cited by 230 · see citing works
Strengthening of the intestinal epithelial tight junction by Bifidobacterium bifidum
Hsieh, C.-Y., Osaka, T., Moriyama, E., Date, Y., Kikuchi, J., & Tsuneda, S. (2015) · Physiological Reports · doi:10.14814/phy2.12327 · Cited by 229 · see citing works
Canfora, E. E., van der Beek, C. M., Hermes, G. D. A., Goossens, G. H., Jocken, J. W. E., Holst, J. J., van Eijk, H. M. H., Venema, K., Smidt, H., Zoetendal, E. G., et al. (2017) · Gastroenterology · doi:10.1053/j.gastro.2017.03.051 · Cited by 227 · see citing works
Farhadi, A., Gundlapalli, S., Shaikh, M. W., Frantzides, C. T., Harrell, L. E., Kwasny, M., & Keshavarzian, A. (2008) · Liver International · doi:10.1111/j.1478-3231.2008.01723.x · Cited by 225 · see citing works
Self-citationDavis, L. M. G., Martínez, I., Walter, J., & Hutkins, R. W. (2010) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2010.10.007 · Cited by 222 · see citing works
Self-citationMetabolic endotoxemia: a molecular link between obesity and cardiovascular risk
Neves, A. L., Coelho, J., Couto, L., Leite-Moreira, A., & Roncon-Albuquerque, R. (2013) · Journal of Molecular Endocrinology · doi:10.1530/jme-13-0079 · Cited by 211 · see citing works
Statin therapy causes gut dysbiosis in mice through a PXR-dependent mechanism
Caparros-Martin, J. A., Lareu, R. R., Ramsay, J. P., Peplies, J., Reen, F. J., Headlam, H. A., Ward, N. C., Croft, K. D., Newsholme, P., Hughes, J., et al. (2017) · Microbiome · doi:10.1186/s40168-017-0312-4 · Cited by 210 · see citing works
Hjorth, M. F., Roager, H. M., Larsen, T. M., Poulsen, S. K., Licht, T. R., Bahl, M. I., Zohar, Y., & Astrup, A. V. (2017) · International Journal of Obesity · doi:10.1038/ijo.2017.220 · Cited by 207 · see citing works
Walter, J., Maldonado-Gómez, M. X., & Martínez, I. (2017) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2017.08.008 · Cited by 198 · see citing works
Self-citationGriffiths, E. A., Duffy, L. C., Schanbacher, F. L., Qiao, H., Dryja, D., Leavens, A., Rossman, J., Rich, G. A., DiRienzo, D. B., & Ogra, P. L. O. (2004) · Digestive Diseases and Sciences · doi:10.1023/b:ddas.0000026302.92898.ae · Cited by 197 · see citing works
Lactobacillus plantarum DSM 2648 is a potential probiotic that enhances intestinal barrier function
Anderson, R. C., Cookson, A. L., McNabb, W. C., Kelly, W. J., & Roy, N. C. (2010) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2010.02038.x · Cited by 194 · see citing works
The Role of Bifidobacteria in Gut Barrier Function After Thermal Injury in Rats
Wang, Z., Xiao, G., Yao, Y.-M., Guo, S., Lu, K., & Sheng, Z. (2006) · The Journal of Trauma: Injury, Infection, and Critical Care · doi:10.1097/01.ta.0000196574.70614.27 · Cited by 193 · see citing works
Resistant starch can improve insulin sensitivity independently of the gut microbiota
Bindels, L. B., Muñoz, R. R. S., Neto, J. C. G., Mutemberezi, V., Martínez, I., Salazar, N., Cody, E. A., Quintero, M., Kittana, H., Reyes‐Gavilán, C. G. D. L., et al. (2017) · Microbiome · doi:10.1186/s40168-017-0230-5 · Cited by 180 · see citing works
Self-citationTalking microbes: When gut bacteria interact with diet and host organs
Cani, P. D., & Everard, A. (2015) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201500406 · Cited by 175 · see citing works
Alander, M., Mättö, J., Kneifel, W., Johansson, M., Kögler, B., Crittenden, R. G., Mattila, T., & Saarela, M. (2001) · International Dairy Journal · doi:10.1016/s0958-6946(01)00100-5 · Cited by 175 · see citing works
Walton, G., van den Heuvel, E. G. H. M., Kosters, M. H. W., Rastall, R. A., Tuohy, K. M., & Gibson, G. R. (2011) · British Journal Of Nutrition · doi:10.1017/s0007114511004697 · Cited by 173 · see citing works
Chen, J., Wang, R., Li, X., & Wang, R.-L. (2011) · British Journal Of Nutrition · doi:10.1017/s0007114511004491 · Cited by 169 · see citing works
Hilsden, R. J., Meddings, J., & Sutherland, L. (1996) · Gastroenterology · doi:10.1053/gast.1996.v110.pm8613043 · Cited by 169 · see citing works
Sierra, C., Bernal, M. J., Blasco‐Alonso, J., Martínez, R., Dalmau, J., Ortuño, I., Espín, B., Vasallo, M.-I., Gil, D., Vidal, M.-L., et al. (2014) · European Journal of Nutrition · doi:10.1007/s00394-014-0689-9 · Cited by 159 · see citing works
Xiao-ming, B., Li, J., Feng, Z., Shi, S.-Y., Lu, Y.-D., Chen, R., & Zhou, X. (2008) · World Journal of Gastroenterology · doi:10.3748/wjg.14.6564 · Cited by 158 · see citing works
Bifidobacteriumanimalis subsp. lactis BB-12 in reducing the risk of infections in infancy
Taipale, T. J., Pienihäkkinen, K., Isolauri, E., Larsen, C. N., Brockmann, E., Alanen, P. J., Jokela, J., & Söderling, E. M. (2010) · British Journal Of Nutrition · doi:10.1017/s0007114510003685 · Cited by 149 · see citing works
Akbari, P., Braber, S., Alizadeh, A., Verheijden, K. A. T., Schoterman, M. H. C., Kraneveld, A. D., Garssen, J., & Fink‐Gremmels, J. (2015) · Journal of Nutrition · doi:10.3945/jn.114.209486 · Cited by 147 · see citing works
The gut microbiota and the metabolic health of the host
Joyce, S. A., & Gahan, C. G. M. (2014) · Current Opinion in Gastroenterology · doi:10.1097/mog.0000000000000039 · Cited by 147 · see citing works
Carbohydrate preference, acid tolerance and bile tolerance in five strains of Bifidobacterium
Vernazza, C. L., Gibson, G. R., & Rastall, R. A. (2006) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2006.02832.x · Cited by 143 · see citing works
Bouhnik, Y., Raskine, L., Simoneau, G., Paineau, D., & Bornet, F. R. J. (2006) · Nutrition Journal · doi:10.1186/1475-2891-5-8 · Cited by 142 · see citing works
Carvalho-Wells, A. L., Helmolz, K., Nodet, C., Mölzer, C., Leonard, C., McKevith, B., Thielecke, F., Jackson, K. G., & Tuohy, K. M. (2010) · British Journal Of Nutrition · doi:10.1017/s0007114510002084 · Cited by 141 · see citing works
Guo, S., Gillingham, T. Z., Guo, Y., Meng, D., Zhu, W., Walker, W. A., & Ganguli, K. A. (2016) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000001310 · Cited by 129 · see citing works
Parche, S., Beleut, M., Rezzonico, E., Jacobs, D. M., Arigoni, F., Titgemeyer, F., & Janković, I. (2006) · Journal of Bacteriology · doi:10.1128/jb.188.4.1260-1265.2006 · Cited by 127 · see citing works
Wang, X., Brown, I. L., Evans, A. J., & Conway, P. L. (1999) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.1999.00836.x · Cited by 122 · see citing works
Fanaro, S., Marten, B., Bagna, R., Vigi, V., Fabris, C., Quintana, L. P., Argüelles‐Arias, F., Scholz-Ahrens, K. E., Sawatzki, G., Zelenka, R., et al. (2009) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0b013e31817b6dd2 · Cited by 116 · see citing works
Satokari, R. M., Vaughan, E. E., Akkermans, A. D. L., Saarela, M., & de Vos, W. M. (2001) · Systematic and Applied Microbiology · doi:10.1078/0723-2020-00035 · Cited by 112 · see citing works
Mujagic, Z., de Vos, P., Boekschoten, M. V., Govers, C., Pieters, H., de Wit, N. J. W., Bron, P. A., Masclee, A., & Troost, F. J. (2017) · Scientific Reports · doi:10.1038/srep40128 · Cited by 108 · 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
Alizadeh, A., Akbari, P., Difilippo, E., Schols, H. A., Ulfman, L. H., Schoterman, M. H. C., Garssen, J., Fink‐Gremmels, J., & Braber, S. (2015) · British Journal Of Nutrition · doi:10.1017/s0007114515004997 · Cited by 106 · see citing works
Akbari, P., Fink‐Gremmels, J., Willems, R., Difilippo, E., Schols, H. A., Schoterman, M. H. C., Garssen, J., & Braber, S. (2016) · European Journal of Nutrition · doi:10.1007/s00394-016-1234-9 · Cited by 97 · see citing works
Morel, F. B., Dai, Q., Ni, J., Thomas, D., Parnet, P., & Fança‐Berthon, P. (2015) · Journal of Nutrition · doi:10.3945/jn.114.204909 · Cited by 92 · see citing works
Prebiotic Galactooligosaccharide Metabolism by Probiotic Lactobacilli and Bifidobacteria
Thongaram, T., Hoeflinger, J. L., Chow, J., & Miller, M. J. (2017) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.7b00851 · Cited by 89 · see citing works
Synbiotics for Improved Human Health: Recent Developments, Challenges, and Opportunities
Krumbeck, J. A., Walter, J., & Hutkins, R. W. (2018) · Annual Review of Food Science and Technology · doi:10.1146/annurev-food-030117-012757 · Cited by 84 · see citing works
Self-citationWu, R., Määttänen, P., Napper, S., Scruten, E., Li, B., Koike, Y., Johnson‐Henry, K. C., Pierro, A., Rossi, L., Botts, S. R., et al. (2017) · Microbiome · doi:10.1186/s40168-017-0357-4 · Cited by 80 · see citing works
Martín, R., Laval, L., Chain, F., Miquel, S., Natividad, J. M., Cherbuy, C., Sokol, H., Verdu, E. F., Vlieg, J. V. H., Bermúdez‐Humarán, L. G., et al. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00608 · Cited by 78 · see citing works
Reichold, A., Brenner, S. A., Spruss, A., Förster‐Fromme, K., Bergheim, I., & Bischoff, S. C. (2013) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2013.09.011 · Cited by 77 · see citing works
Lactic Acid Bacteria May Impact Intestinal Barrier Function by Modulating Goblet Cells
Ren, C., Dokter‐Fokkens, J., Lozano, S. F., et al. (2018) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201700572 · Cited by 77 · see citing works
Zhong, Y., Cai, D., Cai, W., Geng, S., Chen, L., & Han, T. (2009) · Clinical Nutrition · doi:10.1016/j.clnu.2009.04.026 · Cited by 69 · see citing works
Krumbeck, J. A., Maldonado-Gómez, M. X., Martínez, I., Frese, S. A., Burkey, T. E., Rasineni, K., Ramer‐Tait, A. E., Harris, E. N., Hutkins, R. W., & Walter, J. (2015) · Applied and Environmental Microbiology · doi:10.1128/aem.03903-14 · Cited by 68 · see citing works
Self-citationβ2→1-Fructans Modulate the Immune System In Vivo in a Microbiota-Dependent and -Independent Fashion
Fransen, F., Sahasrabudhe, N. M., Elderman, M. E., Bosveld, M., Aidy, S. E., Hugenholtz, F., Borghuis, T., Kousemaker, B., Winkel, S. L., Jongh, C. E. V. D. G., et al. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00154 · Cited by 68 · see citing works
Redefining Lactose as a Conditional Prebiotic
Szilagyi, A. (2004) · Canadian Journal of Gastroenterology · doi:10.1155/2004/350732 · Cited by 63 · see citing works
Shaikh, M. W., Rajan, K. B., Forsyth, C. B., Voigt, R. M., & Keshavarzian, A. (2015) · Clinica Chimica Acta · doi:10.1016/j.cca.2014.12.040 · Cited by 53 · see citing works
Self-citationMalinen, E., Mättö, J., Salmitie, M., et al. (2002) · Systematic and Applied Microbiology · doi:10.1078/0723-2020-00117 · Cited by 49 · see citing works
Tran, C. D., Grice, D. M., Wade, B., Kerr, C. A., Bauer, D. C., Li, D., & Hannan, G. N. (2015) · Future Microbiology · doi:10.2217/fmb.15.54 · Cited by 47 · see citing works
Interactions between gut microbes and host cells control gut barrier and metabolism
Cani, P. D. (2016) · International Journal of Obesity Supplements · doi:10.1038/ijosup.2016.6 · Cited by 47 · see citing works
Intestinal Permeability in Non-alcoholic Fatty LIVER Disease: The Gut-liver Axis
Scarpellini, E., Lupo, M., Iegri, C., Gasbarrini, A., Santis, A. D., & Tack, J. F. (2015) · Reviews on Recent Clinical Trials · doi:10.2174/1574887109666141216104334 · Cited by 36 · see citing works
Malinen, E., Mättö, J., Salmitie, M., et al. (2002) · Systematic and Applied Microbiology · doi:10.1016/s0723-2020(04)70109-5 · Cited by 29 · see citing works
Ogawa, T., Asai, Y., Yasuda, K., & Sakamoto, H. (2005) · Nutrition Research · doi:10.1016/j.nutres.2004.10.012 · Cited by 25 · see citing works
Rodes, L., Saha, S., Tomaro-Duchesneau, C., et al. (2014) · BioMed Research International · doi:10.1155/2014/602832 · Cited by 22 · see citing works
de Freitas, M. B., Moreira, E. A. M., Oliveira, D. D. L., Tomio, C., da Rosa, J. S., Moreno, Y. M. F., Barbosa, E., Neto, N. L., Buccigrossi, V., Guarino, A., et al. (2017) · European Journal of Clinical Nutrition · doi:10.1038/s41430-017-0043-4 · Cited by 22 · see citing works
Samples and techniques highlighting the links between obesity and microbiota
Angelakis, E., & Lagier, J. (2016) · Microbial Pathogenesis · doi:10.1016/j.micpath.2016.01.024 · Cited by 16 · see citing works
Chandel, D. S., Pérez-Muñoz, M. E., Fang, Y., et al. (2017) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000001522 · Cited by 16 · see citing works
Clarke, S. T., Brooks, S. P. J., Inglis, G. D., Yanke, L. J., Green, J., Petronella, N., Ramdath, D. D., Berčík, P., Green-Johnson, J. M., & Kalmokoff, M. L. (2017) · British Journal Of Nutrition · doi:10.1017/s0007114517002318 · Cited by 16 · see citing works
Mills, D. A. (2017) · Current Medical Research and Opinion · doi:10.1080/03007995.2017.1359153 · Cited by 4 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Swanson, K. S., Gibson, G. R., Hutkins, R., Reimer, R. A., Reid, G., Verbeke, K., Scott, K. P., Holscher, H. D., Azad, M. B., Delzenne, N. M., et al. (2020) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-020-0344-2 · Cited by 2,196 · see citing works
Self-citationProbiotics and prebiotics in intestinal health and disease: from biology to the clinic
Sanders, M. E., Merenstein, D. J., Reid, G., Gibson, G. R., & Rastall, R. A. (2019) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-019-0173-3 · Cited by 2,059 · see citing works
The intestinal microbiota fuelling metabolic inflammation
Tilg, H., Zmora, N., Adolph, T. E., & Elinav, E. (2020) · Nature Reviews Immunology · doi:10.1038/s41577-019-0198-4 · Cited by 1,089 · see citing works
Leaky gut: mechanisms, measurement and clinical implications in humans
Camilleri, M. (2019) · Gut · doi:10.1136/gutjnl-2019-318427 · Cited by 1,081 · see citing works
Diet and the human gut microbiome: An international review
Wilson, A. S., Koller, K. R., Ramaboli, M. C., Nesengani, L. T., Ocvirk, S., Chen, C., Flanagan, C. A., Sapp, F. R., Merritt, Z. T., Bhatti, F., et al. (2020) · Digestive Diseases and Sciences · doi:10.1007/s10620-020-06112-w · Cited by 369 · see citing works
Pontes, K. S. D. S., Guedes, M. R., Cunha, M. R. D., Mattos, S. D. S., Barreto Silva, M. I., Neves, M. F., Marques, B. C. A. A., & Klein, M. R. S. T. (2021) · Clinical Nutrition · doi:10.1016/j.clnu.2021.06.023 · Cited by 86 · 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
De Giani, A., Sandionigi, A., Zampolli, J., Michelotti, A., Tursi, F., Labra, M., & Di Gennaro, P. (2022) · Microorganisms · doi:10.3390/microorganisms10061256 · Cited by 46 · see citing works
Effects of bread yeast cell wall beta-glucans on mice with loperamide-induced constipation
Chen, Z., Lin, S., Jiang, Y., Liu, L., Jiang, J., Chen, S., Tong, Y., & Wang, P. (2019) · Journal of Medicinal Food · doi:10.1089/jmf.2019.4407 · Cited by 34 · see citing works
da Silva, T. F., Glória, R. D. A., de Sousa, T. J., Americo, M. F., Freitas, A. D. S., Viana, M. V. C., de Jesus, L. C. L., da Silva Prado, L. C., Daniel, N., Ménard, O., et al. (2023) · BMC Microbiology · doi:10.1186/s12866-023-03112-4 · Cited by 11 · see citing works
- Authors
- Krumbeck, J. A., Rasmussen, H. E., Hutkins, R. W., Clarke, J., Shawron, K., Keshavarzian, A., & Walter, J.
- Affiliations
- University of Nebraska–Lincoln (US)
- Rush University Medical Center (US)
- Corresponding author
- Hutkins, Robert W.
- Keshavarzian, Ali
- Walter, Jens
- ORCID
- Venue
- Microbiome
- Published
- 2018-06-28
- Volume
- 6
- Issue
- 1
- Pages
- 121-121
- ISSN
- 2049-2618 (ISSN-L)
- PMC
- PMC6022452
- OpenAlex
- W2809784323
- Cited by
- 342
- References
- 103
- Citations by year
- 2026: 28 · 2025: 51 · 2024: 59 · 2023: 54 · 2022: 49 · 2021: 47 · 2020: 36 · 2019: 15 · 2018: 2 · 2017: 1
- FWCI
- 23.47
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Microbiome (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Lincoln (University of Nebraska) (submittedVersion)
- Lincoln (University of Nebraska) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- U.S. Department of Agriculture (#2012-67017-19344)
- Nebraska Research Initiative
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Health Sciences › Nursing › Nutrition and Dietetics › Microbial Metabolites in Food Biotechnology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Keywords
- synbiotics, Bifidobacterium animalis subsp. lactis BB-12, galactooligosaccharides, intestinal barrier function, colonic permeability, gut microbiota, endotoxemia, obesity
- MeSH terms
- Gastrointestinal Microbiome, Adult, Bifidobacterium, Double-Blind Method, Female, Humans, Intestines, Male, Middle Aged, Obesity, Oligosaccharides, RNA, Ribosomal, 16S, Sucrose, Tight Junctions, Endotoxemia, Probiotics, Young Adult, Prebiotics, Synbiotics
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
