[en] Intestinal fibrosis is a long–term complication of inflammatory bowel diseases (IBD). Changes in microbial populations have been linked with the onset of fibrosis and some food additives are known to promote intestinal inflammation facilitating fibrosis induction. In this study, we investigated how polysorbate 80, sucralose, titanium dioxide, sodium nitrite and maltodextrin affect the gut microbiota and the metabolic activity in healthy and IBD donors (patients in remission and with a flare of IBD). The Simulator of the Human Intestinal Microbial Ecosystem (SHIME®) with a static (batch) configuration was used to evaluate the effects of food additives on the human intestinal microbiota. Polysorbate 80 and sucralose decreased butyrate–producing bacteria such as Roseburia and Faecalibacterium prausnitzii. Both compounds, also increased bacterial species positively correlated with intestinal inflammation and fibrosis (i.e.: Enterococcus, Veillonella and Mucispirillum schaedleri), especially in donors in remission of IBD. Additionally, polysorbate 80 induced a lower activity of the aryl hydrocarbon receptor (AhR) in the three groups of donors, which can affect the intestinal homeostasis. Maltodextrin, despite increasing short–chain fatty acids production, promoted the growth of Ruminococcus genus, correlated with higher risk of fibrosis, and decreased Oscillospira which is negatively associated with fibrosis. Our findings unveil crucial insights into the potential deleterious effects of polysorbate 80, sucralose and maltodextrin on human gut microbiota in healthy and, to a greater extent, in IBD patients.
Research center :
FARAH - Fundamental and Applied Research for Animals and Health - ULiège [BE]
Gonza Quito, Irma Elizabeth ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH)
Goya-Jorge, Elizabeth ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Santé publique vétérinaire
Douny, Caroline ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Analyse des denrées alimentaires
Boutaleb, Samiha ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA)
Taminiau, Bernard ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Santé publique vétérinaire
Daube, Georges ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires
Scippo, Marie-Louise ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Analyse des denrées alimentaires
Louis, Edouard ; Université de Liège - ULiège > Département des sciences cliniques > Hépato-gastroentérologie
Delcenserie, Véronique ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Gestion de la qualité dans la chaîne alimentaire
Language :
English
Title :
Food additives impair gut microbiota from healthy individuals and IBD patients in a colonic in vitro fermentation model
Original title :
[en] Food additives impair gut microbiota from healthy individuals and IBD patients in a colonic in vitro fermentation model
Abdel-Rahman, L.I.H., Morgan, X.C., Searching for a consensus among inflammatory bowel disease studies: A systematic meta-analysis. Inflammatory Bowel Diseases 29:1 (2023), 125–139, 10.1093/ibd/izac194.
Aguirre, M., Ramiro-Garcia, J., Koenen, M.E., Venema, K., To pool or not to pool? Impact of the use of individual and pooled fecal samples for in vitro fermentation studies. Journal of Microbiological Methods 107 (2014), 1–7, 10.1016/j.mimet.2014.08.022.
Alam, M.T., Amos, G.C.A., Murphy, A.R.J., Murch, S., Wellington, E.M.H., Arasaradnam, R.P., Microbial imbalance in inflammatory bowel disease patients at different taxonomic levels. Gut Pathogens 12:1 (2020), 1–8, 10.1186/s13099-019-0341-6.
Almutairi, R., Basson, A.R., Wearsh, P., Cominelli, F., Rodriguez-Palacios, A., Validity of food additive maltodextrin as placebo and effects on human gut physiology: Systematic review of placebo-controlled clinical trials. European Journal of Nutrition 61:6 (2022), 2853–2871, 10.1007/s00394-022-02802-5.
Arumugam, M., Raes, J., Pelletier, E., Paslier, D.L., Yamada, T., Mende, D.R., Fernandes, G.R., Tap, J., Bruls, T., Batto, J.M., Bertalan, M., Borruel, N., Casellas, F., Fernandez, L., Gautier, L., Hansen, T., Hattori, M., Hayashi, T., Kleerebezem, M., Zeller, G., Enterotypes of the human gut microbiome. Nature 473:7346 (2011), 174–180, 10.1038/nature09944.
Bancil, A.S., Sandall, A.M., Rossi, M., Chassaing, B., Lindsay, J.O., Whelan, K., Food additive emulsifiers and their impact on gut microbiome, permeability, and inflammation: Mechanistic insights in inflammatory bowel disease. Journal of Crohn's and Colitis 15:6 (2021), 1068–1079, 10.1093/ecco-jcc/jjaa254.
Biagini, F., Daddi, C., Calvigioni, M., De Maria, C., Zhang, Y.S., Ghelardi, E., Vozzi, G., Designs and methodologies to recreate in vitro human gut microbiota models. Bio-Design and Manufacturing 6:3 (2022), 298–318, 10.1007/s42242-022-00210-6.
Bian, X., Chi, L., Gao, B., Tu, P., Ru, H., Lu, K., Gut microbiome response to sucralose and its potential role in inducing liver inflammation in mice. Frontiers in Physiology 8:JUL (2017), 1–13, 10.3389/fphys.2017.00487.
Calatayud, M., Van den Abbeele, P., Ghyselinck, J., Marzorati, M., Rohs, E., Birkett, A., Comparative effect of 22 dietary sources of fiber on gut microbiota of healthy humans in vitro. Frontiers in Nutrition 8:July (2021), 1–13, 10.3389/fnut.2021.700571.
Calgaro, M., Pandolfo, M., Salvetti, E., Marotta, A., Larini, I., Pane, M., Amoruso, A., Del Casale, A., Vitulo, N., Fiorio, M., Felis, G.E., Metabarcoding analysis of gut microbiota of healthy individuals reveals impact of probiotic and maltodextrin consumption. Beneficial Microbes 12:2 (2021), 121–136, 10.3920/BM2020.0137.
Chang, T.E., Luo, J.C., Yang, U.C., Huang, Y.H., Hou, M.C., Lee, F.Y., Fecal microbiota profile in patients with inflammatory bowel disease in Taiwan. Journal of the Chinese Medical Association 84:6 (2021), 580–587, 10.1097/JCMA.0000000000000532.
Chassaing, B., Compher, C., Bonhomme, B., Liu, Q., Tian, Y., Walters, W., Nessel, L., Delaroque, C., Hao, F., Gershuni, V., HHS Public Access Randomized Controlled-Feeding Study of Dietary Emulsifier. 162:3 (2022), 743–756, 10.1053/j.gastro.2021.11.006.Randomized.
Chassaing, B., Van De Wiele, T., De Bodt, J., Marzorati, M., Gewirtz, A.T., Dietary emulsifiers directly alter human microbiota composition and gene expression ex vivo potentiating intestinal inflammation. Gut 66:8 (2017), 1414–1427, 10.1136/gutjnl-2016-313099.
Chen, L., Reynolds, C., David, R., Peace, A., Development of an index score for intestinal inflammation - associated dysbiosis using real - world stool test results. Digestive Diseases and Sciences 65:4 (2020), 1111–1124, 10.1007/s10620-019-05828-8.
Clooney, A.G., Eckenberger, J., Laserna-Mendieta, E., Sexton, K.A., Bernstein, M.T., Vagianos, K., Sargent, M., Ryan, F.J., Moran, C., Sheehan, D., Sleator, R.D., Targownik, L.E., Bernstein, C.N., Shanahan, F., Claesson, M.J., Ranking microbiome variance in inflammatory bowel disease: A large longitudinal intercontinental study. Gut 70:3 (2021), 499–510, 10.1136/gutjnl-2020-321106.
Costea, P.I., Hildebrand, F., Arumugam, M., Bäckhed, F., Blaser, M.J., Bushman, F.D., de Vos, W.M., Ehrlich, S.D., Fraser, C.M., Hattori, M., Huttenhower, C., Jeffery, I.B., Knights, D., Lewis, J.D., Ley, R.E., Ochman, H., O'Toole, P.W., Quince, C., Relman, D.A., Bork, P., Enterotypes in the landscape of gut microbial community composition. Nature Microbiology 3:1 (2017), 8–16, 10.1038/s41564-017-0072-8.
D'Alessio, S., Ungaro, F., Noviello, D., Lovisa, S., Peyrin-Biroulet, L., Danese, S., Revisiting fibrosis in inflammatory bowel disease: The gut thickens. Nature Reviews Gastroenterology and Hepatology 19:3 (2022), 169–184, 10.1038/s41575-021-00543-0.
Dai, Z.F., Ma, X.Y., Yang, R., Wang, H., Xu, D., Yang, J., Guo, X., Meng, S., Xu, R., Li, Y., Xu, Y., Li, K., Lin, X., Intestinal flora alterations in patients with ulcerative colitis and their association with inflammation. Experimental and Therapeutic Medicine 22:5 (2021), 1–12, 10.3892/etm.2021.10757.
Daniel, N., Wu, G.D., Walters, W., Compher, C., Ni, J., Delaroque, C., Albenberg, L., Ley, R.E., Patterson, A.D., Lewis, J.D., Gewirtz, A.T., Chassaing, B., Human intestinal microbiome determines individualized inflammatory response to dietary emulsifier carboxymethylcellulose consumption. Cellular and Molecular Gastroenterology and Hepatology, 2023, 10.1016/j.jcmgh.2023.11.001.
Del Pozo, S., Gómez-martínez, S., Díaz, L.E., Nova, E., Urrialde, R., Marcos, A., Potential effects of sucralose and saccharin on gut microbiota: a review. Nutrients 14:8 (2022), 1–16, 10.3390/nu14081682.
Douny, C., Dufourny, S., Brose, F., Verachtert, P., Rondia, P., Lebrun, S., Marzorati, M., Everaert, N., Delcenserie, V., Scippo, M.L., Development of an analytical method to detect short-chain fatty acids by SPME-GC–MS in samples coming from an in vitro gastrointestinal model. Journal of Chromatography B: Analytical Technologies in the Biomedical and Life Sciences 1124:June (2019), 188–196, 10.1016/j.jchromb.2019.06.013.
Drabińska, N., Jarocka-Cyrta, E., Markiewicz, L.H., Krupa-Kozak, U., The effect of oligofructose-enriched inulin on faecal bacterial counts and microbiota-associated characteristics in celiac disease children following a gluten-free diet: Results of a randomized, placebo-controlled trial. Nutrients 10:2 (2018), 1–11, 10.3390/nu10020201.
Escoto, J.A., Martínez-Carrillo, B.E., Ramírez-Durán, N., Ramírez-Saad, H., Aguirre-Garrido, J.F., Valdés-Ramos, R., Consumo crónico de edulcorantes en ratones y su efecto sobre el sistema inmunitario y la microbiota del intestino delgado. Biomédica 41:3 (2021), 504–530, 10.7705/biomedica.5806.
Ezzine, C., Loison, L., Montbrion, N., Bôle-Feysot, C., Déchelotte, P., Coëffier, M., Ribet, D., Fatty acids produced by the gut microbiota dampen host inflammatory responses by modulating intestinal SUMOylation. Gut Microbes, 14(1), 2022, 10.1080/19490976.2022.2108280.
Falony, G., Vandeputte, D., Caenepeel, C., Vieira-Silva, S., Daryoush, T., Vermeire, S., Raes, J., The human microbiome in health and disease: Hype or hope. Acta Clinica Belgica 74:2 (2019), 53–64, 10.1080/17843286.2019.1583782.
Firrman, J., Liu, L.S., Tanes, C., Friedman, E.S., Bittinger, K., Daniel, S., Van Den Abbeele, P., Evans, B., Metabolic analysis of regionally distinct gut microbial communities using an in vitro platform. Journal of Agricultural and Food Chemistry 68:46 (2020), 13056–13067, 10.1021/acs.jafc.9b05202.
Flint, H. J., & Duncan, S. H. (2014). Bacteroides and Prevotella. In Encyclopedia of Food Microbiology: Second Edition (Second Edi, Vol. 1). Elsevier. https://doi.org/10.1016/B978-0-12-384730-0.00031-8.
Franzosa, E.A., Sirota-Madi, A., Avila-Pacheco, J., Fornelos, N., Haiser, H.J., Reinker, S., Vatanen, T., Hall, A.B., Mallick, H., McIver, L.J., Sauk, J.S., Wilson, R.G., Stevens, B.W., Scott, J.M., Pierce, K., Deik, A.A., Bullock, K., Imhann, F., Porter, J.A., Xavier, R.J., Gut microbiome structure and metabolic activity in inflammatory bowel disease. Nature Microbiology 4:2 (2019), 293–305, 10.1038/s41564-018-0306-4.
Gerasimidis, K., Bryden, K., Chen, X., Papachristou, E., Verney, A., Roig, M., Hansen, R., Nichols, B., Papadopoulou, R., Parrett, A., The impact of food additives, artificial sweeteners and domestic hygiene products on the human gut microbiome and its fibre fermentation capacity. European Journal of Nutrition 59:7 (2020), 3213–3230, 10.1007/s00394-019-02161-8.
Ghyselinck, J., Verstrepen, L., Moens, F., Van den Abbeele, P., Said, J., Smith, B., Bjarnason, I., Basit, A.W., Gaisford, S., A 4-strain probiotic supplement influences gut microbiota composition and gut wall function in patients with ulcerative colitis. International Journal of Pharmaceutics, 587(July), 2020, 119648, 10.1016/j.ijpharm.2020.119648.
Glover, J.S., Ticer, T.D., Engevik, M.A., Characterizing the mucin-degrading capacity of the human gut microbiota. Scientific Reports, 12(1), 2022, 8456, 10.1038/s41598-022-11819-z.
Goya-Jorge, E., Gonza, I., Bondue, P., Douny, C., Taminiau, B., Daube, G., Scippo, M.L., Delcenserie, V., Human adult microbiota in a static colon model: AhR Transcriptional activity at the crossroads of host-microbe interaction. Foods, 11(13), 2022, 10.3390/foods11131946.
Goya-Jorge, E., Gonza, I., Douny, C., Scippo, M., Delcenserie, V., M-batches to simulate luminal and mucosal human gut microbial ecosystems: A case study of the effects of coffee and green tea. Microorganisms, 12(2), 2024, 236, 10.3390/microorganisms12020236.
Han, Y., Wang, B., Gao, H., He, C., Hua, R., Liang, C., Xin, S., Wang, Y., Xu, J., Insight into the relationship between oral microbiota and the inflammatory bowel disease. Microorganisms, 10(9), 2022, 1868, 10.3390/microorganisms10091868.
Holder, M.K., Peters, N.V., Whylings, J., Fields, C.T., Gewirtz, A.T., Chassaing, B., de Vries, G.J., Dietary emulsifiers consumption alters anxiety-like and social-related behaviors in mice in a sex-dependent manner. Scientific Reports 9:1 (2019), 1–14, 10.1038/s41598-018-36890-3.
Holmes, I., Harris, K., Quince, C., Dirichlet multinomial mixtures: generative models for microbial metagenomics. PLoS ONE, 7(2), 2012, e30126.
Hosmer, J., McEwan, A. G., & Kappler, U. (2023). Bacterial acetate metabolism and its influence on human epithelia. Emerging Topics in Life Sciences, 0(February), 1–13. /emergtoplifesci/article/doi/10.1042/ETLS20220092/232786/Bacterial-acetate-metabolism-and-its-influence-on%0Ahttps://portlandpress.com/emergtoplifesci/article/doi/10.1042/ETLS20220092/232786/Bacterial-acetate-metabolism-and-its-influence-on.
Hrncirova, L., Hudcovic, T., Sukova, E., Machova, V., Trckova, E., Krejsek, J., Hrncir, T., Human gut microbes are susceptible to antimicrobial food additives in vitro. Folia Microbiologica 64:4 (2019), 497–508, 10.1007/s12223-018-00674-z.
Isenring, J., Bircher, L., Geirnaert, A., Lacroix, C., In vitro human gut microbiota fermentation models: Opportunities, challenges, and pitfalls. Microbiome Research Reports, 2(1), 2023, 2 https://doi.org/10.20517/mrr.2022.15.
Jacob, N., Jacobs, J.P., Kumagai, K., Ha, C.W.Y., Kanazawa, Y., Lagishetty, V., Altmayer, K., Hamill, A.M., Von Arx, A., Sartor, R.B., Devkota, S., Braun, J., Michelsen, K.S., Targan, S.R., Shih, D.Q., Inflammation-independent TL1A-mediated intestinal fibrosis is dependent on the gut microbiome. Mucosal Immunology 11:5 (2018), 1466–1476, 10.1038/s41385-018-0055-y.
Kugathasan, S., Denson, L.A., Walters, T.D., Kim, M.O., Marigorta, U.M., Schirmer, M., Mondal, K., Liu, C., Griffiths, A., Noe, J.D., Crandall, W.V., Snapper, S., Rabizadeh, S., Rosh, J.R., Shapiro, J.M., Guthery, S., Mack, D.R., Kellermayer, R., Kappelman, M.D., Dubinsky, M.C., Prediction of complicated disease course for children newly diagnosed with Crohn's disease: A multicentre inception cohort study. The Lancet 389:10080 (2017), 1710–1718, 10.1016/S0140-6736(17)30317-3.
LaBouyer, M., Holtrop, G., Horgan, G., Gratz, S.W., Belenguer, A., Smith, N., Walker, A.W., Duncan, S.H., Johnstone, A.M., Louis, P., Flint, H.J., Scott, K.P., Higher total faecal short-chain fatty acid concentrations correlate with increasing proportions of butyrate and decreasing proportions of branched-chain fatty acids across multiple human studies. Gut Microbiome 3 (2022), 1–14, 10.1017/gmb.2022.1.
Laudisi, F., Di Fusco, D., Dinallo, V., Stolfi, C., Di Grazia, A., Marafini, I., Colantoni, A., Ortenzi, A., Alteri, C., Guerrieri, F., Mavilio, M., Ceccherini-Silberstein, F., Federici, M., MacDonald, T.T., Monteleone, I., Monteleone, G., The food additive maltodextrin promotes endoplasmic reticulum stress-driven mucus depletion and exacerbates intestinal inflammation. Cmgh 7:2 (2019), 457–473, 10.1016/j.jcmgh.2018.09.002.
Levine, A., Wine, E., Assa, A., Sigall Boneh, R., Shaoul, R., Kori, M., Cohen, S., Peleg, S., Shamaly, H., On, A., Millman, P., Abramas, L., Ziv-Baran, T., Grant, S., Abitbol, G., Dunn, K.A., Bielawski, J.P., Van Limbergen, J., Crohn's disease exclusion diet plus partial enteral nutrition induces sustained remission in a randomized controlled trial. Gastroenterology 157:2 (2019), 440–450.e8, 10.1053/j.gastro.2019.04.021.
Li, X., Liu, Y., Wang, Y., Li, X., Liu, X., Guo, M., Tan, Y., Qin, X., Wang, X., Jiang, M., Sucralose promotes colitis-associated colorectal cancer risk in a murine model along with changes in microbiota. Frontiers in Oncology 10:June (2020), 1–11, 10.3389/fonc.2020.00710.
Livak, K.J., Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:4 (2001), 402–408, 10.1006/meth.2001.1262.
Louis, P., Duncan, S.H., Sheridan, P.O., Walker, A.W., Flint, H.J., Microbial lactate utilisation and the stability of the gut microbiome. Gut Microbiome 3 (2022), 1–16, 10.1017/gmb.2022.3.
Louis, P., Flint, H.J., Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiology Letters 294:1 (2009), 1–8, 10.1111/j.1574-6968.2009.01514.x.
Louis, P., Flint, H.J., Formation of propionate and butyrate by the human colonic microbiota. Environmental Microbiology 19:1 (2017), 29–41, 10.1111/1462-2920.13589.
Ma, Y., Zhang, Y., Xiang, J., Xiang, S., Zhao, Y., Xiao, M., Du, F., Ji, H., Kaboli, P.J., Wu, X., Li, M., Wen, Q., Shen, J., Yang, Z., Li, J., Xiao, Z., Metagenome analysis of intestinal bacteria in healthy people, patients with inflammatory bowel disease and colorectal cancer. Frontiers in Cellular and Infection Microbiology 11:February (2021), 1–12, 10.3389/fcimb.2021.599734.
Mancabelli, L., Milani, C., Lugli, G.A., Turroni, F., Cocconi, D., van Sinderen, D., Ventura, M., Identification of universal gut microbial biomarkers of common human intestinal diseases by meta-analysis. FEMS Microbiology Ecology 93:12 (2017), 1–10, 10.1093/femsec/fix153.
Martin-Gallausiaux, C., Marinelli, L., Blottière, H. M., Larraufie, P., & Lapaque, N. (2021). Conference on diet and digestive disease symposium 2: Sensing and signalling of the gut environment: Scfa: Mechanisms and functional importance in the gut. Proceedings of the Nutrition Society, 80(1), 37–49. https://doi.org/10.1017/S0029665120006916.
Miclotte, L., De Paepe, K., Rymenans, L., Callewaert, C., Raes, J., Rajkovic, A., Van Camp, J., Van de Wiele, T., Dietary emulsifiers alter composition and activity of the human gut microbiota in vitro, irrespective of chemical or natural emulsifier origin. Frontiers in Microbiology, 11(November), 2020, 10.3389/fmicb.2020.577474.
Minnebo, Y., Delbaere, K., Goethals, V., Raes, J., Van de Wiele, T., De Paepe, K., Gut microbiota response to in vitro transit time variation is mediated by microbial growth rates, nutrient use efficiency and adaptation to in vivo transit time. Microbiome 11:1 (2023), 1–15, 10.1186/s40168-023-01691-y.
Modoux, M., Rolhion, N., Lefevre, J.H., Oeuvray, C., Nádvorník, P., Illes, P., Emond, P., Parc, Y., Mani, S., Dvorak, Z., Sokol, H., Butyrate acts through HDAC inhibition to enhance aryl hydrocarbon receptor activation by gut microbiota-derived ligands. Gut Microbes, 14(1), 2022, 10.1080/19490976.2022.2105637.
Monteleone, I., Zorzi, F., Marafini, I., Di Fusco, D., Dinallo, V., Caruso, R., Izzo, R., Franzè, E., Colantoni, A., Pallone, F., Monteleone, G., Aryl hydrocarbon receptor-driven signals inhibit collagen synthesis in the gut. European Journal of Immunology 46:4 (2016), 1047–1057, 10.1002/eji.201445228.
Mu, W., Wang, Y., Huang, C., Fu, Y., Li, J., Wang, H., Jia, X., Ba, Q., Effect of long-term intake of dietary titanium dioxide nanoparticles on intestine inflammation in mice. Journal of Agricultural and Food Chemistry 67:33 (2019), 9382–9389, 10.1021/acs.jafc.9b02391.
Müller, M., Hermes, G.D.A., Canfora, E.E., Smidt, H., Masclee, A.A.M., Zoetendal, E.X.G., Blaak, E.X.E., Distal colonic transit is linked to gut microbiota diversity and microbial fermentation in humans with slow colonic transit. American Journal of Physiology - Gastrointestinal and Liver Physiology 318:2 (2020), G361–G369, 10.1152/AJPGI.00283.2019.
Nagpal, R., Indugu, N., Singh, P., Distinct gut microbiota signatures in mice treated with commonly used food preservatives. Microorganisms, 9(11), 2021, 10.3390/microorganisms9112311.
Naimi, S., Viennois, E., Gewirtz, A.T., Chassaing, B., Direct impact of commonly used dietary emulsifiers on human gut microbiota. Microbiome 9:1 (2021), 1–19, 10.1186/s40168-020-00996-6.
Nomura, K., Ishikawa, D., Okahara, K., Ito, S., Haga, K., Takahashi, M., Arakawa, A., Shibuya, T., Osada, T., Kuwahara-Arai, K., Kirikae, T., Nagahara, A., Bacteroidetes species are correlated with disease activity in ulcerative colitis. Journal of Clinical Medicine, 10(8), 2021, 10.3390/jcm10081749.
Park, J. M., Kim, J., Lee, Y. J., Bae, S. U., & Lee, H. W. (2023). Inflammatory bowel disease – associated intestinal fibrosis. 60–66.
Peng, K., Short-chain fatty acids affect the development of in fl ammatory bowel disease through intestinal barrier, immunology, and microbiota. A promising therapy ? 37 (2022), 1710–1718, 10.1111/jgh.15970.
Pérez-Burillo, S., Molino, S., Navajas-Porras, B., Valverde-Moya, Á.J., Hinojosa-Nogueira, D., López-Maldonado, A., Pastoriza, S., Rufián-Henares, J.Á., An in vitro batch fermentation protocol for studying the contribution of food to gut microbiota composition and functionality. Nature Protocols 16:7 (2021), 3186–3209, 10.1038/s41596-021-00537-x.
Pernomian, L., Duarte-Silva, M., de Barros Cardoso, C.R., The Aryl Hydrocarbon Receptor (AHR) as a potential target for the control of intestinal inflammation: insights from an immune and bacteria sensor receptor. Clinical Reviews in Allergy and Immunology 59:3 (2020), 382–390, 10.1007/s12016-020-08789-3.
Pinget, G., Tan, J., Janac, B., Kaakoush, N.O., Angelatos, A.S., O'Sullivan, J., Koay, Y.C., Sierro, F., Davis, J., Divakarla, S.K., Khanal, D., Moore, R.J., Stanley, D., Chrzanowski, W., Macia, L., Impact of the food additive titanium dioxide (e171) on gut microbiota-host interaction. Frontiers. Nutrition, 6(May), 2019, 10.3389/fnut.2019.00057.
Pisani, A., Rausch, P., Bang, C., Ellul, S., Tabone, T., Cordina, M., Zahra, G., Dysbiosis in the gut microbiota in patients with in fl ammatory. Microbiology Spectrum, 10(3), 2022.
Procházková, N., Falony, G., Dragsted, L.O., Licht, T.R., Raes, J., Roager, H.M., Advancing human gut microbiota research by considering gut transit time. Gut 72:1 (2023), 180–191, 10.1136/gutjnl-2022-328166.
Rannug, A., How the AHR became important in intestinal homeostasis—A diurnal FICZ/AHR/CYP1A1 feedback controls both immunity and immunopathology. International Journal of Molecular Sciences 21:16 (2020), 1–19, 10.3390/ijms21165681.
Raoul, P., Cintoni, M., Palombaro, M., Basso, L., Rinninella, E., Gasbarrini, A., Mele, M.C., Food additives, a key environmental factor in the development of IBD through gut dysbiosis. Microorganisms, 10(1), 2022, 167, 10.3390/microorganisms10010167.
Rios-Covian, D., González, S., Nogacka, A.M., Arboleya, S., Salazar, N., Gueimonde, M., de los Reyes-Gavilán, C.G., An Overview on fecal branched short-chain fatty acids along human life and as related with body mass index: associated dietary and anthropometric factors. Frontiers in Microbiology 11:May (2020), 1–9, 10.3389/fmicb.2020.00973.
Rodriguez-Palacios, A., Harding, A., Menghini, P., Himmelman, C., Retuerto, M., Nickerson, K.P., Lam, M., Croniger, C.M., McLean, M.H., Durum, S.K., Pizarro, T.T., Ghannoum, M.A., Ilic, S., McDonald, C., Cominelli, F., The Artificial sweetener splenda promotes gut proteobacteria, dysbiosis, and myeloperoxidase reactivity in crohn's disease-like ileitis. Inflammatory Bowel Diseases 24:5 (2018), 1005–1020, 10.1093/ibd/izy060.
Rognes, T., Flouri, T., Nichols, B., Quince, C., Mahé, F., VSEARCH: A versatile open source tool for metagenomics. PeerJ 2016:10 (2016), 1–22, 10.7717/peerj.2584.
Rousta, E., Oka, A., Liu, B., Herzog, J., Bhatt, A.P., Wang, J., Habibi Najafi, M.B., Sartor, R.B., The emulsifier carboxymethylcellulose induces more aggressive colitis in humanized mice with inflammatory bowel disease microbiota than polysorbate-80. Nutrients, 13(10), 2021, 10.3390/nu13103565.
Růžičková, M., Vítězová, M., Kushkevych, I., The characterization of Enterococcus genus: Resistance mechanisms and inflammatory bowel disease. Open Medicine (Poland) 15:1 (2020), 211–224, 10.1515/med-2020-0032.
Sezgin, E., Terlemez, G., Bozkurt, B., Bengi, G., Akpinar, H., Büyüktorun, İ., Quantitative real-time PCR analysis of bacterial biomarkers enable fast and accurate monitoring in inflammatory bowel disease. PeerJ 10:Cd (2022), 1–20, 10.7717/peerj.14217.
Singh, V., Lee, G.D., Son, H.W., Koh, H., Kim, E.S., Unno, T., Shin, J.H., Butyrate producers, “The Sentinel of Gut”: Their intestinal significance with and beyond butyrate, and prospective use as microbial therapeutics. Frontiers in Microbiology, 13(January), 2023, 10.3389/fmicb.2022.1103836.
Srour, B., Kordahi, M.C., Bonazzi, E., Deschasaux-Tanguy, M., Touvier, M., Chassaing, B., Ultra-processed foods and human health: From epidemiological evidence to mechanistic insights. The Lancet Gastroenterology & Hepatology 7:12 (2022), 1128–1140, 10.1016/S2468-1253(22)00169-8.
Tang, Y., Liu, H., Song, G., Wu, T., Zhao, Y., Shi, L., A case–control study on the association of intestinal flora with ulcerative colitis. AMB Express, 11(1), 2021, 10.1186/s13568-021-01267-9.
Tottey, W., Feria-Gervasio, D., Gaci, N., Laillet, B., Pujos, E., Martin, J.F., Sebedio, J.L., Sion, B., Jarrige, J.F., Alric, M., Brugère, J.F., Colonic transit time is a driven force of the gut microbiota composition and metabolism: In vitro evidence. Journal of Neurogastroenterology and Motility 23:1 (2017), 124–134, 10.5056/jnm16042.
Trakman, G.L., Lin, W.Y.Y., Hamilton, A.L., Wilson-O'Brien, A.L., Stanley, A., Ching, J.Y., Yu, J., Mak, J.W.Y., Sun, Y., Niu, J., Miao, Y., Lin, X., Feng, R., Chen, M., Shivappa, N., Hebert, J.R., Morrison, M., Ng, S.C., Kamm, M.A., Processed food as a risk factor for the development and perpetuation of crohn's disease—The ENIGMA Study. Nutrients 14:17 (2022), 1–23, 10.3390/nu14173627.
Van Den Abbeele, P., Belzer, C., Goossens, M., Kleerebezem, M., De Vos, W.M., Thas, O., De Weirdt, R., Kerckhof, F.M., Van De Wiele, T., Butyrate-producing Clostridium cluster XIVa species specifically colonize mucins in an in vitro gut model. ISME Journal 7:5 (2013), 949–961, 10.1038/ismej.2012.158.
Vieira-Silva, S., Sabino, J., Valles-Colomer, M., Falony, G., Kathagen, G., Caenepeel, C., Cleynen, I., van der Merwe, S., Vermeire, S., Raes, J., Quantitative microbiome profiling disentangles inflammation- and bile duct obstruction-associated microbiota alterations across PSC/IBD diagnoses. Nature Microbiology 4:11 (2019), 1826–1831, 10.1038/s41564-019-0483-9.
Viennois, E., Bretin, A., Dubé, P.E., Maue, A.C., Dauriat, C.J.G., Barnich, N., Gewirtz, A.T., Chassaing, B., Dietary emulsifiers directly impact adherent-invasive E. coli Gene Expression to Drive Chronic Intestinal Inflammation. Cell Reports, 33(1), 2020, 10.1016/j.celrep.2020.108229.
Viennois, E., Merlin, D., Gewirtz, A.T., Chassaing, B., Dietary emulsifier-induced low-grade inflammation promotes colon carcinogenesis. Cancer Research 77:1 (2017), 27–40, 10.1158/0008-5472.CAN-16-1359.
Watanabe, D., Kamada, N., Contribution of the Gut Microbiota to Intestinal Fibrosis in Crohn's Disease. Frontiers in Medicine 9:February (2022), 1–14, 10.3389/fmed.2022.826240.
Xu, J., Wang, M., Liu, Q., Lin, X., Pu, K., He, Z., Gut microbiota mediated the toxicity of high concentration of dietary nitrite in C57BL/6 mice. Ecotoxicology and Environmental Safety, 231, 2022, 113224, 10.1016/j.ecoenv.2022.113224.
Yu, L.C.H., Microbiota dysbiosis and barrier dysfunction in inflammatory bowel disease: RSM Library Discovery Service. Journal of Biomedical Science, 25, 2018, 79 http://eds.b.ebscohost.com.rsm.idm.oclc.org/eds/pdfviewer/pdfviewer?vid=3&sid=252c8051-fd47-4814-9346-03da140f394a%40pdc-v-sessmgr05.
Zafar, H., Saier, M.H., Gut Bacteroides species in health and disease. Gut Microbes 13:1 (2021), 1–20, 10.1080/19490976.2020.1848158.
Zhan, S., Li, N., Liu, C., Mao, R., Wu, D., Li, T., Chen, M., Zhuang, X., Zeng, Z., Intestinal Fibrosis and gut microbiota: clues from other organs. Frontiers in Microbiology 12:July (2021), 1–10, 10.3389/fmicb.2021.694967.
Zhang, Y.Z., Li, Y.Y., Inflammatory bowel disease: Pathogenesis. World Journal of Gastroenterology 20:1 (2014), 91–99, 10.3748/wjg.v20.i1.91.
Zhang, Z., Zhang, H., Chen, T., Shi, L., Wang, D., Tang, D., Regulatory role of short-chain fatty acids in inflammatory bowel disease. Cell Communication and Signaling 20:1 (2022), 1–10, 10.1186/s12964-022-00869-5.
Zhou, Y., Zhi, F., Lower level of bacteroides in the gut microbiota is associated with inflammatory bowel disease: a meta-analysis. BioMed Research International 2016 (2016), 1–9, 10.1155/2016/5828959.
Zhu, S., Han, M., Liu, S., Fan, L., Shi, H., Li, P., Composition and diverse differences of intestinal microbiota in ulcerative colitis patients. Frontiers in Cellular and Infection Microbiology 12:August (2022), 1–13, 10.3389/fcimb.2022.953962.
