Exploring the Gut Microbiome’s Role in Inflammatory Bowel Disease: Insights and Interventions
Abstract
:1. Introduction
2. Materials and Methods
3. Role of the Gut Microbiome
3.1. Metabolism of Nutritional Components
3.2. Metabolism of Xenobiotics and Drugs
3.3. Antimicrobial Protection
3.4. Gut Barrier’s Integrity
4. The Gut Microbiome in IBD
4.1. Bacterial Dysbiosis
4.2. Fungal Dysbiosis
4.3. Viral Dysbiosis
4.4. Archaeal Dysbiosis
4.5. Metabolic Disparities
5. Diagnostic Approaches to IBD
6. Current Treatment
6.1. Crohn’s Disease
6.2. Ulcerative Colitis
6.3. Limitations
7. Microbiome-Targeted Therapies
7.1. Probiotics, Prebiotics, Symbiotics, Postbiotics
7.1.1. Crohn’s Disease
7.1.2. Ulcerative Colitis
7.2. Faecal Microbiota Transplantation
8. Discussion
8.1. Efficacy and Safety of Microbiome-Targeted Therapies
8.2. Controversies about the Optimal Use of FMT
9. Conclusions and Future Considerations
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Wehkamp, J.; Götz, M.; Herrlinger, K.; Steurer, W.; Stange, E.F. Inflammatory Bowel Disease. Dtsch. Ärztebl. Int. 2016, 113, 72–82. [Google Scholar] [CrossRef]
- Marotto, D.; Atzeni, F.; Ardizzone, S.; Monteleone, G.; Giorgi, V.; Sarzi-Puttini, P. Extra-Intestinal Manifestations of Inflammatory Bowel Diseases. Pharmacol. Res. 2020, 161, 105206. [Google Scholar] [CrossRef] [PubMed]
- Rogler, G.; Singh, A.; Kavanaugh, A.; Rubin, D.T. Extraintestinal Manifestations of Inflammatory Bowel Disease: Current Concepts, Treatment, and Implications for Disease Management. Gastroenterology 2021, 161, 1118–1132. [Google Scholar] [CrossRef]
- Jairath, V.; Feagan, B.G. Global Burden of Inflammatory Bowel Disease. Lancet Gastroenterol. Hepatol. 2020, 5, 2–3. [Google Scholar] [CrossRef]
- Guan, Q. A Comprehensive Review and Update on the Pathogenesis of Inflammatory Bowel Disease. J. Immunol. Res. 2019, 2019, e7247238. [Google Scholar] [CrossRef] [PubMed]
- Jones, J.L.; Nguyen, G.C.; Benchimol, E.I.; Bernstein, C.N.; Bitton, A.; Kaplan, G.G.; Murthy, S.K.; Lee, K.; Cooke-Lauder, J.; Otley, A.R. The Impact of Inflammatory Bowel Disease in Canada 2018: Quality of Life. J. Can. Assoc. Gastroenterol. 2019, 2, S42–S48. [Google Scholar] [CrossRef] [PubMed]
- Stojanov, S.; Berlec, A.; Štrukelj, B. The Influence of Probiotics on the Firmicutes/Bacteroidetes Ratio in the Treatment of Obesity and Inflammatory Bowel Disease. Microorganisms 2020, 8, 1715. [Google Scholar] [CrossRef]
- Vos, W.M.d; Tilg, H.; Hul, M.V.; Cani, P.D. Gut Microbiome and Health: Mechanistic Insights. Gut 2022, 71, 1020–1032. [Google Scholar] [CrossRef]
- Rinninella, E.; Raoul, P.; Cintoni, M.; Franceschi, F.; Miggiano, G.A.D.; Gasbarrini, A.; Mele, M.C. What Is the Healthy Gut Microbiota Composition? A Changing Ecosystem across Age, Environment, Diet, and Diseases. Microorganisms 2019, 7, 14. [Google Scholar] [CrossRef]
- Sender, R.; Fuchs, S.; Milo, R. Are We Really Vastly Outnumbered? Revisiting the Ratio of Bacterial to Host Cells in Humans. Cell 2016, 164, 337–340. [Google Scholar] [CrossRef]
- Andoh, A.; Nishida, A. Alteration of the Gut Microbiome in Inflammatory Bowel Disease. Digestion 2022, 104, 16–23. [Google Scholar] [CrossRef] [PubMed]
- Jandhyala, S.M.; Talukdar, R.; Subramanyam, C.; Vuyyuru, H.; Sasikala, M.; Reddy, D.N. Role of the Normal Gut Microbiota. World J. Gastroenterol. WJG 2015, 21, 8787–8803. [Google Scholar] [CrossRef] [PubMed]
- Rastelli, M.; Cani, P.D.; Knauf, C. The Gut Microbiome Influences Host Endocrine Functions. Endocr. Rev. 2019, 40, 1271–1284. [Google Scholar] [CrossRef] [PubMed]
- Nicholson, J.K.; Holmes, E.; Kinross, J.; Burcelin, R.; Gibson, G.; Jia, W.; Pettersson, S. Host-Gut Microbiota Metabolic Interactions. Science 2012, 336, 1262–1267. [Google Scholar] [CrossRef] [PubMed]
- Thursby, E.; Juge, N. Introduction to the Human Gut Microbiota. Biochem. J. 2017, 474, 1823–1836. [Google Scholar] [CrossRef] [PubMed]
- Catalkaya, G.; Venema, K.; Lucini, L.; Rocchetti, G.; Delmas, D.; Daglia, M.; De Filippis, A.; Xiao, H.; Quiles, J.L.; Xiao, J.; et al. Interaction of Dietary Polyphenols and Gut Microbiota: Microbial Metabolism of Polyphenols, Influence on the Gut Microbiota, and Implications on Host Health. Food Front. 2020, 1, 109–133. [Google Scholar] [CrossRef]
- Koppel, N.; Maini Rekdal, V.; Balskus, E.P. Chemical Transformation of Xenobiotics by the Human Gut Microbiota. Science 2017, 356, eaag2770. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; Wang, Y.; Antony, V.; Sun, H.; Liang, G. Metabolism-Associated Molecular Patterns (MAMPs). Trends Endocrinol. Metab. 2020, 31, 712–724. [Google Scholar] [CrossRef] [PubMed]
- Hasan, N.; Yang, H. Factors Affecting the Composition of the Gut Microbiota, and Its Modulation. PeerJ 2019, 7, e7502. [Google Scholar] [CrossRef] [PubMed]
- Yanagibashi, T.; Hosono, A.; Oyama, A.; Tsuda, M.; Suzuki, A.; Hachimura, S.; Takahashi, Y.; Momose, Y.; Itoh, K.; Hirayama, K.; et al. IgA Production in the Large Intestine Is Modulated by a Different Mechanism than in the Small Intestine: Bacteroides Acidifaciens Promotes IgA Production in the Large Intestine by Inducing Germinal Center Formation and Increasing the Number of IgA+ B Cells. Immunobiology 2013, 218, 645–651. [Google Scholar] [CrossRef]
- Herich, R.; Levkut, M. Lactic Acid Bacteria, Probiotics and Immune System. Veterinární Medicína 2002, 47, 169–180. [Google Scholar] [CrossRef]
- Schoultz, I.; Keita, Å.V. The Intestinal Barrier and Current Techniques for the Assessment of Gut Permeability. Cells 2020, 9, 1909. [Google Scholar] [CrossRef] [PubMed]
- Deng, H.; Yang, S.; Zhang, Y.; Qian, K.; Zhang, Z.; Liu, Y.; Wang, Y.; Bai, Y.; Fan, H.; Zhao, X.; et al. Bacteroides Fragilis Prevents Clostridium Difficile Infection in a Mouse Model by Restoring Gut Barrier and Microbiome Regulation. Front. Microbiol. 2018, 9, 2976. [Google Scholar] [CrossRef] [PubMed]
- Zhang, W.; Zhu, B.; Xu, J.; Liu, Y.; Qiu, E.; Li, Z.; Li, Z.; He, Y.; Zhou, H.; Bai, Y.; et al. Bacteroides Fragilis Protects Against Antibiotic-Associated Diarrhea in Rats by Modulating Intestinal Defenses. Front. Immunol. 2018, 9, 1040. [Google Scholar] [CrossRef] [PubMed]
- Wrzosek, L.; Miquel, S.; Noordine, M.-L.; Bouet, S.; Chevalier-Curt, M.J.; Robert, V.; Philippe, C.; Bridonneau, C.; Cherbuy, C.; Robbe-Masselot, C.; et al. Bacteroides Thetaiotaomicron and Faecalibacterium Prausnitziiinfluence the Production of Mucus Glycans and the Development of Goblet Cells in the Colonic Epithelium of a Gnotobiotic Model Rodent. BMC Biol. 2013, 11, 61. [Google Scholar] [CrossRef] [PubMed]
- Srutkova, D.; Schwarzer, M.; Hudcovic, T.; Zakostelska, Z.; Drab, V.; Spanova, A.; Rittich, B.; Kozakova, H.; Schabussova, I. Bifidobacterium Longum CCM 7952 Promotes Epithelial Barrier Function and Prevents Acute DSS-Induced Colitis in Strictly Strain-Specific Manner. PLoS ONE 2015, 10, e0134050. [Google Scholar] [CrossRef] [PubMed]
- Hiippala, K.; Jouhten, H.; Ronkainen, A.; Hartikainen, A.; Kainulainen, V.; Jalanka, J.; Satokari, R. The Potential of Gut Commensals in Reinforcing Intestinal Barrier Function and Alleviating Inflammation. Nutrients 2018, 10, 988. [Google Scholar] [CrossRef] [PubMed]
- Sartor, R.B.; Wu, G.D. Roles for Intestinal Bacteria, Viruses, and Fungi in Pathogenesis of Inflammatory Bowel Diseases and Therapeutic Approaches. Gastroenterology 2017, 152, 327–339.e4. [Google Scholar] [CrossRef] [PubMed]
- Brüssow, H. Problems with the Concept of Gut Microbiota Dysbiosis. Microb. Biotechnol. 2020, 13, 423–434. [Google Scholar] [CrossRef]
- Santana, P.T.; Rosas, S.L.B.; Ribeiro, B.E.; Marinho, Y.; de Souza, H.S.P. Dysbiosis in Inflammatory Bowel Disease: Pathogenic Role and Potential Therapeutic Targets. Int. J. Mol. Sci. 2022, 23, 3464. [Google Scholar] [CrossRef]
- Aldars-García, L.; Chaparro, M.; Gisbert, J.P. Systematic Review: The Gut Microbiome and Its Potential Clinical Application in Inflammatory Bowel Disease. Microorganisms 2021, 9, 977. [Google Scholar] [CrossRef] [PubMed]
- Morgan, X.C.; Tickle, T.L.; Sokol, H.; Gevers, D.; Devaney, K.L.; Ward, D.V.; Reyes, J.A.; Shah, S.A.; LeLeiko, N.; Snapper, S.B.; et al. Dysfunction of the Intestinal Microbiome in Inflammatory Bowel Disease and Treatment. Genome Biol. 2012, 13, R79. [Google Scholar] [CrossRef] [PubMed]
- Zhou, Y.; Zhi, F. Lower Level of Bacteroides in the Gut Microbiota Is Associated with Inflammatory Bowel Disease: A Meta-Analysis. BioMed Res. Int. 2016, 2016, 5828959. [Google Scholar] [CrossRef] [PubMed]
- Nishida, A.; Inoue, R.; Inatomi, O.; Bamba, S.; Naito, Y.; Andoh, A. Gut Microbiota in the Pathogenesis of Inflammatory Bowel Disease. Clin. J. Gastroenterol. 2018, 11, 1–10. [Google Scholar] [CrossRef] [PubMed]
- Sankarasubramanian, J.; Ahmad, R.; Avuthu, N.; Singh, A.B.; Guda, C. Gut Microbiota and Metabolic Specificity in Ulcerative Colitis and Crohn’s Disease. Front. Med. 2020, 7, 606298. [Google Scholar] [CrossRef] [PubMed]
- Wright, E.K.; Kamm, M.A.; Teo, S.M.; Inouye, M.; Wagner, J.; Kirkwood, C.D. Recent Advances in Characterizing the Gastrointestinal Microbiome in Crohn’s Disease: A Systematic Review. Inflamm. Bowel Dis. 2015, 21, 1219–1228. [Google Scholar] [CrossRef]
- Gevers, D.; Kugathasan, S.; Denson, L.A.; Vázquez-Baeza, Y.; Van Treuren, W.; Ren, B.; Schwager, E.; Knights, D.; Song, S.J.; Yassour, M.; et al. The Treatment-Naïve Microbiome in New-Onset Crohn’s Disease. Cell Host Microbe 2014, 15, 382–392. [Google Scholar] [CrossRef] [PubMed]
- Prosberg, M.; Bendtsen, F.; Vind, I.; Petersen, A.M.; Gluud, L.L. The Association between the Gut Microbiota and the Inflammatory Bowel Disease Activity: A Systematic Review and Meta-Analysis. Scand. J. Gastroenterol. 2016, 51, 1407–1415. [Google Scholar] [CrossRef]
- Liguori, G.; Lamas, B.; Richard, M.L.; Brandi, G.; da Costa, G.; Hoffmann, T.W.; Di Simone, M.P.; Calabrese, C.; Poggioli, G.; Langella, P.; et al. Fungal Dysbiosis in Mucosa-Associated Microbiota of Crohn’s Disease Patients. J. Crohns Colitis 2016, 10, 296–305. [Google Scholar] [CrossRef]
- Sokol, H.; Leducq, V.; Aschard, H.; Pham, H.-P.; Jegou, S.; Landman, C.; Cohen, D.; Liguori, G.; Bourrier, A.; Nion-Larmurier, I.; et al. Fungal Microbiota Dysbiosis in IBD. Gut 2017, 66, 1039–1048. [Google Scholar] [CrossRef]
- Wang, W.; Jovel, J.; Halloran, B.; Wine, E.; Patterson, J.; Ford, G.; O’Keefe, S.; Meng, B.; Song, D.; Zhang, Y.; et al. Metagenomic Analysis of Microbiome in Colon Tissue from Subjects with Inflammatory Bowel Diseases Reveals Interplay of Viruses and Bacteria. Inflamm. Bowel Dis. 2015, 21, 1419–1427. [Google Scholar] [CrossRef] [PubMed]
- Dridi, B.; Raoult, D.; Drancourt, M. Archaea as Emerging Organisms in Complex Human Microbiomes. Anaerobe 2011, 17, 56–63. [Google Scholar] [CrossRef] [PubMed]
- Proctor, L.M.; Creasy, H.H.; Fettweis, J.M.; Lloyd-Price, J.; Mahurkar, A.; Zhou, W.; Buck, G.A.; Snyder, M.P.; Strauss, J.F.; Weinstock, G.M.; et al. The Integrative Human Microbiome Project. Nature 2019, 569, 641–648. [Google Scholar] [CrossRef]
- Blaak, E.E.; Canfora, E.E.; Theis, S.; Frost, G.; Groen, A.K.; Mithieux, G.; Nauta, A.; Scott, K.; Stahl, B.; van Harsselaar, J.; et al. Short Chain Fatty Acids in Human Gut and Metabolic Health. Benef. Microbes 2020, 11, 411–455. [Google Scholar] [CrossRef]
- Ríos-Covián, D.; Ruas-Madiedo, P.; Margolles, A.; Gueimonde, M.; de los Reyes-Gavilán, C.G.; Salazar, N. Intestinal Short Chain Fatty Acids and Their Link with Diet and Human Health. Front. Microbiol. 2016, 7, 185. [Google Scholar] [CrossRef] [PubMed]
- Bourgonje, A.R.; Feelisch, M.; Faber, K.N.; Pasch, A.; Dijkstra, G.; Goor, H. van Oxidative Stress and Redox-Modulating Therapeutics in Inflammatory Bowel Disease. Trends Mol. Med. 2020, 26, 1034–1046. [Google Scholar] [CrossRef]
- Ricciuto, A.; Griffiths, A.M. Clinical Value of Fecal Calprotectin. Crit. Rev. Clin. Lab. Sci. 2019, 56, 307–320. [Google Scholar] [CrossRef]
- Maaser, C.; Sturm, A.; Vavricka, S.R.; Kucharzik, T.; Fiorino, G.; Annese, V.; Calabrese, E.; Baumgart, D.C.; Bettenworth, D.; Borralho Nunes, P.; et al. ECCO-ESGAR Guideline for Diagnostic Assessment in IBD Part 1: Initial Diagnosis, Monitoring of Known IBD, Detection of Complications. J. Crohns Colitis 2019, 13, 144–164K. [Google Scholar] [CrossRef]
- Manandhar, I.; Alimadadi, A.; Aryal, S.; Munroe, P.B.; Joe, B.; Cheng, X. Gut Microbiome-Based Supervised Machine Learning for Clinical Diagnosis of Inflammatory Bowel Diseases. Am. J. Physiol.-Gastrointest. Liver Physiol. 2021, 320, G328–G337. [Google Scholar] [CrossRef]
- Zhou, Y.; Xu, Z.Z.; He, Y.; Yang, Y.; Liu, L.; Lin, Q.; Nie, Y.; Li, M.; Zhi, F.; Liu, S.; et al. Gut Microbiota Offers Universal Biomarkers across Ethnicity in Inflammatory Bowel Disease Diagnosis and Infliximab Response Prediction. mSystems 2018, 3. [Google Scholar] [CrossRef]
- Henry, C.; Bassignani, A.; Berland, M.; Langella, O.; Sokol, H.; Juste, C. Modern Metaproteomics: A Unique Tool to Characterize the Active Microbiome in Health and Diseases, and Pave the Road towards New Biomarkers-Example of Crohn’s Disease and Ulcerative Colitis Flare-Ups. Cells 2022, 11, 1340. [Google Scholar] [CrossRef] [PubMed]
- Sairenji, T.; Collins, K.L.; Evans, D.V. An Update on Inflammatory Bowel Disease. Prim. Care Clin. Off. Pract. 2017, 44, 673–692. [Google Scholar] [CrossRef] [PubMed]
- Dorrington, A.M.; Selinger, C.P.; Parkes, G.C.; Smith, M.; Pollok, R.C.; Raine, T. The Historical Role and Contemporary Use of Corticosteroids in Inflammatory Bowel Disease. J. Crohns Colitis 2020, 14, 1316–1329. [Google Scholar] [CrossRef]
- Lichtenstein, G.R.; Loftus, E.V.; Isaacs, K.L.; Regueiro, M.D.; Gerson, L.B.; Sands, B.E. ACG Clinical Guideline: Management of Crohn’s Disease in Adults. Off. J. Am. Coll. Gastroenterol. ACG 2018, 113, 481. [Google Scholar] [CrossRef] [PubMed]
- Feagan, B.G.; Sandborn, W.J.; Gasink, C.; Jacobstein, D.; Lang, Y.; Friedman, J.R.; Blank, M.A.; Johanns, J.; Gao, L.-L.; Miao, Y.; et al. Ustekinumab as Induction and Maintenance Therapy for Crohn’s Disease. N. Engl. J. Med. 2016, 375, 1946–1960. [Google Scholar] [CrossRef]
- Bemelman, W.A.; Warusavitarne, J.; Sampietro, G.M.; Serclova, Z.; Zmora, O.; Luglio, G.; De Buck Van Overstraeten, A.; Burke, J.P.; Buskens, C.J.; Francesco, C.; et al. ECCO-ESCP Consensus on Surgery for Crohn’s Disease. J. Crohns Colitis 2017, 12, 1–16. [Google Scholar] [CrossRef]
- Ko, C.W.; Singh, S.; Feuerstein, J.D.; Falck-Ytter, C.; Falck-Ytter, Y.; Cross, R.K.; Crockett, S.; Falck-Ytter, Y.; Feuerstein, J.; Flamm, S.; et al. AGA Clinical Practice Guidelines on the Management of Mild-to-Moderate Ulcerative Colitis. Gastroenterology 2019, 156, 748–764. [Google Scholar] [CrossRef]
- Kucharzik, T.; Koletzko, S.; Kannengiesser, K.; Dignass, A. Ulcerative Colitis—Diagnostic and Therapeutic Algorithms. Dtsch. Ärztebl. Int. 2020, 117, 564–574. [Google Scholar] [CrossRef]
- Padda, I.S.; Bhatt, R.; Parmar, M. Golimumab. In StatPearls; StatPearls Publishing: Treasure Island, FL, USA, 2023. [Google Scholar]
- Zhou, Z.; Dai, C.; Liu, W.-X. Anti-TNF-A Therapy about Infliximab and Adalimamab for the Effectiveness in Ulcerative Colitis Compared with Conventional Therapy: A Meta-Analysis. Hepatogastroenterology 2015, 62, 309–318. [Google Scholar]
- Burri, E.; Maillard, M.H.; Schoepfer, A.M.; Seibold, F.; Van Assche, G.; Rivière, P.; Laharie, D.; Manz, M.; on behalf of the Swiss IBDnet, an official working group of the Swiss Society of Gastroenterology. Treatment Algorithm for Mild and Moderate-to-Severe Ulcerative Colitis: An Update. Digestion 2020, 101, 2–15. [Google Scholar] [CrossRef]
- Raine, T.; Bonovas, S.; Burisch, J.; Kucharzik, T.; Adamina, M.; Annese, V.; Bachmann, O.; Bettenworth, D.; Chaparro, M.; Czuber-Dochan, W.; et al. ECCO Guidelines on Therapeutics in Ulcerative Colitis: Medical Treatment. J. Crohns Colitis 2022, 16, 2–17. [Google Scholar] [CrossRef]
- Magro, F.; Cordeiro, G.; Dias, A.M.; Estevinho, M.M. Inflammatory Bowel Disease—Non-Biological Treatment. Pharmacol. Res. 2020, 160, 105075. [Google Scholar] [CrossRef] [PubMed]
- Katsanos, K.H.; Papamichael, K.; Feuerstein, J.D.; Christodoulou, D.K.; Cheifetz, A.S. Biological Therapies in Inflammatory Bowel Disease: Beyond Anti-TNF Therapies. Clin. Immunol. 2019, 206, 9–14. [Google Scholar] [CrossRef] [PubMed]
- Khan, I.; Ullah, N.; Zha, L.; Bai, Y.; Khan, A.; Zhao, T.; Che, T.; Zhang, C. Alteration of Gut Microbiota in Inflammatory Bowel Disease (IBD): Cause or Consequence? IBD Treatment Targeting the Gut Microbiome. Pathogens 2019, 8, 126. [Google Scholar] [CrossRef] [PubMed]
- Stavropoulou, E.; Bezirtzoglou, E. Probiotics in Medicine: A Long Debate. Front. Immunol. 2020, 11, 2192. [Google Scholar] [CrossRef] [PubMed]
- Underwood, M.A. Probiotics and the Prevention of Necrotizing Enterocolitis. J. Pediatr. Surg. 2019, 54, 405–412. [Google Scholar] [CrossRef] [PubMed]
- Goodman, C.; Keating, G.; Georgousopoulou, E.; Hespe, C.; Levett, K. Probiotics for the Prevention of Antibiotic-Associated Diarrhoea: A Systematic Review and Meta-Analysis. BMJ Open 2021, 11, e043054. [Google Scholar] [CrossRef] [PubMed]
- Jakubczyk, D.; Leszczyńska, K.; Górska, S. The Effectiveness of Probiotics in the Treatment of Inflammatory Bowel Disease (IBD)—A Critical Review. Nutrients 2020, 12, 1973. [Google Scholar] [CrossRef] [PubMed]
- Davani-Davari, D.; Negahdaripour, M.; Karimzadeh, I.; Seifan, M.; Mohkam, M.; Masoumi, S.J.; Berenjian, A.; Ghasemi, Y. Prebiotics: Definition, Types, Sources, Mechanisms, and Clinical Applications. Foods 2019, 8, 92. [Google Scholar] [CrossRef]
- Roy, S.; Dhaneshwar, S. Role of Prebiotics, Probiotics, and Synbiotics in Management of Inflammatory Bowel Disease: Current Perspectives. World J. Gastroenterol. 2023, 29, 2078–2100. [Google Scholar] [CrossRef]
- Aguilar-Toalá, J.E.; Garcia-Varela, R.; Garcia, H.S.; Mata-Haro, V.; González-Córdova, A.F.; Vallejo-Cordoba, B.; Hernández-Mendoza, A. Postbiotics: An Evolving Term within the Functional Foods Field. Trends Food Sci. Technol. 2018, 75, 105–114. [Google Scholar] [CrossRef]
- Martyniak, A.; Medyńska-Przęczek, A.; Wędrychowicz, A.; Skoczeń, S.; Tomasik, P.J. Prebiotics, Probiotics, Synbiotics, Paraprobiotics and Postbiotic Compounds in IBD. Biomolecules 2021, 11, 1903. [Google Scholar] [CrossRef] [PubMed]
- Bousvaros, A.; Guandalini, S.; Baldassano, R.N.; Botelho, C.; Evans, J.; Ferry, G.D.; Goldin, B.; Hartigan, L.; Kugathasan, S.; Levy, J.; et al. A Randomized, Double-Blind Trial of Lactobacillus GG versus Placebo in Addition to Standard Maintenance Therapy for Children with Crohn’s Disease. Inflamm. Bowel Dis. 2005, 11, 833–839. [Google Scholar] [CrossRef] [PubMed]
- Marteau, P.; Lémann, M.; Seksik, P.; Laharie, D.; Colombel, J.F.; Bouhnik, Y.; Cadiot, G.; Soulé, J.C.; Bourreille, A.; Metman, E.; et al. Ineffectiveness of Lactobacillus Johnsonii LA1 for Prophylaxis of Postoperative Recurrence in Crohn’s Disease: A Randomised, Double Blind, Placebo Controlled GETAID Trial. Gut 2006, 55, 842. [Google Scholar] [CrossRef]
- Fujimori, S.; Tatsuguchi, A.; Gudis, K.; Kishida, T.; Mitsui, K.; Ehara, A.; Kobayashi, T.; Sekita, Y.; Seo, T.; Sakamoto, C. High Dose Probiotic and Prebiotic Cotherapy for Remission Induction of Active Crohn’s Disease. J. Gastroenterol. Hepatol. 2007, 22, 1199–1204. [Google Scholar] [CrossRef]
- Steed, H.; Macfarlane, G.T.; Blackett, K.L.; Bahrami, B.; Reynolds, N.; Walsh, S.V.; Cummings, J.H.; Macfarlane, S. Clinical Trial: The Microbiological and Immunological Effects of Synbiotic Consumption—A Randomized Double-Blind Placebo-Controlled Study in Active Crohn’s Disease. Aliment. Pharmacol. Ther. 2010, 32, 872–883. [Google Scholar] [CrossRef] [PubMed]
- Cui, Y.; Qi, S.; Zhang, W.; Mao, J.; Tang, R.; Wang, C.; Liu, J.; Luo, X.M.; Wang, H. Lactobacillus Reuteri ZJ617 Culture Supernatant Attenuates Acute Liver Injury Induced in Mice by Lipopolysaccharide. J. Nutr. 2019, 149, 2046–2055. [Google Scholar] [CrossRef]
- Anderson, R.C. Are Postbiotics the Long Sought-After Solution for a Leaky Gut? J. Nutr. 2019, 149, 1873–1874. [Google Scholar] [CrossRef]
- Ishikawa, H.; Akedo, I.; Umesaki, Y.; Tanaka, R.; Imaoka, A.; Otani, T. Randomized Controlled Trial of the Effect of Bifidobacteria-Fermented Milk on Ulcerative Colitis. J. Am. Coll. Nutr. 2003, 22, 56–63. [Google Scholar] [CrossRef]
- Cui, H.-H.; Chen, C.-L.; Wang, J.-D.; Yang, Y.-J.; Cun, Y.; Wu, J.-B.; Liu, Y.-H.; Dan, H.-L.; Jian, Y.-T.; Chen, X.-Q. Effects of Probiotic on Intestinal Mucosa of Patients with Ulcerative Colitis. World J. Gastroenterol. 2004, 10, 1521–1525. [Google Scholar] [CrossRef]
- Furrie, E.; Macfarlane, S.; Kennedy, A.; Cummings, J.H.; Walsh, S.V.; O’Neil, D.A.; Macfarlane, G.T. Synbiotic Therapy (Bifidobacterium Longum/Synergy 1) Initiates Resolution of Inflammation in Patients with Active Ulcerative Colitis: A Randomised Controlled Pilot Trial. Gut 2005, 54, 242–249. [Google Scholar] [CrossRef] [PubMed]
- Vernia, P.; Monteleone, G.; Grandinetti, G.; Villotti, G.; Di Giulio, E.; Frieri, G.; Marcheggiano, A.; Pallone, F.; Caprilli, R.; Torsoli, A. Combined Oral Sodium Butyrate and Mesalazine Treatment Compared to Oral Mesalazine Alone in Ulcerative Colitis: Randomized, Double-Blind, Placebo-Controlled Pilot Study. Dig. Dis. Sci. 2000, 45, 976–981. [Google Scholar] [CrossRef] [PubMed]
- Hamer, H.M.; Jonkers, D.M.A.E.; Vanhoutvin, S.A.L.W.; Troost, F.J.; Rijkers, G.; de Bruïne, A.; Bast, A.; Venema, K.; Brummer, R.-J.M. Effect of Butyrate Enemas on Inflammation and Antioxidant Status in the Colonic Mucosa of Patients with Ulcerative Colitis in Remission. Clin. Nutr. Edinb. Scotl. 2010, 29, 738–744. [Google Scholar] [CrossRef]
- Boicean, A.; Birlutiu, V.; Ichim, C.; Anderco, P.; Birsan, S. Fecal Microbiota Transplantation in Inflammatory Bowel Disease. Biomedicines 2023, 11, 1016. [Google Scholar] [CrossRef] [PubMed]
- Masucci, L.; Quaranta, G. Fecal Microbiota Transplantation: What’s New? Microorganisms 2022, 10, 23. [Google Scholar] [CrossRef] [PubMed]
- Bakker, G.J.; Nieuwdorp, M. Fecal Microbiota Transplantation: Therapeutic Potential for a Multitude of Diseases beyond Clostridium Difficile. In Bugs as Drugs; John Wiley & Sons, Ltd.: Hoboken, NJ, USA, 2018; pp. 291–308. ISBN 978-1-68367-080-3. [Google Scholar]
- Shi, Y.; Dong, Y.; Huang, W.; Zhu, D.; Mao, H.; Su, P. Fecal Microbiota Transplantation for Ulcerative Colitis: A Systematic Review and Meta-Analysis. PLoS ONE 2016, 11, e0157259. [Google Scholar] [CrossRef] [PubMed]
- Tang, L.; Feng, W.; Cheng, J.; Gong, Y. Clinical Remission of Ulcerative Colitis after Different Modes of Faecal Microbiota Transplantation: A Meta-Analysis. Int. J. Color. Dis. 2020, 35, 1025–1034. [Google Scholar] [CrossRef]
- Adler, E.; Tabaa, A.; Kassam, Z.; Zydek, M.; Terdiman, J.; El-Nachef, N. Capsule-Delivered Fecal Microbiota Transplant Is Safe and Well Tolerated in Patients with Ulcerative Colitis. Dig. Dis. Sci. 2019, 64, 2452–2454. [Google Scholar] [CrossRef] [PubMed]
- Cheng, F.; Huang, Z.; Wei, W.; Li, Z. Fecal Microbiota Transplantation for Crohn’s Disease: A Systematic Review and Meta-Analysis. Tech. Coloproctol. 2021, 25, 495–504. [Google Scholar] [CrossRef]
- Fehily, S.R.; Basnayake, C.; Wright, E.K.; Kamm, M.A. Fecal Microbiota Transplantation Therapy in Crohn’s Disease: Systematic Review. J. Gastroenterol. Hepatol. 2021, 36, 2672–2686. [Google Scholar] [CrossRef]
- Moayyedi, P.; Surette, M.G.; Kim, P.T.; Libertucci, J.; Wolfe, M.; Onischi, C.; Armstrong, D.; Marshall, J.K.; Kassam, Z.; Reinisch, W.; et al. Fecal Microbiota Transplantation Induces Remission in Patients With Active Ulcerative Colitis in a Randomized Controlled Trial. Gastroenterology 2015, 149, 102–109.e6. [Google Scholar] [CrossRef]
- Rossen, N.G.; Fuentes, S.; van der Spek, M.J.; Tijssen, J.G.; Hartman, J.H.A.; Duflou, A.; Löwenberg, M.; van den Brink, G.R.; Mathus-Vliegen, E.M.H.; de Vos, W.M.; et al. Findings From a Randomized Controlled Trial of Fecal Transplantation for Patients With Ulcerative Colitis. Gastroenterology 2015, 149, 110–118.e4. [Google Scholar] [CrossRef] [PubMed]
- Paramsothy, S.; Paramsothy, R.; Rubin, D.T.; Kamm, M.A.; Kaakoush, N.O.; Mitchell, H.M.; Castaño-Rodríguez, N. Faecal Microbiota Transplantation for Inflammatory Bowel Disease: A Systematic Review and Meta-Analysis. J. Crohns Colitis 2017, 11, 1180–1199. [Google Scholar] [CrossRef]
- Costello, S.P.; Hughes, P.A.; Waters, O.; Bryant, R.V.; Vincent, A.D.; Blatchford, P.; Katsikeros, R.; Makanyanga, J.; Campaniello, M.A.; Mavrangelos, C.; et al. Effect of Fecal Microbiota Transplantation on 8-Week Remission in Patients with Ulcerative Colitis: A Randomized Clinical Trial. JAMA 2019, 321, 156–164. [Google Scholar] [CrossRef] [PubMed]
- Cui, B.; Feng, Q.; Wang, H.; Wang, M.; Peng, Z.; Li, P.; Huang, G.; Liu, Z.; Wu, P.; Fan, Z.; et al. Fecal Microbiota Transplantation through Mid-Gut for Refractory Crohn’s Disease: Safety, Feasibility, and Efficacy Trial Results. J. Gastroenterol. Hepatol. 2015, 30, 51–58. [Google Scholar] [CrossRef]
- Vaughn, B.P.; Vatanen, T.; Allegretti, J.R.; Bai, A.; Xavier, R.J.; Korzenik, J.; Gevers, D.; Ting, A.; Robson, S.C.; Moss, A.C. Increased Intestinal Microbial Diversity Following Fecal Microbiota Transplant for Active Crohn’s Disease. Inflamm. Bowel Dis. 2016, 22, 2182–2190. [Google Scholar] [CrossRef]
- Gutin, L.; Piceno, Y.; Fadrosh, D.; Lynch, K.; Zydek, M.; Kassam, Z.; LaMere, B.; Terdiman, J.; Ma, A.; Somsouk, M.; et al. Fecal Microbiota Transplant for Crohn Disease: A Study Evaluating Safety, Efficacy, and Microbiome Profile. United Eur. Gastroenterol. J. 2019, 7, 807–814. [Google Scholar] [CrossRef] [PubMed]
- Sokol, H.; Landman, C.; Seksik, P.; Berard, L.; Montil, M.; Nion-Larmurier, I.; Bourrier, A.; Le Gall, G.; Lalande, V.; De Rougemont, A.; et al. Fecal Microbiota Transplantation to Maintain Remission in Crohn’s Disease: A Pilot Randomized Controlled Study. Microbiome 2020, 8, 12. [Google Scholar] [CrossRef]
- Zhang, F.; Cui, B.; He, X.; Nie, Y.; Wu, K.; Fan, D. FMT-standardization Study Group Microbiota Transplantation: Concept, Methodology and Strategy for Its Modernization. Protein Cell 2018, 9, 462–473. [Google Scholar] [CrossRef]
- Marcella, C.; Cui, B.; Kelly, C.R.; Ianiro, G.; Cammarota, G.; Zhang, F. Systematic Review: The Global Incidence of Faecal Microbiota Transplantation-Related Adverse Events from 2000 to 2020. Aliment. Pharmacol. Ther. 2021, 53, 33–42. [Google Scholar] [CrossRef]
- Schmidt, T.S.B.; Raes, J.; Bork, P. The Human Gut Microbiome: From Association to Modulation. Cell 2018, 172, 1198–1215. [Google Scholar] [CrossRef] [PubMed]
- Suskind, D.L.; Brittnacher, M.J.; Wahbeh, G.; Shaffer, M.L.; Hayden, H.S.; Qin, X.; Singh, N.; Damman, C.J.; Hager, K.R.; Nielson, H.; et al. Fecal Microbial Transplant Effect on Clinical Outcomes and Fecal Microbiome in Active Crohn’s Disease. Inflamm. Bowel Dis. 2015, 21, 556–563. [Google Scholar] [CrossRef] [PubMed]
- Goldenberg, S.D.; Batra, R.; Beales, I.; Digby-Bell, J.L.; Irving, P.M.; Kellingray, L.; Narbad, A.; Franslem-Elumogo, N. Comparison of Different Strategies for Providing Fecal Microbiota Transplantation to Treat Patients with Recurrent Clostridium Difficile Infection in Two English Hospitals: A Review. Infect. Dis. Ther. 2018, 7, 71–86. [Google Scholar] [CrossRef] [PubMed]
- Furuya-Kanamori, L.; Doi, S.A.R.; Paterson, D.L.; Helms, S.K.; Yakob, L.; McKenzie, S.J.; Garborg, K.; Emanuelsson, F.; Stollman, N.; Kronman, M.P.; et al. Upper Versus Lower Gastrointestinal Delivery for Transplantation of Fecal Microbiota in Recurrent or Refractory Clostridium Difficile Infection: A Collaborative Analysis of Individual Patient Data From 14 Studies. J. Clin. Gastroenterol. 2017, 51, 145. [Google Scholar] [CrossRef]
- Tang, G.; Yin, W.; Liu, W. Is Frozen Fecal Microbiota Transplantation as Effective as Fresh Fecal Microbiota Transplantation in Patients with Recurrent or Refractory Clostridium Difficile Infection: A Meta-Analysis? Diagn. Microbiol. Infect. Dis. 2017, 88, 322–329. [Google Scholar] [CrossRef]
Study Author and Year | Study Design | Sample Size | IBD Type | Treatment Protocol | Main Findings |
---|---|---|---|---|---|
Moayyedi et al., 2015 [93] | RCT double-blind | 75 | UC | FMT via enema once weekly for 6 weeks | An amount of 24% of FMT recipients achieved remission vs. 5% in placebo. FMT group showed increased microbial diversity. |
Rossen et al., 2015 [94] | RCT double-blind | 50 | UC | Single FMT via nasoduodenal tube | FMT was not superior to placebo in inducing remission. |
Paramsothy et al., 2017 [95] | RCT double-blind | 81 | UC | Multiple FMTs via colonoscopy followed by enemas 5 days/week for 8 weeks | Steroid-free clinical remission with endoscopic remission or response at Week 8 was achieved in 27% of FMT recipients vs. 8% in placebo. Significant changes in gut microbiota were noted towards a healthier composition. |
Costello et al., 2019 [96] | RCT double-blind | 73 | UC | FMT via colonoscopy followed by two enemas | There was a 32% remission rate in the FMT group compared to 9% in the placebo group. Noted improvement in gut bacterial diversity and stability in FMT group. |
Cui et al., 2015 [97] | Cohort | 30 | CD | Single FMT through mid-gut | Clinical improvement and remission at the first month was 86.7% and 76.7%, respectively. Patients’ body weights and lipid profiles were improved after FMT. |
Vaughn et al., 2016 [98] | Cohort | 19 | CD | Single FMT via colonoscopy | An amount of 58% demonstrated a clinical response after FMT. A significant rise in microbial diversity and regulatory T cells was noted in recipients’ lamina propia after FMT. |
Gutin et al., 2019 [99] | Cohort | 10 | CD | Single FMT via colonoscopy | Notably, 3/10 patients responded to FMT, and 2/10 patients had significant adverse events. The bacterial communities in responding patients had a higher abundance of bacteria typically present in the gut microbiota of donors. |
Sokol et al., 2020 [100] | RCT double-blind | 17 | CD | Single FMT via colonoscopy | An amount of 87.5% of patients in the FMT group achieved steroid-free remission at 10 weeks compared to 44.4% in the sham transplantation group. Greater colonisation by donor microbiota was linked to maintenance of remission. |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Gyriki, D.; Nikolaidis, C.; Stavropoulou, E.; Bezirtzoglou, I.; Tsigalou, C.; Vradelis, S.; Bezirtzoglou, E. Exploring the Gut Microbiome’s Role in Inflammatory Bowel Disease: Insights and Interventions. J. Pers. Med. 2024, 14, 507. https://doi.org/10.3390/jpm14050507
Gyriki D, Nikolaidis C, Stavropoulou E, Bezirtzoglou I, Tsigalou C, Vradelis S, Bezirtzoglou E. Exploring the Gut Microbiome’s Role in Inflammatory Bowel Disease: Insights and Interventions. Journal of Personalized Medicine. 2024; 14(5):507. https://doi.org/10.3390/jpm14050507
Chicago/Turabian StyleGyriki, Despoina, Christos Nikolaidis, Elisavet Stavropoulou, Ioanna Bezirtzoglou, Christina Tsigalou, Stergios Vradelis, and Eugenia Bezirtzoglou. 2024. "Exploring the Gut Microbiome’s Role in Inflammatory Bowel Disease: Insights and Interventions" Journal of Personalized Medicine 14, no. 5: 507. https://doi.org/10.3390/jpm14050507