In the labyrinths of pathogenesis of inflammatory bowel diseases: evolution of microbiology theory
L.S. MKRTCHAN, K.E. MAZOVKA, A.V. TKACHEV
Rostov State Medical University, Rostov-on-Don, Russia
Contact details:
Tkachev A.V. — MD, Professor, Head of the Department of Propedeutics of Internal Diseases
Address: 29 Nakhichevanskiy per., Rostov-on-Don, Russian Federation, 344022, tel.: +7-918-557-11-73, e-mail: tkachev@aaanet.ru
Traditionally, the search of the causes and study of the development mechanisms of inflammatory bowel diseases have been of great interest over the past decades. Previously, attention was focused on the genetic and immunological aspects of this group of diseases. At the same time, numerous studies are currently focused on the study of the intestinal microbiome, which is associated with the supposition that IBD develops as a result of the interaction of environmental factors, microbiome and the immune system in genetically susceptible individuals. This supposition was confirmed in a number of studies in which mutations were found in the genes that regulate the interaction between the microbiome and the immune system of IBD patients. The article discusses the role of the intestinal microbiome in IBD and various factors that can influence it, such as smoking, hygiene, diet, and use of antibacterial drugs.
Key words: intestinal microbiome, ulcerative colitis, Crohn’s disease.
REFERENCES
- DuPont A.W., DuPont H.L. The intestinal microbiota and chronic disorders of the gut. Nat. Rev. Gastroenterol. Hepatol, 2011, vol. 8(9), pp. 523-531.
- Zhang Y. Multidrug resistance gene and its relationship to ulcerative colitis and immune status of ulcerative colitis. Genet. Mol. Res., 2014, vol. 13(4), pp. 10837-10851, available at: https://pubmed.ncbi.nlm.nih.gov/?term=Wang%20JL%5BAuthor%5D&cauthor=true&cauthor_uid=25526204
- Stange E.F., Travis S.P. The European consensus on ulcerative colitis: new horizons? Gut, 2008, vol. 57(8), pp. 1029-1031, available at: https://pubmed.ncbi.nlm.nih.gov/?term=Stange%20EF%5BAuthor%5D3.%20&3.%20cauthor=true3.%20&3.%20cauthor_uid=18448568
- Stange E.F., Travis S.P., Vermeire S., Beglinger C. et al. European evidence-based consensus on the diagnostic and management of Crohn’s disease: definitions and diagnostic. Gut, 2006, vol. 55(1), rr. 1-15.
- Hisamatsu T., Suzuki M., Reinecker H.C., Nadeau W.J., McCormick B.A., Podolsky D.K. CARD15/NOD2 functions as an antibacterial factor in human intestinal epithelial cells. Gastroenterology, 2003, vol. 124, pp. 993-1000.
- Petnicki-Ocwieja T., Hrncir T., Liu Y.J., Biswas A., Hudcovic T., Tlaskalova-Hogenova H. et al. Nod2 is required for the regulation of commensal microbiota in the intestine. Proc Natl. Acad. sci. USA, 2009, vol. 106, pp. 15813-15818.
- Kobayashi K.S., Chamaillard M., Ogura Y., Henegariu O., Inohara N., Nunez G. et al. Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science, 2005, vol. 307, pp. 731–734.
- Swidsinski A., Ladhoff A., Pernthaler A., Swidsinski S., Loening-Baucke V., Ortner M. et al. Mucosal flora in inflammatory bowel disease. Gastroenterology, 2002, vol. 122, pp. 44–54.
- Rehman A., Sina C., Gavrilova O., Hasler R., Ott S., Baines J.F. et al. Nod2 is essential for temporal development of intestinal microbial communities. Gut, 2011, vol. 60, pp. 1354–1362.
- Iliev I.D., Funari V.A., Taylor K.D., Nguyen Q., Reyes C.N., Strom S.P. et al. Interactions between commensal fungi and the C-type lectin receptor Dectin-1 influence colitis. Science, 2012, vol. 336, pp. 1314-1317.
- Drummond R.A., Franco L.M., Lionakis M.S. Human CARD9: a critical molecule of fungal immune surveillance. Front Immunol., 2018, vol. 9, p. 1836.
- Janowitz H.D., Croen E.C., Sachar D.B. The role of the fecal stream in Crohn’s disease: an historical and analytic review. Inflamm Bowel Dis., 1998, vol. 4, pp. 29–39.
- Knox N.C., Forbes J.D., Peterson C.L., Van Domselaar G., Bernstein C.N. The gut microbiome in inflammatory bowel disease: lessons learned from other immune-mediated inflammatory diseases. Am J Gastroenterol., 2019, vol. 114, pp. 1051-1070.
- Sartor R.B., Wu G.D. Roles for intestinal bacteria, viruses, and fungi in pathogenesis of inflammatory bowel diseases and therapeutic approaches. Gastroenterology, 2017, vol. 152, pp. 327–239.
- Chiodini R.J., Kruiningen H.J.V., Thayer W.R. et al. Possible role of mycobacteria in inflammatory bowel disease. I. An unclassified Mycobacterium species isolated from patients with Crohn’s disease. Dig. Dis. sci., 1984, vol. 29, pp. 1073-1079.
- Qin J., Li R., Raes J., Arumugam M., Burgdorf K.S., Manichanh C. A human gut microbial gene catalog established by metagenomic sequencing. Nature, 2010, vol. 464, pp. 59–65.
- Sokol H., Leducq V., Aschard H., et al. Fungal microbiota dysbiosis in IBD. Gut, 2017, vol. 66, pp. 1039-1048.
- Demyanova E.V., Sitkin S.I., Vakhitov T.Ya., Shalaeva O.N. Features of the composition of the intestinal microbiota and blood metabolome in patients with autoimmune diseases of the gastrointestinal tract. Russian Journal of Immunology, 2018, vol. 12, no. 4, pp. 654–656.
- Pascal V., Pozuelo M., Borruel N., Casellas F., Campos D., Santiago A. et al. A microbial signature for Crohn’s disease. Gut, 2017, vol. 66, pp. 813–822.
- Yilmaz B., Juillerat P., Oyas O., Ramon C., Bravo F.D., Franc Y. et al. Microbial network disturbances in relapsing refractory Crohn’s disease. Nat Med, 2019, vol. 25, pp. 323–336.
- Halfvarson J., Brislawn C.J., Lamendella R., Vazquez-Baeza Y., Walters W.A., Bramer L.M. et al. Dynamics of the human gut microbiome in inflammatory bowel disease. Nat Microbiol, 2017, pp. 2–17004.
- Suvorova G.N., Myakisheva Yu.V., Katorkin S.E., Andreev P.S., Davydova O.E., Lyamin A.V., Kruglov E.E., Sukhachev P.A. Histological picture and microbial landscape in ulcerative colitis. Vestnik novykh meditsinskikh tekhnologiy, 2018, no. 4, pp. 170–175 (in Russ.).
- Kupaeva V.A., Loranskaya I.D., Boldyreva M.N. Profile of parietal and cavitary intestinal microbiome in patients with ulcerative colitis. Klin farmakol ter., 2020, vol. 29 (3), pp. 49–54 (in Russ.).
- Kupaeva V.A., Loranskaya I.D., Boldyreva M.N., Nanaeva B.A., Shapina M.V. Features of the intestinal microbiota in ulcerative colitis. Eksperimental’naya i klinicheskaya gastroenterologiya, 2020, no. 179 (7), pp. 78–85 (in Russ.).
- Altomare A., Putignani L., Del Chierico F. et al. Gut mucosal-associated microbiota better discloses inflammatory bowel disease differential patterns than fecal microbiota. Dig Liver Dis, 2019, vol. 51 (5), pp. 648–656.
- McMullen L., Leach S.T., Lemberg D.A., Day A.S. Current roles of specific bacteria in the pathogenesis of inflammatory bowel disease. Microbiology, 2015, vol. 1 (1), pp. 82–91.
- De Cruz P., Prideaux L., Wagner J. et al. Characterization of the gastrointestinal microbiota in health and inflammatory bowel disease. Inflamm. Bowel. Dis, 2012, pp. 18–372.
- Quevrain E., Maubert M.A., Michon C., Chain F., Marquant R., Tailhades J. et al. Identification of an anti-inflammatory protein from Faecalibacteriumprausnitzii, a commensal bacterium deficient in Crohn’s disease. Gut, 2016, vol. 65, pp. 415–425.
- Sokol H., Pigneur B., Watterlot L., Lakhdari O., Bermudez-Humaran L.G., Gratadoux J.J. et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci USA, 2008, vol. 105, pp. 16731–16736.
- Rajca S., Grondin V., Louis E., Vernier-Massouille G., Grimaud J.C., Bouhnik Y. et al. Alterations in the intestinal microbiome (dysbiosis) as a predictor of relapse after infliximab withdrawal in Crohn’s disease. Inflamm Bowel Dis, 2014, vol. 20, pp. 978–986.
- Martin R., Chain F., Miquel S., Lu J., Gratadoux J.J., Sokol H. et al. The commensal bacterium Faecalibacterium prausnitzii is protective in DNBS-induced chronic moderate and severe colitis models. Inflamm Bowel Dis, 2014, vol. 20, pp. 417–430.
- Zhang M., Qiu X., Zhang H., Yang X., Hong N., Yang Y. et al. Faecalibacterium prausnitzii inhibits interleukin-17 to ameliorate colorectal colitis in rats. PLoS One, 2014, pp. 9-e109146.
- Ott S.J. et al. Fungi and inflammatory bowel diseases: alterations of composition and diversity. Scand. J. Gastroenterol, 2008, vol. 43, pp. 831–841.
- Li Q. et al. Dysbiosis of gut fungal microbiota is associated with mucosal inflammation in Crohn’s disease. J. Clin. Gastroenterol, 2014, vol. 48, pp. 513–523.
- Lewis J.D. et al. Inflammation, antibiotics, and diet as environmental stressors of the gut microbiome in pediatric Crohn’s disease. Cell Host Microbe, 2005, vol. 18, pp. 489–500.
- Limon J.J., Tang J., Li D., Wolf A.J., Michelsen K.S., Funari V. et al. Malassezia is associated with Crohn’s disease and exacerbates colitis in mouse models. Cell Host Microbe, 2019, vol. 25, pp. 377–388.
- Tito R.Y., Chaff ron S., Caenepeel C. et al. Population-level analysis of Blastocystis subtype prevalence and variation in the human gut microbiota. Gut, gutjnl, 2018.
- Zuo T., Lu X., Zhang Y., et al. Gut mucosal virome alterations in ulcerative colitis. Gut, 2019, vol. 68, pp. 1169–1179.
- Elson C.O., McCracken V.J., Dimmit R.A. et al. Experimental models of inflammatory bowel disease reveal innate, adaptive and regulatory mechanisms of host dialogue with the microbiota. Immunol. Rev, 2005, vol. 206, pp. 260–276.
- Ng S.C., Shi H.Y., Hamidi N., Underwood F.E., Tang W., Benchimol E.I. et al. Worldwide incidence and prevalence of inflammatory bowel disease in the 21st century: a systematic review of population-based studies. Lancet, 2018, vol. 390, pp. 2769–2778.
- Shaw S.Y., Blanchard J.F., Bernstein C.N. Association between the use of antibiotics in the first year of life and pediatric inflammatory bowel disease. Am J Gastroenterol, 2010, vol. 105, pp. 2687–2692.
- Shaw S.Y., Blanchard J.F., Bernstein C.N. Association between the use of antibiotics and new diagnoses of Crohn’s disease and ulcerative colitis. Am J Gastroenterol, 2011, vol. 106, pp. 2133–2142.
- Porter C.K., Tribble D.R., Aliaga P.A., Halvorson H.A., Riddle M.S. Infectious gastroenteritis and risk of developing inflammatory bowel disease. Gastroenterology, 2008, vol. 135, pp. 781–786.
- Garcia Rodriguez L.A., Ruigomez A., Panes J. Acute gastroenteritis is followed by an increased risk of inflammatory bowel disease. Gastroenterology, 2006, vol. 130, pp. 1588–1594.
- Moossavi S., Miliku K., Sepehri S., Khafipour E., Azad M.B. The prebiotic and probiotic properties of human milk: implications for infant immune development and pediatric asthma. Front Pediatr, 2018, pp. 6–197.
- Parigi S.M., Eldh M., Larssen P., Gabrielsson S., Villablanca E.J. Breast milk and solid food shaping intestinal immunity. Front Immunol, 2015, pp. 6–415.
- Coppa G.V., Zampini L., Galeazzi T., Facinelli B., Ferrante L., Capretti R. et al. Human milk oligosaccharides inhibit the adhesion to Caco-2 cells of diarrheal pathogens: Escherichia coli, Vibrio cholerae, and Salmonella fyris. Pediatr Res, 2006, vol. 59, pp. 377–382.
- Azad M.B., Konya T., Maughan H., Guttman D.S., Field C.J., Chari R.S. et al. Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. CMAJ, 2013, vol. 185, pp. 385–394.
- De Filippo C., Cavalieri D., Di Paola M. et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl. Acad. Sci. USA, 2010, 107, pp. 14691-6.
- Wu G.D., Chen J., Hoffmann C. et al. Linking longterm dietary patterns with gut microbial enterotypes. Science, 2011, 334, pp. 105-8.
- Kuenzig M.E., Lee S.M., Eksteen B., Seow C.H., Barnabe C., Panaccione R. et al. Smoking influences the need for surgery in patients with the inflammatory bowel diseases: a systematic review and meta-analysis incorporating disease duration. BMC Gastroenterol, 2016, pp. 16–143.
- Tkachev A.V., Mkrtchyan A.V., Mazovka K.E., Bokhanova E.G. In the labyrinths of pathogenesis: the environment and metamorphosis of the appearance of IBD. Yuzhno-Rossiyskiy zhurnal terapevticheskoy praktiki, 2021, no. 2 (3), pp. 30–39 (in Russ.).
- Bikbavova G.R., Livzan M.A., Zastavnaya A.A. Intestinal virome and ulcerative colitis: new facets of interaction. Eksperimental’naya i klinicheskaya gastroenterologiya, 2019, no. 170 (10), pp. 66–71 (in Russ.).