Microbiome, gut dysbiosis and inflammatory bowel disease: That moment when the function is more important than taxonomy

Cover Page


Cite item

Full Text

Abstract

The altered gut microbiome (dysbiosis) is involved in the  pathogenesis of most  non-infectious  gastrointestinal diseases, such as inflammatory bowel disease (IBD), irritable bowel syndrome, colorectal cancer, celiac disease, hepatic encephalopathy, non-alcoholic  fatty  liver disease,  alcoholic  liver disease, cholelithiasis and  others. The molecular aspects  of the interaction  between dysbiotic microbiota and host immune system are considered in the context of IBD pathogenesis. The authors do provide  original interpretations  of the  concepts of taxonomic (microbiological) and metabolic (functional) dysbiosis. Special attention is paid to the hypothesis  that gut dysbiosis is caused not so much by structural changes  in the microbiome as by alterations  in microbial metabolism. Thus, the metabolome is a greater  predictor  of dysbiosis, than  the  taxonomic  composition  of the  microbiome. It is important to consider dysbiotic changes in the  gut  microbiota  in patients  with ulcerative colitis and  Crohn's  disease,  since  they  may  significantly affect the course and prognosis  of IBD. Factors  hampering  the   microbiota   assessment in  clinical practice  are  discussed  in  detail,  and advanced  dysbiosis tests, including  the  GA-map Dysbiosis  Test  (GA-test) and  the   Colonoflor-16 Test, are described. By means of clinical studies it is demonstrated that  a reduction  in the  genetic capacity of the  microbiome  for butyrate  synthesis, together with an increase in pathobionts and a decrease  in microbial diversity, is an important and necessary feature of dysbiosis in IBD patients. Thus, the butyryl-CoA:acetate CoA-transferase (BCoAT) gene  level can be considered  as a valuable biomarker to assess gut microbiota  function in clinical practice.  In  conclusion,  approaches to correct gut dysbiosis using probiotics, prebiotics, metabiotics  and fecal microbiota  transplantation as an addition to conventional treatment in IBD are critically discussed.

About the authors

S. I. Sitkin

State Research Institute of Highly Pure Biopreparations; North-Western State Medical University named after I.I. Mechnikov

Author for correspondence.
Email: drsitkin@gmail.com

Stanislav I. Sitkin – MD, PhD, Leading Research Fellow, Laboratory of Microbiology, State Research Institute of Highly Pure Biopreparations; Associate Professor, Chair of Internal Diseases, Gastroenterology and Dietetics, North-Western State Medical University named after I.I. Mechnikov.

7 Pudozhskaya ul., Saint Petersburg, 197110; 47 Piskarevsky prospekt, Saint Petersburg, 195067.

Tel.: +7 (812) 498 48 56.

Россия

T. Ya. Vakhitov

State Research Institute of Highly Pure Biopreparations

Email: fake@neicon.ru

Timur Ya. Vakhitov – ScD in Biology, Head of the Laboratory of Microbiology.

7 Pudozhskaya ul., Saint Petersburg, 197110.

Россия

E. V. Demyanova

State Research Institute of Highly Pure Biopreparations

Email: fake@neicon.ru

Elena V. Demyanova – PharmD, PhD, Deputy Head of the Laboratory of Microbiology.

7 Pudozhskaya ul., Saint Petersburg, 197110.

Россия

References

  1. Putignani L, Del Chierico F, Vernocchi P, Cicala M, Cucchiara S, Dallapiccola B; Dysbiotrack Study Group. Gut microbiota dysbiosis as risk and premorbid factors of IBD and IBS along the childhood-adulthood transition. Inflamm Bowel Dis. 2016;22(2):487–504. doi: 10.1097/MIB.0000000000000602.
  2. Gilbert JA, Blaser MJ, Caporaso JG, Jansson JK, Lynch SV, Knight R. Current understanding of the human microbiome. Nat Med. 2018;24(4): 392–400. doi: 10.1038/nm.4517.
  3. Вахитов ТЯ, Ситкин СИ. Концепция суперорганизма в биологии и медицине. Экспериментальная и клиническая гастроэнтерология. 2014;(7):72–85.
  4. Bäckhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. Host-bacterial mutualism in the human intestine. Science. 2005;307(5717): 1915–20. doi: 10.1126/science.1104816.
  5. Clarke G, Grenham S, Scully P, Fitzgerald P, Moloney RD, Shanahan F, Dinan TG, Cryan JF. The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. Mol Psychiatry. 2013;18(6):666–73. doi: 10.1038/mp.2012.77.
  6. Carbonero F. Human epigenetics and microbiome: the potential for a revolution in both research areas by integrative studies. Future Sci OA. 2017;3(3):FSO207. doi: 10.4155/fsoa-2017-0046.
  7. Nagao-Kitamoto H, Kitamoto S, Kuffa P, Kamada N. Pathogenic role of the gut microbiota in gastrointestinal diseases. Intest Res. 2016;14(2): 127–38. doi: 10.5217/ir.2016.14.2.127.
  8. Ситкин СИ, Вахитов ТЯ, Ткаченко ЕИ, Орешко ЛС, Жигалова ТН, Радченко ВГ, Селиверстов ПВ, Авалуева ЕБ, Суворова МА, Комличенко ЭВ. Микробиота кишечника при язвенном колите и целиакии. Экспериментальная и клиническая гастроэнтерология. 2017;(1):8–30.
  9. Lopetuso LR, Petito V, Graziani C, Schiavoni E, Paroni Sterbini F, Poscia A, Gaetani E, Franceschi F, Cammarota G, Sanguinetti M, Masucci L, Scaldaferri F, Gasbarrini A. Gut microbiota in health, diverticular disease, irritable bowel syndrome, and inflammatory bowel diseases: time for microbial marker of gastrointestinal disorders. Dig Dis. 2018;36(1):56–65. doi: 10.1159/000477205.
  10. Селиверстов ПВ, Ситкин СИ, Радченко ВГ, Лазебник ЛБ, Авалуева ЕБ, Вахитов ТЯ, Демьянова ЕВ, Скворцова ТЭ, Приходько ЕМ, Суворова МА. Saccharomyces boulardii модулируют состав микробиоты кишечника у пациентов с неалкогольной жировой болезнью печени, препятствуя прогрессированию заболевания. Экспериментальная и клиническая гастроэнтерология. 2018;(2):4–18.
  11. Opazo MC, Ortega-Rocha EM, Coronado-Arrázola I, Bonifaz LC, Boudin H, Neunlist M, Bueno SM, Kalergis AM, Riedel CA. Intestinal microbiota influences non-intestinal related autoimmune diseases. Front Microbiol. 2018;9:432. doi: 10.3389/fmicb.2018.00432.
  12. Neurath MF. Cytokines in inflammatory bowel disease. Nat Rev Immunol. 2014;14(5):329–42. doi: 10.1038/nri3661.
  13. Miner-Williams WM, Moughan PJ. Intestinal barrier dysfunction: implications for chronic inflammatory conditions of the bowel. Nutr Res Rev. 2016;29(1):40–59. doi: 10.1017/S0954422416000019.
  14. Chen SJ, Liu XW, Liu JP, Yang XY, Lu FG. Ulcerative colitis as a polymicrobial infection characterized by sustained broken mucus barrier. World J Gastroenterol. 2014;20(28):9468–75. doi: 10.3748/wjg.v20.i28.9468.
  15. Sartor RB, Wu GD. Roles for intestinal bacteria, viruses, and fungi in pathogenesis of inflammatory bowel diseases and therapeutic approaches. Gastroenterology. 2017;152(2): 327–39.e4. doi: 10.1053/j.gastro.2016.10.012.
  16. Waldschmitt N, Metwaly A, Fischer S, Haller D. Microbial Signatures as a Predictive Tool in IBD-Pearls and Pitfalls. Inflamm Bowel Dis. 2018;24(6):1123–32. doi: 10.1093/ibd/izy059.
  17. Ситкин СИ, Вахитов ТЯ, Ткаченко ЕИ, Орешко ЛС, Жигалова ТН, Радченко ВГ, Селиверстов ПВ, Авалуева ЕБ, Суворова МА, Утсаль ВА. Дисбиоз кишечника при язвенном колите и целиакии и его терапевтическая коррекция с помощью масляной кислоты в комбинации с инулином. Экспериментальная и клиническая гастроэнтерология. 2017;(6):77–98.
  18. Meisel M, Mayassi T, Fehlner-Peach H, Koval JC, O'Brien SL, Hinterleitner R, Lesko K, Kim S, Bouziat R, Chen L, Weber CR, Mazmanian SK, Jabri B, Antonopoulos DA. Interleukin-15 promotes intestinal dysbiosis with butyrate deficiency associated with increased susceptibility to colitis. ISME J. 2017;11(1):15–30. doi: 10.1038/ismej.2016.114.
  19. Hodzic Z, Schill EM, Bolock AM, Good M. IL-33 and the intestine: the good, the bad, and the inflammatory. Cytokine. 2017;100:1–10. doi: 10.1016/j.cyto.2017.06.017.
  20. Griesenauer B, Paczesny S. The ST2/IL-33 axis in immune cells during inflammatory diseases. Front Immunol. 2017;8:475. doi: 10.3389/fimmu.2017.00475.
  21. Ni J, Wu GD, Albenberg L, Tomov VT. Gut microbiota and IBD: causation or correlation? Nat Rev Gastroenterol Hepatol. 2017;14(10): 573–84. doi: 10.1038/nrgastro.2017.88.
  22. Lee YK, Mazmanian SK. Has the microbiota played a critical role in the evolution of the adaptive immune system? Science. 2010;330(6012):1768–73. doi: 10.1126/science.1195568.
  23. de Zoete MR, Flavell RA. Interactions between nod-like receptors and intestinal bacteria. Front Immunol. 2013;4:462. doi: 10.3389/fimmu.2013.00462.
  24. Lamas B, Richard ML, Leducq V, Pham HP, Michel ML, Da Costa G, Bridon-neau C, Jegou S, Hoffmann TW, Natividad JM, Brot L, Taleb S, Couturier-Maillard A, Nion-Larmurier I, Merabtene F, Seksik P, Bourrier A, Cosnes J, Ryffel B, Beaugerie L, Launay JM, Langella P, Xavier RJ, Sokol H. CARD9 impacts colitis by altering gut microbiota metabolism of tryptophan into aryl hydrocarbon receptor ligands. Nat Med. 2016;22(6):598–605. doi: 10.1038/nm.4102.
  25. Holzapfel WH, Haberer P, Snel J, Schillinger U, Huis in't Veld JH. Overview of gut flora and probiotics. Int J Food Microbiol. 1998;41(2): 85–101. doi: 10.1016/S0168-1605(98)00044-0.
  26. Levy M, Kolodziejczyk AA, Thaiss CA, Elinav E. Dysbiosis and the immune system. Nat Rev Immunol. 2017;17(4):219–32. doi: 10.1038/nri.2017.7.
  27. Petersen C, Round JL. Defining dysbiosis and its influence on host immunity and disease. Cell Microbiol. 2014;16(7):1024–33. doi: 10.1111/cmi.12308.
  28. Vangay P, Ward T, Gerber JS, Knights D. Antibiotics, pediatric dysbiosis, and disease. Cell Host Microbe. 2015;17(5):553–64. doi: 10.1016/j.chom.2015.04.006.
  29. Ситкин СИ, Ткаченко ЕИ, Вахитов ТЯ. Метаболический дисбиоз кишечника и его биомаркеры. Экспериментальная и клиническая гастроэнтерология. 2015;(12):6–29.
  30. Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A. 2007;104(34): 13780–5. doi: 10.1073/pnas.0706625104.
  31. Sartor RB. Gut microbiota: Diet promotes dysbiosis and colitis in susceptible hosts. Nat Rev Gastroenterol Hepatol. 2012;9(10):561–2. doi: 10.1038/nrgastro.2012.157.
  32. Lozupone CA, Stombaugh J, Gonzalez A, Ackermann G, Wendel D, Vázquez-Baeza Y, Jansson JK, Gordon JI, Knight R. Meta-analyses of studies of the human microbiota. Genome Res. 2013;23(10):1704–14. doi: 10.1101/gr.151803.112.
  33. Kriss M, Hazleton KZ, Nusbacher NM, Martin CG, Lozupone CA. Low diversity gut microbiota dysbiosis: drivers, functional implications and recovery. Curr Opin Microbiol. 2018;44:34– 40. doi: 10.1016/j.mib.2018.07.003.
  34. Walujkar SA, Dhotre DP, Marathe NP, Lawate PS, Bharadwaj RS, Shouche YS. Characterization of bacterial community shift in human Ulcerative Colitis patients revealed by Illumina based 16S rRNA gene amplicon sequencing. Gut Pathog. 2014;6:22. doi: 10.1186/1757-4749-6-22.
  35. Fite A, Macfarlane S, Furrie E, Bahrami B, Cummings JH, Steinke DT, Macfarlane GT. Longitudinal analyses of gut mucosal microbiotas in ulcerative colitis in relation to patient age and disease severity and duration. J Clin Microbiol. 2013;51(3):849–56. doi: 10.1128/JCM.02574-12.
  36. Li KY, Wang JL, Wei JP, Gao SY, Zhang YY, Wang LT, Liu G. Fecal microbiota in pouchitis and ulcerative colitis. World J Gastroenterol. 2016;22(40):8929–39. doi: 10.3748/wjg.v22.i40.8929.
  37. Halfvarson J, Brislawn CJ, Lamendella R, Vázquez-Baeza Y, Walters WA, Bramer LM, D'Amato M, Bonfiglio F, McDonald D, Gonzalez A, McClure EE, Dunklebarger MF, Knight R, Jansson JK. Dynamics of the human gut microbiome in inflammatory bowel disease. Nat Microbiol. 2017;2:17004. doi: 10.1038/nmicrobiol.2017.4.
  38. Yang Y, Jobin C. Novel insights into microbiome in colitis and colorectal cancer. Curr Opin Gastroenterol. 2017;33(6):422–7. doi: 10.1097/MOG.0000000000000399.
  39. Gonçalves P, Araújo JR, Di Santo JP. A cross-talk between microbiota-derived short-chain fatty acids and the host mucosal immune system regulates intestinal homeostasis and inflammatory bowel disease. Inflamm Bowel Dis. 2018;24(3):558–72. doi: 10.1093/ibd/izx029.
  40. Morgan XC, Tickle TL, Sokol H, Gevers D, Devaney KL, Ward DV, Reyes JA, Shah SA, LeLeiko N, Snapper SB, Bousvaros A, Korzenik J, Sands BE, Xavier RJ, Huttenhower C. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol. 2012;13(9):R79. doi: 10.1186/gb-2012-13-9-r79.
  41. Chen B, Chen H, Shu X, Yin Y, Li J, Qin J, Chen L, Peng K, Xu F, Gu W, Zhao H, Jiang L, Li L, Song J, Elitsur Y, Yu HD, Jiang M, Wang X, Xiang C. Presence of segmented filamentous bacteria in human children and its potential role in the modulation of human gut immunity. Front Microbiol. 2018;9:1403. doi: 10.3389/fmicb.2018.01403.
  42. Hansen R, Thomson JM, El-Omar EM, Hold GL. The role of infection in the aetiology of inflammatory bowel disease. J Gastroenterol. 2010;45(3):266–76. doi: 10.1007/s00535-009-0191-y.
  43. Timms VJ, Daskalopoulos G, Mitchell HM, Neilan BA. The association of Mycobacterium avium subsp. paratuberculosis with inflammatory bowel disease. PLoS One. 2016;11(2):e0148731. doi: 10.1371/journal.pone.0148731.
  44. Peng JC, Shen J, Zhu Q, Ran ZH. The impact of Clostridum difficile on surgical rate among ulcerative colitis patients: A systemic review and meta-analysis. Saudi J Gastroenterol. 2015;21(4):208–12. doi: 10.4103/1319-3767.161644.
  45. Волчкова ЕВ, Белоусова ЕА, Макарчук ПА, Русанова ЕВ, Великанов ЕВ. Частота выявления инфекции Clostridium difficile в больничных условиях. Альманах клинической медицины. 2014;33:71–6. doi: 10.18786/2072-0505-2014-33-71-76.
  46. Bien J, Palagani V, Bozko P. The intestinal microbiota dysbiosis and Clostridium difficile infection: is there a relationship with inflammatory bowel disease? Therap Adv Gastroenterol. 2013;6(1):53–68. doi: 10.1177/1756283X12454590.
  47. Byndloss MX, Olsan EE, Rivera-Chávez F, Tiffany CR, Cevallos SA, Lokken KL, Torres TP, Byndloss AJ, Faber F, Gao Y, Litvak Y, Lopez CA, Xu G, Napoli E, Giulivi C, Tsolis RM, Revzin A, Lebrilla CB, Bäumler AJ. Microbiota-activated PPAR-γ signaling inhibits dysbiotic Enterobacteriaceae expansion. Science. 2017;357(6351): 570–5. doi: 10.1126/science.aam9949.
  48. Zeng MY, Inohara N, Nuñez G. Mechanisms of inflammation-driven bacterial dysbiosis in the gut. Mucosal Immunol. 2017;10(1):18–26. doi: 10.1038/mi.2016.75.
  49. Laserna-Mendieta EJ, Clooney AG, Carretero-Gomez JF, Moran C, Sheehan D, Nolan JA, Hill C, Gahan CGM, Joyce SA, Shanahan F, Claesson MJ. Determinants of Reduced Genetic Capacity for Butyrate Synthesis by the Gut Microbiome in Crohn's Disease and Ulcerative Colitis. J Crohns Colitis. 2018;12(2):204–16. doi: 10.1093/ecco-jcc/jjx137.
  50. Litvak Y, Byndloss MX, Tsolis RM, Bäumler AJ. Dysbiotic Proteobacteria expansion: a microbial signature of epithelial dysfunction. Curr Opin Microbiol. 2017;39:1–6. doi: 10.1016/j.mib.2017.07.003.
  51. Sokol H, Seksik P, Furet JP, Firmesse O, Nion-Larmurier I, Beaugerie L, Cosnes J, Corthier G, Marteau P, Doré J. Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm Bowel Dis. 2009;15(8):1183–9. doi: 10.1002/ibd.20903.
  52. Machiels K, Joossens M, Sabino J, De Preter V, Arijs I, Eeckhaut V, Ballet V, Claes K, Van Immerseel F, Verbeke K, Ferrante M, Verhaegen J, Rutgeerts P, Vermeire S. A decrease of the butyrate-producing species Roseburia hominis and Faecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis. Gut. 2014;63(8):1275–83. doi: 10.1136/gutjnl-2013-304833.
  53. Takahashi K, Nishida A, Fujimoto T, Fujii M, Shioya M, Imaeda H, Inatomi O, Bamba S, Sugimoto M, Andoh A. Reduced abundance of butyrate-producing bacteria species in the fecal microbial community in Crohn's disease. Digestion. 2016;93(1):59–65. doi: 10.1159/000441768.
  54. Duboc H, Rajca S, Rainteau D, Benarous D, Maubert MA, Quervain E, Thomas G, Barbu V, Humbert L, Despras G, Bridonneau C, Dumetz F, Grill JP, Masliah J, Beaugerie L, Cosnes J, Chazouillères O, Poupon R, Wolf C, Mallet JM, Langella P, Trugnan G, Sokol H, Seksik P. Connecting dysbiosis, bile-acid dysmetabolismand gut inflammation in inflammatory bowel diseases. Gut. 2013;62(4):531–9. doi: 10.1136/gutjnl-2012-302578.
  55. Rehman A, Rausch P, Wang J, Skieceviciene J, Kiudelis G, Bhagalia K, Amarapurkar D, Kupcinskas L, Schreiber S, Rosenstiel P, Baines JF, Ott S. Geographical patterns of the standing and active human gut microbiome in health and IBD. Gut. 2016;65(2):238–48. doi: 10.1136/gutjnl-2014-308341.
  56. Kang S, Denman SE, Morrison M, Yu Z, Dore J, Leclerc M, McSweeney CS. Dysbiosis of fecal microbiota in Crohn's disease patients as revealed by a custom phylogenetic microarray. Inflamm Bowel Dis. 2010;16(12):2034–42. doi: 10.1002/ibd.21319.
  57. Png CW, Lindén SK, Gilshenan KS, Zoetendal EG, McSweeney CS, Sly LI, McGuckin MA, Florin TH. Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria. Am J Gastroenterol. 2010;105(11):2420–8. doi: 10.1038/ajg.2010.281.
  58. Vigsnæs LK, Brynskov J, Steenholdt C, Wilcks A, Licht TR. Gram-negative bacteria account for main differences between faecal microbiota from patients with ulcerative colitis and healthy controls. Benef Microbes. 2012;3(4): 287–97. doi: 10.3920/BM2012.0018.
  59. Wrzosek L, Miquel S, Noordine ML, Bouet S, Joncquel Chevalier-Curt M, Robert V, Philippe C, Bridonneau C, Cherbuy C, Robbe-Masselot C, Langella P, Thomas M. Bacteroides thetaiotaomicron and Faecalibacterium prausnitzii influence 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. doi: 10.1186/1741-7007-11-61.
  60. Vigsnaes LK, van den Abbeele P, Sulek K, Frandsen HL, Steenholdt C, Brynskov J, Vermeiren J, van de Wiele T, Licht TR. Microbiotas from UC patients display altered metabolism and reduced ability of LAB to colonize mucus. Sci Rep. 2013;3:1110. doi: 10.1038/srep01110.
  61. Fyderek K, Strus M, Kowalska-Duplaga K, Gosiewski T, Wedrychowicz A, Jedynak-Wasowicz U, Sładek M, Pieczarkowski S, Adamski P, Kochan P, Heczko PB. Mucosal bacterial microflora and mucus layer thickness in adolescents with inflammatory bowel disease. World J Gastroenterol. 2009;15(42):5287–94. doi: 10.3748/wjg.15.5287.
  62. Kabeerdoss J, Jayakanthan P, Pugazhendhi S, Ramakrishna BS. Alterations of mucosal microbiota in the colon of patients with inflammatory bowel disease revealed by real time polymerase chain reaction amplification of 16S ribosomal ribonucleic acid. Indian J Med Res. 2015;142(1): 23–32. doi: 10.4103/0971-5916.162091.
  63. Thorkildsen LT, Nwosu FC, Avershina E, Ricanek P, Perminow G, Brackmann S, Vatn MH, Rudi K. Dominant fecal microbiota in newly diagnosed untreated inflammatory bowel disease patients. Gastroenterol Res Pract. 2013;2013:636785. doi: 10.1155/2013/636785.
  64. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. Diversity, stability and resilience of the human gut microbiota. Nature. 2012;489(7415):220–30. doi: 10.1038/nature11550.
  65. Ситкин СИ, Ткаченко ЕИ, Вахитов ТЯ. Филометаболическое ядро микробиоты кишечника. Альманах клинической медицины. 2015;40:12–34. doi: 10.18786/2072-0505-2015-40-12-34.
  66. Salonen A, Salojärvi J, Lahti L, de Vos WM. The adult intestinal core microbiota is determined by analysis depth and health status. Clin Microbiol Infect. 2012;18 Suppl 4:16–20. doi: 10.1111/j.1469-0691.2012.03855.x.
  67. Prosberg M, Bendtsen F, Vind I, Petersen AM, Gluud LL. The association between the gut microbiota and the inflammatory bowel disease activity: a systematic review and meta-analysis. Scand J Gastroenterol. 2016;51(12):1407– 15. doi: 10.1080/00365521.2016.1216587.
  68. Magnusson MK, Strid H, Isaksson S, Simrén M, Öhman L. The mucosal antibacterial response profile and fecal microbiota composition are linked to the disease course in patients with newly diagnosed ulcerative colitis. Inflamm Bowel Dis. 2017;23(6):956–66. doi: 10.1097/MIB.0000000000001130.
  69. Sokol H, Jegou S, McQuitty C, Straub M, Leducq V, Landman C, Kirchgesner J, Le Gall G, Bourrier A, Nion-Larmurier I, Cosnes J, Seksik P, Richard ML, Beaugerie L. Specificities of the intestinal microbiota in patients with inflammatory bowel disease and Clostridium difficile infection. Gut Microbes. 2018;9(1):55–60. doi: 10.1080/19490976.2017.1361092.
  70. Rajca S, Grondin V, Louis E, Vernier-Massouille G, Grimaud JC, Bouhnik Y, Laharie D, Dupas JL, Pillant H, Picon L, Veyrac M, Flamant M, Savoye G, Jian R, Devos M, Paintaud G, Piver E, Allez M, Mary JY, Sokol H, Colombel JF, Seksik P. Alterations in the intestinal microbiome (dysbiosis) as a predictor of relapse after infliximab withdrawal in Crohn's disease. Inflamm Bowel Dis. 2014;20(6):978–86. doi: 10.1097/MIB.0000000000000036.
  71. Magnusson MK, Strid H, Sapnara M, Lasson A, Bajor A, Ung KA, Öhman L. Anti-TNF therapy response in patients with ulcerative colitis is associated with colonic antimicrobial peptide expression and microbiota composition. J Crohns Colitis. 2016;10(8):943–52. doi: 10.1093/ecco-jcc/jjw051.
  72. Ananthakrishnan AN, Luo C, Yajnik V, Khalili H, Garber JJ, Stevens BW, Cleland T, Xavier RJ. Gut microbiome function predicts response to anti-integrin biologic therapy in inflammatorybowel diseases. Cell Host Microbe. 2017;21(5): 603–10.e3. doi: 10.1016/j.chom.2017.04.010.
  73. Doherty MK, Ding T, Koumpouras C, Telesco SE, Monast C, Das A, Brodmerkel C, Schloss PD. Fecal Microbiota Signatures Are Associated with Response to Ustekinumab Therapy among Crohn's Disease Patients. MBio. 2018;9(2). pii: e02120–17. doi: 10.1128/mBio.02120-17.
  74. Casén C, Vebø HC, Sekelja M, Hegge FT, Karlsson MK, Ciemniejewska E, Dzankovic S, Frøyland C, Nestestog R, Engstrand L, Munkholm P, Nielsen OH, Rogler G, Simrén M, Öhman L, Vatn MH, Rudi K. Deviations in human gut microbiota: a novel diagnostic test for determining dysbiosis in patients with IBS or IBD. Aliment Pharmacol Ther. 2015;42(1):71–83. doi: 10.1111/apt.13236.
  75. Pascal V, Pozuelo M, Borruel N, Casellas F, Campos D, Santiago A, Martinez X, Varela E, Sarrabayrouse G, Machiels K, Vermeire S, Sokol H, Guarner F, Manichanh C. A microbial signature for Crohn's disease. Gut. 2017;66(5):813–22. doi: 10.1136/gutjnl-2016-313235.
  76. Montassier E, Al-Ghalith GA, Hillmann B, Viskocil K, Kabage AJ, McKinlay CE, Sadowsky MJ, Khoruts A, Knights D. CLOUD: a non-parametric detection test for microbiome outliers. Microbiome. 2018;6(1):137. doi: 10.1186/s40168-018-0514-4.
  77. Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R. Bacterial community variation in human body habitats across space and time. Science. 2009;326(5960):1694–7. doi: 10.1126/science.1177486.
  78. Lavelle A, Lennon G, O'Sullivan O, Docherty N, Balfe A, Maguire A, Mulcahy HE, Doherty G, O'Donoghue D, Hyland J, Ross RP, Coffey JC, Sheahan K, Cotter PD, Shanahan F, Winter DC, O'Connell PR. Spatial variation of the colonic microbiota in patients with ulcerative colitis and control volunteers. Gut. 2015;64(10): 1553–61. doi: 10.1136/gutjnl-2014-307873.
  79. Kralik P, Ricchi M. A Basic Guide to Real Time PCR in Microbial Diagnostics: Definitions, Parameters, and Everything. Front Microbiol. 2017;8:108. doi: 10.3389/fmicb.2017.00108.
  80. Gerber GK. The dynamic microbiome. FEBS Lett. 2014;588(22):4131–9. doi: 10.1016/j.febslet.2014.02.037.
  81. Schippa S, Conte MP. Dysbiotic events in gut microbiota: impact on human health. Nutrients. 2014;6(12):5786–805. doi: 10.3390/nu6125786.
  82. Flores GE, Caporaso JG, Henley JB, Rideout JR, Domogala D, Chase J, Leff JW, Vázquez-Baeza Y, Gonzalez A, Knight R, Dunn RR, Fierer N. Temporal variability is a personalized feature of the human microbiome. Genome Biol. 2014;15(12):531. doi: 10.1186/s13059-014-0531-y.
  83. Holmes I, Harris K, Quince C. Dirichlet multinomial mixtures: generative models for microbial metagenomics. PLoS One. 2012;7(2):e30126. doi: 10.1371/journal.pone.0030126.
  84. Zaneveld JR, McMinds R, Vega Thurber R. Stress and stability: applying the Anna Karenina principle to animal microbiomes. Nat Microbiol. 2017;2:17121. doi: 10.1038/nmicrobiol.2017.121.
  85. Gonze D, Coyte KZ, Lahti L, Faust K. Microbial communities as dynamical systems. Curr Opin Microbiol. 2018;44:41–9. doi: 10.1016/j.mib.2018.07.004.
  86. Arnol'd VI. Catastrophe Theory. 3rd edition. Berlin – Heidelberg: Springer-Verlag; 1992. 150 p. doi: 10.1007/978-3-642-58124-3.
  87. Gibbons SM, Kearney SM, Smillie CS, Alm EJ. Two dynamic regimes in the human gut microbiome. PLoS Comput Biol. 2017;13(2):e1005364. doi: 10.1371/journal.pcbi.1005364.
  88. David LA, Materna AC, Friedman J, Campos-Baptista MI, Blackburn MC, Perrotta A, Erdman SE, Alm EJ. Host lifestyle affects human microbiota on daily timescales. Genome Biol. 2014;15(7):R89. doi: 10.1186/gb-2014-15-7-r89.
  89. Sommer F, Anderson JM, Bharti R, Raes J, Rosenstiel P. The resilience of the intestinal microbiota influences health and disease. Nat Rev Microbiol. 2017;15(10):630–8. doi: 10.1038/nrmicro.2017.58.
  90. Donskey CJ, Hujer AM, Das SM, Pultz NJ, Bonomo RA, Rice LB. Use of denaturing gradient gel electrophoresis for analysis of the stool microbiota of hospitalized patients. J Microbiol Methods. 2003;54(2):249–56. doi: 10.1016/S0167-7012(03)00059-9.
  91. Jernberg C, Löfmark S, Edlund C, Jansson JK. Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. ISME J. 2007;1(1):56–66. doi: 10.1038/ismej.2007.3.
  92. Jakobsson HE, Jernberg C, Andersson AF, Sjölund-Karlsson M, Jansson JK, Engstrand L. Short-term antibiotic treatment has differing long-term impacts on the human throat and gut microbiome. PLoS One. 2010;5(3):e9836. doi: 10.1371/journal.pone.0009836.
  93. Shenderov BA. Metabiotics: novel idea or natural development of probiotic conception. Microb Ecol Health Dis. 2013;24. doi: 10.3402/mehd.v24i0.20399.
  94. Reinisch W. Fecal microbiota transplantation in inflammatory bowel disease. Dig Dis. 2017;35(1–2):123–6. doi: 10.1159/000449092.
  95. Sitkin S, Pokrotnieks J. Clinical Potential of Anti-inflammatory Effects of Faecalibacterium prausnitzii and Butyrate in Inflammatory Bowel Disease. Inflamm Bowel Dis. 2018. doi: 10.1093/ibd/izy258. [Epub ahead of print].
  96. Lavelle A, Lennon G, Winter DC, O'Connell PR. Colonic biogeography in health and ulcerative colitis. Gut Microbes. 2016;7(5):435–42. doi: 10.1080/19490976.2016.1216748.
  97. McIlroy J, Ianiro G, Mukhopadhya I, Hansen R, Hold GL. Review article: the gut microbiome in inflammatory bowel disease-avenues for microbial management. Aliment Pharmacol Ther. 2018;47(1):26–42. doi: 10.1111/apt.14384.
  98. Walujkar SA, Kumbhare SV, Marathe NP, Patangia DV, Lawate PS, Bharadwaj RS, Shouche YS. Molecular profiling of mucosal tissue associated microbiota in patients manifesting acute exacerbations and remission stage of ulcerative colitis. World J Microbiol Biotechnol. 2018;34(6):76. doi: 10.1007/s11274-018-2449-0.
  99. Prideaux L, Kang S, Wagner J, Buckley M, Mahar JE, De Cruz P, Wen Z, Chen L, Xia B, van Langenberg DR, Lockett T, Ng SC, Sung JJ, Desmond P, McSweeney C, Morrison M, Kirkwood CD, Kamm MA. Impact of ethnicity, geography, and disease on the microbiota in health and inflammatory bowel disease. Inflamm Bowel Dis. 2013;19(13):2906–18. doi: 10.1097/01.MIB.0000435759.05577.12.
  100. Fedorak RN, Ismond KP. Practical considerations and the intestinal microbiome in disease: antibiotics for IBD therapy. Dig Dis. 2016;34(1– 2):112–21. doi: 10.1159/000443014.
  101. Le Bastard Q, Al-Ghalith GA, Grégoire M, Chapelet G, Javaudin F, Dailly E, Batard E, Knights D, Montassier E. Systematic review: human gut dysbiosis induced by non-antibiotic prescription medications. Aliment Pharmacol Ther. 2018;47(3):332–45. doi: 10.1111/apt.14451.
  102. Marchesi JR. Shifting from a gene-centric to metabolite-centric strategy to determine the core gut microbiome. Bioeng Bugs. 2011;2(6): 309–14. doi: 10.4161/bbug.2.6.17235.
  103. Wang WL, Xu SY, Ren ZG, Tao L, Jiang JW, Zheng SS. Application of metagenomics in the human gut microbiome. World J Gastroenterol. 2015;21(3):803–14. doi: 10.3748/wjg.v21.i3.803.
  104. Ситкин СИ, Вахитов ТЯ, Ткаченко ЕИ, Лазебник ЛБ, Орешко ЛС, Жигалова ТН, Радченко ВГ, Авалуева ЕБ, Селиверстов ПВ, Утсаль ВА, Комличенко ЭВ. Нарушения микробного и эндогенного метаболизма при язвенном колите и целиакии: метаболомный подход к выявлению потенциальных биомаркеров хронического воспаления в кишечнике, связанного с дисбиозом. Экспериментальная и клиническая гастроэнтерология. 2017;(7):4–50.
  105. Schirmer M, Franzosa EA, Lloyd-Price J, McIver LJ, Schwager R, Poon TW, Ananthakrishnan AN, Andrews E, Barron G, Lake K, Prasad M, Sauk J, Stevens B, Wilson RG, Braun J, Denson LA, Kugathasan S, McGovern DPB, Vlamakis H, Xavier RJ, Huttenhower C. Dynamics of metatranscription in the inflammatory bowel disease gut microbiome. Nat Microbiol. 2018;3(3):337–46. doi: 10.1038/s41564-017-0089-z.
  106. Lavelle A, Sokol H. Gut microbiota: beyond metagenomics, metatranscriptomics illumi-nates microbiome functionality in IBD. Nat Rev Gastroenterol Hepatol. 2018;15(4):193–4. doi: 10.1038/nrgastro.2018.15.
  107. Larsen PE, Dai Y. Metabolome of human gut microbiome is predictive of host dysbiosis. Gigascience. 2015;4:42. doi: 10.1186/s13742-015-0084-3.
  108. Marchesi JR, Holmes E, Khan F, Kochhar S, Scanlan P, Shanahan F, Wilson ID, Wang Y. Rapid and noninvasive metabonomic characterization of inflammatory bowel disease. J Proteome Res. 2007;6(2):546–51. doi: 10.1021/pr060470d.
  109. Huda-Faujan N, Abdulamir AS, Fatimah AB, Anas OM, Shuhaimi M, Yazid AM, Loong YY. The impact of the level of the intestinal short chain Fatty acids in inflammatory bowel disease patients versus healthy subjects. Open Biochem J. 2010;4:53–8. doi: 10.2174/1874091X01004010053.
  110. Venkatesh M, Mukherjee S, Wang H, Li H, Sun K, Benechet AP, Qiu Z, Maher L, Redinbo MR, Phillips RS, Fleet JC, Kortagere S, Mukherjee P, Fasano A, Le Ven J, Nicholson JK, Dumas ME, Khanna KM, Mani S. Symbiotic bacterial metabolites regulate gastrointestinal barrier function via the xenobiotic sensor PXR and Toll-like receptor 4. Immunity. 2014;41(2):296–310. doi: 10.1016/j.immuni.2014.06.014.
  111. Agus A, Planchais J, Sokol H. Gut Microbiota Regulation of Tryptophan Metabolism in Health and Disease. Cell Host Microbe. 2018;23(6):716–24. doi: 10.1016/j.chom.2018.05.003.
  112. Beloborodova N, Bairamov I, Olenin A, Shubina V, Teplova V, Fedotcheva N. Effect of phenolic acids of microbial origin on production of reactive oxygen species in mitochondria and neutrophils. J Biomed Sci. 2012;19:89. doi: 10.1186/1423-0127-19-89.
  113. Osipov GA, Verkhovtseva NV. Study of human microecology by mass spectrometry of microbial markers. Benef Microbes. 2011;2(1):63–78. doi: 10.3920/BM2010.0017.
  114. Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S. Host-gut microbiota metabolic interactions. Science. 2012;336(6086):1262–7. doi: 10.1126/science.1223813.
  115. Verbeke KA, Boobis AR, Chiodini A, Edwards CA, Franck A, Kleerebezem M, Nauta A, Raes J, van Tol EA, Tuohy KM. Towards microbial fermentation metabolites as markers for health benefits of prebiotics. Nutr Res Rev. 2015;28(1):42–66. doi: 10.1017/S0954422415000037.
  116. Santoru ML, Piras C, Murgia A, Palmas V, Camboni T, Liggi S, Ibba I, Lai MA, Orrù S, Blois S, Loizedda AL, Griffin JL, Usai P, Caboni P, Atzori L, Manzin A. Cross sectional evaluation of the gut-microbiome metabolome axis in an Italian cohort of IBD patients. Sci Rep. 2017;7(1):9523. doi: 10.1038/s41598-017-10034-5.
  117. Ley RE, Peterson DA, Gordon JI. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell. 2006;124(4): 837–48. doi: 10.1016/j.cell.2006.02.017.
  118. Dethlefsen L, McFall-Ngai M, Relman DA. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature. 2007;449(7164):811–8. doi: 10.1038/nature06245.
  119. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, Sogin ML, Jones WJ, Roe BA, Affourtit JP, Egholm M, Henrissat B, Heath AC, Knight R, Gordon JI. A core gut microbiome in obese and lean twins. Nature. 2009;457(7228):480–4. doi: 10.1038/nature07540.
  120. Moya A, Ferrer M. Functional Redundancy-Induced Stability of Gut Microbiota Subjected to Disturbance. Trends Microbiol. 2016;24(5): 402–13. doi: 10.1016/j.tim.2016.02.002.
  121. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486(7402): 207–14. doi: 10.1038/nature11234.
  122. Ардатская МД, Бельмер СВ, Добрица ВП, Захаренко СМ, Лазебник ЛБ, Минушкин ОН, Орешко ЛС, Ситкин СИ, Ткаченко ЕИ, Суворов АН, Хавкин АИ, Шендеров БА. Дисбиоз (дисбактериоз) кишечника: современное состояние проблемы, комплексная диагностика и лечебная коррекция. Экспериментальная и клиническая гастроэнтерология. 2015;(5):13–50.
  123. Flint HJ, Scott KP, Duncan SH, Louis P, Forano E. Microbial degradation of complex carbohydrates in the gut. Gut Microbes. 2012;3(4): 289–306. doi: 10.4161/gmic.19897.
  124. Rajilić-Stojanović M, de Vos WM. The first 1000 cultured species of the human gastrointestinal microbiota. FEMS Microbiol Rev. 2014;38(5):996–1047. doi: 10.1111/1574-6976.12075.
  125. Walker AW. Studying the human microbiota. Adv Exp Med Biol. 2016;902:5–32. doi: 10.1007/978-3-319-31248-4_2.
  126. Tarasova E, Abdurasulova I, Matsulevich A, Skulyabin D, Bisaga G, Ermolenko E, Suvorov A, Klimenko V. Intestinal microbiota composition in patients with multiple sclerosis. Abstracts of 26th ECCMID Congress, the European Congress of Clinical Microbiology and Infectious Diseases. Amsterdam, Netherlands, 9–12 April, 2016. 2016. ESCMID eLibrary. P1001. Abstract 4608 [Internet]. Available from: https://www.researchgate.net/publication/303633786_Intestinal_microbiota_composition_in_patients_with_multiple_sclerosis.
  127. Sitkin S, Vakhitov T, Tkachenko E, Zhigalova T, Oreshko L, Suvorova M. P749. Not only butyrate-producing bacteria but possibly also Bacteroides thetaiotaomicron protects against ulcerative colitis. J Crohns Colitis. 2016;10(Sup-pl 1):S489. doi: 10.1093/ecco-jcc/jjw019.868.
  128. Багненко СФ, Захаренко АА, Суворов АН, Шлык ИВ, Тен ОА, Джамилов ШР, Беляев МА, Трушин АА, Натха АС, Зайцев ДА, Вовин КН, Рыбальченко ВА. Периоперационные изменения кишечного микробиоценоза у больных раком толстой кишки. Вестник хирургии им. И.И. Грекова. 2016;175(6):33–7. doi: 10.24884/0042-4625-2016-175-6-33-37.
  129. Sitkin S, Vakhitov T, Tkachenko E, Avalueva E, Oreshko L, Zhigalova T, Demyanova E, Shalaeva O, Utsal V, Suvorova M, Komlichenko E. P852. A metabolomics approach to discover biomarkers of chronic intestinal inflammation associated with gut microbiota dysbiosis in ulcerative colitis and Celiac Disease. J Crohns Colitis. 2018;12(Suppl 1):S547–8. doi: 10.1093/ecco-jcc/jjx180.979.
  130. Mancabelli L, Milani C, Lugli GA, Turroni F, Cocconi D, van Sinderen D, Ventura M. Identification of universal gut microbial biomarkers of common human intestinal diseases by meta-analysis. FEMS Microbiol Ecol. 2017;93(12). doi: 10.1093/femsec/fix153.
  131. Duvallet C, Gibbons SM, Gurry T, Irizarry RA, Alm EJ. Meta-analysis of gut microbiome studies identifies disease-specific and shared responses. Nat Commun. 2017;8(1):1784. doi: 10.1038/s41467-017-01973-8.
  132. Rosen CE, Palm NW. Functional Classification of the Gut Microbiota: The Key to Cracking the Microbiota Composition Code: Functional classifications of the gut microbiota reveal previously hidden contributions of indigenous gut bacteria to human health and disease. Bioessays. 2017;39(12). doi: 10.1002/bies.201700032.
  133. Walker AW, Duncan SH, Louis P, Flint HJ. Phylogeny, culturing, and metagenomics of the human gut microbiota. Trends Microbiol. 2014;22(5):267–74. doi: 10.1016/j.tim.2014.03.001.
  134. Devlin AS, Fischbach MA. A biosynthetic pathway for a prominent class of microbiota-derived bile acids. Nat Chem Biol. 2015;11(9): 685–90. doi: 10.1038/nchembio.1864.
  135. Kettle H, Louis P, Holtrop G, Duncan SH, Flint HJ. Modelling the emergent dynamics and major metabolites of the human colonic microbiota. Environ Microbiol. 2015;17(5): 1615–30. doi: 10.1111/1462-2920.12599.
  136. Dodd D, Spitzer MH, Van Treuren W, Merrill BD, Hryckowian AJ, Higginbottom SK, Le A, Cowan TM, Nolan GP, Fischbach MA, Sonnenburg JL. A gut bacterial pathway metabolizes aromatic amino acids into nine circulating metabolites. Nature. 2017;551(7682):648–52. doi: 10.1038/nature24661.
  137. Sitkin S, Vakhitov T, Pokrotnieks J. How to increase the butyrate-producing capacity of thegut microbiome: do IBD patients really need butyrate replacement and butyrogenic therapy? J Crohns Colitis. 2018;12(7):881–2. doi: 10.1093/ecco-jcc/jjy033.
  138. Donohoe DR, Garge N, Zhang X, Sun W, O'Connell TM, Bunger MK, Bultman SJ. The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab. 2011;13(5):517–26. doi: 10.1016/j.cmet.2011.02.018.
  139. Dumas ME. The microbial-mammalian metabolic axis: beyond simple metabolism. Cell Metab. 2011;13(5):489–90. doi: 10.1016/j.cmet.2011.04.005.
  140. Wang A, Si H, Liu D, Jiang H. Butyrate activates the cAMP-protein kinase A-cAMP response element-binding protein signaling pathway in Caco-2 cells. J Nutr. 2012;142(1):1–6. doi: 10.3945/jn.111.148155.
  141. Hamer HM, Jonkers D, Venema K, Vanhoutvin S, Troost FJ, Brummer RJ. Review article: the role of butyrate on colonic function. Aliment Pharmacol Ther. 2008;27(2):104–19. doi: 10.1111/j.1365-2036.2007.03562.x.
  142. Louis P, Flint HJ. Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiol Lett. 2009;294(1):1–8. doi: 10.1111/j.1574-6968.2009.01514.x.
  143. Vital M, Howe AC, Tiedje JM. Revealing the bacterial butyrate synthesis pathways by analyzing (meta)genomic data. MBio. 2014;5(2):e00889. doi: 10.1128/mBio.00889-14.
  144. Zhou L, Zhang M, Wang Y, Dorfman RG, Liu H, Yu T, Chen X, Tang D, Xu L, Yin Y, Pan Y, Zhou Q, Zhou Y, Yu C. Faecalibacterium prausnitzii produces butyrate to maintain Th17/Treg balance and to ameliorate colorectal colitis by inhibiting histone deacetylase 1. Inflamm Bowel Dis. 2018;24(9):1926–40. doi: 10.1093/ibd/izy182.
  145. Zheng L, Kelly CJ, Battista KD, Schaefer R, Lanis JM, Alexeev EE, Wang RX, Onyiah JC, Kominsky DJ, Colgan SP. Microbial-derived butyrate promotes epithelial barrier function through IL-10 receptor-dependent repression of claudin-2. J Immunol. 2017;199(8):2976–84. doi: 10.4049/jimmunol.1700105.
  146. Thibault R, Blachier F, Darcy-Vrillon B, de Coppet P, Bourreille A, Segain JP. Butyrate utilization by the colonic mucosa in inflammatory bowel diseases: a transport deficiency. Inflamm Bowel Dis. 2010;16(4):684–95. doi: 10.1002/ibd.21108.
  147. Boesmans L, Ramakers M, Arijs I, Windey K, Vanhove W, Schuit F, Rutgeerts P, Verbeke K, De Preter V. Inflammation-induced downregulation of butyrate uptake and oxidation is not caused by a reduced gene expression. J Cell Physiol. 2015;230(2):418–26. doi: 10.1002/jcp.24725.
  148. Kumar A, Alrefai WA, Borthakur A, Dudeja PK. Lactobacillus acidophilus counteracts en-teropathogenic E. coli-induced inhibition of butyrate uptake in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol. 2015;309(7):G602–7. doi: 10.1152/ajpgi.00186.2015.
  149. Hulin SJ, Singh S, Chapman MA, Allan A, Langman MJ, Eggo MC. Sulphide-induced energy deficiency in colonic cells is prevented by glucose but not by butyrate. Aliment Pharmacol Ther. 2002;16(2):325–31. doi: 10.1046/j.1365-2036.2002.01164.x.
  150. Reichardt N, Vollmer M, Holtrop G, Farquharson FM, Wefers D, Bunzel M, Duncan SH, Drew JE, Williams LM, Milligan G, Preston T, Morrison D, Flint HJ, Louis P. Specific substrate-driven changes in human faecal microbiota composition contrast with functional redundancy in short-chain fatty acid production. ISME J. 2018;12(2):610–22. doi: 10.1038/ismej.2017.196.
  151. Quévrain E, Maubert MA, Michon C, Chain F, Marquant R, Tailhades J, Miquel S, Carlier L, Bermúdez-Humarán LG, Pigneur B, Lequin O, Kharrat P, Thomas G, Rainteau D, Aubry C, Breyner N, Afonso C, Lavielle S, Grill JP, Chassaing G, Chatel JM, Trugnan G, Xavier R, Langella P, Sokol H, Seksik P. Identification of an anti-inflammatory protein from Faecalibacterium prausnitzii, a commensal bacterium deficient in Crohn's disease. Gut. 2016;65(3):415–25. doi: 10.1136/gutjnl-2014-307649.
  152. Breyner NM, Michon C, de Sousa CS, Vilas Boas PB, Chain F, Azevedo VA, Langella P, Chatel JM. Microbial Anti-Inflammatory Molecule (MAM) from Faecalibacterium prausnitzii shows a protective effect on DNBS and DSS-induced colitis model in mice through inhibition of NF-κB pathway. Front Microbiol. 2017;8:114. doi: 10.3389/fmicb.2017.00114.
  153. Fernandes J, Su W, Rahat-Rozenbloom S, Wolever TM, Comelli EM. Adiposity, gut microbiota and faecal short chain fatty acids are linked in adult humans. Nutr Diabetes. 2014;4:e121. doi: 10.1038/nutd.2014.23.
  154. den Besten G, van Eunen K, Groen AK, Venema K, Reijngoud DJ, Bakker BM. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res. 2013;54(9):2325–40. doi: 10.1194/jlr.R036012.
  155. Lewis SJ, Heaton KW. Increasing butyrate concentration in the distal colon by accelerating intestinal transit. Gut. 1997;41(2):245–51. doi: 10.1136/gut.41.2.245.
  156. Boets E, Deroover L, Houben E, Vermeulen K, Gomand SV, Delcour JA, Verbeke K. Quantification of in vivo colonic short chain fatty acid production from inulin. Nutrients. 2015;7(11): 8916–29. doi: 10.3390/nu7115440.
  157. van der Beek CM, Bloemen JG, van den Broek MA, Lenaerts K, Venema K, Buurman WA, Dejong CH. Hepatic uptake of rectally ad-ministered butyrate prevents an increase in systemic butyrate concentrations in humans. J Nutr. 2015;145(9):2019–24. doi: 10.3945/jn.115.211193.
  158. Louis P, Duncan SH, McCrae SI, Millar J, Jackson MS, Flint HJ. Restricted distribution of the butyrate kinase pathway among butyrate-producing bacteria from the human colon. J Bacteriol. 2004;186(7):2099–106. doi: 10.1128/JB.186.7.2099-2106.2004.
  159. Vital M, Karch A, Pieper DH. Colonic butyrate-producing communities in humans: an overview using Omics data. mSystems. 2017;2(6). pii: e00130-17. doi: 10.1128/mSystems.00130-17.
  160. de Sousa Moraes LF, Grzeskowiak LM, de Sales Teixeira TF, Gouveia Peluzio Mdo C. Intestinal microbiota and probiotics in celiac disease. Clin Microbiol Rev. 2014;27(3):482–9. doi: 10.1128/CMR.00106-13.
  161. Costello SP, Soo W, Bryant RV, Jairath V, Hart AL, Andrews JM. Systematic review with meta-analysis: faecal microbiota transplantation for the induction of remission for active ulcerative colitis. Aliment Pharmacol Ther. 2017;46(3):213–24. doi: 10.1111/apt.14173.
  162. Derwa Y, Gracie DJ, Hamlin PJ, Ford AC. Systematic review with meta-analysis: the efficacy of probiotics in inflammatory bowel disease. Aliment Pharmacol Ther. 2017;46(4): 389–400. doi: 10.1111/apt.14203.
  163. Jacobi CA, Malfertheiner P. Escherichia coli Nissle 1917 (Mutaflor): new insights into an old probiotic bacterium. Dig Dis. 2011;29(6): 600–7. doi: 10.1159/000333307.
  164. Zocco MA, dal Verme LZ, Cremonini F, Piscaglia AC, Nista EC, Candelli M, Novi M, Rigante D, Cazzato IA, Ojetti V, Armuzzi A, Gasbarrini G, Gasbarrini A. Efficacy of Lactobacillus GG in maintaining remission of ulcerative colitis. Aliment Pharmacol Ther. 2006;23(11):1567–74. doi: 10.1111/j.1365-2036.2006.02927.x.
  165. World Gastroenterology Organisation Global Guidelines ‘Probiotics and Prebiotics’. 2017 Feb. Available from: http://www. worldgastroenterology.org/guidelines/globalguidelines/probiotics-and-prebiotics/ probiotics-and-prebiotics-english [Accessed 05 September 2018].
  166. Laurell A, Sjöberg K. Prebiotics and synbiotics in ulcerative colitis. Scand J Gastroenterol. 2017;52(4):477–85. doi: 10.1080/00365521.2016.1263680.
  167. Fernández-Bañares F, Hinojosa J, Sánchez-Lombraña JL, Navarro E, Martínez-Salmerón JF, García-Pugés A, González-Huix F, Riera J, González-Lara V, Domínguez-Abascal F, Giné JJ, Moles J, Gomollón F, Gassull MA. Randomized clinical trial of Plantago ovata seeds (dietary fiber) as compared with mesalamine in maintaining remission in ulcerative coli-tis. Spanish Group for the Study of Crohn's Disease and Ulcerative Colitis (GETECCU). Am J Gastroenterol. 1999;94(2):427–33. doi: 10.1111/j.1572-0241.1999.872_a.x.
  168. Sagar NM, Cree IA, Covington JA, Arasaradnam RP. The interplay of the gut microbiome, bile acids, and volatile organic compounds. Gastroenterol Res Pract. 2015;2015:398585. doi: 10.1155/2015/398585.
  169. Vakhitov TY, Chalisova NI, Sitkin SI, Sall TS, Shalaeva ON, Demyanova EV, Morugina AS, Vinogradova AF, Petrov AV, Nozdrachev AD. Low-molecular-weight components of the metabolome control the proliferative activity in cellular and bacterial cultures. Dokl Biol Sci. 2017;472(1):8–10. doi: 10.1134/S0012496617010069.
  170. 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(5):976–81. doi: 10.1023/A:1005537411244.
  171. Assisi RF; GISDI Study Group. Combined butyric acid/mesalazine treatment in ulcerative colitis with mild-moderate activity. Results of a multicentre pilot study. Minerva Gastroenterol Dietol. 2008;54(3):231–8.
  172. Sitkin S, Tkachenko E, Vakhitov T, Oreshko L, Zhigalova T. P399. Oral butyrate plus inulin improve serum metabolomic profile and gut microbiota composition in ulcerative colitis and celiac disease. J Crohns Colitis. 2014;8(Suppl 1):S232. doi: 10.1016/S1873-9946(14)60519-5.
  173. Chang PV, Hao L, Offermanns S, Medzhitov R. The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. Proc Natl Acad Sci U S A. 2014;111(6):2247–52. doi: 10.1073/pnas.1322269111.
  174. Moayyedi P, Surette MG, Kim PT, Libertucci J, Wolfe M, Onischi C, Armstrong D, Marshall JK, Kassam Z, Reinisch W, Lee CH. Fecal microbiota transplantation induces remission in patients with active ulcerative colitis in a randomized controlled Trial. Gastroenterology. 2015;149(1):102–9.e6. doi: 10.1053/j.gastro.2015.04.001.
  175. Vaughn BP, Vatanen T, Allegretti JR, Bai A, Xavier RJ, Korzenik J, Gevers D, Ting A, Robson SC, Moss AC. Increased intestinal microbial diversity following fecal microbiota transplant for active Crohn's disease. Inflamm Bowel Dis. 2016;22(9):2182–90. doi: 10.1097/MIB.0000000000000893.
  176. Blumstein DT, Levy K, Mayer E, Harte J. Gastrointestinal dysbiosis. Evol Med Public Health. 2014;2014(1):163. doi: 10.1093/emph/eou029.
  177. Wang HG, Liu SP, Ma TH, Yan W, Zhou JF, Shi YT, Shen P, Yang XZ, Wu SN. Fecal microbiota transplantation treatment for refractory ulcerative colitis with allergy to 5-aminosalicylic acid: a case report. Medicine (Baltimore). 2018;97(19):e0675. doi: 10.1097/MD.0000000000010675.
  178. Martin FP, Su MM, Xie GX, Guiraud SP, Kussmann M, Godin JP, Jia W, Nydegger A. Urinary metabolic insights into host-gut microbial interactions in healthy and IBD children. World J Gastroenterol. 2017;23(20):3643–54. doi: 10.3748/wjg.v23.i20.3643.
  179. Qu D, Shen L, Liu S, Li H, Ma Y, Zhang R, Wu K, Yao L, Li J, Zhang J. Chronic inflammation confers to the metabolic reprogramming associated with tumorigenesis of colorectal cancer. Cancer Biol Ther. 2017;18(4):237–44. doi: 10.1080/15384047.2017.1294292.
  180. Ip WKE, Hoshi N, Shouval DS, Snapper S, Medzhitov R. Anti-inflammatory effect of IL-10 mediated by metabolic reprogramming of macrophages. Science. 2017;356(6337): 513–9. doi: 10.1126/science.aal3535.
  181. Abraham BP, Quigley EMM. A probiotic for ulcerative colitis: the culture wars continue. Dig Dis Sci. 2018;63(7):1678–80. doi: 10.1007/s10620-018-5097-1.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2018 Sitkin S.I., Vakhitov T.Y., Demyanova E.V.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies