The role of oral bacteria in inflammatory bowel disease.
Journal
Nature reviews. Gastroenterology & hepatology
ISSN: 1759-5053
Titre abrégé: Nat Rev Gastroenterol Hepatol
Pays: England
ID NLM: 101500079
Informations de publication
Date de publication:
10 2021
10 2021
Historique:
accepted:
23
06
2021
pubmed:
18
8
2021
medline:
23
11
2021
entrez:
17
8
2021
Statut:
ppublish
Résumé
Over the past two decades, the importance of the microbiota in health and disease has become evident. Pathological changes to the oral bacterial microbiota, such as those occurring during periodontal disease, are associated with multiple inflammatory conditions, including inflammatory bowel disease. However, the degree to which this association is a consequence of elevated oral inflammation or because oral bacteria can directly drive inflammation at distal sites remains under debate. In this Perspective, we propose that in inflammatory bowel disease, oral disease-associated bacteria translocate to the intestine and directly exacerbate disease. We propose a multistage model that involves pathological changes to the microbial and immune compartments of both the oral cavity and intestine. The evidence to support this hypothesis is critically evaluated and the relevance to other diseases in which oral bacteria have been implicated (including colorectal cancer and liver disease) are discussed.
Identifiants
pubmed: 34400822
doi: 10.1038/s41575-021-00488-4
pii: 10.1038/s41575-021-00488-4
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
731-742Subventions
Organisme : Medical Research Council
ID : MR/J011118/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/R024812/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/P012175/2
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 215027/Z/18/Z
Pays : United Kingdom
Informations de copyright
© 2021. Springer Nature Limited.
Références
Davenport, E. R. et al. The human microbiome in evolution. BMC Biol. 15, 1–12 (2017).
doi: 10.1186/s12915-017-0454-7
Flint, H. J., Scott, K. P., Louis, P. & Duncan, S. H. The role of the gut microbiota in nutrition and health. Nat. Rev. Gastroenterol. Hepatol. 9, 577–589 (2012).
pubmed: 22945443
doi: 10.1038/nrgastro.2012.156
Ni, J., Wu, G. D., Albenberg, L. & Tomov, V. T. Gut microbiota and IBD: causation or correlation? Nat. Rev. Gastroenterol. Hepatol. 14, 573–584 (2017).
pubmed: 28743984
pmcid: 5880536
doi: 10.1038/nrgastro.2017.88
Lamont, R. J., Koo, H. & Hajishengallis, G. The oral microbiota: dynamic communities and host interactions. Nat. Rev. Microbiol. 16, 745–759 (2018).
pubmed: 30301974
pmcid: 6278837
doi: 10.1038/s41579-018-0089-x
Tilg, H., Cani, P. D. & Mayer, E. A. Gut microbiome and liver diseases. Gut 65, 2035–2044 (2016).
pubmed: 27802157
doi: 10.1136/gutjnl-2016-312729
Wong, S. H. & Yu, J. Gut microbiota in colorectal cancer: mechanisms of action and clinical applications. Nat. Rev. Gastroenterol. Hepatol. 16, 690–704 (2019).
doi: 10.1038/s41575-019-0209-8
pubmed: 31554963
Ng, S. C. et al. Worldwide incidence and prevalence of inflammatory bowel disease in the 21st century: a systematic review of population-based studies. Lancet 390, 2769–2778 (2018).
doi: 10.1016/S0140-6736(17)32448-0
de Souza, H. S. P. & Fiocchi, C. Immunopathogenesis of IBD: current state of the art. Nat. Rev. Gastroenterol. Hepatol. 13, 13–27 (2016).
pubmed: 26627550
doi: 10.1038/nrgastro.2015.186
Hajishengallis, G. Periodontitis: from microbial immune subversion to systemic inflammation. Nat. Rev. Immunol. 15, 30–44 (2015).
pubmed: 25534621
pmcid: 4276050
doi: 10.1038/nri3785
Chavakis, T., Mitroulis, I. & Hajishengallis, G. Hematopoietic progenitor cells as integrative hubs for adaptation to and fine-tuning of inflammation. Nat. Immunol. 20, 802–811 (2019).
pubmed: 31213716
pmcid: 6709414
doi: 10.1038/s41590-019-0402-5
Mark Welch, J. L., Dewhirst, F. E. & Borisy, G. G. Biogeography of the oral microbiome: the site-specialist hypothesis. Annu. Rev. Microbiol. 73, 335–358 (2019).
pubmed: 31180804
pmcid: 7153577
doi: 10.1146/annurev-micro-090817-062503
Donaldson, G. P., Lee, S. M. & Mazmanian, S. K. Gut biogeography of the bacterial microbiota. Nat. Rev. Microbiol. 14, 20–32 (2016).
pubmed: 26499895
doi: 10.1038/nrmicro3552
Lloyd-Price, J. et al. Strains, functions and dynamics in the expanded Human Microbiome Project. Nature 550, 61–66 (2017).
pubmed: 28953883
pmcid: 5831082
doi: 10.1038/nature23889
Schirmer, M. et al. Dynamics of metatranscription in the inflammatory bowel disease gut microbiome. Nat. Microbiol. 3, 337–346 (2018).
pubmed: 29311644
pmcid: 6131705
doi: 10.1038/s41564-017-0089-z
Halfvarson, J. et al. Dynamics of the human gut microbiome in inflammatory bowel disease. Nat. Microbiol. 2, 17004 (2017).
pubmed: 28191884
pmcid: 5319707
doi: 10.1038/nmicrobiol.2017.4
Vandeputte, D. et al. Quantitative microbiome profiling links gut community variation to microbial load. Nature 551, 507–511 (2017).
pubmed: 29143816
doi: 10.1038/nature24460
Andoh, A. et al. Comparison of the fecal microbiota profiles between ulcerative colitis and Crohn’s disease using terminal restriction fragment length polymorphism analysis. J. Gastroenterol. 46, 479–486 (2011).
pubmed: 21253779
doi: 10.1007/s00535-010-0368-4
Gevers, D. et al. The treatment-naive microbiome in new-onset Crohn’s disease. Cell Host Microbe 15, 382–392 (2014).
pubmed: 24629344
pmcid: 4059512
doi: 10.1016/j.chom.2014.02.005
Ohkusa, T. et al. Fusobacterium varium localized in the colonic mucosa of patients with ulcerative colitis stimulates species-specific antibody. J. Gastroenterol. Hepatol. 17, 849–53 (2002).
pubmed: 12164960
doi: 10.1046/j.1440-1746.2002.02834.x
Sokol, H. et al. Fungal microbiota dysbiosis in IBD. Gut 66, 1039–1048 (2017).
pubmed: 26843508
doi: 10.1136/gutjnl-2015-310746
Peters, B. A., Wu, J., Hayes, R. B. & Ahn, J. The oral fungal mycobiome: characteristics and relation to periodontitis in a pilot study. BMC Microbiol. 17, 157 (2017).
pubmed: 28701186
pmcid: 5508751
doi: 10.1186/s12866-017-1064-9
She, Y. Y. et al. Periodontitis and inflammatory bowel disease: a meta-analysis. BMC Oral. Health 20, 67 (2020).
pubmed: 32164696
pmcid: 7069057
doi: 10.1186/s12903-020-1053-5
Singhal, S. et al. The role of oral hygiene in inflammatory bowel disease. Dig. Dis. Sci. 56, 170–175 (2011).
pubmed: 20458622
doi: 10.1007/s10620-010-1263-9
Vavricka, S. R. et al. Periodontitis and gingivitis in inflammatory bowel disease: a case-control study. Inflamm. Bowel Dis. 19, 2768–2777 (2013).
pubmed: 24216685
doi: 10.1097/01.MIB.0000438356.84263.3b
Habashneh, R. A., Khader, Y. S., Alhumouz, M. K., Jadallah, K. & Ajlouni, Y. The association between inflammatory bowel disease and periodontitis among Jordanians: a case-control study. J. Periodontal. Res. 47, 293–298 (2012).
pubmed: 22050539
doi: 10.1111/j.1600-0765.2011.01431.x
Koutsochristou, V. et al. Dental caries and periodontal disease in children and adolescents with inflammatory bowel disease: a case-control study. Inflamm. Bowel Dis. 21, 1839–1846 (2015).
pubmed: 25985243
doi: 10.1097/MIB.0000000000000452
Xu, X. et al. Oral cavity contains distinct niches with dynamic microbial communities. Environ. Microbiol. 17, 699–710 (2015).
pubmed: 24800728
doi: 10.1111/1462-2920.12502
Caselli, E. et al. Defining the oral microbiome by whole-genome sequencing and resistome analysis: the complexity of the healthy picture. BMC Microbiol. 20, 120 (2020).
pubmed: 32423437
pmcid: 7236360
doi: 10.1186/s12866-020-01801-y
Schmidt, T. S. et al. Extensive transmission of microbes along the gastrointestinal tract. eLife 8, e42693 (2019).
pubmed: 30747106
pmcid: 6424576
doi: 10.7554/eLife.42693
Wilbert, S. A., Mark Welch, J. L. & Borisy, G. G. Spatial ecology of the human tongue dorsum microbiome. Cell Rep. 30, 4003–4015.e3 (2020).
pubmed: 32209464
pmcid: 7179516
doi: 10.1016/j.celrep.2020.02.097
Welch, J. L. M., Rossetti, B. J., Rieken, C. W., Dewhirst, F. E. & Borisy, G. G. Biogeography of a human oral microbiome at the micron scale. Proc. Natl Acad. Sci. USA 113, E791–E800 (2016).
Curtis, M. A., Diaz, P. I. & Van Dyke, T. E. The role of the microbiota in periodontal disease. Periodontology 2000 83, 14–25 (2020).
pubmed: 32385883
doi: 10.1111/prd.12296
Sender, R., Fuchs, S. & Milo, R. Revised estimates for the number of human and bacteria cells in the body. PLoS Biol. 14, e1002533 (2016).
pubmed: 27541692
pmcid: 4991899
doi: 10.1371/journal.pbio.1002533
Humphrey, S. P. & Williamson, R. T. A review of saliva: normal composition, flow, and function. J. Prosthet. Dent. 85, 162–169 (2001).
pubmed: 11208206
doi: 10.1067/mpr.2001.113778
van den Bogert, B. et al. Diversity of human small intestinal Streptococcus and Veillonella populations. FEMS Microbiol. Ecol. 85, 376–388 (2013).
pubmed: 23614882
doi: 10.1111/1574-6941.12127
Kirk, K. F. et al. Molecular epidemiology and comparative genomics of Campylobacter concisus strains from saliva, faeces and gut mucosal biopsies in inflammatory bowel disease. Sci. Rep. 8, 1902 (2018).
pubmed: 29382867
pmcid: 5790007
doi: 10.1038/s41598-018-20135-4
Strauss, J. et al. Invasive potential of gut mucosa-derived Fusobacterium nucleatum positively correlates with IBD status of the host. Inflamm. Bowel Dis. 17, 1971–1978 (2011).
pubmed: 21830275
doi: 10.1002/ibd.21606
Giannella, R. A., Broitman, S. A. & Zamcheck, N. Gastric acid barrier to ingested microorganisms in man: studies in vivo and in vitro. Gut 13, 251–256 (1972).
pubmed: 4556018
pmcid: 1412163
doi: 10.1136/gut.13.4.251
Lawley, T. D. & Walker, A. W. Intestinal colonization resistance. Immunology 138, 1–11 (2013).
pubmed: 23240815
doi: 10.1111/j.1365-2567.2012.03616.x
Sequeira, R. P., McDonald, J. A. K., Marchesi, J. R. & Clarke, T. B. Commensal Bacteroidetes protect against Klebsiella pneumoniae colonization and transmission through IL-36 signalling. Nat. Microbiol. 5, 304–313 (2020).
pubmed: 31907407
pmcid: 7610889
doi: 10.1038/s41564-019-0640-1
Li, B. et al. Oral bacteria colonize and compete with gut microbiota in gnotobiotic mice. Int. J. Oral. Sci. 11, 10 (2019).
pubmed: 30833566
pmcid: 6399334
doi: 10.1038/s41368-018-0043-9
Segata, N. et al. Composition of the adult digestive tract bacterial microbiome based on seven mouth surfaces, tonsils, throat and stool samples. Genome Biol. 13, R42 (2012).
pubmed: 22698087
pmcid: 3446314
doi: 10.1186/gb-2012-13-6-r42
Eren, A. M., Borisy, G. G., Huse, S. M. & Mark Welch, J. L. Oligotyping analysis of the human oral microbiome. Proc. Natl Acad. Sci. USA 111, E2875–2884 (2014).
pubmed: 24965363
pmcid: 4104879
doi: 10.1073/pnas.1409644111
Tierney, B. T. et al. The landscape of genetic content in the gut and oral human microbiome. Cell Host Microbe 26, 283–295.e8 (2019).
pubmed: 31415755
pmcid: 6716383
doi: 10.1016/j.chom.2019.07.008
Carr, V. R. et al. Abundance and diversity of resistomes differ between healthy human oral cavities and gut. Nat. Commun. 11, 693 (2020).
pubmed: 32019923
pmcid: 7000725
doi: 10.1038/s41467-020-14422-w
Man, S. M. et al. Campylobacter concisus and other Campylobacter species in children with newly diagnosed Crohn’s disease. Inflamm. Bowel Dis. 16, 1008–1016 (2010).
pubmed: 19885905
doi: 10.1002/ibd.21157
Kirk, K. F., Nielsen, H. L., Thorlacius-Ussing, O. & Nielsen, H. Optimized cultivation of Campylobacter concisus from gut mucosal biopsies in inflammatory bowel disease. Gut Pathog. 8, 27 (2016).
pubmed: 27252786
pmcid: 4888738
doi: 10.1186/s13099-016-0111-7
Schirmer, M. et al. Compositional and temporal changes in the gut microbiome of pediatric ulcerative colitis patients are linked to disease course. Cell Host Microbe 24, 600–610.e4 (2018).
pubmed: 30308161
pmcid: 6277984
doi: 10.1016/j.chom.2018.09.009
Dinakaran, V. et al. Identification of specific oral and gut pathogens in full thickness colon of colitis patients: implications for colon motility. Front. Microbiol. 10, 3220 (2019).
doi: 10.3389/fmicb.2018.03220
Pascal, V. et al. A microbial signature for Crohn’s disease. Gut 66, 813–822 (2017).
pubmed: 28179361
doi: 10.1136/gutjnl-2016-313235
Atarashi, K. et al. Ectopic colonization of oral bacteria in the intestine drives T
pubmed: 29051379
pmcid: 5682622
doi: 10.1126/science.aan4526
Baker, J. L. et al. Klebsiella and Providencia emerge as lone survivors following long-term starvation of oral microbiota. Proc. Natl Acad. Sci. USA 116, 8499–8504 (2019).
pubmed: 30975748
pmcid: 6486781
doi: 10.1073/pnas.1820594116
Sayad, A. et al. Genetic susceptibility for periodontitis with special focus on immune-related genes: a concise review. Gene Rep. 21, 100814 (2020).
doi: 10.1016/j.genrep.2020.100814
Graham, D. B. & Xavier, R. J. Pathway paradigms revealed from the genetics of inflammatory bowel disease. Nature 578, 527–539 (2020).
pubmed: 32103191
pmcid: 7871366
doi: 10.1038/s41586-020-2025-2
Xun, Z., Zhang, Q., Xu, T., Chen, N. & Chen, F. Dysbiosis and ecotypes of the salivary microbiome associated with inflammatory bowel diseases and the assistance in diagnosis of diseases using oral bacterial profiles. Front. Microbiol. 9, 1136 (2018).
pubmed: 29899737
pmcid: 5988890
doi: 10.3389/fmicb.2018.01136
Said, H. S. et al. Dysbiosis of salivary microbiota in inflammatory bowel disease and its association with oral immunological biomarkers. DNA Res. 21, 15–25 (2015).
doi: 10.1093/dnares/dst037
Szafrański, S. P. et al. Functional biomarkers for chronic periodontitis and insights into the roles of Prevotella nigrescens and Fusobacterium nucleatum; a metatranscriptome analysis. NPJ Biofilms Microbiomes 1, 15017 (2015).
pubmed: 28721234
pmcid: 5515211
doi: 10.1038/npjbiofilms.2015.17
Kumar, P. S., Griffen, A. L., Moeschberger, M. L. & Leys, E. J. Identification of candidate periodontal pathogens and beneficial species by quantitative 16S clonal analysis. J. Clin. Microbiol. 43, 3944–3955 (2005).
pubmed: 16081935
pmcid: 1233920
doi: 10.1128/JCM.43.8.3944-3955.2005
Kelsen, J. et al. Alterations of the subgingival microbiota in pediatric Crohn’s disease studied longitudinally in discovery and validation cohorts. Inflamm. Bowel Dis. 21, 2797–2805 (2015).
pubmed: 26288001
doi: 10.1097/MIB.0000000000000557
Moutsopoulos, N. M. & Konkel, J. E. Tissue-specific immunity at the oral mucosal barrier. Trends Immunol. 39, 276–287 (2018).
pubmed: 28923364
doi: 10.1016/j.it.2017.08.005
Dutzan, N., Konkel, J. E., Greenwell-Wild, T. & Moutsopoulos, N. M. Characterization of the human immune cell network at the gingival barrier. Mucosal Immunol. 9, 1163–1172 (2016).
pubmed: 26732676
pmcid: 4820049
doi: 10.1038/mi.2015.136
Pan, W., Wang, Q. & Chen, Q. The cytokine network involved in the host immune response to periodontitis. Int. J. Oral. Sci. 11, 30 (2019).
pubmed: 31685798
pmcid: 6828663
doi: 10.1038/s41368-019-0064-z
Herrero, E. R. et al. Dysbiotic biofilms deregulate the periodontal inflammatory response. J. Dent. Res. 97, 547–555 (2018).
pubmed: 29394879
doi: 10.1177/0022034517752675
Hajishengallis, G., Shakhatreh, M.-A. K., Wang, M. & Liang, S. Complement receptor 3 blockade promotes IL-12-mediated clearance of porphyromonas gingivalis and negates its virulence in vivo. J. Immunol. 179, 2359–2367 (2007).
pubmed: 17675497
doi: 10.4049/jimmunol.179.4.2359
Dutzan, N. et al. A dysbiotic microbiome triggers TH17 cells to mediate oral mucosal immunopathology in mice and humans. Sci. Transl. Med. 10, eaat0797 (2018).
pubmed: 30333238
pmcid: 6330016
doi: 10.1126/scitranslmed.aat0797
Suárez, L. J., Vargas, D. E., Rodríguez, A., Arce, R. M. & Roa, N. S. Systemic Th17 response in the presence of periodontal inflammation. J. Appl. Oral. Sci. 28, e20190490 (2020).
pubmed: 32267379
pmcid: 7135952
doi: 10.1590/1678-7757-2019-0490
Aleksandra Nielsen, A., Nederby Nielsen, J., Schmedes, A., Brandslund, I. & Hey, H. Saliva Interleukin-6 in patients with inflammatory bowel disease. Scand. J. Gastroenterol. 40, 1444–1448 (2005).
pubmed: 16316893
doi: 10.1080/00365520510023774
Szczeklik, K., Owczarek, D., Pytko-Polończyk, J., Kȩsek, B. & Mach, T. H. Proinflammatory cytokines in the saliva of patients with active and nonactive Crohn’s disease. Pol. Arch. Med. Wewn. 122, 200–208 (2012).
pubmed: 22538761
Rezaie, A. et al. Alterations in salivary antioxidants, nitric oxide, and transforming growth factor-β1 in relation to disease activity in Crohn’s disease patients. Ann. N. Y. Acad. Sci. 1091, 110–122 (2006).
pubmed: 17341608
doi: 10.1196/annals.1378.060
Rezaie, A. et al. Study on the correlations among disease activity index and salivary transforming growth factor-β1 and nitric oxide in ulcerative colitis patients. Ann. N. Y. Acad. Sci. 1095, 305–314 (2007).
pubmed: 17404043
doi: 10.1196/annals.1397.034
Lamster, I. B., Rodrick, M. L., Sonis, S. T. & Falchuk, Z. M. An analysis of peripheral blood and salivary polymorphonuclear leukocyte function, circulating immune complex levels and oral status in patients with inflammatory bowel disease. J. Periodontol. 53, 231–238 (1982).
pubmed: 6951992
doi: 10.1902/jop.1982.53.4.231
van Dyke, T. E., Dowell, V. R., Offenbacher, S., Snyder, W. & Hersh, T. Potential role of microorganisms isolated from periodontal lesions in the pathogenesis of inflammatory bowel disease. Infect. Immun. 53, 671–677 (1986).
pubmed: 3462153
pmcid: 260846
doi: 10.1128/iai.53.3.671-677.1986
Fournier, B. M. & Parkos, C. A. The role of neutrophils during intestinal inflammation. Mucosal Immunol. 5, 354–366 (2012).
pubmed: 22491176
doi: 10.1038/mi.2012.24
Mowat, A. M. & Agace, W. W. Regional specialization within the intestinal immune system. Nat. Rev. Immunol. 14, 667–685 (2014).
pubmed: 25234148
doi: 10.1038/nri3738
Antoni, L., Nuding, S., Wehkamp, J. & Stange, E. F. Intestinal barrier in inflammatory bowel disease. World J. Gastroenterol. 20, 1165–1179 (2014).
pubmed: 24574793
pmcid: 3921501
doi: 10.3748/wjg.v20.i5.1165
Friedrich, M., Pohin, M. & Powrie, F. Cytokine networks in the pathophysiology of inflammatory bowel disease. Immunity 50, 992–1006 (2019).
pubmed: 30995511
doi: 10.1016/j.immuni.2019.03.017
Winter, S. E. et al. Host-derived nitrate boosts growth of E. coli in the inflamed gut. Science 339, 708–711 (2013).
pubmed: 23393266
pmcid: 4004111
doi: 10.1126/science.1232467
Nassar, M. et al. GAS6 is a key homeostatic immunological regulator of host-commensal interactions in the oral mucosa. Proc. Natl Acad. Sci. USA 114, E337–E346 (2017).
pubmed: 28049839
pmcid: 5255577
doi: 10.1073/pnas.1614926114
Duran-Pinedo, A. E. et al. Community-wide transcriptome of the oral microbiome in subjects with and without periodontitis. ISME J. 8, 1659–1672 (2014).
pubmed: 24599074
pmcid: 4817619
doi: 10.1038/ismej.2014.23
Goggins, M. G. et al. Increased urinary nitrite, a marker of nitric oxide, in active inflammatory bowel disease. Mediators Inflamm. 10, 69–73 (2001).
pubmed: 11405552
pmcid: 1781692
doi: 10.1080/09629350120054536
Avdagić, N. et al. Nitric oxide as a potential biomarker in inflammatory bowel disease. Bosn. J. Basic Med. Sci. 13, 5–9 (2013).
pubmed: 23448603
pmcid: 4333920
doi: 10.17305/bjbms.2013.2402
Ali, O. T. et al. Nitrite and nitrate levels of gingival crevicular fluid and saliva in subjects with gingivitis and chronic periodontitis. J. Oral Maxillofac. Res. 5, e5 (2014).
Hyde, E. R. et al. Metagenomic analysis of nitrate-reducing bacteria in the oral cavity: implications for nitric oxide homeostasis. PLoS One 9, e88645 (2014).
pubmed: 24670812
pmcid: 3966736
doi: 10.1371/journal.pone.0088645
Kitamoto, S. et al. The intermucosal connection between the mouth and gut in commensal pathobiont-driven colitis. Cell 182, 447–462.e14 (2020).
pubmed: 32758418
pmcid: 7414097
doi: 10.1016/j.cell.2020.05.048
Bamias, G. & Cominelli, F. Role of type 2 immunity in intestinal inflammation. Curr. Opin. Gastroenterol. 31, 471–476 (2015).
pubmed: 26376478
pmcid: 4668267
doi: 10.1097/MOG.0000000000000212
Maloy, K. J. & Powrie, F. Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature 474, 298–306 (2011).
pubmed: 21677746
doi: 10.1038/nature10208
Komiya, Y. et al. Patients with colorectal cancer have identical strains of Fusobacterium nucleatum in their colorectal cancer and oral cavity. Gut 68, 1335–1337 (2018).
pubmed: 29934439
doi: 10.1136/gutjnl-2018-316661
Mahendran, V. et al. Delineation of genetic relatedness and population structure of oral and enteric Campylobacter concisus strains by analysis of housekeeping genes. Microbiology 161, 1600–1612 (2015).
pubmed: 26002953
doi: 10.1099/mic.0.000112
Ismail, Y. et al. Investigation of the enteric pathogenic potential of oral Campylobacter concisus strains isolated from patients with inflammatory bowel disease. PLoS One 7, e38217 (2012).
pubmed: 22666490
pmcid: 3364211
doi: 10.1371/journal.pone.0038217
Chung, H. K. L. et al. Genome analysis of Campylobacter concisus strains from patients with inflammatory bowel disease and gastroenteritis provides new insights into pathogenicity. Sci. Rep. 6, 38442 (2016).
pubmed: 27910936
pmcid: 5133609
doi: 10.1038/srep38442
Wang, Y. et al. Campylobacter concisus genomospecies 2 is better adapted to the human gastrointestinal tract as compared with Campylobacter concisus genomospecies 1. Front. Physiol. 8, 543 (2017).
pubmed: 28824443
pmcid: 5541300
doi: 10.3389/fphys.2017.00543
Liu, F. et al. Genomic analysis of oral Campylobacter concisus strains identified a potential bacterial molecular marker associated with active Crohn’s disease. Emerg. Microbes Infect. 7, 64 (2018).
pubmed: 29636463
pmcid: 5893538
doi: 10.1038/s41426-018-0065-6
Maier, L. et al. Extensive impact of non-antibiotic drugs on human gut bacteria. Nature 555, 623–628 (2018).
pubmed: 29555994
pmcid: 6108420
doi: 10.1038/nature25979
Zaura, E. et al. Same exposure but two radically different responses to antibiotics: resilience of the salivary microbiome versus long-term microbial shifts in feces. mBio 6, e01693-15 (2015).
Shaw, L. P. et al. Modelling microbiome recovery after antibiotics using a stability landscape framework. ISME J. 13, 1845–1856 (2019).
pubmed: 30877283
pmcid: 6591120
doi: 10.1038/s41396-019-0392-1
Oswal, S., Ravindra, S., Sinha, A. & Manjunath, S. Antibiotics in periodontal surgeries: A prospective randomised cross over clinical trial. J. Indian. Soc. Periodontol. 18, 570–574 (2014).
pubmed: 25425817
pmcid: 4239745
doi: 10.4103/0972-124X.142443
Bernstein, C. N. Is antibiotic use a cause of IBD worldwide? Inflamm. Bowel Dis. 26, 448–449 (2020).
pubmed: 31265061
Horliana, A. C. R. T. et al. Dissemination of periodontal pathogens in the bloodstream after periodontal procedures: a systematic review. PLoS One 9, e98271 (2014).
pubmed: 24870125
pmcid: 4037200
doi: 10.1371/journal.pone.0098271
Kojima, A. et al. Aggravation of inflammatory bowel diseases by oral streptococci. Oral. Dis. 20, 359–366 (2014).
pubmed: 23679203
doi: 10.1111/odi.12125
Goren, I. et al. Risk of bacteremia in hospitalised patients with inflammatory bowel disease: a 9-year cohort study. United European Gastroenterol. J. 8, 195–203 (2020).
pubmed: 32213075
doi: 10.1177/2050640619874524
Xue, Y. et al. Indoleamine 2,3-dioxygenase expression regulates the survival and proliferation of Fusobacterium nucleatum in THP-1-derived macrophages. Cell Death Dis. 9, 355 (2018).
pubmed: 29500439
pmcid: 5834448
doi: 10.1038/s41419-018-0389-0
Parhi, L. et al. Breast cancer colonization by Fusobacterium nucleatum accelerates tumor growth and metastatic progression. Nat. Commun. 11, 3295 (2020).
doi: 10.1038/s41467-020-16967-2
Seedorf, H. et al. Bacteria from diverse habitats colonize and compete in the mouse gut. Cell 159, 253–266 (2014).
pubmed: 25284151
pmcid: 4194163
doi: 10.1016/j.cell.2014.09.008
Zhernakova, A. et al. Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity. Science 352, 565–569 (2016).
pubmed: 27126040
pmcid: 5240844
doi: 10.1126/science.aad3369
Imhann, F. et al. Proton pump inhibitors affect the gut microbiome. Gut 65, 740–748 (2016).
pubmed: 26657899
doi: 10.1136/gutjnl-2015-310376
Jackson, M. A. et al. Proton pump inhibitors alter the composition of the gut microbiota. Gut 65, 749–756 (2016).
pubmed: 26719299
doi: 10.1136/gutjnl-2015-310861
Vich Vila, A. et al. Impact of commonly used drugs on the composition and metabolic function of the gut microbiota. Nat. Commun. 11, 362 (2020).
pubmed: 31953381
pmcid: 6969170
doi: 10.1038/s41467-019-14177-z
Hojo, M. et al. Gut microbiota composition before and after use of proton pump inhibitors. Dig. Dis. Sci. 63, 2940–2949 (2018).
pubmed: 29796911
pmcid: 6182435
doi: 10.1007/s10620-018-5122-4
Mishiro, T. et al. Oral microbiome alterations of healthy volunteers with proton pump inhibitor. J. Gastroenterol. Hepatol. 33, 1059–1066 (2018).
pubmed: 29105152
doi: 10.1111/jgh.14040
Schwartz, N. R. M. et al. Proton pump inhibitors, H2 blocker use, and risk of inflammatory bowel disease in children. J. Pediatr. Pharmacol. Ther. 24, 489–496 (2019).
pubmed: 31719810
pmcid: 6836698
Juillerat, P. et al. Drugs that inhibit gastric acid secretion may alter the course of inflammatory bowel disease. Aliment. Pharmacol. Ther. 36, 239–247 (2012).
pubmed: 22670722
doi: 10.1111/j.1365-2036.2012.05173.x
Shah, R., Richardson, P., Yu, H., Kramer, J. & Hou, J. K. Gastric acid suppression is associated with an increased risk of adverse outcomes in inflammatory bowel disease. Digestion 95, 188–193 (2017).
pubmed: 28288458
doi: 10.1159/000455008
Liu, H. et al. Fusobacterium nucleatum exacerbates colitis by damaging epithelial barrier and inducing aberrant inflammation. J. Dig. Dis. 21, 385–398 (2020).
pubmed: 32441482
doi: 10.1111/1751-2980.12909
Caballero, S. et al. Distinct but spatially overlapping intestinal niches for vancomycin-resistant enterococcus faecium and carbapenem-resistant Klebsiella pneumoniae. PLoS Pathog. 11, e1005132 (2015).
pubmed: 26334306
pmcid: 4559429
doi: 10.1371/journal.ppat.1005132
Rubinstein, M. R. et al. Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/β-catenin signaling via its FadA adhesin. Cell Host Microbe 14, 195–206 (2013).
pubmed: 23954158
pmcid: 3770529
doi: 10.1016/j.chom.2013.07.012
Rubinstein, M. R. et al. Fusobacterium nucleatum promotes colorectal cancer by inducing Wnt/β-catenin modulator Annexin A1. EMBO Rep. 20, e47638 (2019).
pubmed: 30833345
pmcid: 6446206
doi: 10.15252/embr.201847638
Maroncle, N., Balestrino, D., Rich, C. & Forestier, C. Identification of Klebsiella pneumoniae genes involved in intestinal colonization and adhesion using signature-tagged mutagenesis. Infect. Immun. 70, 4729–4734 (2002).
pubmed: 12117993
pmcid: 128202
doi: 10.1128/IAI.70.8.4729-4734.2002
Hsu, C. R. et al. Klebsiella pneumoniae translocates across the intestinal epithelium via rho GTPase-and phosphatidylinositol 3-kinase/Akt-dependent cell invasion. Infect. Immun. 83, 769–779 (2015).
pubmed: 25452552
pmcid: 4294243
doi: 10.1128/IAI.02345-14
Lee, I. A. & Kim, D. H. Klebsiella pneumoniae increases the risk of inflammation and colitis in a murine model of intestinal bowel disease. Scand. J. Gastroenterol. 46, 684–693 (2011).
pubmed: 21410316
doi: 10.3109/00365521.2011.560678
Deshpande, N. P. et al. Campylobacter concisus pathotypes induce distinct global responses in intestinal epithelial cells. Sci. Rep. 6, 34288 (2016).
pubmed: 27677841
pmcid: 5039708
doi: 10.1038/srep34288
Kaakoush, N. O. et al. The pathogenic potential of Campylobacter concisus strains associated with chronic intestinal diseases. PLoS One 6, e29045 (2011).
pubmed: 22194985
pmcid: 3237587
doi: 10.1371/journal.pone.0029045
Tang, B. et al. Fusobacterium nucleatum-induced impairment of autophagic flux enhances the expression of proinflammatory cytokines via ROS in Caco-2 cells. PLoS One 11, e0165701 (2016).
pubmed: 27828984
pmcid: 5102440
doi: 10.1371/journal.pone.0165701
Dharmani, P., Strauss, J., Ambrose, C., Allen-Vercoe, E. & Chadee, K. Fusobacterium nucleatum infection of colonic cells stimulates MUC2 mucin and tumor necrosis factor alpha. Infect. Immun. 79, 2597–2607 (2011).
pubmed: 21536792
pmcid: 3191979
doi: 10.1128/IAI.05118-11
Pope, J. L. et al. Microbial colonization coordinates the pathogenesis of a Klebsiella pneumoniae infant isolate. Sci. Rep. 9, 3380 (2019).
pubmed: 30833613
pmcid: 6399262
doi: 10.1038/s41598-019-39887-8
Mahendran, V. et al. Examination of the effects of Campylobacter concisus zonula occludens toxin on intestinal epithelial cells and macrophages. Gut Pathog. 8, 18 (2016).
pubmed: 27195022
pmcid: 4870807
doi: 10.1186/s13099-016-0101-9
Gur, C. et al. Binding of the Fap2 protein of Fusobacterium nucleatum to human inhibitory receptor TIGIT protects tumors from immune cell attack. Immunity 42, 344–355 (2015).
pubmed: 25680274
pmcid: 4361732
doi: 10.1016/j.immuni.2015.01.010
Hajishengallis, G., Darveau, R. P. & Curtis, M. A. The keystone-pathogen hypothesis. Nat. Rev. Microbiol. 10, 717–725 (2012).
pubmed: 22941505
pmcid: 3498498
doi: 10.1038/nrmicro2873
Gupta, V. K. et al. A predictive index for health status using species-level gut microbiome profiling. Nat. Commun. 11, 4635 (2020).
pubmed: 32934239
pmcid: 7492273
doi: 10.1038/s41467-020-18476-8
Vieira-Silva, S. et al. Quantitative microbiome profiling disentangles inflammation- and bile duct obstruction-associated microbiota alterations across PSC/IBD diagnoses. Nat. Microbiol. 4, 1826–1831 (2019).
pubmed: 31209308
doi: 10.1038/s41564-019-0483-9
Lloyd-Price, J. et al. Multi-omics of the gut microbial ecosystem in inflammatory bowel diseases. Nature 569, 655–662 (2019).
pubmed: 31142855
pmcid: 6650278
doi: 10.1038/s41586-019-1237-9
Ryan, F. J. et al. Colonic microbiota is associated with inflammation and host epigenomic alterations in inflammatory bowel disease. Nat. Commun. 11, 1512 (2020).
pubmed: 32251296
pmcid: 7089947
doi: 10.1038/s41467-020-15342-5
Tang, Q. et al. Current sampling methods for gut microbiota: a call for more precise devices. Front. Cell Infect. Microbiol. 10, 151 (2020).
pubmed: 32328469
pmcid: 7161087
doi: 10.3389/fcimb.2020.00151
Man, S. M. et al. Host attachment, invasion, and stimulation of proinflammatory cytokines by Campylobacter concisus and other non-Campylobacter jejuni Campylobacter species. J. Infect. Dis. 202, 1855–1865 (2010).
pubmed: 21050118
doi: 10.1086/657316
Brennan, C. A. & Garrett, W. S. Fusobacterium nucleatum — symbiont, opportunist and oncobacterium. Nat. Rev. Microbiol. 17, 156–166 (2019).
pubmed: 30546113
pmcid: 6589823
doi: 10.1038/s41579-018-0129-6
Mohammed, H. et al. Oral dysbiosis in pancreatic cancer and liver cirrhosis: a review of the literature. Biomedicines 6, 115 (2018).
pmcid: 6316311
doi: 10.3390/biomedicines6040115
Karlsen, T. H., Folseraas, T., Thorburn, D. & Vesterhus, M. Primary sclerosing cholangitis – a comprehensive review. J. Hepatol. 67, 1298–1323 (2017).
pubmed: 28802875
doi: 10.1016/j.jhep.2017.07.022
De Vries, A. B., Janse, M., Blokzijl, H. & Weersma, R. K. Distinctive inflammatory bowel disease phenotype in primary sclerosing cholangitis. World J. Gastroenterol. 21, 1956–1971 (2015).
pubmed: 25684965
pmcid: 4323476
doi: 10.3748/wjg.v21.i6.1956
Iwasawa, K. et al. Dysbiosis of the salivary microbiota in pediatric-onset primary sclerosing cholangitis and its potential as a biomarker. Sci. Rep. 8, 5480 (2018).
pubmed: 29615776
pmcid: 5882660
doi: 10.1038/s41598-018-23870-w
Bajer, L. et al. Distinct gut microbiota profiles in patients with primary sclerosing cholangitis and ulcerative colitis. World J. Gastroenterol. 23, 4548–4558 (2017).
pubmed: 28740343
pmcid: 5504370
doi: 10.3748/wjg.v23.i25.4548
Sebastian, S. et al. Colorectal cancer in inflammatory bowel disease: results of the 3rd ECCO pathogenesis scientific workshop (I). J. Crohns Colitis 8, 5–18 (2014).
pubmed: 23664897
doi: 10.1016/j.crohns.2013.04.008
Ternes, D. et al. Microbiome in colorectal cancer: how to get from meta-omics to mechanism? Trends Microbiol. 28, 401–423 (2020).
pubmed: 32298617
doi: 10.1016/j.tim.2020.01.001
Kim, G. W. et al. Periodontitis is associated with an increased risk for proximal colorectal neoplasms. Sci. Rep. 9, 7528 (2019).
pubmed: 31101852
pmcid: 6525177
doi: 10.1038/s41598-019-44014-8
Flemer, B. et al. The oral microbiota in colorectal cancer is distinctive and predictive. Gut 67, 1454–1463 (2018).
doi: 10.1136/gutjnl-2017-314814
pubmed: 28988196
Abed, J. et al. Fap2 mediates Fusobacterium nucleatum colorectal adenocarcinoma enrichment by binding to tumor-expressed Gal-GalNAc. Cell Host Microbe 20, 215–225 (2016).
pubmed: 27512904
pmcid: 5465824
doi: 10.1016/j.chom.2016.07.006