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Composition of the colon microbiota in the individuals with inflammatory bowel disease and colon cancer

. 2024 Apr ; 69 (2) : 333-345. [epub] 20230622

Language English Country United States Media print-electronic

Document type Journal Article

Grant support
FCD-2020-2065 Inönü Üniversitesi

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PubMed 37344611
DOI 10.1007/s12223-023-01072-w
PII: 10.1007/s12223-023-01072-w
Knihovny.cz E-resources

The human intestine is a habitat for microorganisms and, recently, the composition of the intestinal microbiota has been correlated with the etiology of diseases such as inflammations, sores, and tumors. Although many studies have been conducted to understand the composition of that microbiota, expanding these studies to more samples and different backgrounds will improve our knowledge. In this work, we showed the colon microbiota composition and diversity of healthy subjects, patients with inflammatory bowel disease (IBD), and colon cancer by metagenomic sequencing. Our results indicated that the relative abundance of prokaryotic and eukaryotic microbes differs between the healthy vs. tumor biopsies, tumor vs. IBD biopsies, and fresh vs. paraffin-embedded tumor biopsies. Fusobacterium, Escherichia-Shigella, and Streptococcus genera were relatively abundant in fresh tumor biopsies, while Pseudomonas was significantly elevated in IBD biopsies. Additionally, another opportunist pathogen Malasseziales was revealed as the most abundant fungal clade in IBD biopsies, especially in ulcerative colitis. We also found that, while the Basidiomycota:Ascomycota ratio was slightly lower in tumor biopsies compared to biopsies from healthy subjects, there was a significant increase in IBD biopsies. Our work will contribute to the known diversity of prokaryotic and eukaryotic microbes in the colon biopsies in patients with IBD and colon cancer.

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Alhinai EA, Walton GE, Commane DM (2019) The role of the gut microbiota in colorectal cancer causation. Int J Mol Sci 20:5295. https://doi.org/10.3390/ijms20215295 DOI

Amaral-Zettler LA, McCliment EA, Ducklow HW, Huse SM (2009) A method for studying protistan diversity using massively parallel sequencing of V9 hypervariable regions of small-subunit ribosomal RNA genes. PLOS One 4:e6372. https://doi.org/10.1371/journal.pone.0006372

Antonopoulos DA, Huse SM, Morrison HG, Schmidt TM, Sogin ML, Young VB (2009) Reproducible community dynamics of the gastrointestinal microbiota following antibiotic perturbation. Infect Immun 77:2367–2375. https://doi.org/10.1128/iai.01520-08 DOI

Arthur JC et al (2012) Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 338:120–123. https://doi.org/10.1126/science.1224820 DOI

Bisht V, Nash K, Xu Y, Agarwal P, Bosch S, Gkoutos GV, Acharjee A (2021) Integration of the Microbiome, Metabolome and Transcriptomics Data Identified Novel Metabolic Pathway Regulation in Colorectal Cancer. Int J Mol Sci 22:5763. https://doi.org/10.3390/ijms22115763 DOI

Blais Lecours P, Marsolais D, Cormier Y, Berberi M, Haché C, Bourdages R, Duchaine C (2014) Increased prevalence of Methanosphaera stadtmanae in inflammatory bowel diseases. PLoS One 9:e87734. https://doi.org/10.1371/journal.pone.0087734

Borgognone A et al (2021) Performance of 16S Metagenomic Profiling in Formalin-Fixed Paraffin-Embedded versus Fresh-Frozen Colorectal Cancer Tissues. Cancers (Basel) pp. 5421. https://doi.org/10.3390/cancers13215421

Bouter KE, van Raalte DH, Groen AK, Nieuwdorp M (2017) Role of the gut microbiome in the pathogenesis of obesity and obesity-related metabolic dysfunction. Gastroenterology 152:1671–1678. https://doi.org/10.1053/j.gastro.2016.12.048 DOI

Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68:394–424. https://doi.org/10.3322/caac.21492 DOI

Cao Y, Shen J, Ran ZH (2014) Association between Faecalibacterium prausnitzii reduction and inflammatory bowel disease: A meta-analysis and systematic review of the literature. Gastroenterol Res Pract 2014:872725. https://doi.org/10.1155/2014/872725

Castellarin M et al (2012) Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res 22:299–306. https://doi.org/10.1101/gr.126516.111 DOI

Chan SN, Low END, Raja Ali RA, Mokhtar NM (2018) Delineating inflammatory bowel disease through transcriptomic studies: current review of progress and evidence. Intest Res 16:374–383. https://doi.org/10.5217/ir.2018.16.3.374 DOI

Chaudhary PP, Conway PL, Schlundt J (2018) Methanogens in humans: potentially beneficial or harmful for health. Appl Microbiol Biotechnol 102:3095–3104. https://doi.org/10.1007/s00253-018-8871-2 DOI

Christl SU, Eisner HD, Dusel G, Kasper H, Scheppach W (1996) Antagonistic effects of sulfide and butyrate on proliferation of colonic mucosa: a potential role for these agents in the pathogenesis of ulcerative colitis. Dig Dis Sci 41:2477–2481. https://doi.org/10.1007/BF02100146 DOI

Coker OO, Wu WKK, Wong SH, Sung JJY, Yu J (2020) Altered gut archaea composition and interaction with bacteria are associated with colorectal cancer. Gastroenterology 159:1459-1470.e1455. https://doi.org/10.1053/j.gastro.2020.06.042 DOI

David LA et al (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature 505:559–563. https://doi.org/10.1038/nature12820 DOI

De Filippo C et al (2017) A preliminary investigation in children living in rural and urban Burkina Faso and Italy. Front Microbiol 8:1979. https://doi.org/10.3389/fmicb.2017.01979 DOI

Debesa-Tur G, Pérez-Brocal V, Ruiz-Ruiz S, Castillejo A, Latorre A, Soto JL, Moya A (2021) Metagenomic analysis of formalin-fixed paraffin-embedded tumor and normal mucosa reveals differences in the microbiome of colorectal cancer patients. Sci Rep 11:391. https://doi.org/10.1038/s41598-020-79874-y DOI

Di Paola M et al (2020) Comparative immunophenotyping of Saccharomyces cerevisiae and Candida spp. strains from Crohn's disease patients and their interactions with the gut microbiome. J Transl Autoimmun 3:100036. https://doi.org/10.1016/j.jtauto.2020.100036

Dzutsev A, Goldszmid RS, Viaud S, Zitvogel L, Trinchieri G (2015) The role of the microbiota in inflammation, carcinogenesis, and cancer therapy. Eur J Immunol 45:17–31. https://doi.org/10.1002/eji.201444972 DOI

Erdem B, Kucukyildirim S, Saglar E, Polat Z, Mergen H (2014) Promoter hypermethylation of p16 and APC in gastrointestinal cancer patients. Turk J Gastroenterol 25:512–517. https://doi.org/10.5152/tjg.2014.4791 DOI

Feng Q et al (2015) Gut microbiome development along the colorectal adenoma-carcinoma sequence. Nat Commun 6:6528. https://doi.org/10.1038/ncomms7528 DOI

Flemer B et al (2017) Tumour-associated and non-tumour-associated microbiota in colorectal cancer. Gut 66:633–643. https://doi.org/10.1136/gutjnl-2015-309595 DOI

Franzosa EA et al (2014) Relating the metatranscriptome and metagenome of the human gut. Proc Nat Acad Sci USA 111:E2329–E2338. https://doi.org/10.1073/pnas.1319284111 DOI

Fulbright LE, Ellermann M, Arthur JC (2017) The microbiome and the hallmarks of cancer. PLoS Pathog 13:e1006480. https://doi.org/10.1371/journal.ppat.1006480

Gaci N, Borrel G, Tottey W, O’Toole PW, Brugère JF (2014) Archaea and the human gut: new beginning of an old story. World J Gastroenterol 20:16062–16078. https://doi.org/10.3748/wjg.v20.i43.16062 DOI

Gao R, Kong C, Li H, Huang L, Qu X, Qin N, Qin H (2017) Dysbiosis signature of mycobiota in colon polyp and colorectal cancer. Eur J Clin Microbiol Infect Dis 36:2457–2468. https://doi.org/10.1007/s10096-017-3085-6 DOI

Gao Z, Guo B, Gao R, Zhu Q, Wu W, Qin H (2015) Probiotics modify human intestinal mucosa-associated microbiota in patients with colorectal cancer. Mol Med Rep 12:6119–6127. https://doi.org/10.3892/mmr.2015.4124 DOI

Gaulke CA, Sharpton TJ (2018) The influence of ethnicity and geography on human gut microbiome composition. Nat Med 24:1495–1496. https://doi.org/10.1038/s41591-018-0210-8 DOI

Gibson GR, MacFarlane GT, Cummings JH (1988) Ocurrence of sulphate-reducing bacteria in human faeces and the relationship of dissimilatory sulphate reduction to methanogenesis in the large gut. J Appl Bacteriol 65:103–111 DOI

Gill SR et al (2006) Metagenomic analysis of the human distal gut microbiome. Science 312:1355–1359. https://doi.org/10.1126/science.1124234 DOI

Gillen CD, Walmsley RS, Prior P, Andrews HA, Allan RN (1994) Ulcerative colitis and Crohn’s disease: a comparison of the colorectal cancer risk in extensive colitis. Gut 35:1590–1592. https://doi.org/10.1136/gut.35.11.1590 DOI

Gomaa EZ (2020) Human gut microbiota/microbiome in health and diseases: a review. Antonie Van Leewenhoek 113:2019–2040. https://doi.org/10.1007/s10482-020-01474-7 DOI

Goodrich JK et al (2014) Human genetics shape the gut microbiome. Cell 159:789–799. https://doi.org/10.1016/j.cell.2014.09.053 DOI

Gupta VK, Paul S, Dutta C (2017) Geography, ethnicity or subsistence-specific variations in human microbiome composition and diversity. Front Microbiol 8:1162. https://doi.org/10.3389/fmicb.2017.01162 DOI

Han S, Zhuang J, Pan Y, Wu W, Ding K (2022) Different characteristics in gut microbiome between advanced adenoma patients and colorectal cancer patients by metagenomic analysis. Microbiol Spectr 10:e0159322. https://doi.org/10.1128/spectrum.01593-22

Hoegenauer C, Hammer HF, Mahnert A, Moissl-Eichinger C (2022) Methanogenic archaea in the human gastrointestinal tract. Nat Rev Gastroenterol Hepatol 19:805–813. https://doi.org/10.1038/s41575-022-00673-z DOI

Hoffmann C et al (2013) Archaea and fungi of the human gut microbiome: correlations with diet and bacterial residents. PLoS One 8:e66019. https://doi.org/10.1371/journal.pone.0066019

Hong SN et al (2017) RNA-seq reveals transcriptomic differences in inflamed and noninflamed intestinal mucosa of Crohn’s disease patients compared with normal mucosa of healthy controls. Inflamm Bowel Dis 23:1098–1108. https://doi.org/10.1097/MIB.0000000000001066 DOI

IARC Working Gorup on the Evaluation of Carcinogenic Risks to Humans (2012) Biological agents. vol 100 B. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans

Iljazovic A, Roy U, Gálvez EJC et al (2021) Perturbation of the gut microbiome by Prevotella spp. enhances host susceptibility to mucosal inflammation. Mucosal Immunol 14:113–124. https://doi.org/10.1038/s41385-020-0296-4

Johnson CH, Spilker ME, Goetz L, Peterson SN, Siuzdak G (2016) Metabolite and microbiome interplay in cancer immunotherapy. Cancer Res 76:6146–6152. https://doi.org/10.1158/0008-5472.CAN-16-0309 DOI

Kim G et al (2012) Methanobrevibacter smithii is the predominant methanogen in patients with constipation-predominant IBS and methane on breath. Dig Dis Sci 57:3213–3218. https://doi.org/10.1007/s10620-012-2197-1 DOI

Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glöckner FO (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41:e1. https://doi.org/10.1093/nar/gks808

Koskinen K et al (2017) First insights into the diverse human archaeome: Specific detection of archaea in the gastrointestinal tract, lung, and nose and on skin. mBio 8:e00824–00817. https://doi.org/10.1128/mBio.00824-17

Kostic AD et al (2012) Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res 22:292–298. https://doi.org/10.1101/gr.126573.111 DOI

Kourkoumpetis T et al (2021) Colonic mucosa-associated mycobiota in individuals with normal colons. Research Square:Preprint. https://doi.org/10.21203/rs.3.rs-1147234/v1

Kucukyildirim S, Erdem B, Saglar E, Polat Z, Mergen H (2014) Evaluation of MUC1, CK20 and hTERT expression in preipheral blood of gastrointestinal cancer patients in search of diagnostic criteria. Turkish J Biol 38:848–858. https://doi.org/10.3906/biy-1403-73 DOI

Lam SY et al (2021) Technical challenges regarding the use of formalin-fixed paraffin embedded (FFPE) tissue specimens for the detection of bacterial alterations in colorectal cancer. BMC Microbiol 21:297. https://doi.org/10.1186/s12866-021-02359-z DOI

Ley RE (2016) Prevotella in the gut: choose carefully. Nat Rev Gastroenterol Hepatol 13:69–70. https://doi.org/10.1038/nrgastro.2016.4 DOI

Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI (2005) Obesity alters gut microbial ecology. Proc Nat Acad Sci USA 102:11070–11075. https://doi.org/10.1073/pnas.0504978102 DOI

Li R, Shen J, Xu Y (2022) Fusobacterium nucleatum and colorectal cancer. Infect Drug Resist 15:1115–1120. https://doi.org/10.2147/IDR.S357922 DOI

Liu H, Xu X, Liang J, Wang J, Li Y (2022) The relationship between Clostridium butyricum and colorectal cancer. J Cancer Res Ther 18:1855–1859. https://doi.org/10.4103/jcrt.jcrt_1565_21 DOI

Lloyd-Price J, Abu-Ali G, Huttenhower C (2016) The healthy human microbiome. Genome Med 8:51. https://doi.org/10.1186/s13073-016-0307-y DOI

Lopez-Siles M et al (2016) Changes in the abundance of Faecalibacterium prausnitzii phylogroups I and II in the intestinal mucosa of inflammatory bowel disease and patients with colorectal cancer. Inflammation Bowel Dis 22:28–41. https://doi.org/10.1097/MIB.0000000000000590 DOI

Louca S, Parfrey LW, Doebeli M (2016) Decoupling function and taxonomy in the global ocean microbiome. Science 353:1272–1277. https://doi.org/10.1126/science.aaf4507 DOI

Lu K et al (2014) Arsenic exposure perturbs the gut microbiome and its metabolic profile in mice: an integrated metagenomics and metabolomics analysis. Envrion Health Perspect 122:284–291. https://doi.org/10.1289/ehp.1307429 DOI

Lynch SV, Pedersen O (2016) The human intestinal microbiome in health and disease. N Eng J Med 375:2369–2379. https://doi.org/10.1056/NEJMra1600266 DOI

Machiels K et al (2014) A decrease of the butyrate-producing species Roseburia hominis and Faecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis. Gut 63:1275–1283. https://doi.org/10.1136/gutjnl-2013-304833 DOI

Manichanh C et al (2006) Reduced diversity of faecal microbiota in Crohn’s disease revealed by a metagenomic approach. Gut 55:205–211. https://doi.org/10.1136/gut.2005.073817 DOI

Mbakwa CA, Penders J, Savelkoul PH, Thijs C, Dagnelie PC, Mommers M, Arts IC (2015) Gut colonization with Methanobrevibacter smithii is associated with childhood weight development. Obesity 23:2508–2516. https://doi.org/10.1002/oby.21266 DOI

McLean MH et al (2011) The inflammatory microenvironment in colorectal neoplasia. PLOS One 6:e15366. https://doi.org/10.1371/journal.pone.0015366

McMurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8:e61217. https://doi.org/10.1371/journal.pone.0061217

Mima K et al (2016) Fusobacterium nucleatum in colorectal carcinoma tissue and patient prognosis. Gut 65:1973–1980. https://doi.org/10.1136/gutjnl-2015-310101 DOI

Mutignani M et al (2021) Blood bacterial DNA load and profiling differ in colorectal cancer patients compared to tumor-free controls. Cancers (basel) 13:6363. https://doi.org/10.3390/cancers13246363 DOI

Nardelli C et al (2021) 16S rRNA of mucosal colon microbiome and CCL2 circulating levels are potential biomarkers in colorectal cancer. Int J Mol Sci 22:10747. https://doi.org/10.3390/ijms221910747 DOI

Narunsky-Haziza L et al (2022) Pan-cancer analyses reveal cancer-type-specific fungal ecologies and bacteriome interactions. Cell 185:3789–3806. https://doi.org/10.1016/j.cell.2022.09.005 DOI

Ni J, Wu GD, Albenberg L, Tomov VT (2017) Gut microbiota and IBD: causation or correlation? Nat Rev Gastroenterol Hepatol 14:573–584. https://doi.org/10.1038/nrgastro.2017.88 DOI

Nishida A, Inoue R, Inatomi O, Bamba S, Naito Y, Andoh A (2018) Gut microbiota in the pathogenesis of inflammatory bowel disease. Clin J Gastroenterol 11:1–10. https://doi.org/10.1007/s12328-017-0813-5 DOI

Oh HJ, Kim JH, Bae JM, Kim HJ, Cho NY, Kang GH (2019) Prognostic impact of Fusobacterium nucleatum depends on combined tumor location and microsatellite instability status in stage II/III colorectal cancers treated with adjuvant chemotherapy. J Pathol Transl Med 53:40–49. https://doi.org/10.4132/jptm.2018.11.29 DOI

Oksanen J et al (2013) vegan: Community ecology package. R package version 2.0–10. http://CRAN.Rproject.org/package=vegan

Panebianco C, Andriulli A, Pazienza V (2018) Pharmacomicrobiomics: exploiting the drug-microbiota interactions in anticancer therapies. Microbiome 6:92. https://doi.org/10.1186/s40168-018-0483-7 DOI

Park CH, Eun CS, Han DS (2018) Intestinal microbiota, chronic inflammation, and colorectal cancer. Intest Res 16:338–345. https://doi.org/10.5217/ir.2018.16.3.338 DOI

Pascal V et al (2017) A microbial signature for Crohn’s disease. Gut 66:813–822. https://doi.org/10.1136/gutjnl-2016-313235 DOI

Peterson DA, Frank DN, Pace NR, Gordon JI (2008) Metagenomic approaches for defining the pathogenesis of inflammatory bowel diseases. Cell Host Microbe 3:417–427. https://doi.org/10.1016/j.chom.2008.05.001 DOI

Planell N et al (2013) Transcriptional analysis of the intestinal mucosa of patients with ulcerative colitis in remission reveals lasting epithelial cell alterations. Gut 62:967–976. https://doi.org/10.1136/gutjnl-2012-303333 DOI

Pleguezuelos-Manzano C et al (2020) Mutational signature in colorectal cancer caused by genotoxic pks+ E. coli. Nature 580:269–273. https://doi.org/10.1038/s41586-020-2080-8 DOI

Qin J et al (2012) A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490:55–60. https://doi.org/10.1038/nature11450 DOI

Qin X, Gu Y, Liu T, Wang C, Zhong W, Wang B, Cao H (2021) Gut mycobiome: A promising target for colorectal cancer. Biochim Biophys Acta Rev Cancer 1875:188489. https://doi.org/10.1016/j.bbcan.2020.188489

Quaglio AEV, Grillo TG, De Oliveira ECS, Di Stasi LC, Sassaki LY (2022) Gut microbiota, inflammatory bowel disease and colorectal cancer. World J Gastroenterol 28:4053–4060. https://doi.org/10.3748/wjg.v28.i30.4053 DOI

R Development Core Team (2015) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria

Rognes T, Flouri T, Nichols B, Quince C, Mahé F (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 4:e2584. https://doi.org/10.7717/peerj.2584

Rothschild D et al (2018) Environment dominates over host genetics in shaping human gut microbiota. Nature 555:210–215. https://doi.org/10.1038/nature25973 DOI

Ryma T, Samer A, Soufli I, Rafa H, Touil-Boukoffa C (2021) Role of probiotics and their metabolites in inflammatory bowel diseases (IBDs). Gastroenterol Insights 12:56–66. https://doi.org/10.3390/gastroent12010006 DOI

Saad MJ, Santos A, Prada PO (2016) Linking gut microbiota and inflammation to obesity and insulin resistance. Physiology (bethesda) 31:283–293. https://doi.org/10.1152/physiol.00041.2015 DOI

Schroeder BO, Bäckhed F (2016) Signals from the gut microbiota to distant organs in physiology and disease. Nat Med 22:1079–1089. https://doi.org/10.1038/nm.4185 DOI

Schwabe RF, Jobin C (2013) The microbiome and cancer. Nat Rev Cancer 13:800–812. https://doi.org/10.1038/nrc3610 DOI

Shah MS, DeSantis T, Yamal JM, Weir T, Ryan EP, Cope JL, Hollister EB (2018) Re-purposing 16S rRNA gene sequence data from within case paired tumor biopsy and tumor-adjacent biopsy or fecal samples to identify microbial markers for colorectal cancer. PloS One 13:e0207002. https://doi.org/10.1371/journal.pone.0207002

Shen XJ et al (2010) Molecular characterization of mucosal adherent bacteria and associations with colorectal adenomas. Gut Microbes 1:138–147. https://doi.org/10.4161/gmic.1.3.12360 DOI

Sokol H et al (2009) Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm Bowel Dis 15:1183–1189. https://doi.org/10.1002/ibd.20903 DOI

Strauss J et al (2011) Invasive potential of gut mucosa-derived Fusobacterium nucleatum positively correlates with IBD status of the host. Inflamm Bowel Dis 17:1971–1978. https://doi.org/10.1002/ibd.21606 DOI

The Human Microbiome Project Consortium (2012a) A framework for human microbiome research. Nature 486:215–221. https://doi.org/10.1038/nature11209 DOI

The Human Microbiome Project Consortium (2012b) Structure, function and diversity of the healthy human microbiome. Nature 486:207–214. https://doi.org/10.1038/nature11234 DOI

Tilg H, Adolph TE, Gerner RR, Moschen AR (2018) The intestinal microbiota in colorectal cancer. Cancer Cell 33:954–964. https://doi.org/10.1016/j.ccell.2018.03.004 DOI

Tiso M, Schechter AN (2015) Nitrate reduction to nitrite, nitric oxide and ammonia by gut bacteria under physiological conditions. PLOS One 10:e0119712. https://doi.org/10.1371/journal.pone.0119712

Tu P et al (2020) Gut microbiome toxicity: Connecting the environment and gut microbiome-associated diseases. Toxics 8:19. https://doi.org/10.3390/toxics8010019 DOI

Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, Gordon JI (2009) The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Trans Med 1:6ra14. https://doi.org/10.1126/scitranslmed.3000322

Tyakht AV et al (2013) Human gut microbiota community structures in urban and rural populations in Russia. Nat Commun 4:2469. https://doi.org/10.1038/ncomms3469 DOI

Vallianou N, Kounatidis D, Christodoulatos GS, Panagopoulos F, Karampela I, Dalamaga M (2021) Mycobiome and cancer: What is the evidence? Cancers (basel) 13:3149. https://doi.org/10.3390/cancers13133149 DOI

Volant S et al (2020) SHAMAN: a user-friendly website for metataxonomic analysis from raw reads to statistical analysis BMC Bioinformatics 21:345. https://doi.org/10.1186/s12859-020-03666-4

Walker AW et al (2011) High-throughput clone library analysis of the mucosa-associated microbiota reveals dysbiosis and differences between inflamed and non-inflamed regions of the intestine in inflammatory bowel disease. BMC Microbiol 11:7. https://doi.org/10.1186/1471-2180-11-7 DOI

Walujkar SA, Kumbhare SV, Marathe NP, Patangia DV, Lawate PS, Bharadwaj RS, Shouche YS (2018) Molecular profiling of mucosal tissue associated microbiota in patients manifesting acute exacerbations and remission stage of ulcerative colitis. World J Microbiol Biotechnol 34:76. https://doi.org/10.1007/s11274-018-2449-0 DOI

Wang T et al (2012) Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers. ISME J 6:320–329. https://doi.org/10.1038/ismej.2011.109 DOI

Wickham H (2016) ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag New York. https://ggplot2.tidyverse.org

Willing BP et al (2010) A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology 139:1844–1854. https://doi.org/10.1053/j.gastro.2010.08.049 DOI

Wirbel J et al (2019) Meta-analysis of fecal metagenomes reveals global microbial signatures that are specific for colorectal cancer. Nat Med 25:679–689. https://doi.org/10.1038/s41591-019-0406-6 DOI

Wu J, Li Q, Fu X (2019) Fusobacterium nucleatum contributes to the carcinogenesis of colorectal cancer by inducing inflammation and suppressing host immunity. Transl Oncol 12:846–851. https://doi.org/10.1016/j.tranon.2019.03.003 DOI

Wu N et al (2013) Dysbiosis signature of fecal microbiota in colorectal cancer patients. Microb Ecol 66:462–470. https://doi.org/10.1007/s00248-013-0245-9 DOI

Wu S et al (2009) A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat Med 15:1016–1022. https://doi.org/10.1038/nm.2015 DOI

Yang L et al (2019) Difference in pathomechanism between Crohn’s disease and ulcerative colitis revealed by colon transcriptome. Inflamm Bowel Dis 25:722–731. https://doi.org/10.1093/ibd/izy359 DOI

Zeller G et al (2014) Potential of fecal microbiota for early-stage detection of colorectal cancer. Mol Syst Biol 10:766. https://doi.org/10.15252/msb.20145645 .

Zhang X et al (2022) Salivary Fusobacterium nucleatum serves as a potential biomarker for colorectal cancer. iScience 25:104203. https://doi.org/10.1016/j.isci.2022.104203

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