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Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers
Open accessAbstract
Despite a long-suspected role in the development of human colorectal cancer (CRC), the composition of gut microbiota in CRC patients has not been adequately described. In this study, fecal bacterial diversity in CRC patients (n=46) and healthy volunteers (n=56) were profiled by 454 pyrosequencing of the V3 region of the 16S ribosomal RNA gene. Both principal component analysis and UniFrac analysis showed structural segregation between the two populations. Forty-eight operational taxonomic units (OTUs) were identified by redundancy analysis as key variables significantly associated with the structural difference. One OTU closely related to Bacteroides fragilis was enriched in the gut microbiota of CRC patients, whereas three OTUs related to Bacteroides vulgatus and Bacteroides uniformis were enriched in that of healthy volunteers. A total of 11 OTUs belonging to the genera Enterococcus, Escherichia/Shigella, Klebsiella, Streptococcus and Peptostreptococcus were significantly more abundant in the gut microbiota of CRC patients, and 5 OTUs belonging to the genus Roseburia and other butyrate-producing bacteria of the family Lachnospiraceae were less abundant. Real-time quantitative PCR further validated the significant reduction of butyrate-producing bacteria in the gut microbiota of CRC patients by measuring the copy numbers of butyryl-coenzyme A CoA transferase genes (Mann-Whitney test, P<0.01). Reduction of butyrate producers and increase of opportunistic pathogens may constitute a major structural imbalance of gut microbiota in CRC patients.
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“However, ETBF was reported to be enriched in fecal samples of patients with CRC compared with controls.35, 44, 45”
From Influence of the Gut Microbiome, Diet, and Environment on Risk of Colorectal Cancer (2020) · cites this paper as [45]
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“several studies have shown that compared with controls, patients with CRC had lower abundances of Bifidobacterium and Lactobacillus spp,16, 18 and other SCFA-producing bacteria, such as the genera Clostridium and Roseburia, the family Lachnospiraceae, and Faecalibacterium prausnitzii.15, 35, 37, 45, 53, 129”
From Influence of the Gut Microbiome, Diet, and Environment on Risk of Colorectal Cancer (2020) · cites this paper as [45]
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Cites
Jemal, A., Bray, F., Ferlay, J., Ward, E., & Forman, D. (2011) · CA A Cancer Journal for Clinicians · doi:10.3322/caac.20107 · Cited by 55,044
Muyzer, G., de Waal, E. C., & Uitterlinden, A. G. (1993) · Applied and Environmental Microbiology · doi:10.1128/aem.59.3.695-700.1993 · Cited by 11,490
Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences
Li, W.-Z., & Godzik, A. (2006) · Bioinform. · doi:10.1093/bioinformatics/btl158 · Cited by 10,996
ARB: a software environment for sequence data
Ludwig, W. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh293 · Cited by 6,714
De Filippo, C., Cavalieri, D., Di Paola, M., Ramazzotti, M., Poullet, J. B., Massart, S., Collini, S., Pieraccini, G., & Lionetti, P. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1005963107 · Cited by 5,579
The Ribosomal Database Project: improved alignments and new tools for rRNA analysis
Cole, J. R., Wang, Q., Cardenas, E., Fish, J., Chai, B., Farris, R. J., Kulam-Syed-Mohideen, A. S., McGarrell, D. M., Marsh, T. L., Garrity, G. M., et al. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn879 · Cited by 4,873
Frank, D. N., St. Amand, A. L., Feldman, R. A., Boedeker, E. C., Harpaz, N., & Pace, N. R. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0706625104 · Cited by 4,611
THE POPULATION FREQUENCIES OF SPECIES AND THE ESTIMATION OF POPULATION PARAMETERS
Good, I. J. (1953) · Biometrika · doi:10.1093/biomet/40.3-4.237 · Cited by 3,427
Beighton, P., & Beighton, G. (1997) · Springer eBooks · doi:10.1007/978-1-4471-0925-9_118 · Cited by 3,165
Schloss, P. D., & Handelsman, J. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.3.1501-1506.2005 · Cited by 2,529
Dethlefsen, L., Huse, S., Sogin, M. L., & Relman, D. A. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060280 · Cited by 2,361
A microbial symbiosis factor prevents intestinal inflammatory disease
Mazmanian, S. K., Round, J. L., & Kasper, D. L. (2008) · Nature · doi:10.1038/nature07008 · Cited by 2,340
Lynch, H. T., & de la Chapelle, A. (2003) · New England Journal of Medicine · doi:10.1056/nejmra012242 · Cited by 2,240
Louis, P., & Flint, H. J. (2009) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2009.01514.x · Cited by 2,179
Terzić, J., Grivennikov, S., Karin, E., & Karin, M. (2010) · Gastroenterology · doi:10.1053/j.gastro.2010.01.058 · Cited by 1,974
Wu, S., Rhee, K.-J., Albesiano, E., Rabizadeh, S., Wu, X., Yen, H.-R., Huso, D. L., Brancati, F. L., Wick, E., McAllister, F., et al. (2009) · Nature Medicine · doi:10.1038/nm.2015 · Cited by 1,812
Dominant and diet-responsive groups of bacteria within the human colonic microbiota
Walker, A. W., Ince, J., Duncan, S. H., Webster, L. M., Holtrop, G., Ze, X., Brown, D., Stares, M. D., Scott, P., Bergerat, A., et al. (2011) · The ISME Journal · doi:10.1038/ismej.2010.118 · Cited by 1,632
The microbiology of butyrate formation in the human colon
Pryde, S. E., Duncan, S. H., Hold, G. L., Stewart, C. S., & Flint, H. J. (2002) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2002.tb11467.x · Cited by 1,320
Ott, S. J., Musfeldt, M., Wenderoth, D. F., Hampe, J., Brant, O., Fölsch, U. R., Timmis, K. N., & Schreiber, S. (2004) · Gut · doi:10.1136/gut.2003.025403 · Cited by 1,311
Symbiotic gut microbes modulate human metabolic phenotypes
Li, M., Wang, B., Zhang, M., Rantalainen, M., Wang, S., Zhou, H., Zhang, Y., Shen, J., Pang, X., Zhang, M., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0712038105 · Cited by 1,144
Self-citationHamady, M., Lozupone, C., & Knight, R. D. (2009) · The ISME Journal · doi:10.1038/ismej.2009.97 · Cited by 1,113
Comparative Analysis of Human Gut Microbiota by Barcoded Pyrosequencing
Andersson, A. F., Lindberg, M., Jakobsson, H. E., Bäckhed, F., Nyrén, P., & Engstrand, L. G. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002836 · Cited by 1,079
ARB: A Software Environment for Sequence Data
Westram, R., Bader, K. C., Pruesse, E., Kumar, Y., Meier, H., Glöckner, F. O., & Ludwig, W. (2011) · Wiley eBooks · doi:10.1002/9781118010518.ch46 · Cited by 1,064
Willing, B. P., Dicksved, J., Halfvarson, J., Andersson, A. F., Lucio, M., Zheng, Z., Järnerot, G., Tysk, C., Jansson, J. K., & Engstrand, L. (2010) · Gastroenterology · doi:10.1053/j.gastro.2010.08.049 · Cited by 1,032
NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes
DeSantis, T. Z., Hugenholtz, P., Keller, K., Brodie, E., Larsen, N., Piceno, Y. M., Phan, R., & Andersen, G. L. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkl244 · Cited by 1,028
Zhang, C., Zhang, M., Wang, S., Han, R., Cao, Y., Hua, W., Mao, Y., Zhang, X., Pang, X., Wei, C., et al. (2010) · The ISME Journal · doi:10.1038/ismej.2009.112 · Cited by 1,024
Self-citationGut microorganisms, mammalian metabolism and personalized health care
Nicholson, J. K., Holmes, E., & Wilson, I. D. (2005) · Nature Reviews Microbiology · doi:10.1038/nrmicro1152 · Cited by 945
Duncan, S. H., Belenguer, A., Holtrop, G., Johnstone, A. M., Flint, H. J., & Lobley, G. E. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.02340-06 · Cited by 941
Microbial Dysbiosis in Colorectal Cancer (CRC) Patients
Sobhani, I., Tap, J., Roudot‐Thoraval, F., Roperch, J. P., Letulle, S., Langella, P., Corthier, G., Nhieu, J. T. V., & Furet, J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016393 · Cited by 859
Ramirez-Farias, C., Slezak, K., Fuller, Z., Duncan, A., Holtrop, G., & Louis, P. (2008) · British Journal of Nutrition · doi:10.1017/s0007114508019880 · Cited by 822
Primary Prevention of Colorectal Cancer
Chan, A. T., & Giovannucci, E. L. (2010) · Gastroenterology · doi:10.1053/j.gastro.2010.01.057 · Cited by 758
Martin, H., Campbell, B. J., Hart, C. A., Mpofu, C., Nayar, M. K., Singh, R., Englyst, H. N., Williams, H. F., & Rhodes, J. M. (2004) · Gastroenterology · doi:10.1053/j.gastro.2004.03.054 · Cited by 719
Huycke, M. M., Abrams, V., & Moore, D. R. (2002) · Carcinogenesis · doi:10.1093/carcin/23.3.529 · Cited by 503
Intestinal floras of populations that have a high risk of colon cancer
Moore, W. E., & Moore, L. H. (1995) · Applied and Environmental Microbiology · doi:10.1128/aem.61.9.3202-3207.1995 · Cited by 483
Willing, B., Halfvarson, J., Dicksved, J., Rosenquist, M., Järnerot, G., Engstrand, L., Tysk, C., & Jansson, J. K. (2009) · Inflammatory Bowel Diseases · doi:10.1002/ibd.20783 · Cited by 455
Modulation of the Intestinal Microbiota Alters Colitis-Associated Colorectal Cancer Susceptibility
Uronis, J. M., Mühlbauer, M., Herfarth, H. H., Rubinas, T. C., Jones, G. S., & Jobin, C. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006026 · Cited by 425
Molecular characterization of mucosal adherent bacteria and associations with colorectal adenomas
Shen, X. J., Rawls, J. F., Randall, T. A., Burcall, L., Mpande, C., Jenkins, N., Jovov, B., Abdo, Z., Sandler, R. S., & Keku, T. O. (2010) · Gut Microbes · doi:10.4161/gmic.1.3.12360 · Cited by 418
Innate immune mechanisms of colitis and colitis-associated colorectal cancer
Saleh, M., & Trinchieri, G. (2010) · Nature reviews. Immunology · doi:10.1038/nri2891 · Cited by 406
Imbalance in the composition of the duodenal microbiota of children with coeliac disease
Nadal, I., Donant, E., Ribes‐Koninckx, C., Calabuig, M., & Sanz, Y. (2007) · Journal of Medical Microbiology · doi:10.1099/jmm.0.47410-0 · Cited by 396
Treatment of Ulcerative Colitis Using Fecal Bacteriotherapy
Borody, T. J., Warren, E. F., Leis, S., Surace, R., & Ashman, O. (2003) · Journal of Clinical Gastroenterology · doi:10.1097/00004836-200307000-00012 · Cited by 388
Gastrointestinal microflora, food components and colon cancer prevention
Davis, C. D., & Milner, J. A. (2009) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2009.06.001 · Cited by 340
Scharlau, D., Borowicki, A., Habermann, N., Hofmann, T., Klenow, S., Miene, C., Munjal, U., Stein, K., & Glei, M. (2009) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2009.04.001 · Cited by 340
Bile acids as endogenous etiologic agents in gastrointestinal cancer
Bernstein, H., Bernstein, C., Payne, C. M., & Dvorak, K. (2009) · World Journal of Gastroenterology · doi:10.3748/wjg.15.3329 · Cited by 340
Ramadass, B., Rajendiran, E., George, S., Samuel, G. V., & Ramakrishna, B. (2008) · Journal of Gastroenterology and Hepatology · doi:10.1111/j.1440-1746.2008.05490.x · Cited by 307
Devillard, E., McIntosh, F. M., Duncan, S. H., & Wallace, R. J. (2007) · Journal of Bacteriology · doi:10.1128/jb.01359-06 · Cited by 285
Commensal Bacteria, Redox Stress, and Colorectal Cancer: Mechanisms and Models
Huycke, M. M., & Gaskins, H. R. (2004) · Experimental Biology and Medicine · doi:10.1177/153537020422900702 · Cited by 244
Promotion of intestinal carcinogenesis by Streptococcus bovis
Ellmerich, S., Scholler, M., Duranton, B., Gossé, F., Galluser, M., Klein, J.-P., & Raul, F. (2000) · Carcinogenesis · doi:10.1093/carcin/21.4.753 · Cited by 244
Dietary Fiber and Colorectal Cancer Risk: A Nested Case-Control Study Using Food Diaries
Dahm, C. C., Keogh, R. H., Spencer, E. A., Greenwood, D. C., Key, T. J., Fentiman, I. S., Shipley, M. J., Brunner, E. J., Cade, J. E., Burley, V. J., et al. (2010) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djq092 · Cited by 241
Biarc, J. (2004) · Carcinogenesis · doi:10.1093/carcin/bgh091 · Cited by 240
Waidmann, M., Bechtold, O., Frick, J.-S., Lehr, H.-A., Schubert, S., Dobrindt, U., Loeffler, J., Bohn, E., & Autenrieth, I. B. (2003) · Gastroenterology · doi:10.1016/s0016-5085(03)00672-3 · Cited by 234
Role of intestinal flora in the development of allergy
Kalliomäki, M. A., & Isolauri, E. (2003) · Current Opinion in Allergy and Clinical Immunology · doi:10.1097/00130832-200302000-00003 · Cited by 211
Louis, P., & Flint, H. J. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.02561-06 · Cited by 192
Rose, D. J., DeMeo, M. T., Keshavarzian, A., & Hamaker, B. R. (2008) · Nutrition Reviews · doi:10.1111/j.1753-4887.2007.tb00282.x · Cited by 181
Microbial and viral pathogens in colorectal cancer
Collins, D., Hogan, A. M., & Winter, D. C. (2010) · The Lancet Oncology · doi:10.1016/s1470-2045(10)70186-8 · Cited by 172
Palombo, J. D., Ganguly, A., Bistrian, B. R., & Menard, M. P. (2002) · Cancer Letters · doi:10.1016/s0304-3835(01)00796-0 · Cited by 168
Why Do African Americans Get More Colon Cancer than Native Africans?
O’Keefe, S. J., Chung, D., Mahmoud, N., Sepulveda, A. R., Manafe, M., Arch, J. E., Adada, H., & van der Merwe, T. (2007) · Journal of Nutrition · doi:10.1093/jn/137.1.175s · Cited by 167
Maddocks, O. D. K., Short, A., Donnenberg, M. S., Bader, S. A., & Harrison, D. J. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005517 · Cited by 150
Vlieg, J. E. V. H., Veiga, P., Zhang, C., Derrien, M., & Zhao, L. (2011) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2010.12.004 · Cited by 136
Self-citationScanlan, P. D., Shanahan, F., & Marchesi, J. R. (2009) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2009.00709.x · Cited by 124
Huycke, M. M., & Moore, D. R. (2002) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(02)00977-2 · Cited by 106
Diet and colorectal cancer prevention
Bingham, S. A. (2000) · Biochemical Society Transactions · doi:10.1042/bst0280012 · Cited by 104
Loss of heterozygosity and tumor suppressor activity ofBin1 in prostate carcinoma
Ge, K., Minhas, F., DuHadaway, J. B., Mao, N.-C., Wilson, D. M., Buccafusca, R., Sakamuro, D., Nelson, P. S., Malkowicz, S. B., Tomaszewski, J., et al. (2000) · International Journal of Cancer · doi:10.1002/(sici)1097-0215(20000415)86:2 · Cited by 96
Association between Fecal Bile Acids and Colorectal Cancer: A Meta-analysis of Observational Studies
Tong, J. L., Ran, Z. H., Shen, J., Fan, G. Q., & Shu Dong, X. I. A. O. (2008) · Yonsei Medical Journal · doi:10.3349/ymj.2008.49.5.792 · Cited by 68
Wei, H., Dong, L., Wang, T., Zhang, M. H., Hua, W., Zhang, C., Pang, X., Chen, M., Su, M., Qiu, Y., et al. (2010) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2010.00924.x · Cited by 57
Self-citationZhang, M., Zhang, C., Zhang, C., Du, H., Wei, G., Pang, X., Zhou, H., Liu, B., & Zhao, L. (2009) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2009.00694.x · Cited by 38
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Koh, A., De Vadder, F., Kovatcheva-Datchary, P., & Bäckhed, F. (2016) · Cell · doi:10.1016/j.cell.2016.05.041 · Cited by 7,070
A metagenome-wide association study of gut microbiota in type 2 diabetes
Qin, J., Li, Y., Cai, Z., Li, S., Zhu, J., Zhang, F., Liang, S., Zhang, W., Guan, Y., Shen, D., et al. (2012) · Nature · doi:10.1038/nature11450 · Cited by 6,762
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Louis, P., Hold, G. L., & Flint, H. J. (2014) · Nature Reviews Microbiology · doi:10.1038/nrmicro3344 · Cited by 2,925
Yarza, P., Yilmaz, P., Pruesse, E., Glöckner, F. O., Ludwig, W., SCHLEIFER, K. H., Whitman, W. B., Euzéby, J. P., Amann, R., & Rossello-Mora, R. A. (2014) · Nature Reviews Microbiology · doi:10.1038/nrmicro3330 · Cited by 2,651
Metadata
- Authors
- Wang, T., Cai, G., Qiu, Y., Fei, N., Zhang, M., Pang, X., Jia, W., Cai, S., & Zhao, L.
- Affiliations
- Shanghai Jiao Tong University (CN)
- Shanghai Medical College of Fudan University (CN)
- University of North Carolina at Greensboro (US)
- Corresponding author
- Zhao, Liping
- ORCID
- Venue
- The ISME Journal
- Publisher
- Oxford University Press (OUP)
- Published
- 2011-08-18
- Volume
- 6
- Issue
- 2
- Pages
- 320-329
- ISSN
- 1751-7362 (ISSN-L)
- 1751-7370
- PMC
- PMC3260502
- OpenAlex
- W2015567271
- Cited by
- 1,287
- References
- 65
- Citations by year
- 2026: 49 · 2025: 80 · 2024: 126 · 2023: 118 · 2022: 139 · 2021: 155 · 2020: 134 · 2019: 106 · 2018: 101 · 2017: 80 · 2016: 53 · 2015: 46 · 2014: 38 · 2013: 39 · 2012: 19
- FWCI
- 12.71
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The ISME Journal (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Natural Science Foundation of China (30730005)
- National Science and Technology Major Project
- National Key Research and Development Program of China
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Infectious Diseases › Clostridium difficile and Clostridium perfringens research
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Keywords
- colorectal cancer, gut microbiota, microbial community structure, Bacteroides fragilis, Bacteroides vulgatus, Bacteroides uniformis, butyrate-producing bacteria, Lachnospiraceae, Roseburia, opportunistic pathogens, Enterococcus, Escherichia-Shigella, Klebsiella, Streptococcus, Peptostreptococcus, dysbiosis
- MeSH terms
- Acyl Coenzyme A, Adult, Aged, Bacteria, Feces, Female, Humans, Male, Middle Aged, RNA, Ribosomal, 16S, Colorectal Neoplasms, Reproducibility of Results, Coenzyme A-Transferases, Bacterial Physiological Phenomena, Principal Component Analysis, Gastrointestinal Tract, Biodiversity, Metagenome
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