Quantitation of faecal Fusobacterium improves faecal immunochemical test in detecting advanced colorectal neoplasia
Open accessAbstract
Objective There is a need for an improved biomarker for colorectal cancer (CRC) and advanced adenoma. We evaluated faecal microbial markers for clinical use in detecting CRC and advanced adenoma. Design We measured relative abundance of Fusobacterium nucleatum (Fn), Peptostreptococcus anaerobius (Pa) and Parvimonas micra (Pm) by quantitative PCR in 309 subjects, including 104 patients with CRC, 103 patients with advanced adenoma and 102 controls. We evaluated the diagnostic performance of these biomarkers with respect to faecal immunochemical test (FIT), and validated the results in an independent cohort of 181 subjects. Results The abundance was higher for all three individual markers in patients with CRC than controls (p<0.001), and for marker Fn in patients with advanced adenoma than controls (p=0.022). The marker Fn, when combined with FIT, showed superior sensitivity (92.3% vs 73.1%, p<0.001) and area under the receiver-operating characteristic curve (AUC) (0.95 vs 0.86, p<0.001) than stand-alone FIT in detecting CRC in the same patient cohort. This combined test also increased the sensitivity (38.6% vs 15.5%, p<0.001) and AUC (0.65 vs 0.57, p=0.007) for detecting advanced adenoma. The performance gain for both CRC and advanced adenoma was confirmed in the validation cohort (p=0.0014 and p=0.031, respectively). Conclusions This study identified marker Fn as a valuable marker to improve diagnostic performance of FIT, providing a complementary role to detect lesions missed by FIT alone. This simple approach may improve the clinical utility of the current FIT, and takes one step further towards a non-invasive, potentially more accurate and affordable diagnosis of advanced colorectal neoplasia.
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Adding stool microbiome data to risk-factor model scores or to screening tests like FOBT and FIT improves detection accuracy for advanced adenomas.
“Combining the fecal microbiome data with scores from risk factor-based models or results of screening tests (such as fecal occult blood test and fecal immunochemical test) increases the accuracy of detection for advanced adenomas.35, 186, 187”
From Influence of the Gut Microbiome, Diet, and Environment on Risk of Colorectal Cancer (2020) · cites this paper as [186]
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Cites
Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008
Ferlay, J., Shin, H., Bray, F., Forman, D., Mathers, C. D., & Parkin, D. M. (2010) · International Journal of Cancer · doi:10.1002/ijc.25516 · Cited by 21,271 · see citing works
Kostic, A. D., Chun, E., Robertson, L., Glickman, J. N., Gallini, C. A., Michaud, M., Clancy, T. E., Chung, D. C., Lochhead, P., Hold, G. L., et al. (2013) · Cell Host & Microbe · doi:10.1016/j.chom.2013.07.007 · Cited by 2,718 · see citing works
Rubinstein, M. R., Wang, X., Liu, W., Hao, Y., Cai, G., & Han, Y. W. (2013) · Cell Host & Microbe · doi:10.1016/j.chom.2013.07.012 · Cited by 2,476 · see citing works
<i>Fusobacterium nucleatum</i> infection is prevalent in human colorectal carcinoma
Castellarin, M., Warren, R. L., Freeman, J. D., Dreolini, L., Krzywinski, M., Strauss, J., Barnes, R., Watson, P., Allen-Vercoe, E., Moore, R. A., et al. (2012) · Genome Research · doi:10.1101/gr.126516.111 · Cited by 2,043 · see citing works
Multitarget Stool DNA Testing for Colorectal-Cancer Screening
Imperiale, T. F., Ransohoff, D. F., Itzkowitz, S. H., Levin, T. R., Lavin, P., Lidgard, G. P., Ahlquist, D. A., & Berger, B. M. (2014) · New England Journal of Medicine · doi:10.1056/nejmoa1311194 · Cited by 1,900 · see citing works
Quality indicators for colonoscopy
Rex, D. K., Schoenfeld, P. S., Cohen, J., Pike, I. M., Adler, D. G., Fennerty, M. B., Lieb, J. G., Park, W. G., Rizk, M. K., Sawhney, M. S., et al. (2015) · Gastrointestinal Endoscopy · doi:10.1016/j.gie.2014.07.058 · Cited by 1,764 · see citing works
Atkin, W. S., Edwards, R., Kralj‐Hans, I., Wooldrage, K., Hart, A. R., Northover, J. M. A., Parkin, D. M., Wardle, J., Duffy, S. W., & Cuzick, J. M. (2010) · The Lancet · doi:10.1016/s0140-6736(10)60551-x · Cited by 1,618 · see citing works
Gut microbiome development along the colorectal adenoma-carcinoma sequence
Feng, Q., Liang, S., Jia, H., Stadlmayr, A., Tang, L., Lan, Z., Zhang, D., Xia, H., Xu, X., Jie, Z., et al. (2015) · Nature Communications · doi:10.1038/ncomms7528 · Cited by 1,506 · see citing works
American College of Gastroenterology Guidelines for Colorectal Cancer Screening 2008
Rex, D. K., Johnson, D. A., Anderson, J. C., Schoenfeld, P. S., Burke, C. A., & Inadomi, J. M. (2009) · The American Journal of Gastroenterology · doi:10.1038/ajg.2009.104 · Cited by 1,397 · see citing works
Potential of fecal microbiota for early-stage detection of colorectal cancer
Zeller, G., Tap, J., Voigt, A. Y., Sunagawa, S., Kultima, J. R., Costea, P. I., Amiot, A., Böhm, J., Brunetti, F., Habermann, N., et al. (2014) · Molecular Systems Biology · doi:10.15252/msb.20145645 · Cited by 1,375 · see citing works
Yu, J. Q., Feng, Q., Wong, S. H., Zhang, D., Liang, Q. Y., Qin, Y., Tang, L., Zhao, H., Stenvang, J., Li, Y., et al. (2015) · Gut · doi:10.1136/gutjnl-2015-309800 · Cited by 1,247 · see citing works
Self-citation<i>Fusobacterium nucleatum</i> in colorectal carcinoma tissue and patient prognosis
Mima, K., Nishihara, R., Qian, Z. R., Cao, Y., Sukawa, Y., Nowak, J. A., Yang, J., Dou, R., Masugi, Y., Song, M., et al. (2016) · Gut · doi:10.1136/gutjnl-2015-310101 · Cited by 1,080 · see citing works
Colorectal-Cancer Incidence and Mortality with Screening Flexible Sigmoidoscopy
Schoen, R. E., Pinsky, P. F., Weissfeld, J. L., Yokochi, L. A., Church, T. R., Laiyemo, A. O., Bresalier, R. S., Andriole, G. L., Buys, S. S., Crawford, E. D., et al. (2012) · New England Journal of Medicine · doi:10.1056/nejmoa1114635 · Cited by 1,014 · see citing works
Abed, J., Emgård, J. E. M., Zamir, G., Faroja, M., Almogy, G., Grenov, A., Sol, A., Naor, R., Pikarsky, E., Atlan, K. A., et al. (2016) · Cell Host & Microbe · doi:10.1016/j.chom.2016.07.006 · Cited by 888 · see citing works
Increasing incidence of colorectal cancer in Asia: implications for screening
Sung, J. J. �., Lau, J., Goh, K., & Leung, W. K. (2005) · The Lancet Oncology · doi:10.1016/s1470-2045(05)70422-8 · Cited by 740 · see citing works
Self-citationAccuracy of Fecal Immunochemical Tests for Colorectal Cancer
Lee, J. K., Liles, E. G., Bent, S., Levin, T. R., & Corley, D. A. (2014) · Annals of Internal Medicine · doi:10.7326/m13-1484 · Cited by 707 · see citing works
Gut mucosal microbiome across stages of colorectal carcinogenesis
Nakatsu, G., Li, X., Zhou, H., Sheng, J., Wong, S. H., Wu, W. K. K., Ng, S. C., Tsoi, H., Dong, Y., Zhang, N., et al. (2015) · Nature Communications · doi:10.1038/ncomms9727 · Cited by 701 · see citing works
Self-citationThe human gut microbiome as a screening tool for colorectal cancer
Zackular, J. P., Rogers, M. A. M., Ruffin, M. T., & Schloss, P. D. (2014) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-14-0129 · Cited by 551 · see citing works
Fusobacterium Is Associated with Colorectal Adenomas
McCoy, A. N., Araújo-Pérez, F., Azcárate-Peril, M. A., Yeh, J. J., Sandler, R. S., & Keku, T. O. (2013) · PLoS ONE · doi:10.1371/journal.pone.0053653 · Cited by 516 · see citing works
Quality indicators for colonoscopy
Rex, D. K., Petrini, J. L., Baron, T. H., Chak, A., Cohen, J., Deal, S. E., Hoffman, B. J., Jacobson, B. C., Mergener, K., Petersen, B. T., et al. (2006) · Gastrointestinal Endoscopy · doi:10.1016/j.gie.2006.02.021 · Cited by 494 · see citing works
An updated Asia Pacific Consensus Recommendations on colorectal cancer screening
Sung, J. J. �., Ng, S. C., Chan, F. K. L., Chiu, H., Kim, H. S., Matsuda, T., Ng, S. S. M., Lau, J. Y. W., Zheng, S. S., Adler, S. N., et al. (2014) · Gut · doi:10.1136/gutjnl-2013-306503 · Cited by 406 · see citing works
Self-citationBaxter, N. T., Ruffin, M. T., Rogers, M. A. M., & Schloss, P. D. (2016) · Genome Medicine · doi:10.1186/s13073-016-0290-3 · Cited by 354 · see citing works
Comparative Evaluation of Immunochemical Fecal Occult Blood Tests for Colorectal Adenoma Detection
Hundt, S., Haug, U., & Brenner, H. (2009) · Annals of Internal Medicine · doi:10.7326/0003-4819-150-3-200902030-00005 · Cited by 330 · see citing works
Sung, J. J. �., Chan, F. K. L., Leung, W. K., Wu, J. C., Lau, J. Y. W., Ching, J. Y. L., To, K. F., Lee, Y. T., Luk, Y. W., Kung, N. N. S., et al. (2003) · Gastroenterology · doi:10.1053/gast.2003.50090 · Cited by 166 · see citing works
Self-citationLadabaum, U., & Mannalithara, A. (2016) · Gastroenterology · doi:10.1053/j.gastro.2016.06.003 · Cited by 165 · see citing works
Multitarget Stool DNA Testing for Colorectal-Cancer Screening
Brenner, H., Werner, S., & Chen, H. (2014) · New England Journal of Medicine · doi:10.1056/nejmc1405215 · Cited by 164 · see citing works
Wu, C. W., Ng, S. C., Dong, Y., Tian, L., Ng, S. S. M., Leung, W. W., Law, W. T., Yau, T. O., Chan, F. K. L., Sung, J. J. Y., et al. (2014) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-13-1750 · Cited by 119 · see citing works
Self-citationColorectal cancer screening in Asia
Ng, S. S. S., & Wong, S. (2013) · British Medical Bulletin · doi:10.1093/bmb/lds040 · Cited by 106 · see citing works
Self-citationHaug, U., Hundt, S., & Brenner, H. (2009) · The American Journal of Gastroenterology · doi:10.1038/ajg.2009.668 · Cited by 98 · see citing works
Combining biomarkers to detect disease with application to prostate cancer
Etzioni, R. (2003) · Biostatistics · doi:10.1093/biostatistics/4.4.523 · Cited by 95 · see citing works
Wong, M. C. S., Ching, J. Y. L., Chan, V. C. W., & Sung, J. J. �. (2015) · Scientific Reports · doi:10.1038/srep13568 · Cited by 44 · see citing works
Self-citationA standard for Faecal Immunochemical TesTs for Haemoglobin Evaluation Reporting (FITTER)
Fraser, C. G., Allison, J. E., Young, G. P., Halloran, S. P., & Seaman, H. E. (2013) · Annals of Clinical Biochemistry International Journal of Laboratory Medicine · doi:10.1177/0004563213514392 · Cited by 31 · see citing works
Logistic regression analysis with standardized markers
Huang, Y., PEPE, M. S., & Feng, Z. (2013) · The Annals of Applied Statistics · doi:10.1214/13-aoas634 · Cited by 10 · see citing works
Flagged first, then by citations
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Sorted by citations
Gut microbiota in colorectal cancer: mechanisms of action and clinical applications
Wong, S. H., & Yu, J. (2019) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-019-0209-8 · Cited by 1,355 · see citing works
Self-citationSawicki, T., Ruszkowska, M., Danielewicz, A., Niedźwiedzka, E., Arłukowicz, T., & Przybyłowicz, K. E. (2021) · Cancers · doi:10.3390/cancers13092025 · Cited by 1,017 · see citing works
Influence of the Gut Microbiome, Diet, and Environment on Risk of Colorectal Cancer
Song, M., Chan, A. T., & Sun, J. (2020) · Gastroenterology · doi:10.1053/j.gastro.2019.06.048 · Cited by 752 · see citing works
Gut microbiota in colorectal cancer development and therapy
Wong, C. C., & Yu, J. (2023) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-023-00766-x · Cited by 751 · see citing works
Self-citationThe Intestinal Microbiota and Colorectal Cancer
Cheng, Y., Ling, Z., & Li, L. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.615056 · Cited by 588 · see citing works
Dai, Z., Coker, O. O., Nakatsu, G., Wu, W. K. K., Zhao, L., Chen, Z., Chan, F. K. L., Kristiansen, K., Sung, J. J. Y., Wong, S. H., et al. (2018) · Microbiome · doi:10.1186/s40168-018-0451-2 · Cited by 545 · see citing works
Self-citationTumor initiation and early tumorigenesis: molecular mechanisms and interventional targets
Zhang, S., Xiao, X., Yi, Y., Wang, X., Zhu, L., Shen, Y., Lin, D., & Wu, C. H. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01848-7 · Cited by 440 · see citing works
Fusobacterium nucleatum, a key pathogenic factor and microbial biomarker for colorectal cancer
Wang, N., & Fang, J. (2022) · Trends in Microbiology · doi:10.1016/j.tim.2022.08.010 · Cited by 395 · see citing works
Alterations in Enteric Virome Are Associated With Colorectal Cancer and Survival Outcomes
Nakatsu, G., Zhou, H., Wu, W. K. K., Wong, S. H., Coker, O. O., Dai, Z., Li, X., Szeto, C.-H., Sugimura, N., Lam, T. Y.-T., et al. (2018) · Gastroenterology · doi:10.1053/j.gastro.2018.04.018 · Cited by 386 · see citing works
Self-citationThe role of gut microbiota in cancer treatment: friend or foe?
Cheng, W. Y., Wu, C.-Y., & Yu, J. (2020) · Gut · doi:10.1136/gutjnl-2020-321153 · Cited by 384 · see citing works
Self-citationHibberd, A. A., Lyra, A., Ouwehand, A. C., Rolny, P., Lindegren, H., Cedgård, L., & Wettergren, Y. (2017) · BMJ Open Gastroenterology · doi:10.1136/bmjgast-2017-000145 · Cited by 373 · see citing works
Microbiome and colorectal cancer: Roles in carcinogenesis and clinical potential
Saus, E., Iraola‐Guzmán, S., Willis, J. R., Brunet‐Vega, A., & Gabaldón, T. (2019) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2019.05.001 · Cited by 348 · see citing works
Liang, Q., Li, T., Nakatsu, G., Chen, Y., Yau, T. O., Chu, E. S., Wong, S. H., Szeto, C. H., Ng, S. C., Chan, F. K. L., et al. (2019) · Gut · doi:10.1136/gutjnl-2019-318532 · Cited by 344 · see citing works
Self-citationFecal microbiota transplantation in cancer management: Current status and perspectives
Chen, D., Wu, J., Jin, D., Wang, B., & Cao, H. (2018) · International Journal of Cancer · doi:10.1002/ijc.32003 · Cited by 330 · see citing works
Self-citationRole of the Gut Microbiota and Its Metabolites in Tumorigenesis or Development of Colorectal Cancer
Qu, R., Zhang, Y., Ma, Y., Zhou, X., Sun, L., Jiang, C., Zhang, Z., & Fu, W. (2023) · Advanced Science · doi:10.1002/advs.202205563 · Cited by 303 · see citing works
Association Between Bacteremia From Specific Microbes and Subsequent Diagnosis of Colorectal Cancer
Kwong, T. N. Y., Wang, X., Nakatsu, G., Chow, T. C., Tipoe, T., Dai, R. Z. W., Tsoi, K. K. K., Wong, M. C. S., Tse, G., Chan, M. T. V., et al. (2018) · Gastroenterology · doi:10.1053/j.gastro.2018.04.028 · Cited by 280 · see citing works
Self-citationTopçuoğlu, B. D., Lesniak, N. A., Ruffin, M. T., Wiens, J., & Schloss, P. D. (2020) · mBio · doi:10.1128/mbio.00434-20 · Cited by 278 · see citing works
Hsieh, Y.-Y., Tung, S.-Y., Pan, H.-Y., Yen, C.-W., Xu, H.-W., Lin, Y.-J., Deng, Y.-F., Hsu, W.-T., Wu, C.-S., & Li, C. (2018) · Scientific Reports · doi:10.1038/s41598-017-18596-0 · Cited by 269 · see citing works
Machine learning for microbiologists
Asnicar, F., Thomas, A. M., Passerini, A., Waldron, L., & Segata, N. (2023) · Nature Reviews Microbiology · doi:10.1038/s41579-023-00984-1 · Cited by 269 · see citing works
<i>Fusobacterium nucleatum</i>and colorectal cancer: A review
Shang, F.-M., & Liu, H.-L. (2018) · World Journal of Gastrointestinal Oncology · doi:10.4251/wjgo.v10.i3.71 · Cited by 258 · see citing works
Coker, O. O., Liu, C., Wu, W. K. K., Wong, S. H., Jia, W. P., Sung, J. J. �., & Yu, J. Q. (2022) · Microbiome · doi:10.1186/s40168-021-01208-5 · Cited by 259 · see citing works
Self-citationMicrobiome in Colorectal Cancer: How to Get from Meta-omics to Mechanism?
Ternes, D., Karta, J., Tsenkova, M., Wilmes, P., Haan, S., & Letellier, E. (2020) · Trends in Microbiology · doi:10.1016/j.tim.2020.01.001 · Cited by 256 · see citing works
Novel Diagnostic Biomarkers in Colorectal Cancer
Zygulska, A. L., & Pierzchalski, P. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23020852 · Cited by 253 · see citing works
Fusobacterium nucleatum promotes colorectal cancer metastasis by modulating KRT7-AS /KRT7
Chen, S., Su, T., Zhang, Y., Lee, A. A., He, J., Ge, Q., Wang, L., Si, J., Zhuo, W., & Wang, L. (2020) · Gut Microbes · doi:10.1080/19490976.2019.1695494 · Cited by 232 · see citing works
Cancer‐associated fecal microbial markers in colorectal cancer detection
Eklöf, V., Löfgren‐Burström, A., Zingmark, C., Edin, S., Larsson, P. G., Karling, P., Alexeyev, O. A., Rutegård, M., Wikberg, M. L., & Palmqvist, R. (2017) · International Journal of Cancer · doi:10.1002/ijc.31011 · Cited by 209 · see citing works
Fusobacterium nucleatum and cancer
Alon‐Maimon, T., Mandelboim, O., & Bachrach, G. (2022) · Periodontology 2000 · doi:10.1111/prd.12426 · Cited by 200 · see citing works
Xie, Y., Gao, Q., Cai, G. X., Sun, X. M., Zou, T.-H., Chen, H. M., Yu, S.-Y., Qiu, Y.-W., Gu, W.-Q., Chen, X. Y., et al. (2017) · EBioMedicine · doi:10.1016/j.ebiom.2017.10.005 · Cited by 192 · see citing works
Osman, M. A., Neoh, H., Mutalib, N. A., Chin, S., Mazlan, L., Ali, R. A. R., Zakaria, A. D., Ngiu, C. S., Ang, M. Y., & Jamal, R. (2021) · Scientific Reports · doi:10.1038/s41598-021-82465-0 · Cited by 185 · see citing works
Hong, M., Li, Z., Liu, H., Zheng, S., Zhang, F., Zhu, J., Shi, H., Ye, H., Chou, Z., Gao, L., et al. (2023) · Cell Host & Microbe · doi:10.1016/j.chom.2023.03.018 · Cited by 180 · see citing works
Guo, S., Li, L., Xu, B., Mang-hui, L., Zeng, Q., Han, X., Ying, X., Wu, Y., Wang, Y., Liu, W., et al. (2018) · Clinical Chemistry · doi:10.1373/clinchem.2018.289728 · Cited by 171 · see citing works
Gut Microbiota in Colorectal Cancer: Biological Role and Therapeutic Opportunities
Pandey, H., Tang, D. W. T., Wong, S. H., & Lal, D. (2023) · Cancers · doi:10.3390/cancers15030866 · Cited by 165 · see citing works
Self-citationSun, Y., Zhang, X., Hang, D., Lau, H. C.-H., Du, J., Liu, C., Xie, M., Pan, Y., Wang, L., Liang, C., et al. (2024) · Cancer Cell · doi:10.1016/j.ccell.2024.07.005 · Cited by 164 · see citing works
Self-citationFan, Z., Tang, P., Li, C., Yang, Q., Xu, Y., Su, C., & Li, L. (2023) · Journal of Oral Microbiology · doi:10.1080/20002297.2022.2145729 · Cited by 150 · see citing works
Role of gut microbiota in the pathogenesis of colorectal cancer; a review article.
Sherafat, S. J., Alebouyeh, M., Moghim, S., Amoli, H. A., & Ghasemian-Safaei, H. (2018) · Gastroenterology and hepatology from bed to bench. · doi:10.22037/ghfbb.v0i0.1052 · Cited by 147 · see citing works
Bacteriophages and their potential for treatment of gastrointestinal diseases
Duan, Y., Young, R., & Schnabl, B. (2021) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-021-00536-z · Cited by 143 · see citing works
Zhao, L., Zhang, X., Zhou, Y., Fu, K., Lau, H. C.-H., Chun, T. W.-Y., Cheung, A. H. K., Coker, O. O., Wei, H., Wu, W. K. K., et al. (2022) · Oncogene · doi:10.1038/s41388-022-02395-7 · Cited by 142 · see citing works
Self-citationMicrobial markers in colorectal cancer detection and/or prognosis
Villéger, R., Lopès, A., Véziant, J., Gagnière, J., Barnich, N., Billard, E., Boucher, D., & Bonnet, M. (2018) · World Journal of Gastroenterology · doi:10.3748/wjg.v24.i22.2327 · Cited by 139 · see citing works
Fusobacterium and Colorectal Cancer
Zhou, Z., Chen, J., Yao, H., & Hu, H. (2018) · Frontiers in Oncology · doi:10.3389/fonc.2018.00371 · Cited by 137 · see citing works
Gethings-Behncke, C., Coleman, H. G., Jordão, H. W. T., Longley, D. B., Crawford, N., Murray, L., & Kunzmann, A. T. (2020) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-18-1295 · Cited by 137 · see citing works
Biomarkers for detecting colorectal cancer non-invasively: DNA, RNA or proteins?
Loktionov, A. S. (2020) · World Journal of Gastrointestinal Oncology · doi:10.4251/wjgo.v12.i2.124 · Cited by 129 · see citing works
Wang, S., Liu, Y., Li, J., Zhao, L., Yan, W., Lin, B., Guo, X., & Wei, Y. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.710165 · Cited by 126 · see citing works
Role of Gut Microbiota in the Development and Treatment of Colorectal Cancer
Lin, C., Cai, X., Zhang, J., Wang, W., Sheng, Q., Hua, H., & Zhou, X. (2018) · Digestion · doi:10.1159/000494052 · Cited by 121 · see citing works
Mucosa-associated microbiota signature in colorectal cancer
Gao, R., Kong, C., Huang, L., Li, H., Qu, X., Liu, Z., Lan, P., Wang, J., & Qin, H. (2017) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-017-3026-4 · Cited by 120 · see citing works
Zhou, C., Pan, S., Jin, P., Deng, J., Xue, J., Ma, X., Xie, Y., Cao, H., Liu, Q., Xie, W., et al. (2021) · Gastroenterology · doi:10.1053/j.gastro.2022.02.015 · Cited by 116 · see citing works
Tumorigenic bacteria in colorectal cancer: mechanisms and treatments
Li, S., Liu, J., Zheng, X., Ren, L., Yang, Y., Li, W., Fu, W., Wang, J., & Du, G. (2021) · Cancer Biology and Medicine · doi:10.20892/j.issn.2095-3941.2020.0651 · Cited by 115 · see citing works
Yan, X., Liu, L., Li, H., Qin, H., & Sun, Z. (2017) · OncoTargets and Therapy · doi:10.2147/ott.s145949 · Cited by 110 · see citing works
Non-Invasive Colorectal Cancer Screening: An Overview
Tepus, M., & Yau, T. O. (2020) · Gastrointestinal Tumors · doi:10.1159/000507701 · Cited by 110 · see citing works
Niedermaier, T., Balavarca, Y., & Brenner, H. (2019) · The American Journal of Gastroenterology · doi:10.14309/ajg.0000000000000465 · Cited by 109 · see citing works
Clinical applications of gut microbiota in cancer biology
Wong, S. H., Kwong, T. N. Y., Wu, C., & Yu, J. Q. (2018) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2018.05.003 · Cited by 100 · see citing works
Self-citationGut Microbiome in Colorectal Cancer: Clinical Diagnosis and Treatment
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Self-citationDong, J., Li, Y., Xiao, H., Zhang, S., Wang, B., Wang, H., Li, Y., Fan, S., & Cui, M. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109886 · Cited by 95 · see citing works
Parvimonas micra as a putative non-invasive faecal biomarker for colorectal cancer
Löwenmark, T., Löfgren‐Burström, A., Zingmark, C., Eklöf, V., Dahlberg, M. L., Wai, S. N., Larsson, P. G., Ljuslinder, I., Edin, S., & Palmqvist, R. (2020) · Scientific Reports · doi:10.1038/s41598-020-72132-1 · Cited by 94 · see citing works
Cruz, B. C. D. S., da Conceição, L. L., Mendes, T. A. D. O., Ferreira, C. L. D. L. F., Gonçalves, R. V., & Pelúzio, M. D. C. G. (2020) · Food Research International · doi:10.1016/j.foodres.2020.109721 · Cited by 92 · see citing works
Lin, A., Xiong, M., Jiang, A., Huang, L., Wong, H. Z. H., Feng, S., Zhang, C., Yu, H., Chen, L., Chi, H., et al. (2025) · iMeta · doi:10.1002/imt2.70070 · Cited by 91 · see citing works
Self-citationChang, Y., Huang, Z., Hou, F., Liu, Y., Wang, L., Wang, Z., Sun, Y., Pan, Z., Tan, Y., Ding, L., et al. (2023) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-022-02572-2 · Cited by 89 · see citing works
The Role of Microbiota in Gastrointestinal Cancer and Cancer Treatment: Chance or Curse?
Smet, A., Kupčinskas, J., Link, A., Hold, G. L., & Bornschein, J. (2021) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2021.08.013 · Cited by 86 · see citing works
Advances in tests for colorectal cancer screening and diagnosis
Chan, S. C. H., & Liang, Q. (2022) · Expert Review of Molecular Diagnostics · doi:10.1080/14737159.2022.2065197 · Cited by 85 · see citing works
Opportunistic detection of Fusobacterium nucleatum as a marker for the early gut microbial dysbiosis
Huh, J., & Roh, T. (2020) · BMC Microbiology · doi:10.1186/s12866-020-01887-4 · Cited by 78 · see citing works
Ai, L., Tian, H., Chen, Z., Chen, H., Xu, J., & Fang, J. (2017) · Oncotarget · doi:10.18632/oncotarget.14488 · Cited by 78 · see citing works
Ullah, I., Yang, L., Yin, F., Sun, Y., Li, X., Li, J., & Wang, X. (2022) · Cancers · doi:10.3390/cancers14225545 · Cited by 76 · see citing works
Yamamoto, H., & Imai, K. (2019) · Seminars in Oncology · doi:10.1053/j.seminoncol.2019.08.003 · Cited by 74 · see citing works
From taxonomy to metabolic output: what factors define gut microbiome health?
Wilmanski, T., Rappaport, N., Diener, C., Gibbons, S. M., & Price, N. D. (2021) · Gut Microbes · doi:10.1080/19490976.2021.1907270 · Cited by 73 · see citing works
Association between Fusobacterium nucleatum and colorectal cancer: Progress and future directions
Zhang, S., Cai, S., & Ma, Y. (2018) · Journal of Cancer · doi:10.7150/jca.24048 · Cited by 73 · see citing works
Yang, J., Li, D., Yang, Z., Dai, W., Feng, X., Liu, Y., Jiang, Y., Li, P., Li, Y., Tang, B., et al. (2020) · Gut Microbes · doi:10.1080/19490976.2020.1712986 · Cited by 73 · see citing works
Self-citationFusobacterium’s link to colorectal neoplasia sequenced: A systematic review and future insights
Hussan, H., Clinton, S. K., Roberts, K., & Bailey, M. T. (2017) · World Journal of Gastroenterology · doi:10.3748/wjg.v23.i48.8626 · Cited by 73 · see citing works
Saber, S., El-Fattah, E. E. A., Yahya, G., Gobba, N. A., Maghmomeh, A. O., Khodir, A. E., Mourad, A. A. E., Saad, A. S., Mohammed, H. G., Nouh, N. A. T., et al. (2021) · Pharmaceuticals · doi:10.3390/ph14040341 · Cited by 72 · see citing works
Véziant, J., Villéger, R., Barnich, N., & Bonnet, M. (2021) · Cancers · doi:10.3390/cancers13092215 · Cited by 72 · see citing works
Gut microbiota as a new target for anticancer therapy: from mechanism to means of regulation
Sun, J., Song, S., Liu, J., Chen, F., Li, X., & Wu, G. (2025) · npj Biofilms and Microbiomes · doi:10.1038/s41522-025-00678-x · Cited by 72 · see citing works
Kasper, S. H., Morell-Perez, C., Wyche, T. P., Sana, T. R., Lieberman, L. A., & Hett, E. C. (2020) · Scientific Reports · doi:10.1038/s41598-020-62139-z · Cited by 69 · see citing works
Role of gut microbiota in epigenetic regulation of colorectal Cancer
Zhao, Y., Wang, C., & Goel, A. (2020) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2020.188490 · Cited by 68 · see citing works
Fusobacterium nucleatum: ecology, pathogenesis and clinical implications
Jiang, S., Chen, Y., & Fang, J. (2025) · Nature Reviews Microbiology · doi:10.1038/s41579-025-01237-z · Cited by 70 · see citing works
Niedermaier, T., Tikk, K., Gies, A., Bieck, S., & Brenner, H. (2020) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2020.01.025 · Cited by 67 · see citing works
Zhang, X., Zhu, X., Cao, Y., Fang, J., Hong, J., & Chen, H. (2019) · Cancer Medicine · doi:10.1002/cam4.1850 · Cited by 63 · see citing works
de Carvalho, A. C., Pereira, L. D. M., Datorre, J. G., dos Santos, W., Berardinelli, G. N., Matsushita, M. D. M., de Oliveira, M. A., Durães, R. O., Guimarães, D. P., & Reis, R. M. (2019) · Frontiers in Oncology · doi:10.3389/fonc.2019.00813 · Cited by 63 · see citing works
El-Baz, A. M., Khodir, A. E., El‐Sokkary, M. M. A., & Shata, A. (2020) · Life Sciences · doi:10.1016/j.lfs.2020.117927 · Cited by 63 · see citing works
Pu, L. Z. C. T., Yamamoto, K., Honda, T., Nakamura, M., Yamamura, T., Hattori, S., Burt, A. D., Singh, R., Hirooka, Y., & Fujishiro, M. (2019) · Journal of Gastroenterology and Hepatology · doi:10.1111/jgh.14868 · Cited by 61 · see citing works
Faecal microbial biomarkers in early diagnosis of colorectal cancer
Olovo, C. V., Huang, X., Zheng, X., & Xu, M. (2021) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.17010 · Cited by 60 · see citing works
Global Investigations of Fusobacterium nucleatum in Human Colorectal Cancer
Lee, S. A., Liu, F., Riordan, S. M., Lee, C. S., & Zhang, L. (2019) · Frontiers in Oncology · doi:10.3389/fonc.2019.00566 · Cited by 59 · see citing works
Self-citationMicrobiome and colorectal carcinogenesis: Linked mechanisms and racial differences
Tortora, S. C., Bodiwala, V., Quinn, A., Martello, L. A., & Vignesh, S. (2022) · World Journal of Gastrointestinal Oncology · doi:10.4251/wjgo.v14.i2.375 · Cited by 58 · see citing works
Targeting Programmed Fusobacterium nucleatum Fap2 for Colorectal Cancer Therapy
Ganesan, K., Guo, S., Fayyaz, S., Zhang, G., & Xu, B. (2019) · Cancers · doi:10.3390/cancers11101592 · Cited by 58 · see citing works
Cancer-associated inflammation: pathophysiology and clinical significance
Pęczek, P., Gajda, M., Rutkowski, K., Fudalej, M. M., Deptała, A., & Badowska-Kozakiewicz, A. M. (2022) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-022-04399-y · Cited by 56 · see citing works
Emerging clinical relevance of microbiome in cancer: promising biomarkers and therapeutic targets
Dai, J.-H., Tan, X.-R., Qiao, H., & Liu, N. (2023) · Protein & Cell · doi:10.1093/procel/pwad052 · Cited by 56 · see citing works
Tunsjø, H. S., Gundersen, G., Rangnes, F., Noone, J. C., Endres, A., & Bemanian, V. (2019) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-019-03562-7 · Cited by 55 · see citing works
Liu, K., Yang, X., Zeng, M., Yuan, Y., Sun, J., He, P., Sun, J., Xie, Q., Chang, X., Zhang, S., et al. (2021) · Disease Markers · doi:10.1155/2021/1171239 · Cited by 54 · see citing works
Gao, R., Wang, Z., Li, H., Cao, Z., Gao, Z., Chen, H., Zhang, X., Pan, D., Yang, R., Zhong, H., et al. (2020) · Journal of Gastroenterology and Hepatology · doi:10.1111/jgh.15077 · Cited by 50 · see citing works
Huang, X., Hong, X., Wang, J., Sun, T., Yu, T., Yu, Y., Fang, J., & Xiong, H. (2020) · EBioMedicine · doi:10.1016/j.ebiom.2020.103037 · Cited by 50 · see citing works
Hsieh, Y., Tung, S., Pan, H.-Y., Chang, T., Wei, K., Chen, W., Deng, Y.-F., Lu, C.-K., Lai, Y., Wu, C., et al. (2021) · World Journal of Gastroenterology · doi:10.3748/wjg.v27.i42.7311 · Cited by 50 · see citing works
Mukherjee, S., Chopra, A., Karmakar, S., & Bhat, G. S. (2024) · Critical Reviews in Microbiology · doi:10.1080/1040841x.2024.2339260 · Cited by 49 · see citing works
Fang, C., Chen, J., Hsu, B., Hussain, B., Rathod, J., & Lee, K. (2021) · Microorganisms · doi:10.3390/microorganisms9081548 · Cited by 47 · see citing works
Lin, L., Shi, Y.-C., Choong, C.-Y., & Tai, C. (2021) · Molecules · doi:10.3390/molecules26134081 · Cited by 47 · see citing works
Liu, H., Yu, Y., Dong, A., Elsabahy, M., Yang, Y., & Gao, H. (2023) · Exploration · doi:10.1002/exp.20230092 · Cited by 46 · see citing works
Progress in characterizing the linkage between Fusobacterium nucleatum and gastrointestinal cancer
Liu, Y., Baba, Y., Ishimoto, T., Iwatsuki, M., Hiyoshi, Y., Miyamoto, Y., Yoshida, N., Wu, R., & Baba, H. (2018) · Journal of Gastroenterology · doi:10.1007/s00535-018-1512-9 · Cited by 47 · see citing works
The pathogenic oral–gut–liver axis: new understandings and clinical implications
Imai, J., Kitamoto, S., & Kamada, N. (2021) · Expert Review of Clinical Immunology · doi:10.1080/1744666x.2021.1935877 · Cited by 45 · see citing works
The gastrointestinal microbiota and its role in oncogenesis
Lam, S. Y., Yu, J. Q., Wong, S. H., Peppelenbosch, M. P., & Fuhler, G. M. (2017) · Best Practice & Research Clinical Gastroenterology · doi:10.1016/j.bpg.2017.09.010 · Cited by 45 · see citing works
Self-citationRole of the gut microbiota in tumorigenesis and treatment
Liu, Q., Yang, Y., Pan, M., Yang, F., Yu, Y., & Qian, Z. (2024) · Theranostics · doi:10.7150/thno.91700 · Cited by 43 · see citing works
Iadsee, N., Chuaypen, N., Techawiwattanaboon, T., Jinato, T., Patcharatrakul, T., Malakorn, S., Petchlorlian, A., Praditpornsilpa, K., & Patarakul, K. (2023) · Scientific Reports · doi:10.1038/s41598-023-33794-9 · Cited by 42 · see citing works
Oral Microbiota Alteration and Roles in Epstein-Barr Virus Reactivation in Nasopharyngeal Carcinoma
Liao, Y., Zhang, J., Lu, L., Jia, Y., Zheng, M., Debelius, J. W., He, Y., Wang, T., Deng, C., Tong, X., et al. (2023) · Microbiology Spectrum · doi:10.1128/spectrum.03448-22 · Cited by 41 · see citing works
Fellows, R. C., Chun, S. K., Larson, N., Fortin, B. M., Mahieu, A. L., Song, W. A., Seldin, M. M., Pannunzio, N. R., & Masri, S. (2024) · Science Advances · doi:10.1126/sciadv.ado1458 · Cited by 41 · see citing works
The Gut Microbiome and Colorectal Cancer: An Integrative Review of the Underlying Mechanisms
Karam, F., Deghel, Y. E., Iratni, R., Dakroub, A. H., & Eid, A. H. (2025) · Cell Biochemistry and Biophysics · doi:10.1007/s12013-025-01683-9 · Cited by 41 · see citing works
Alteration of the abundance of Parvimonas micra in the gut along the adenoma‑carcinoma sequence
Xu, J., Yang, M. H., Wang, D., Zhang, S., Yan, S., Zhu, Y., & Chen, W. (2020) · Oncology Letters · doi:10.3892/ol.2020.11967 · Cited by 41 · see citing works
- Authors
- Wong, S. H., Kwong, T. N. Y., Chow, T.-C., Luk, A. K. C., Dai, R. Z. W., Nakatsu, G., Lam, T. Y. T., Zhang, L., Wu, J. C. Y., Chan, F. K. L., Ng, S. S. M., Wong, M. C. S., Ng, S. C., Wu, W. K. K., Yu, J., & Sung, J. J. Y.
- Affiliations
- Chinese University of Hong Kong (HK)
- Corresponding author
- Sung, Joseph J Y
- ORCID
- Venue
- Gut
- Publisher
- BMJ
- Published
- 2016-10-24
- Volume
- 66
- Issue
- 8
- Pages
- 1441-1448
- ISSN
- 0017-5749 (ISSN-L)
- 1468-3288
- PMC
- PMC5530471
- OpenAlex
- W2537258608
- Cited by
- 310
- References
- 32
- Citations by year
- 2026: 28 · 2025: 32 · 2024: 41 · 2023: 40 · 2022: 40 · 2021: 36 · 2020: 34 · 2019: 22 · 2018: 24 · 2017: 13
- FWCI
- 10.61
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc
- Locations
- Gut (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- HighWire Press Open Archive (submittedVersion)
- Funders
- Croucher Foundation
- Shenzhen Virtual University Park
- National Key Research and Development Program of China (2013CB531401)
- Topics
- Health Sciences › Medicine › Oncology › Colorectal Cancer Screening and Detection
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Pathology and Forensic Medicine › Genetic factors in colorectal cancer
- Keywords
- Fusobacterium nucleatum, Peptostreptococcus anaerobius, Parvimonas micra, fecal immunochemical test, colorectal cancer, advanced adenoma, colorectal neoplasia detection, diagnostic sensitivity, non-invasive diagnosis
- MeSH terms
- Adenocarcinoma, Adenoma, DNA, Bacterial, Feces, Female, Humans, Male, Middle Aged, Occult Blood, Peptostreptococcus, ROC Curve, Biomarkers, Tumor, Colorectal Neoplasms, Fusobacterium nucleatum, Area Under Curve
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