Human colon mucosal biofilms from healthy or colon cancer hosts are carcinogenic
Open accessAbstract
Mucus-invasive bacterial biofilms are identified on the colon mucosa of approximately 50% of colorectal cancer (CRC) patients and approximately 13% of healthy subjects. Here, we test the hypothesis that human colon biofilms comprise microbial communities that are carcinogenic in CRC mouse models. Homogenates of human biofilm-positive colon mucosa were prepared from tumor patients (tumor and paired normal tissues from surgical resections) or biofilm-positive biopsies from healthy individuals undergoing screening colonoscopy; homogenates of biofilm-negative colon biopsies from healthy individuals undergoing screening colonoscopy served as controls. After 12 weeks, biofilm-positive, but not biofilm-negative, human colon mucosal homogenates induced colon tumor formation in 3 mouse colon tumor models (germ-free ApcMinΔ850/+;Il10-/- or ApcMinΔ850/+ and specific pathogen-free ApcMinΔ716/+ mice). Remarkably, biofilm-positive communities from healthy colonoscopy biopsies induced colon inflammation and tumors similarly to biofilm-positive tumor tissues. By 1 week, biofilm-positive human tumor homogenates, but not healthy biopsies, displayed consistent bacterial mucus invasion and biofilm formation in mouse colons. 16S rRNA gene sequencing and RNA-Seq analyses identified compositional and functional microbiota differences between mice colonized with biofilm-positive and biofilm-negative communities. These results suggest human colon mucosal biofilms, whether from tumor hosts or healthy individuals undergoing screening colonoscopy, are carcinogenic in murine models of CRC.
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Self-citationMicrobiota Effects on Carcinogenesis: Initiation, Promotion, and Progression
Lopez, L. R., Bleich, R. M., & Arthur, J. C. (2020) · Annual Review of Medicine · doi:10.1146/annurev-med-080719-091604 · Cited by 133 · 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
Microbiome or Infections: Amyloid-Containing Biofilms as a Trigger for Complex Human Diseases
Miller, A. L., Bessho, S., Grando, K. C. M., & Tükel, Ç. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.638867 · Cited by 131 · see citing works
“In contrast, inocula prepared from biofilm-negative mucosa did not (198).”
BackgroundHenn, M. R., O’Brien, E. J., Diao, L., Feagan, B. G., Sandborn, W. J., Huttenhower, C., Wortman, J. R., McGovern, B., Wang‐Weigand, S., Lichter, D. I., et al. (2020) · Gastroenterology · doi:10.1053/j.gastro.2020.07.048 · Cited by 119 · see citing works
“In addition, FMT carries risk of transmission of proinflammatory strains and potentially carcinogenic bacteria.(9,43) In contrast, SER-287 is a multifunctional consortia of bacterial spores purified under stringent manufacturing processes.”
BackgroundMontalban‐Arques, A., & Scharl, M. M. (2019) · EBioMedicine · doi:10.1016/j.ebiom.2019.09.050 · Cited by 118 · see citing works
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The Cancer Microbiome: Recent Highlights and Knowledge Gaps
Knippel, R. J., Drewes, J. L., & Sears, C. L. (2021) · Cancer Discovery · doi:10.1158/2159-8290.cd-21-0324 · Cited by 111 · see citing works
“In subsequent work, human colon biofilms were found to be directly tumorigenic in murine models (25).”
BackgroundSelf-citationCould Microplastics Be a Driver for Early Onset Colorectal Cancer?
Li, S., Keenan, J. I., Shaw, I. C., & Frizelle, F. (2023) · Cancers · doi:10.3390/cancers15133323 · Cited by 96 · see citing works
“The increased risk of biofilm-associated carcinogenesis [70] may reflect the close proximity a biofilm affords MPs to the intestinal epithelium.”
BackgroundInamura, K., Hamada, T., Bullman, S., Ugai, T., Yachida, S., & Ogino, S. (2022) · Gut · doi:10.1136/gutjnl-2022-327209 · Cited by 94 · see citing works
Bacterial biofilms in the human body: prevalence and impacts on health and disease
Perry, E. K., & Tan, M. (2023) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2023.1237164 · Cited by 95 · see citing works
“into the germ-free mice, suggesting that certain bacteria are inherently more capable of breaching the mucus barrier (Tomkovich et al., 2019).”
BackgroundResultInfluentialThe 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
Genetic and epigenetic dependencies in colorectal cancer development
Parmar, S., & Easwaran, H. (2022) · Gastroenterology report · doi:10.1093/gastro/goac035 · Cited by 86 · see citing works
Fidelle, M., Yonekura, S., Picard, M., Cogdill, A. P., Hollebecque, A., Roberti, M. P., & Zitvogel, L. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.600886 · Cited by 82 · see citing works
Shining a Light on Colibactin Biology
Dougherty, M. W., & Jobin, C. (2021) · Toxins · doi:10.3390/toxins13050346 · Cited by 80 · see citing works
“fi fro both normal and tumor tissue from CRC increase mucosal invasion by gut microbes a induce a higher tumo burden in murine models [60], suggesting some el ment of core b ofilm structure, a co monly distributed biofilm-associated species, or a combination of these factors, promotes carcinogenesis.”
BackgroundSelf-citation“Driver-passenger” bacteria and their metabolites in the pathogenesis of colorectal cancer
Avril, M., & DePaolo, R. W. (2021) · Gut Microbes · doi:10.1080/19490976.2021.1941710 · Cited by 78 · see citing works
Mycobiome and Cancer: What Is the Evidence?
Vallianou, N. G., Kounatidis, D. C., Christodoulatos, G. S., Panagopoulos, F., Karampela, Ι., & Dalamaga, Μ. (2021) · Cancers · doi:10.3390/cancers13133149 · Cited by 76 · see citing works
“The intestinal mucosal biofilm may be an inducing factor in colorectal carcinogenesis [64].”
BackgroundGut Microbiome: Profound Implications for Diet and Disease
Hills, R. D., Pontefract, B., Mishcon, H. R., Black, C. A., Sutton, S. C., & Theberge, C. R. (2022) · Kompass Nutrition & Dietetics · doi:10.1159/000523712 · Cited by 79 · see citing works
“Rather than a specific pathogen, a matrix-enclosed ecosystem of bacteria, or biofilm, extracted from tumor patients was found to induce tumorigenesis in mice [163].”
BackgroundThe Role of the Microbiome in the Etiopathogenesis of Colon Cancer
Tekle, G. E., Andreeva, N., & Garrett, W. S. (2024) · Annual Review of Physiology · doi:10.1146/annurev-physiol-042022-025619 · Cited by 75 · see citing works
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Host responses to mucosal biofilms in the lung and gut
Domingue, J. C., Drewes, J. L., Merlo, C. A., Housseau, F., & Sears, C. L. (2020) · Mucosal Immunology · doi:10.1038/s41385-020-0270-1 · Cited by 67 · see citing works
Self-citationSaftien, A., Puschhof, J., & Elinav, E. (2023) · Gut · doi:10.1136/gutjnl-2022-327952 · Cited by 67 · see citing works
Intestinal microbiota modulates pancreatic carcinogenesis through intratumoral natural killer cells
Qin, Y., Newsome, R. C., Beveridge, M. J., Hernandez, M. C., Gharaibeh, R. Z., Jobin, C., & Thomas, R. M. (2022) · Gut Microbes · doi:10.1080/19490976.2022.2112881 · Cited by 66 · see citing works
Self-citationGut mycobiome: A promising target for colorectal cancer
Qin, X., Gu, Y., Liu, T., Wang, C., Zhong, W., Wang, B., & Cao, H. (2020) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2020.188489 · Cited by 64 · see citing works
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Immunometabolism in biofilm infection: lessons from cancer
Mirzaei, R., Sabokroo, N., Ahmadyousefi, Y., Motamedi, H., & Karampoor, S. (2022) · Molecular Medicine · doi:10.1186/s10020-022-00435-2 · Cited by 59 · see citing works
Bautista, J., Maceiras, M. L., Hidalgo‐Tinoco, C., Guerra-Guerrero, A., Betancourt-Velarde, A., & López‐Cortés, A. (2026) · npj Biofilms and Microbiomes · doi:10.1038/s41522-025-00883-8 · Cited by 66 · see citing works
“The extracellular polymeric matrix protects constituent taxa from immune clearance and antimicrobial stress, favoring the persistence of genotoxin-producing pathobionts and the ampli fi cation of tumor-promoting signals 15,16,18,183 .”
Targeting Gut Microbial Biofilms—A Key to Hinder Colon Carcinogenesis?
Chew, S.-S., Tan, L. T., Law, J. W., Pusparajah, P., Goh, B. H., Mutalib, N. A., & Lee, L. (2020) · Cancers · doi:10.3390/cancers12082272 · Cited by 58 · see citing works
“Furthermore, the latest finding also showed that similar levels of inflammation were observed in both mice inoculated with biofilm-positive and biofilm-negative control homogenates, but a lower degree of immunosuppressive myeloid cell recruitment and IL-17 production was triggered by biofilm-negative control homogenat…”
BackgroundResultInfluentialThe human gut microbiota is neither an organ nor a commensal
Riccio, P., & Rossano, R. (2020) · FEBS Letters · doi:10.1002/1873-3468.13946 · Cited by 57 · see citing works
Garvey, M. (2024) · Biomedicines · doi:10.3390/biomedicines12040740 · Cited by 55 · see citing works
“The biofilms present in CRC patients contain Veillonellaceae, Lachnospiraceae, Coriobacteriaceae, Bacteroidetes , and Firmicutes species, CRC developed in mice transplanted with samples from CRC patients [48].”
BackgroundMontanari, E., Bernardo, G., Noci, V. L., Anselmi, M., Pupa, S. M., Tagliabue, E., Sommariva, M., & Sfondrini, L. (2025) · Molecular Cancer · doi:10.1186/s12943-025-02348-0 · Cited by 62 · see citing works
“Tomkovich et al. demonstrated that tumor-associated biofilms promote colon cancer development in genetically engineered mouse models prone to develop tumor [59].”
Young, C., Wood, H. M., Seshadri, R. A., Nang, P. V., Vaccaro, C. A., Contreras, L., Bose, M., Doi, M. V., Piñero, T. A., Valladares, C. T., et al. (2021) · Genome Medicine · doi:10.1186/s13073-021-00844-8 · Cited by 54 · see citing works
Biofilm and Cancer: Interactions and Future Directions for Cancer Therapy
Choi, E., Murray, B., & Choi, S. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241612836 · Cited by 53 · see citing works
“For instance, Bacteroides fragilis and Enterobacteriaceae bacteria have been found in the mucosal biofilms of patients with inflammatory bowel disease (IBD), increasing host susceptibility to CRC [36].”
BackgroundThe chemistry of gut microbiome in health and diseases
Lau, A., Tan, L. T., Mutalib, N. A., Wong, S. H., Letchumanan, V., & Lee, L. (2021) · Progress In Microbes & Molecular Biology · doi:10.36877/pmmb.a0000175 · Cited by 52 · see citing works
“This has been seen in mice studies in which biofilms formation has been an imperative factor in promoting the oncogenic potential of microbiome in CRC development([107,108]).”
BackgroundGut biofilms:Bacteroidesas model symbionts to study biofilm formation by intestinal anaerobes
Béchon, N., & Ghigo, J. (2021) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuab054 · Cited by 50 · see citing works
Microbiome in cancer progression and therapy
Andreeva, N., Gabbasova, R. R., & Grivennikov, S. I. (2020) · Current Opinion in Microbiology · doi:10.1016/j.mib.2020.09.001 · Cited by 47 · see citing works
“Overgrowth of bacterial biofilms in the direct proximity of transformed tissue is likely to enforce stronger and persistent interactions between microbes and transformed tissue surface [53] and could facilitate reciprocal loss of epithelial barrier function at the tumor site.”
BackgroundPollutants, microbiota and immune system: frenemies within the gut
Rio, P., Gasbarrini, A., Gambassi, G., & Cianci, R. (2024) · Frontiers in Public Health · doi:10.3389/fpubh.2024.1285186 · Cited by 55 · see citing works
Gastrointestinal Biofilms: Endoscopic Detection, Disease Relevance, and Therapeutic Strategies
Jandl, B., Dighe, S. N., Baumgartner, M., Makristathis, A., Gasché, C., & Muttenthaler, M. (2024) · Gastroenterology · doi:10.1053/j.gastro.2024.04.032 · Cited by 46 · see citing works
Common themes in antimicrobial and anticancer drug resistance
Chifiriuc, M. C., Filip, R., Constantin, M., Pîrcălăbioru, G. G., Bleoţu, C., Burlibaşa, L., Ionica, E., Corcionivoschi, N., & Mihăescu, G. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.960693 · Cited by 41 · see citing works
“It has been shown that the adenomatous polyps, CRC, and healthy epithelium at distance from benign or malignant tumors are covered with biofilms formed by tumorigenic invasive polymicrobial associations incorporated in a polysaccharide matrix (Bufill, 1990; Swidsinski et al., 2005; Dejea et al., 2014, 2018; Tomkovich…”
BackgroundEscherichia coli and Colorectal Cancer: Unfolding the Enigmatic Relationship
Rezaee, M. A., Nouri, R., Hasani, A., Shirazi, K. M., Alivand, M. R., Sepehri, B., Sotoodeh, S., & Hemmati, F. (2021) · Current Pharmaceutical Biotechnology · doi:10.2174/1389201022666210910094827 · Cited by 45 · see citing works
Queen, J., Zhang, J., & Sears, C. L. (2020) · Gut Microbes · doi:10.1080/19490976.2019.1706425 · Cited by 40 · see citing works
“Several studies show that CRC tissues are enriched for polymicrobial biofilms, particularly on proximal colon tumors.(8,10,11) This observation correlates with our CPRD cohort findings in which antibiotic exposure was associated with increased risk of proximal/right colon cancer.”
ResultSelf-citationThe Mycobiome: Cancer Pathogenesis, Diagnosis, and Therapy
Gamal, A., Elshaer, M. Y. S., Alabdely, M. H., Kadry, A., McCormick, T. S., & Ghannoum, M. A. (2022) · Cancers · doi:10.3390/cancers14122875 · Cited by 40 · see citing works
“Importantly, some of the most compelling evidence demonstrates that colonic biofilms can cause colorectal cancer in mice [56].”
BackgroundYoung, C., Wood, H. M., Balaguer, A. F., Bottomley, D., Gallop, N., Wilkinson, L., Benton, S. C., Brealey, M., John, C., Burtonwood, C., et al. (2021) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-20-3807 · Cited by 40 · see citing works
Ma, L., Feng, J., Zhang, J., & Lu, X. (2022) · Microbiological Research · doi:10.1016/j.micres.2022.127149 · Cited by 38 · see citing works
Tomkovich, S., Gharaibeh, R. Z., Dejea, C. M., Pope, J. L., Jiang, J., Winglee, K., Gauthier, J., Newsome, R. C., Yang, Y., Fodor, A. A., et al. (2020) · mSystems · doi:10.1128/msystems.00451-19 · Cited by 40 · see citing works
“Additional FISH analysis was conducted on biofilm-positive tumor tissues with probes to detect Bacteroidetes , Lachnospiraceae , Fusobacteria , and Proteobacteria (12, 13).”
InfluentialSelf-citationBacteriophage-mediated manipulations of microbiota in gastrointestinal diseases
Haddad, L. E., Mendoza, J. F., & Jobin, C. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.1055427 · Cited by 40 · see citing works
“Since bacterial biofilm formation is associated with CRC and could promote tumorigenesis in preclinical models (Dejea et al., 2014; Tomkovich et al., 2019), these findings may have chemo-preventive implication.”
BackgroundSelf-citationZhou, Q., Lei, L., Cheng, J., Chen, J., Du, Y., Zhang, X., Li, Q., Li, C., Deng, H., Wong, C. C., et al. (2024) · Gut · doi:10.1136/gutjnl-2024-332193 · Cited by 36 · see citing works
Fluoroquinolones and Biofilm: A Narrative Review
Geremia, N., Giovagnorio, F., Colpani, A., VITO, A. D., Botan, A., Stroffolini, G., Țoc, D. A., Zerbato, V., Principe, L., Madeddu, G., et al. (2024) · Pharmaceuticals · doi:10.3390/ph17121673 · Cited by 36 · see citing works
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“Invasive polymicrobial bio fi lms, composed of Fuso-bacterium spp., Lachnospiraceae , Bacteroidetes, and Proteobacteria exhibit pro-cancerogenic potential by activating epithelial signaling pathways relevant to tumorigenesis 113 – 115 .”
In sickness and health: Effects of gut microbial metabolites on human physiology
Glowacki, R. W. P., & Martens, E. C. (2020) · PLoS Pathogens · doi:10.1371/journal.ppat.1008370 · Cited by 37 · see citing works
“Although the gut microbiome is typically described as being composed of nonharmful or beneficial microorganisms, it is now appreciated that both individual species [8] or multiple community members acting together [9, 10] can exert pathogenic effects, which are often more subtle than those of classical pathogens.”
BackgroundThe effects of biofilms on tumor progression in a 3D cancer-biofilm microfluidic model
Deng, Y., Liu, S. Y., Chua, S. L., & Khoo, B. L. (2021) · Biosensors and Bioelectronics · doi:10.1016/j.bios.2021.113113 · Cited by 36 · see citing works
Bacterial Involvement in Progression and Metastasis of Colorectal Neoplasia
Seely, K. D., Morgan, A. D., Hagenstein, L. D., Florey, G. M., & Small, J. M. (2022) · Cancers · doi:10.3390/cancers14041019 · Cited by 36 · see citing works
Nouri, R., Hasani, A., Shirazi, K. M., Alivand, M. R., Sepehri, B., Sotoudeh, S., Hemmati, F., Fattahzadeh, A., Abdinia, B., & Rezaee, M. A. (2021) · Canadian Journal of Infectious Diseases and Medical Microbiology · doi:10.1155/2021/2131787 · Cited by 35 · see citing works
“have previously reported the presence of mucus-invasive biofilms on the colon mucosa of about half CRC samples and in only 13% of control specimens [23].”
BackgroundIntestinal biofilms: pathophysiological relevance, host defense, and therapeutic opportunities
Jandl, B., Dighe, S. N., Gasché, C., Makristathis, A., & Muttenthaler, M. (2024) · Clinical Microbiology Reviews · doi:10.1128/cmr.00133-23 · Cited by 35 · see citing works
“Pronounced polymicrobial biofilms have a high prevalence in patients with colorectal cancer (64, 130, 165), and mucus-invasive bacterial biofilms on the colon mucosa are observed in ~50% of cases compared to ~13% of healthy controls (143, 166).”
InfluentialLin, H., Wang, Q., Liu, L., Chen, Z., Das, R., Zhao, Y., Mao, D., & Luo, Y. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.01256 · Cited by 34 · see citing works
“The association of biofilm formation with the virulence of pathogens has been confirmed to be correlated with inflammation, including a decrease in E-cadherin levels, an increase in IL-6 levels and activation of the STAT3 pathway (Tomkovich et al., 2019).”
BackgroundGut fungal mycobiome: A significant factor of tumor occurrence and development
Li, F., Gao, Y., Cheng, W., Su, L., & Yang, R. (2023) · Cancer Letters · doi:10.1016/j.canlet.2023.216302 · Cited by 36 · see citing works
Masheghati, F., Asgharzadeh, M. R., Jafari, A., Masoudi, N., & Maleki, H. (2024) · Life Sciences · doi:10.1016/j.lfs.2024.122529 · Cited by 36 · see citing works
Hwang, S., Jo, M., Hong, J.-E., Park, C. O., Lee, C.-G., Yun, M., & Rhee, K. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20184560 · Cited by 33 · see citing works
“A recent study showed that human colon mucosal biofilms obtained from tumor hosts or healthy individuals are required for tumorigenesis in murine models of APCMin−/+ mice [59].”
BackgroundDoes the Gut Microbiota Modulate Host Physiology through Polymicrobial Biofilms?
Yang, J., Yang, Y., Ishii, M., Nagata, M., Aw, W., Obana, N., Tomita, M., Nomura, N., & Fukuda, S. (2020) · Microbes and Environments · doi:10.1264/jsme2.me20037 · Cited by 31 · see citing works
“The same group also discovered that biofilm communities on the colon epi‐ thelium prepared from CRC patients and even healthy indi‐ viduals were carcinogenic in murine CRC models (Tomkovich et al., 2019).”
BackgroundSelf-citationAnnavajhala, M. K., May, M. S., Compres, G., Freedberg, D. E., Graham, R., Stump, S., Que, J., Korem, T., Uhlemann, A., & Abrams, J. A. (2020) · Clinical and Translational Gastroenterology · doi:10.14309/ctg.0000000000000235 · Cited by 32 · see citing works
“In the colon, bio fi lms are present on proximal tumors and adjacent paired normal mucosa (15) and promote the development of colonic neoplasia in mice (16).”
Queen, J., Shaikh, F. Y., & Sears, C. L. (2023) · Nature Cancer · doi:10.1038/s43018-023-00602-2 · Cited by 33 · see citing works
“Phase 1, single center ICI-refractory metastatic melanoma (10) FMT (two donors) by colonoscopy and oral capsules with anti-PD-1 ICI therapy One CR Two PR There were responses only with one of the two donors No serious adverse events were noted”
Self-citationThe oral-gut-circulatory axis: from homeostasis to colon cancer
Tortora, S. C., Agurto, M. I. G., & Martello, L. A. (2023) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2023.1289452 · Cited by 31 · see citing works
Intestinal dysbiosis and colorectal cancer
Kang, Z., Jiang, S., Fang, J., & Chen, H. (2025) · Chinese Medical Journal · doi:10.1097/cm9.0000000000003617 · Cited by 34 · see citing works
“[130] This is driven by immune cell infiltration, especially IL-17-producing cells, which are involved in fostering tumorigenesis.”
Crypt residing bacteria and proximal colonic carcinogenesis in a mouse model of Lynch syndrome
Lang, M., Baumgartner, M., Rożalska, A., Frick, A. P., Riva, A., Jarek, M., Berry, D., & Gasché, C. (2020) · International Journal of Cancer · doi:10.1002/ijc.33028 · Cited by 27 · see citing works
“other researchers points to a mutagenic mucosal biofilm microbiota which can be transmitted from humans to tumor-susceptible mice.(4) Which microbes are residing in the mucus of tumor crypts and”
BackgroundTunçer, S., & Karaçam, S. (2020) · Archives of Microbiology · doi:10.1007/s00203-020-02005-8 · Cited by 29 · see citing works
“Besides, the recent reports emphasize that biofilm formation has a potential etiological role in the development of cancers attributable to chronic infection (Raskov et al. 2018; Li et al. 2019; Rizzato et al. 2019; Tomkovich et al. 2019).”
BackgroundThe Role of the Microbiome on the Pathogenesis and Treatment of Colorectal Cancer
Yu, I., Wu, R., Tokumaru, Y., Terracina, K. P., & Takabe, K. (2022) · Cancers · doi:10.3390/cancers14225685 · Cited by 29 · see citing works
Exploiting unique features of the gut-brain interface to combat gastrointestinal cancer
Schledwitz, A., Xie, G., & Raufman, J. (2021) · Journal of Clinical Investigation · doi:10.1172/jci143776 · Cited by 30 · see citing works
“Mucosal microbial biofilms from humans with CRC are carcinogenic in murine models (101), and some bacterial products (e.”
Sheikh, A. A., Taube, J. H., & Greathouse, K. L. (2021) · Carcinogenesis · doi:10.1093/carcin/bgab060 · Cited by 26 · see citing works
Pedrogo, D. A. M., Sears, C. L., & Melia, J. (2024) · Journal of Crohn s and Colitis · doi:10.1093/ecco-jcc/jjae061 · Cited by 29 · see citing works
Self-citationGut microbial biofilm composition and organisation holds the key to CRC
Hold, G. L., & Allen‐Vercoe, E. (2019) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-019-0148-4 · Cited by 25 · see citing works
Gut Microbiota and Colorectal Cancer Risk Factors
Feizi, H., Rezaee, M. A., Ghotaslou, R., Sadrkabir, M., Jadidi‐Niaragh, F., Gholizadeh, P., Taghizadeh, S., Ghanbarov, K., Yousefi, M., & Kafil, H. S. (2022) · Current Pharmaceutical Biotechnology · doi:10.2174/1389201023666221005103340 · Cited by 24 · see citing works
Fungi and tumors: The role of fungi in tumorigenesis (Review)
Cheng, W., Li, F., Gao, Y., & Yang, R. (2024) · International Journal of Oncology · doi:10.3892/ijo.2024.5640 · Cited by 24 · see citing works
“Interestingly, biofilm homogenates from patients with CRC can cause colon tumorigenesis in mice (62).”
Antibiotics, cancer risk and oncologic treatment efficacy: a practical review of the literature
Lopes, M. S. M., Machado, L. M., Silva, P. A. I. A., Uchiyama, A. A. T., Yen, C. T., Ricardo, E. D., Mutão, T. S., Pimento, J. R., Shimba, D. S., Hanriot, R. D. M., et al. (2020) · ecancermedicalscience · doi:10.3332/ecancer.2020.1106 · Cited by 24 · see citing works
A tale of two bacteria – Bacteroides fragilis, Escherichia coli, and colorectal cancer
Lichtenstern, C. R., & Lamichhane-Khadka, R. (2023) · Frontiers in Bacteriology · doi:10.3389/fbrio.2023.1229077 · Cited by 23 · see citing works
Cancer microbiota: a focus on tumor-resident bacteria
Vella, G., & Rescigno, M. (2025) · EMBO Reports · doi:10.1038/s44319-025-00482-w · Cited by 25 · see citing works
“Moreover, some of the bacterial species form bio fi lm, which consists of complex microbial communities enclosed in self-produced polymeric matrix, facilitating their protection to the immune system (Chessa et al, 2016; Drusano et al, 2011; Tomkovich et al, 2019).”
Biofilm Formation and Virulence of Shigella flexneri Are Modulated by pH of Gastrointestinal Tract
Chiang, I.-L., Wang, Y., Fujii, S., Muegge, B. D., Lu, Q., Tarr, P. I., & Stappenbeck, T. S. (2021) · Infection and Immunity · doi:10.1128/iai.00387-21 · Cited by 22 · see citing works
“Our work may have implications beyond acute Shigella infections, as gut biofilms have been associated with colorectal cancer and inflammatory bowel disease, and may further the investigation of biofilms related to disorders of the gastrointestinal tract (32, 33).”
Background
- Authors
- Tomkovich, S., Dejea, C. M., Winglee, K., Drewes, J. L., Chung, L., Housseau, F., Pope, J. L., Gauthier, J., Sun, X., Mühlbauer, M., Liu, X., Fathi, P., Anders, R. A., Besharati, S., Perez-Chanona, E., Yang, Y., Ding, H., Wu, X., Wu, S., White, J. R., Gharaibeh, R. Z., Fodor, A. A., Wang, H., Pardoll, D. M., Jobin, C., & Sears, C. L.
- Affiliations
- University of Florida (US)
- Johns Hopkins University (US)
- University of North Carolina at Charlotte (US)
- Resphera Biosciences (US)
- Corresponding author
- Jobin, Christian
- Sears, Cynthia L.
- ORCID
- Tomkovich, Sarah
- Dejea, Christine M.
- Winglee, Kathryn
- Drewes, Julia L.
- Chung, Liam
- Housseau, Franck
- Sun, Xiaolun
- Mühlbauer, Marcus
- Liu, Xiuli
- Anders, Robert A.
- Besharati, Sepideh
- Yang, Ye
- Ding, Hua
- Wu, Xinqun
- Wu, Shaoguang
- White, James R.
- Gharaibeh, Raad Z.
- Fodor, Anthony A.
- Wang, Hao
- Pardoll, Drew M.
- Jobin, Christian
- Sears, Cynthia L.
- Venue
- Journal of Clinical Investigation
- Published
- 2019-03-11
- Volume
- 129
- Issue
- 4
- Pages
- 1699-1712
- ISSN
- 0021-9738 (ISSN-L)
- 1558-8238
- PMC
- PMC6436866
- OpenAlex
- W2921953499
- Cited by
- 209
- References
- 49
- Citations by year
- 2026: 15 · 2025: 20 · 2024: 29 · 2023: 33 · 2022: 24 · 2021: 45 · 2020: 31 · 2019: 11 · 2018: 1
- FWCI
- 9.18
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- NIH (R01DK073338, R01DK47700, R01 CA151393, R01CA196845, P50 CA62924, P30 CA006973, P30 DK089502, K99 CA230192, S10OD016374)
- Bloomberg Philanthropies (Microbiome Project)
- Johns Hopkins Discovery Award (Internal award)
- Commonwealth Foundation (Johns Hopkins)
- Cancer Research Institute/Fight Colorectal Cancer coalition (CRC discovery award)
- University of Florida Health Cancer Center Funds (internal award)
- University of Florida Department of Medicine Gatorade Fund (internal award)
- Crohn’s and Colitis Foundation (CCFA Ref. #409472)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Escherichia coli research studies
- Keywords
- colorectal cancer, carcinogenesis, gut microbiota, ApcMin/+ mice, germ-free mice, colonic inflammation, tumor formation, microbial communities, 16S rRNA gene sequencing, RNA-seq
- MeSH terms
- Gastrointestinal Microbiome, Animals, Colon, Colonic Neoplasms, Humans, Neoplasms, Experimental, Mice, Knockout, Biofilms, Mice, Carcinogenesis
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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