A review of the role of enterotoxigenic Bacteroides fragilis in the development of colorectal cancer
-
Abolfazl Jafari-Sales
,
Maryam Farahnaki-Sadabadi
,
Elham Nozohour-Leilabadi
,
Negin Yagoubi Azar
,
Maryam Safari
,
Mehrdad Pashazadeh
Abstract
Enterotoxigenic Bacteroides fragilis (ETBF) plays a significant role in the development and progression of colorectal cancer (CRC) through the production of Bacteroides fragilis toxin (BFT). This toxin activates Wnt, NF-κB, and STAT3 signaling pathways, leading to chronic inflammation, DNA damage, and abnormal cellular proliferation. The presence of ETBF in the gut microbiota can increase the risk of CRC by enhancing immune cell infiltration, triggering inflammatory responses, and disrupting cell cycle regulation. ETBF detection is performed using molecular methods such as polymerase chain reaction (PCR) and immunomagnetic separation-PCR (IMS-PCR), which offer high accuracy in identifying this bacterium. Immunomagnetic separation enhances the sensitivity and precision of detection. In addition to precise diagnostic methods, preventive strategies play a crucial role in reducing the risk of CRC. A healthy diet, including increased fiber intake, reduced consumption of processed meats and saturated fats, along with maintaining a healthy weight and regular physical activity, are among the effective factors in preventing this disease. Furthermore, stress reduction and avoidance of alcohol and tobacco can positively impact lowering the risk of CRC. A deeper understanding of the role of ETBF in CRC and its effects on molecular pathways can contribute to the development of novel preventive approaches. Investigating the composition of the gut microbiota and implementing preventive strategies based on lifestyle modifications not only aids in identifying at-risk individuals but also plays a significant role in reducing the prevalence and progression of this disease.
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7. Haghi F, Goli E, Mirzaei B, Zeighami H. The association between fecal enterotoxigenic B. fragilis with colorectal cancer. BMC cancer. 2019;19:1-4.
8. Alhinai EA, Walton GE, Commane DM. The role of the gut microbiota in colorectal cancer causation. International Journal of Molecular Sciences. 2019;20(21):5295.
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32. Sánchez E, Laparra J, Sanz Y. Discerning the role of Bacteroides fragilis in celiac disease pathogenesis. Appl Environ Microbiol. 2012;78(18):6507-15.
33. Wang C, Li S, Hong K, Yu L, Tian F, Zhao J, et al. The roles of different Bacteroides fragilis strains in protecting against DSS-induced ulcerative colitis and related functional genes. Food Funct. 2021;12(18):8300-13.
34. Gao R, Gao Z, Huang L, Qin H. Gut microbiota and colorectal cancer. European Journal of Clinical Microbiology & Infectious Diseases. 2017;36:757-69.
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53. Joo JE, Chu YL, Georgeson P, Walker R, Mahmood K, Clendenning M, et al. Intratumoral presence of the genotoxic gut bacteria pks+ E. coli, Enterotoxigenic Bacteroides fragilis, and Fusobacterium nucleatum and their association with clinicopathological and molecular features of colorectal cancer. British Journal of Cancer. 2024;130(5):728-40.
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2. Ionescu VA, Gheorghe G, Bacalbasa N, Chiotoroiu AL, Diaconu C. Colorectal cancer: from risk factors to oncogenesis. Medicina. 2023;59(9):1646.
3. Mármol I, Sánchez-de-Diego C, Pradilla Dieste A, Cerrada E, Rodriguez Yoldi MJ. Colorectal carcinoma: a general overview and future perspectives in colorectal cancer. International journal of molecular sciences. 2017;18(1):197.
4. Dadgar-Zankbar L, Shariati A, Bostanghadiri N, Elahi Z, Mirkalantari S, Razavi S, et al. Evaluation of enterotoxigenic Bacteroides fragilis correlation with the expression of cellular signaling pathway genes in Iranian patients with colorectal cancer. Infectious Agents and Cancer. 2023;18(1):48.
5. Khodaverdi N, Zeighami H, Jalilvand A, Haghi F, Hesami N. High frequency of enterotoxigenic Bacteroides fragilis and Enterococcus faecalis in the paraffin-embedded tissues of Iranian colorectal cancer patients. BMC cancer. 2021;21(1):1353.
6. Scott N, Whittle E, Jeraldo P, Chia N. A systemic review of the role of enterotoxic Bacteroides fragilis in colorectal cancer. Neoplasia. 2022;29:100797.
7. Haghi F, Goli E, Mirzaei B, Zeighami H. The association between fecal enterotoxigenic B. fragilis with colorectal cancer. BMC cancer. 2019;19:1-4.
8. Alhinai EA, Walton GE, Commane DM. The role of the gut microbiota in colorectal cancer causation. International Journal of Molecular Sciences. 2019;20(21):5295.
9. Jasemi S, Emaneini M, Fazeli MS, Ahmadinejad Z, Nomanpour B, Sadeghpour Heravi F, et al. Toxigenic and non-toxigenic patterns I, II and III and biofilm-forming ability in Bacteroides fragilis strains isolated from patients diagnosed with colorectal cancer. Gut pathogens. 2020;12:1-7.
10. Boleij A, Hechenbleikner EM, Goodwin AC, Badani R, Stein EM, Lazarev MG, et al. The Bacteroides fragilis toxin gene is prevalent in the colon mucosa of colorectal cancer patients. Clinical Infectious Diseases. 2015;60(2):208-15.
11. Kaźmierczak-Siedlecka K, Daca A, Fic M, van de Wetering T, Folwarski M, Makarewicz W. Therapeutic methods of gut microbiota modification in colorectal cancer management–fecal microbiota transplantation, prebiotics, probiotics, and synbiotics. Gut microbes. 2020;11(6):1518-30.
12. Alzahrani SM, Al Doghaither HA, Al-Ghafari AB. General insight into cancer: An overview of colorectal cancer. Molecular and clinical oncology. 2021;15(6):271.
13. Sawicki T, Ruszkowska M, Danielewicz A, Niedźwiedzka E, Arłukowicz T, Przybyłowicz KE. A review of colorectal cancer in terms of epidemiology, risk factors, development, symptoms and diagnosis. Cancers. 2021;13(9):2025.
14. Sehgal R, Sheahan K, O’Connell PR, Hanly AM, Martin ST, Winter DC. Lynch syndrome: an updated review. Genes. 2014;5(3):497-507.
15. Shussman N, Wexner SD. Colorectal polyps and polyposis syndromes. Gastroenterology report. 2014;2(1):1-15.
16. Thélin C, Sikka S. Epidemiology of colorectal Cancer—incidence, lifetime risk factors statistics and temporal trends. Screening for colorectal Cancer with colonoscopy London: IntechOpen Limited. 2015:61-77.
17. Pietrzyk Ł. Food properties and dietary habits in colorectal cancer prevention and development. International Journal of Food Properties. 2017;20(10):2323-43.
18. Zackular JP, Rogers MA, Ruffin IV MT, Schloss PD. The human gut microbiome as a screening tool for colorectal cancer. Cancer prevention research. 2014;7(11):1112-21.
19. Borges-Canha M, Portela-Cidade JP, Dinis-Ribeiro M, Leite-Moreira AF, Pimentel-Nunes P. Role of colonic microbiota in colorectal carcinogenesis: a systematic review. Revista Española de Enfermedades Digestivas. 2015;107(11):659-71.
20. Sánchez-Alcoholado L, Ramos-Molina B, Otero A, Laborda-Illanes A, Ordóñez R, Medina JA, et al. The role of the gut microbiome in colorectal cancer development and therapy response. Cancers. 2020;12(6):1406.
21. Gagnière J, Raisch J, Veziant J, Barnich N, Bonnet R, Buc E, et al. Gut microbiota imbalance and colorectal cancer. World journal of gastroenterology. 2016;22(2):501.
22. Dai Z, Zhang J, Wu Q, Chen J, Liu J, Wang L, et al. The role of microbiota in the development of colorectal cancer. International journal of cancer. 2019;145(8):2032-41.
23. Pasquereau-Kotula E, Martins M, Aymeric L, Dramsi S. Significance of Streptococcus gallolyticus subsp. gallolyticus association with colorectal cancer. Frontiers in microbiology. 2018;9:614.
24. Sun C-H, Li B-B, Wang B, Zhao J, Zhang X-Y, Li T-T, et al. The role of Fusobacterium nucleatum in colorectal cancer: from carcinogenesis to clinical management. Chronic diseases and translational medicine. 2019;5(03):178-87.
25. Zuo Y, Jing Z, Bie M, Xu C, Hao X, Wang B. Association between Helicobacter pylori infection and the risk of colorectal cancer: A systematic review and meta-analysis. Medicine. 2020;99(37):e21832.
26. Ulger Toprak N, Yagci A, Gulluoglu B, Akin M, Demirkalem P, Celenk T, et al. A possible role of Bacteroides fragilis enterotoxin in the aetiology of colorectal cancer. Clinical microbiology and infection. 2006;12(8):782-6.
27. Namavar F, Theunissen E, Verweij-Van Vught A, Peerbooms P, Bal M, Hoitsma H, et al. Epidemiology of the Bacteroides fragilis group in the colonic flora in 10 patients with colonic cancer. Journal of medical microbiology. 1989;29(3):171-6.
28. Jean S, Wallace MJ, Dantas G, Burnham C-AD. Time for some group therapy: update on identification, antimicrobial resistance, taxonomy, and clinical significance of the Bacteroides fragilis group. Journal of clinical microbiology. 2022;60(9):e02361-20.
29. Brook I. Pathogenicity of the Bacteroides fragilis group. Annals of Clinical & Laboratory Science. 1989;19(5):360-76.
30. Azboy Y. Fiziksel aktivite ve sağlık. Sağlık ve Yaşam Bilimleri Dergisi. 2021.
31. Cheng WT, Kantilal HK, Davamani F. The Mechanism of Bacteroides fragilis Toxin Contributes to Colon Cancer Formation. Malays J Med Sci. 2020;27(4):9-21.
32. Sánchez E, Laparra J, Sanz Y. Discerning the role of Bacteroides fragilis in celiac disease pathogenesis. Appl Environ Microbiol. 2012;78(18):6507-15.
33. Wang C, Li S, Hong K, Yu L, Tian F, Zhao J, et al. The roles of different Bacteroides fragilis strains in protecting against DSS-induced ulcerative colitis and related functional genes. Food Funct. 2021;12(18):8300-13.
34. Gao R, Gao Z, Huang L, Qin H. Gut microbiota and colorectal cancer. European Journal of Clinical Microbiology & Infectious Diseases. 2017;36:757-69.
35. Viljoen KS, Dakshinamurthy A, Goldberg P, Blackburn JM. Quantitative profiling of colorectal cancer-associated bacteria reveals associations between fusobacterium spp., enterotoxigenic Bacteroides fragilis (ETBF) and clinicopathological features of colorectal cancer. PloS one. 2015;10(3):e0119462.
36. Nobles Jr ER. Bacteroides infections. Annals of Surgery. 1973;177(5):601.
37. Leigh D. Clinical importance of infections due to Bacteroides fragilis and role of antibiotic therapy. Br Med J. 1974;3(5925):225-8.
38. Casarotto M, Tartaglia M, Gibellini D, Mazzariol A. Antimicrobial susceptibility of anaerobic clinical isolates: A two-year surveillance. Anaerobe. 2023;80:102715.
39. Liu Y, Lau HC-H, Cheng WY, Yu J. Gut microbiome in colorectal cancer: Clinical diagnosis and treatment. Genomics, Proteomics & Bioinformatics. 2023;21(1):84-96.
40. Nazarinejad N, Hajikhani B, Vaezi AA, Firoozeh F, Sameni F, Yaslianifard S, et al. Association between colorectal cancer, the frequency of Bacteroides fragilis, and the level of mismatch repair genes expression in the biopsy samples of Iranian patients. BMC gastroenterology. 2024;24(1):82.
41. Finegold SM. Anaerobic infections in humans: an overview. Anaerobe. 1995;1(1):3-9.
42. Zhu Q, Gao R, Wu W, Qin H. The role of gut microbiota in the pathogenesis of colorectal cancer. Tumor Biology. 2013;34:1285-300.
43. Jahani-Sherafat S, Alebouyeh M, Moghim S, Amoli HA, Ghasemian-Safaei H. Role of gut microbiota in the pathogenesis of colorectal cancer; a review article. Gastroenterology and hepatology from bed to bench. 2018;11(2):101.
44. Wieczorska K, Stolarek M, Stec R. The role of the gut microbiome in colorectal cancer: where are we? Where are we going? Clinical Colorectal Cancer. 2020;19(1):5-12.
45. Geis AL, Fan H, Wu X, Wu S, Huso DL, Wolfe JL, et al. Regulatory T-cell response to enterotoxigenic Bacteroides fragilis colonization triggers IL17-dependent colon carcinogenesis. Cancer discovery. 2015;5(10):1098-109.
46. Qu R, Zhang Y, Ma Y, Zhou X, Sun L, Jiang C, et al. Role of the gut microbiota and its metabolites in tumorigenesis or development of colorectal cancer. Advanced Science. 2023;10(23):2205563.
47. Snezhkina AV, Krasnov GS, Lipatova AV, Sadritdinova AF, Kardymon OL, Fedorova MS, et al. The Dysregulation of Polyamine Metabolism in Colorectal Cancer Is Associated with Overexpression of c‐Myc and C/EBPβ rather than Enterotoxigenic Bacteroides fragilis Infection. Oxidative medicine and cellular longevity. 2016;2016(1):2353560.
48. Chung L, Orberg ET, Geis AL, Chan JL, Fu K, Shields CED, et al. Bacteroides fragilis toxin coordinates a pro-carcinogenic inflammatory cascade via targeting of colonic epithelial cells. Cell host & microbe. 2018;23(2):203-14. e5.
49. Zamani S, Taslimi R, Sarabi A, Jasemi S, Sechi LA, Feizabadi MM. Enterotoxigenic Bacteroides fragilis: a possible etiological candidate for bacterially-induced colorectal precancerous and cancerous lesions. Frontiers in cellular and infection microbiology. 2020;9:449.
50. Lichtenstern CR, Lamichhane-Khadka R. A tale of two bacteria–Bacteroides fragilis, Escherichia coli, and colorectal cancer. Frontiers in Bacteriology. 2023;2:1229077.
51. Cheng WT, Kantilal HK, Davamani F. The mechanism of Bacteroides fragilis toxin contributes to colon cancer formation. The Malaysian journal of medical sciences: MJMS. 2020;27(4):9.
52. Sears CL, Geis AL, Housseau F. Bacteroides fragilis subverts mucosal biology: from symbiont to colon carcinogenesis. The Journal of clinical investigation. 2014;124(10):4166-72.
53. Joo JE, Chu YL, Georgeson P, Walker R, Mahmood K, Clendenning M, et al. Intratumoral presence of the genotoxic gut bacteria pks+ E. coli, Enterotoxigenic Bacteroides fragilis, and Fusobacterium nucleatum and their association with clinicopathological and molecular features of colorectal cancer. British Journal of Cancer. 2024;130(5):728-40.
54. Ko SH, Jeon JI, Woo HA, Kim JM. Bacteroides fragilis enterotoxin upregulates heme oxygenase-1 in dendritic cells via reactive oxygen species-, mitogen-activated protein kinase-, and Nrf2-dependent pathway. World Journal of Gastroenterology. 2020;26(3):291.
55. Lee C-G, Hwang S, Gwon S-Y, Park C, Jo M, Hong J-E, et al. Bacteroides fragilis toxin induces intestinal epithelial cell secretion of interleukin-8 by the e-Cadherin/β-Catenin/NF-κB dependent pathway. Biomedicines. 2022;10(4):827.
56. Ko SH, Rho DJ, Jeon JI, Kim Y-J, Woo HA, Lee YK, et al. Bacteroides fragilis enterotoxin upregulates heme oxygenase-1 in intestinal epithelial cells via a mitogen-activated protein kinase-and NF-κB-dependent pathway, leading to modulation of apoptosis. Infection and immunity. 2016;84(9):2541-54.
57. Faizo NL. The intestinal stem cell as a target: A review. Medicine. 2024;103(34):e39456.
58. Li S, Liu J, Zheng X, Ren L, Yang Y, Li W, et al. Tumorigenic bacteria in colorectal cancer: mechanisms and treatments. Cancer biology & medicine. 2022;19(2):147-62.
59.Metz P, Tjan MJ, Wu S, Pervaiz M, Hermans S, Shettigar A, et al. Drug discovery and repurposing inhibits a major gut pathogen-derived oncogenic toxin. Frontiers in cellular and infection microbiology. 2019;9:364.
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| Files | ||
| Issue | Vol 16 No 3 (2024) | |
| Section | Reviews | |
| Keywords | ||
| Colorectal cancer Bacteroides fragilis Bacteroides fragilis toxin | ||
| Rights and permissions | |
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Jafari-Sales A, Farahnaki-Sadabadi M, Nozohour-Leilabadi E, Yagoubi Azar N, Safari M, Pashazadeh M. A review of the role of enterotoxigenic Bacteroides fragilis in the development of colorectal cancer. Basic Clin Cancer Res. 2025;16(3):160-170.
