Regulation of Gut Microbiota: Is It Hope for Cure of Colorectal Cancer?
Creators
- 1. Department of General Surgery, Ankara City Hospital (Bilkent), Ankara, Türkiye.
- 2. Department of Medical Microbiology, Gulhane Training and Research Hospital, Ankara, Türkiye.
- 3. Department of General Surgery, Konya City Hospital, Konya, Türkiye.
- 4. Department of Gastroenterology, Lokman Hekim Etlik Hospital, Ankara, Türkiye.
Description
Abstract
The gut microbiota dysbiosis is linked with inflammatory bowel diseases, hypertension, atherosclerosis, hepatitis, neuropsychiatric disorders, diabetes, obesity, asthma, and development of cancer. Despite the substantial developments in oncology, cancer is still not in the category of curative diseases. However, significant steps are being taken in this direction through the identification of factors that play a role in the stages of complex carcinogenesis. Recent data obtained from human gut microbiota has shown that commensal microorganism species living on the epithelial surfaces of the intestines have an active role in this process and are also associated with personal responses to cancer treatment and toxicity. We now know more about the role of Fusobacterium nucleatum, an important member of the gut microbiota complex, as well as other microorganisms in the formation, treatment, diagnosis, and screening of colorectal cancer. In conclusion, the growing knowledge of microbiota, a key factor in colorectal cancer formation and treatment stages, will be able to change the early detection, treatment, and follow-up of these cancers. In this review, the role of gut microbiota in colorectal carcinogenesis and cancer formation mechanisms, significance in treatment and prognosis, and potential use in cancer prevention and screening have evaluated based on the data obtained from recent studies.
Özet
Bağırsak mikrobiyota disbiyozu inflamatuar bağırsak hastalıkları, nöropsikiyatrik bozukluklar, hipertansiyon, ateroskleroz, hepatit, diyabet, obezite, astım ve kanser gelişimi ile ilişkilendirilmektedir. Onkolojideki önemli gelişmelere rağmen kanser halen tamamen tedavi edilebilir hastalıklar kategorisinde yer almamaktadır. Ancak kompleks karsinogenezin evrelerinde rol oynayan faktörlerin belirlenmesi ile bu yönde önemli adımlar atılmaktadır. İnsan bağırsak mikrobiyotasından elde edilen son veriler, bağırsakların epitelyal yüzeylerinde yaşayan kommensal mikroorganizma türlerinin bu süreçte aktif rol oynadığını ve ayrıca kanser tedavisine ve toksisiteye verilen bireysel yanıtlarla ilişkili olduğunu göstermiştir. Bağırsak mikrobiyota kompleksinin önemli bir üyesi olan Fusobacterium nucleatum'un ve bazı diğer mikroorganizmaların kolorektal kanserin oluşumu, tedavisi, teşhisi ve taranmasındaki rolü hakkında günümüzde daha fazla şey biliyoruz. Sonuç olarak, kolorektal kanser oluşumunda ve tedavi aşamalarında önemli bir faktör olan mikrobiyota konusunda artan bilgi birikimi, bu kanserlerin erken teşhis, tedavi ve takibini değiştirecektir. Bu derlemede, son çalışmalardan elde edilen veriler temelinde, bağırsak mikrobiyotasının kolorektal karsinogenez ve kanser oluşum mekanizmalarındaki rolü, tedavi ve prognozdaki önemi ve kanser önleme ve taramasında kullanım potansiyeli değerlendirilmiştir.
Notes
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References
- 1. Mandal P. Molecular mechanistic pathway of colorectal carcinogenesis associated with intestinal microbiota. Anaerobe 2018; 49: 63-70. [Crossref]
- 2. Paul B, Barnes S, Demark-Wahnefried W, Morrow C, Salvador C, Skibola C, et al. Influences of diet and the gut microbiome on epigenetic modulation in cancer and other diseases. Clin Epigenetics 2015; 7: 112. [Crossref]
- 3. Hou K, Wu ZX, Chen XY, Wang JQ, Zhang D, Xiao C, et al. Microbiota in health and diseases. Signal Transduct Target Ther 2022; 7(1): 135. [Crossref]
- 4. Xu Z, Knight R. Dietary effects on human gut microbiome diversity. Br J Nutr 2015; 113 Suppl (Suppl 0): S1-5. [Crossref]
- 5. Dzutsev A, Goldszmid RS, Viaud S, Zitvogel L, Trinchieri G. The role of the microbiota in inflammation, carcinogenesis, and cancer therapy. Eur J Immunol 2015; 45(1): 17-31. [Crossref]
- 6. Iebba V, Totino V, Gagliardi A, Santangelo F, Cacciotti F, Trancassini M, et al. Eubiosis and dysbiosis: the two sides of the microbiota. New Microbiol 2016; 39(1): 1-12. [PubMed]
- 7. Tremaroli V, Bäckhed F. Functional interactions between the gut microbiota and host metabolism. Nature 2012; 489(7415): 242-9. [Crossref]
- 8. Gagnière J, Raisch J, Veziant J, Barnich N, Bonnet R, Buc E, et al. Gut microbiota imbalance and colorectal cancer. World J Gastroenterol 2016; 22(2): 501-18. [Crossref]
- 9. Rawla P, Sunkara T, Barsouk A. Epidemiology of colorectal cancer: incidence, mortality, survival, and risk factors. Prz Gastroenterol 2019; 14(2): 89-103. [Crossref]
- 10. Castellarin M, Warren RL, Freeman JD, Dreolini L, Krzywinski M, Strauss J, et al. Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res 2012; 22(2): 299-306. [Crossref]
- 11. Rebersek M. Gut microbiome and its role in colorectal cancer. BMC Cancer 2021; 21(1): 1325. [Crossref]
- 12. Garrett WS. Cancer and the microbiota. Science 2015; 348(6230): 80-6. [Crossref]
- 13. Sharma NK, Sarode SC, Sarode GS, Patil S. Vomocytosis by macrophages: a crucial event in the local niche of tumors. Future Oncol 2019; 15(14): 1545-50. [Crossref]
- 14. Dias-Jácome E, Libânio D, Borges-Canha M, Galaghar A, Pimentel-Nunes P. Gastric microbiota and carcinogenesis: the role of non-Helicobacter pylori bacteria - A systematic review. Rev Esp Enferm Dig 2016; 108(9): 530-40. [PubMed]
- 15. Fox JG, Wang TC. Inflammation, atrophy, and gastric cancer. J Clin Invest 2007; 117(1): 60-9. [Crossref]
- 16. O'Keefe SJ. Diet, microorganisms and their metabolites, and colon cancer. Nat Rev Gastroenterol Hepatol 2016; 13(12): 691-706. [Crossref]
- 17. Yoon H, Kim N, Park JH, Kim YS, Lee J, Kim HW, et al. Comparisons of Gut Microbiota Among Healthy Control, Patients With Conventional Adenoma, Sessile Serrated Adenoma, and Colorectal Cancer. J Cancer Prev 2017; 22(2): 108-14. [Crossref]
- 18. Davies RJ, Miller R, Coleman N. Colorectal cancer screening: prospects for molecular stool analysis. Nat Rev Cancer 2005; 5(3): 199-209. [Crossref]
- 19. McCoy AN, Araújo-Pérez F, Azcárate-Peril A, Yeh JJ, Sandler RS, Keku TO. Fusobacterium is associated with colorectal adenomas. PLoS One 2013; 8(1): e53653. [Crossref]
- 20. Leggett B, Whitehall V. Role of the serrated pathway in colorectal cancer pathogenesis. Gastroenterology 2010; 138(6): 2088-100. [Crossref]
- 21. Kostic AD, Chun E, Robertson L, Glickman JN, Gallini CA, Michaud M, et al. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe 2013; 14(2): 207-15. [Crossref]
- 22. Wu Y, Wu J, Chen T, Li Q, Peng W, Li H, et al. Fusobacterium nucleatum Potentiates Intestinal Tumorigenesis in Mice via a Toll-Like Receptor 4/p21-Activated Kinase 1 Cascade. Dig Dis Sci 2018; 63(5): 1210-8. [Crossref]
- 23. World Health Organization (WHO), Geneva, Switzerland. Cancer Today. Available at: https://gco.iarc.fr/today/home [Accessed September 18, 2022].
- 24. Etxeberria J, Ugarte MD, Goicoa T, Militino AF. Age- and sex-specific spatio-temporal patterns of colorectal cancer mortality in Spain (1975-2008). Popul Health Metr 2014; 12: 17. [Crossref]
- 25. Migliore L, Migheli F, Spisni R, Coppedè F. Genetics, cytogenetics, and epigenetics of colorectal cancer. J Biomed Biotechnol 2011; 2011: 792362. [Crossref]
- 26. Xu XT, Xu Q, Tong JL, Zhu MM, Huang ML, Ran ZH, et al. Meta-analysis: circulating adiponectin levels and risk of colorectal cancer and adenoma. J Dig Dis 2011; 12(4): 234-44. [Crossref]
- 27. Nishihara R, Morikawa T, Kuchiba A, Lochhead P, Yamauchi M, Liao X, et al. A prospective study of duration of smoking cessation and colorectal cancer risk by epigenetics-related tumor classification. Am J Epidemiol 2013; 178(1): 84-100. [Crossref]
- 28. Ou J, Carbonero F, Zoetendal EG, DeLany JP, Wang M, Newton K, et al. Diet, microbiota, and microbial metabolites in colon cancer risk in rural Africans and African Americans. Am J Clin Nutr 2013; 98(1): 111-20. [Crossref]
- 29. Center MM, Jemal A, Smith RA, Ward E. Worldwide variations in colorectal cancer. CA Cancer J Clin 2009; 59(6): 366-78. [Crossref]
- 30. O'Keefe SJ, Kidd M, Espitalier-Noel G, Owira P. Rarity of colon cancer in Africans is associated with low animal product consumption, not fiber. Am J Gastroenterol 1999; 94(5): 1373-80. [Crossref]
- 31. Yavari P, Hislop TG, Bajdik C, Sadjadi A, Nouraie M, Babai M, et al. Comparison of cancer incidence in Iran and Iranian immigrants to British Columbia, Canada. Asian Pac J Cancer Prev 2006; 7(1): 86-90. [PubMed]
- 32. Vargas AJ, Thompson PA. Diet and nutrient factors in colorectal cancer risk. Nutr Clin Pract 2012; 27(5): 613-23. [Crossref]
- 33. Chen YC, Chien CY, Hsu CC, Lee CH, Chou YT, Shiah SG, et al. Obesity-associated leptin promotes chemoresistance in colorectal cancer through YAP-dependent AXL upregulation. Am J Cancer Res 2021; 11(9): 4220-40. [PubMed]
- 34. Nistal E, Fernández-Fernández N, Vivas S, Olcoz JL. Factors determining colorectal cancer: the role of the intestinal microbiota. Frontiers in oncology 2015; 5: 220. [Crossref]
- 35. Buffie CG, Pamer EG. Microbiota-mediated colonization resistance against intestinal pathogens. Nat Rev Immunol 2013; 13(11): 790-801. [Crossref]
- 36. Kostic AD, Xavier RJ, Gevers D. The microbiome in inflammatory bowel disease: current status and the future ahead. Gastroenterology 2014; 146(6): 1489-99. [Crossref]
- 37. Zackular JP, Baxter NT, Iverson KD, Sadler WD, Petrosino JF, Chen GY, et al. The gut microbiome modulates colon tumorigenesis. mBio 2013; 4(6): e00692-13. [Crossref]
- 38. Cheesman SE, Neal JT, Mittge E, Seredick BM, Guillemin K. Epithelial cell proliferation in the developing zebrafish intestine is regulated by the Wnt pathway and microbial signaling via Myd88. Proc Natl Acad Sci U S A 2011; 108 Suppl 1(Suppl 1): 4570-7. [Crossref]
- 39. Zhou H, Yuan Y, Wang H, Xiang W, Li S, Zheng H, et al. Gut Microbiota: A Potential Target for Cancer Interventions. Cancer Manag Res 2021; 13: 8281-96. [Crossref]
- 40. Hirota SA, Ng J, Lueng A, Khajah M, Parhar K, Li Y, et al. NLRP3 inflammasome plays a key role in the regulation of intestinal homeostasis. Inflamm Bowel Dis 2011; 17(6): 1359-72. [Crossref]
- 41. Baxter NT, Zackular JP, Chen GY, Schloss PD. Structure of the gut microbiome following colonization with human feces determines colonic tumor burden. Microbiome 2014; 2: 20. [Crossref]
- 42. Vaughan EE, Schut F, Heilig HG, Zoetendal EG, de Vos WM, Akkermans AD. A molecular view of the intestinal ecosystem. Curr Issues Intest Microbiol 2000; 1(1): 1-12. [PubMed]
- 43. Zoetendal EG, Collier CT, Koike S, Mackie RI, Gaskins HR. Molecular ecological analysis of the gastrointestinal microbiota: a review. J Nutr. 2004 Feb;134(2):465-72. [Crossref]
- 44. Frank DN, Pace NR. Gastrointestinal microbiology enters the metagenomics era. Curr Opin Gastroenterol 2008; 24(1): 4-10. [Crossref]
- 45. Di Domenico M, Ballini A, Boccellino M, Scacco S, Lovero R, Charitos IA, et al. The Intestinal Microbiota May Be a Potential Theranostic Tool for Personalized Medicine. J Pers Med 2022; 12(4): 523. [Crossref]
- 46. Thursby E, Juge N. Introduction to the human gut microbiota. Biochem J 2017; 474(11): 1823-36. [Crossref]
- 47. Hollister EB, Gao C, Versalovic J. Compositional and functional features of the gastrointestinal microbiome and their effects on human health. Gastroenterology 2014; 146(6): 1449-58. [Crossref]
- 48. Tlaskalová-Hogenová H, Stepánková R, Hudcovic T, Tucková L, Cukrowska B, Lodinová-Zádníková R. Commensal bacteria (normal microflora), mucosal immunity and chronic inflammatory and autoimmune diseases. Immunol Lett 2004; 93(2-3): 97-108. [Crossref]
- 49. Singhal R, Shah YM. Oxygen battle in the gut: Hypoxia and hypoxia-inducible factors in metabolic and inflammatory responses in the intestine. J Biol Chem 2020; 295(30): 10493-505. [Crossref]
- 50. Roy S, Trinchieri G. Microbiota: a key orchestrator of cancer therapy. Nat Rev Cancer 2017; 17(5): 271-85. [Crossref]
- 51. Sun CH, Li BB, Wang B, Zhao J, Zhang XY, Li TT, et al. The role of Fusobacterium nucleatum in colorectal cancer: from carcinogenesis to clinical management. Chronic Dis Transl Med 2019; 5(3): 178-87. [Crossref]
- 52. Zygulska AL, Pierzchalski P. Novel Diagnostic Biomarkers in Colorectal Cancer. Int J Mol Sci 2022; 23(2): 852. [Crossref]
- 53. Abed J, Maalouf N, Manson AL, Earl AM, Parhi L, Emgård JEM, et al. Colon Cancer-Associated Fusobacterium nucleatum May Originate From the Oral Cavity and Reach Colon Tumors via the Circulatory System. Front Cell Infect Microbiol 2020; 10: 400. [Crossref]
- 54. Falony G, Vlachou A, Verbrugghe K, De Vuyst L. Cross-feeding between Bifidobacterium longum BB536 and acetate-converting, butyrate-producing colon bacteria during growth on oligofructose. Appl Environ Microbiol 2006; 72(12): 7835-41. [Crossref]
- 55. Lefebvre P, Cariou B, Lien F, Kuipers F, Staels B. Role of bile acids and bile acid receptors in metabolic regulation. Physiol Rev 2009; 89(1): 147-91. [Crossref]
- 56. Keku TO, Dulal S, Deveaux A, Jovov B, Han X. The gastrointestinal microbiota and colorectal cancer. Am J Physiol Gastrointest Liver Physiol 2015; 308(5): G351-63. [Crossref]
- 57. Jones ML, Martoni CJ, Ganopolsky JG, Labbé A, Prakash S. The human microbiome and bile acid metabolism: dysbiosis, dysmetabolism, disease and intervention. Expert Opin Biol Ther 2014; 14(4): 467-82. [Crossref]
- 58. Barman M, Unold D, Shifley K, Amir E, Hung K, Bos N, et al. Enteric salmonellosis disrupts the microbial ecology of the murine gastrointestinal tract. Infect Immun 2008; 76(3): 907-15. [Crossref]
- 59. Abreu MT, Peek RM Jr. Gastrointestinal malignancy and the microbiome. Gastroenterology 2014; 146(6): 1534-1546.e3. [Crossref]
- 60. Mima K, Cao Y, Chan AT, Qian ZR, Nowak JA, Masugi Y, et al. Fusobacterium nucleatum in Colorectal Carcinoma Tissue According to Tumor Location. Clin Transl Gastroenterol 2016; 7(11): e200. [Crossref]
- 61. Yamamura K, Baba Y, Miyake K, Nakamura K, Shigaki H, Mima K, et al. Fusobacterium nucleatum in gastroenterological cancer: Evaluation of measurement methods using quantitative polymerase chain reaction and a literature review. Oncol Lett 2017; 14(6): 6373-8. [Crossref]
- 62. Holt RA, Cochrane K. Tumor Potentiating Mechanisms of Fusobacterium nucleatum, A Multifaceted Microbe. Gastroenterology 2017; 152(4): 694-6. [Crossref]
- 63. Candela M, Turroni S, Biagi E, Carbonero F, Rampelli S, Fiorentini C, et al. Inflammation and colorectal cancer, when microbiota-host mutualism breaks. World J Gastroenterol 2014; 20(4): 908-22. [Crossref]
- 64. Arthur JC, Perez-Chanona E, Mühlbauer M, Tomkovich S, Uronis JM, Fan TJ, et al. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 2012; 338(6103): 120-3. [Crossref]
- 65. Siddiqui R, Boghossian A, Alharbi AM, Alfahemi H, Khan NA. The Pivotal Role of the Gut Microbiome in Colorectal Cancer. Biology (Basel) 2022; 11(11): 1642. [Crossref]
- 66. Burns MB, Lynch J, Starr TK, Knights D, Blekhman R. Virulence genes are a signature of the microbiome in the colorectal tumor microenvironment. Genome Med 2015; 7(1): 55. [PubMed]
- 67. Grivennikov SI, Karin M. Dangerous liaisons: STAT3 and NF-kappaB collaboration and crosstalk in cancer. Cytokine Growth Factor Rev 2010; 21(1): 11-9. [Crossref]
- 68. Ivanov K, Kolev N, Tonev A, Nikolova G, Krasnaliev I, Softova E, et al. Comparative analysis of prognostic significance of molecular markers of apoptosis with clinical stage and tumor differentiation in patients with colorectal cancer: a single institute experience. Hepatogastroenterology 2009; 56(89): 94-8. [PubMed]
- 69. Schwabe RF, Wang TC. Cancer. Bacteria deliver a genotoxic hit. Science 2012; 338(6103): 52-3. [Crossref]
- 70. Abed J, Emgård JE, Zamir G, Faroja M, Almogy G, Grenov A, et al. Fap2 Mediates Fusobacterium nucleatum Colorectal Adenocarcinoma Enrichment by Binding to Tumor-Expressed Gal-GalNAc. Cell Host Microbe 2016; 20(2): 215-25. [Crossref]
- 71. Rubinstein MR, Wang X, Liu W, Hao Y, Cai G, Han YW. Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/β-catenin signaling via its FadA adhesin. Cell Host Microbe 2013; 14(2): 195-206. [Crossref]
- 72. Radley S, Davis AE, Imray CH, Barker G, Morton DG, Baker PR, et al. Biliary bile acid profiles in familial adenomatous polyposis. Br J Surg 1992; 79(1): 89-90. [Crossref]
- 73. Iida N, Dzutsev A, Stewart CA, Smith L, Bouladoux N, Weingarten RA, et al. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science 2013; 342(6161): 967-70. [Crossref]
- 74. Roy CC, Kien CL, Bouthillier L, Levy E. Short-chain fatty acids: ready for prime time? Nutr Clin Pract 2006; 21(4): 351-66. [Crossref]
- 75. Canani RB, Costanzo MD, Leone L, Pedata M, Meli R, Calignano A. Potential beneficial effects of butyrate in intestinal and extraintestinal diseases. World J Gastroenterol 2011; 17(12): 1519-28. [Crossref]
- 76. Louis P, Hold GL, Flint HJ. The gut microbiota, bacterial metabolites and colorectal cancer. Nat Rev Microbiol 2014; 12(10): 661-72. [Crossref]
- 77. Berni Canani R, Di Costanzo M, Leone L. The epigenetic effects of butyrate: potential therapeutic implications for clinical practice. Clin Epigenetics 2012; 4(1): 4. [Crossref]
- 78. Scharlau D, Borowicki A, Habermann N, Hofmann T, Klenow S, Miene C, et al. Mechanisms of primary cancer prevention by butyrate and other products formed during gut flora-mediated fermentation of dietary fibre. Mutat Res 2009; 682(1): 39-53. [Crossref]
- 79. Zackular JP, Baxter NT, Chen GY, Schloss PD. Manipulation of the Gut Microbiota Reveals Role in Colon Tumorigenesis. mSphere 2015; 1(1): e00001-15. [Crossref]
- 80. Bullman S, Pedamallu CS, Sicinska E, Clancy TE, Zhang X, Cai D, et al. Analysis of Fusobacterium persistence and antibiotic response in colorectal cancer. Science 2017; 358(6369): 1443-8. [Crossref]
- 81. Çakır İ. Çakmakçı ML. Probiyotikler: tanımı, etki mekanizması, seçim ve güvenilirlik kriterleri. Gıda 2004; 29(6): 427-34.
- 82. Ceyhan N, Alıç H. Bağırsak mikroflorası ve probiyotikler. Türk Bilimsel Derlemeler Dergisi 2012; 5(1): 107-13.
- 83. Vera C, Guerrero C, Illanes A. Trends in lactose-derived bioactives: synthesis and purification. Syst Microbiol and Biomanuf 2022; 2(3): 393-412. [Crossref]
- 84. Yılmaz K, Altındiş M. Sindirim Sistemi Mikrobiyotasi ve Fekal Transplantasyon. Nobel Med 2017; 13(1): 9-15.
- 85. Swanson KS, Gibson GR, Hutkins R, Reimer RA, Reid G, Verbeke K, et al. The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of synbiotics. Nat Rev Gastroenterol Hepatol 2020; 17(11): 687-701. [Crossref]
- 86. Plaza-Diaz J, Ruiz-Ojeda FJ, Gil-Campos M, Gil A. Mechanisms of Action of Probiotics. Adv Nutr 2019; 10(suppl_1): S49-S66. [Crossref]
- 87. Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, et al. Expert consensus document: The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol 2017; 14(8): 491-502. [Crossref]
- 88. Vétizou M, Pitt JM, Daillère R, Lepage P, Waldschmitt N, Flament C, et al. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science 2015; 350(6264): 1079-84. [Crossref]
- 89. Chitapanarux I, Chitapanarux T, Traisathit P, Kudumpee S, Tharavichitkul E, Lorvidhaya V. Randomized controlled trial of live lactobacillus acidophilus plus bifidobacterium bifidum in prophylaxis of diarrhea during radiotherapy in cervical cancer patients. Radiat Oncol 2010; 5: 31. [Crossref]
- 90. Yeh KY, Wang HM, Chang JW, Huang JS, Lai CH, Lan YJ, et al. Omega-3 fatty acid-, micronutrient-, and probiotic-enriched nutrition helps body weight stabilization in head and neck cancer cachexia. Oral Surg Oral Med Oral Pathol Oral Radiol 2013; 116(1): 41-8. [Crossref]
- 91. Jones RM, Desai C, Darby TM, Luo L, Wolfarth AA, Scharer CD, et al. Lactobacilli Modulate Epithelial Cytoprotection through the Nrf2 Pathway. Cell Rep 2015; 12(8): 1217-25. [Crossref]
- 92. Gianotti L, Morelli L, Galbiati F, Rocchetti S, Coppola S, Beneduce A, et al. A randomized double-blind trial on perioperative administration of probiotics in colorectal cancer patients. World J Gastroenterol 2010; 16(2): 167-75. [Crossref]
- 93. Şahin M, Özlü B, Türkmenoğlu Ö, Çolak T. The Impact of Probiotics (Bifidobacterium Animalis and Lactobacillus BB-12) on the Quality of Life and Defecation Habits after Colorectal Excision Surgery. Turk J Colorectal Dis 2016; 26(3): 71-6.
- 94. Ramos A, Hemann MT. Drugs, Bugs, and Cancer: Fusobacterium nucleatum Promotes Chemoresistance in Colorectal Cancer. Cell 2017; 170(3): 411-3. [Crossref]
- 95. Yan X, Liu L, Li H, Qin H, Sun Z. Clinical significance of Fusobacterium nucleatum, epithelial-mesenchymal transition, and cancer stem cell markers in stage III/IV colorectal cancer patients. Onco Targets Ther 2017; 10: 5031-46. [Crossref]
- 96. Daillère R, Vétizou M, Waldschmitt N, Yamazaki T, Isnard C, Poirier-Colame V, et al. Enterococcus hirae and Barnesiella intestinihominis Facilitate Cyclophosphamide-Induced Therapeutic Immunomodulatory Effects. Immunity 2016; 45(4): 931-43. [Crossref]
- 97. Flanagan L, Schmid J, Ebert M, Soucek P, Kunicka T, Liska V, et al. Fusobacterium nucleatum associates with stages of colorectal neoplasia development, colorectal cancer and disease outcome. Eur J Clin Microbiol Infect Dis 2014; 33(8): 1381-90. [Crossref]
- 98. Davis CD, Milner JA. Gastrointestinal microflora, food components and colon cancer prevention. J Nutr Biochem 2009; 20(10): 743-52. [Crossref]
- 99. Ventura M, Turroni F, Motherway MO, MacSharry J, van Sinderen D. Host-microbe interactions that facilitate gut colonization by commensal bifidobacteria. Trends Microbiol 2012; 20(10): 467-76. [Crossref]
- 100. Ruas-Madiedo P, Medrano M, Salazar N, De Los Reyes-Gavilán CG, Pérez PF, Abraham AG. Exopolysaccharides produced by Lactobacillus and Bifidobacterium strains abrogate in vitro the cytotoxic effect of bacterial toxins on eukaryotic cells. J Appl Microbiol 2010; 109(6): 2079-86. [Crossref]
- 101. Bayoumi MA, Griffiths MW. In vitro inhibition of expression of virulence genes responsible for colonization and systemic spread of enteric pathogens using Bifidobacterium bifidum secreted molecules. Int J Food Microbiol 2012; 156(3): 255-63. [Crossref]
- 102. Chong ES. A potential role of probiotics in colorectal cancer prevention: review of possible mechanisms of action. World J Microbiol Biotechnol 2014; 30(2): 351-74. [Crossref]
- 103. Gao Z, Guo B, Gao R, Zhu Q, Wu W, Qin H. Probiotics modify human intestinal mucosa-associated microbiota in patients with colorectal cancer. Mol Med Rep 2015; 12(4): 6119-27. [Crossref]
- 104. Leonel AJ, Alvarez-Leite JI. Butyrate: implications for intestinal function. Curr Opin Clin Nutr Metab Care 2012; 15(5): 474-9. [Crossref]
- 105. Macfarlane GT, Macfarlane S. Bacteria, colonic fermentation, and gastrointestinal health. J AOAC Int 2012; 95(1): 50-60. [Crossref]
- 106. Pryde SE, Duncan SH, Hold GL, Stewart CS, Flint HJ. The microbiology of butyrate formation in the human colon. FEMS Microbiol Lett 2002; 217(2): 133-9. [Crossref]
- 107. Zhang Y, Zhou L, Bao YL, Wu Y, Yu CL, Huang YX, et al. Butyrate induces cell apoptosis through activation of JNK MAP kinase pathway in human colon cancer RKO cells. Chem Biol Interact 2010; 185(3): 174-81. [Crossref]
- 108. Guilloteau P, Martin L, Eeckhaut V, Ducatelle R, Zabielski R, Van Immerseel F. From the gut to the peripheral tissues: the multiple effects of butyrate. Nutr Res Rev 2010; 23(2): 366-84. [Crossref]
- 109. Tomasello G, Tralongo P, Damiani P, Sinagra E, Di Trapani B, Zeenny MN, et al. Dismicrobism in inflammatory bowel disease and colorectal cancer: changes in response of colocytes. World J Gastroenterol 2014; 20(48): 18121-30. [Crossref]
- 110. Gao Z, Guo B, Gao R, Zhu Q, Qin H. Microbiota disbiosis is associated with colorectal cancer. Front Microbiol 2015; 6: 20. [Crossref]
- 111. Zeller G, Tap J, Voigt AY, Sunagawa S, Kultima JR, Costea PI, et al. Potential of fecal microbiota for early-stage detection of colorectal cancer. Mol Syst Biol 2014; 10(11): 766. [Crossref]
- 112. Eklöf V, Löfgren-Burström A, Zingmark C, Edin S, Larsson P, Karling P, et al. Cancer-associated fecal microbial markers in colorectal cancer detection. Int J Cancer 2017; 141(12): 2528-36. [Crossref]
- 113. Imperiale TF, Ransohoff DF, Itzkowitz SH, Levin TR, Lavin P, Lidgard GP, et al. Multitarget stool DNA testing for colorectal-cancer screening. N Engl J Med 2014; 370(14): 1287-97. [Crossref]
- 114. Wong SH, Kwong TNY, Chow TC, Luk AKC, Dai RZW, Nakatsu G, et al. Quantitation of faecal Fusobacterium improves faecal immunochemical test in detecting advanced colorectal neoplasia. Gut 2017; 66(8): 1441-8. [Crossref]
- 115. 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. Clin Infect Dis 2015; 60(2): 208-15. [Crossref]
- 116. Kostic AD, Gevers D, Pedamallu CS, Michaud M, Duke F, Earl AM, et al. Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res 2012; 22(2): 292-8. [Crossref]
- 117. Yu J, Feng Q, Wong SH, Zhang D, Liang QY, Qin Y, et al. Metagenomic analysis of faecal microbiome as a tool towards targeted non-invasive biomarkers for colorectal cancer. Gut 2017; 66(1): 70-8. [Crossref]
- 118. Zackular JP, Rogers MA, Ruffin MT 4th, Schloss PD. The human gut microbiome as a screening tool for colorectal cancer. Cancer Prev Res (Phila) 2014; 7(11): 1112-21. [Crossref]
- 119. Scott AJ, Merrifield CA, Alexander JL, Marchesi JR, Kinross JM. Highlights from the Inaugural International Cancer Microbiome Consortium Meeting (ICMC), 5-6 September 2017, London, UK. Ecancermedicalscience 2017; 11: 791. [Crossref]
- 120. Şahiner F. Overview of bacteria in the colon microbiota and their relationship to colorectal cancer (Figure 1, Microbiology). In: tibbiviroloji.com (http://tibbiviroloji.com/4/tr/microbiology/sh/m.p1.htm), Türkiye. Available at: http://tibbiviroloji.com/4/tr/microbiology/en.1.microbiota.crc.png [Published; December 11, 2022]
- 121. Flemer B, Warren RD, Barrett MP, Cisek K, Das A, Jeffery IB, et al. The oral microbiota in colorectal cancer is distinctive and predictive. Gut 2018; 67(8): 1454-63. [Crossref]
- 122. Hu Y, Le Leu RK, Christophersen CT, Somashekar R, Conlon MA, Meng XQ, et al. Manipulation of the gut microbiota using resistant starch is associated with protection against colitis-associated colorectal cancer in rats. Carcinogenesis 2016; 37(4): 366-75. [Crossref]
- 123. Loke YL, Chew MT, Ngeow YF, Lim WWD, Peh SC. Colon Carcinogenesis: The Interplay Between Diet and Gut Microbiota. Front Cell Infect Microbiol 2020; 10: 603086. [Crossref]