Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Oncology Letters
      • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Biomedical Reports
      • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • Information for Authors
    • Information for Reviewers
    • Information for Librarians
    • Information for Advertisers
    • Conferences
  • Language Editing
Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • For Authors
    • For Reviewers
    • For Librarians
    • For Advertisers
    • Conferences
  • Language Editing
Login Register Submit
  • This site uses cookies
  • You can change your cookie settings at any time by following the instructions in our Cookie Policy. To find out more, you may read our Privacy Policy.

    I agree
Search articles by DOI, keyword, author or affiliation
Search
Advanced Search
presentation
International Journal of Oncology
Join Editorial Board Propose a Special Issue
Print ISSN: 1019-6439 Online ISSN: 1791-2423
Journal Cover
May-2021 Volume 58 Issue 5

Full Size Image

Cover Legend PDF

Sign up for eToc alerts
Recommend to Library

Journals

International Journal of Molecular Medicine

International Journal of Molecular Medicine

International Journal of Molecular Medicine is an international journal devoted to molecular mechanisms of human disease.

International Journal of Oncology

International Journal of Oncology

International Journal of Oncology is an international journal devoted to oncology research and cancer treatment.

Molecular Medicine Reports

Molecular Medicine Reports

Covers molecular medicine topics such as pharmacology, pathology, genetics, neuroscience, infectious diseases, molecular cardiology, and molecular surgery.

Oncology Reports

Oncology Reports

Oncology Reports is an international journal devoted to fundamental and applied research in Oncology.

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine is an international journal devoted to laboratory and clinical medicine.

Oncology Letters

Oncology Letters

Oncology Letters is an international journal devoted to Experimental and Clinical Oncology.

Biomedical Reports

Biomedical Reports

Explores a wide range of biological and medical fields, including pharmacology, genetics, microbiology, neuroscience, and molecular cardiology.

Molecular and Clinical Oncology

Molecular and Clinical Oncology

International journal addressing all aspects of oncology research, from tumorigenesis and oncogenes to chemotherapy and metastasis.

World Academy of Sciences Journal

World Academy of Sciences Journal

Multidisciplinary open-access journal spanning biochemistry, genetics, neuroscience, environmental health, and synthetic biology.

International Journal of Functional Nutrition

International Journal of Functional Nutrition

Open-access journal combining biochemistry, pharmacology, immunology, and genetics to advance health through functional nutrition.

International Journal of Epigenetics

International Journal of Epigenetics

Publishes open-access research on using epigenetics to advance understanding and treatment of human disease.

Medicine International

Medicine International

An International Open Access Journal Devoted to General Medicine.

Journal Cover
May-2021 Volume 58 Issue 5

Full Size Image

Cover Legend PDF

Sign up for eToc alerts
Recommend to Library

  • Article
  • Citations
    • Cite This Article
    • Download Citation
    • Create Citation Alert
    • Remove Citation Alert
    • Cited By
  • Similar Articles
    • Related Articles (in Spandidos Publications)
    • Similar Articles (Google Scholar)
    • Similar Articles (PubMed)
  • Download PDF
  • Download XML
  • View XML
Review

Association of the microbiome with colorectal cancer development (Review)

  • Authors:
    • Maha-Hamadien Abdulla
    • Disha Agarwal
    • Jaikee Kumar Singh
    • Thamer Bin Traiki
    • Manoj Kumar Pandey
    • Rehan Ahmad
    • Sandeep Kumar Srivastava
  • View Affiliations / Copyright

    Affiliations: Colorectal Research Chair, Department of Surgery, King Saud University College of Medicine, King Saud University, Riyadh 11472, Saudi Arabia, Department of Biosciences, Manipal University Jaipur, Jaipur, Rajasthan 303007, India, Department of Biomedical Sciences, Cooper Medical School of Rowan University, Camden, NJ 08103, USA
  • Article Number: 17
    |
    Published online on: March 3, 2021
       https://doi.org/10.3892/ijo.2021.5197
  • Expand metrics +
Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )
Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )
Cited By (CrossRef): 0 citations Loading Articles...

This article is mentioned in:



Abstract

Colorectal cancer (CRC) is the second most common malignancy causing cancer‑related mortality globally. It is the third most common type of cancer detected worldwide. The recent concept of the human body supporting a diverse community of microbes has revealed the important role these microbes play synergistically in maintaining normal homeostasis. The balance between the microbiomes and epithelial cells of the human body is essential for normal physiology. Evidence from meta‑genome analysis indicates that an imbalance in the microbiome is prominent in the guts of patients with CRC. Several studies have suggested that the gut microbiota can secrete metabolites [short‑chain fatty acids (SCFAs), vitamins, polyphenols and polyamines] that modulate the susceptibility of the colon and rectum by altering inflammation and DNA damage. The state of microbiome imbalance (dysbiosis) has been reported in patients with CRC, with an increasing population of ‘bad’ microbes and a decrease in ‘good’ microbes. The ‘good’ microbes, also known as commensal microbes, produce butyrate; however, ‘bad’ microbes cause a pro‑inflammatory state. The complex association between pathological microbial communities leading to cancer progression is not yet fully understood. An altered microbial metabolite profile plays a direct role in CRC metabolism. Furthermore, diet plays an essential role in the risk of gastrointestinal cancer development. High‑fiber diets regulate the gut microbiome and reduce the risk of CRC development, and may be fruitful in the better management of therapeutics. In the present review, the current status of the microbiome in CRC development is discussed.12
View Figures

Figure 1

Figure 2

View References

1 

Siegel RL, Miller KD, Goding Sauer A, Fedewa SA, Butterly LF, Anderson JC, Cercek A, Smith RA and Jemal A: Colorectal cancer statistics, 2020. CA Cancer J Clin. 70:145–164. 2020. View Article : Google Scholar : PubMed/NCBI

2 

Keum N and Giovannucci E: Global burden of colorectal cancer: Emerging trends, risk factors and prevention strategies. Nat Rev Gastroenterol Hepatol. 16:713–732. 2019. View Article : Google Scholar : PubMed/NCBI

3 

Helmink BA, Khan MAW, Hermann A, Gopalakrishnan V and Wargo JA: The microbiome, cancer, and cancer therapy. Nat Med. 25:377–388. 2019. View Article : Google Scholar : PubMed/NCBI

4 

Dahmus JD, Kotler DL, Kastenberg DM and Kistler CA: The gut microbiome and colorectal cancer: A review of bacterial pathogenesis. J Gastrointest Oncol. 9:769–777. 2018. View Article : Google Scholar : PubMed/NCBI

5 

Gagnière J, Raisch J, Veziant J, Barnich N, Bonnet R, Buc E, Bringer MA, Pezet D and Bonnet M: Gut microbiota imbalance and colorectal cancer. World J Gastroenterol. 22:501–518. 2016. View Article : Google Scholar : PubMed/NCBI

6 

Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER and Gordon JI: An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 444:1027–1031. 2006. View Article : Google Scholar : PubMed/NCBI

7 

Chung H, Pamp SJ, Hill JA, Surana NK, Edelman SM, Troy EB, Reading NC, Villablanca EJ, Wang S, Mora JR, et al: Gut immune maturation depends on colonization with a host-specific microbiota. Cell. 149:1578–1593. 2012. View Article : Google Scholar : PubMed/NCBI

8 

John GK and Mullin GE: The gut microbiome and obesity. Corr Oncol Rep. 18:452016. View Article : Google Scholar

9 

Dabke K, Hendrick G and Devkota S: The gut microbiome and metabolic syndrome. J Clin Invest. 129:4050–4057. 2019. View Article : Google Scholar : PubMed/NCBI

10 

Xu H, Liu M, Cao J, Li X, Fan D, Xia Y, Lu X, Li J, Ju D and Zhao H: The dynamic interplay between the gut microbiota and autoimmune diseases. J Immunol Res. 2019:75460472019. View Article : Google Scholar : PubMed/NCBI

11 

Kostic AD, Chun E, Robertson L, Glickman JN, Gallini CA, Michaud M, Clancy TE, Chung DC, Lochhead P, Hold GL, et al: Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe. 14:207–215. 2013. View Article : Google Scholar : PubMed/NCBI

12 

Ternes D, Karta J, Tsenkova M, Wilmes P, Haan S and Letellier E: Microbiome in colorectal cancer: How to get from Meta-omics to Mechanism. Trends Microbiol. 28:401–423. 2020. View Article : Google Scholar : PubMed/NCBI

13 

Schwabe RF and Jobin C: The microbiome and cancer. Nat Rev Cancer. 13:800–812. 2013. View Article : Google Scholar : PubMed/NCBI

14 

Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI and Knight R: Bacterial community variation in human body habitats across space and time. Science. 326:1694–1697. 2009. View Article : Google Scholar : PubMed/NCBI

15 

Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, Bewtra M, Knights D, Walters WA, Knight R, et al: Linking long-term dietary patterns with gut microbial enterotypes. Science. 334:105–108. 2011. View Article : Google Scholar : PubMed/NCBI

16 

Bhat MI and Kapila R: Dietary metabolites derived from gut microbiota: Critical modulators of epigenetic changes in mammals. Nutr Rev. 75:374–389. 2017. View Article : Google Scholar : PubMed/NCBI

17 

Wong SH, Kwong TNY, Chow TC, Luk AKC, Dai RZW, Nakatsu G, Lam TYT, Zhang L, Wu JCY, Chan FKL, et al: Quantitation of faecal Fusobacterium improves faecal immunochemical test in detecting advanced colorectal neoplasia. Gut. 66:1441–1448. 2017. View Article : Google Scholar :

18 

Coker OO, Nakatsu G, Dai RZ, Wu WKK, Wong SH, Ng SC, Chan FKL, Sung JJY and Yu J: Enteric fungal microbiota dysbiosis and ecological alterations in colorectal cancer. Gut. 68:654–662. 2019. View Article : Google Scholar :

19 

Ley RE, Peterson DA and Gordon JI: Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell. 124:837–848. 2006. View Article : Google Scholar : PubMed/NCBI

20 

Tlaskalová-Hogenová H, Stepánková R, Hudcovic T, Tucková L, Cukrowska B, Lodinová-Zádníková R, Kozáková H, Rossmann P, Bártová J, Sokol D, et al: Commensal bacteria (normal microflora), mucosal immunity and chronic inflammatory and autoimmune diseases. Immunol Lett. 93:97–108. 2004. View Article : Google Scholar : PubMed/NCBI

21 

Wang T, Cai G, Qiu Y, Fei N, Zhang M, Pang X, Jia W, Cai S and Zhao L: Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers. ISME J. 6:320–329. 2012. View Article : Google Scholar :

22 

Zackular JP, Rogers MA, Ruffin MT IV and Schloss PD: The human gut microbiome as a screening tool for colorectal cancer. Cancer Prev Res (Phila). 7:1112–1121. 2014. View Article : Google Scholar

23 

Yu YN and Fang JY: Gut microbiota and colorectal cancer. Gastrointest Tumors. 2:26–32. 2015. View Article : Google Scholar : PubMed/NCBI

24 

Wong SH and Yu J: Gut microbiota in colorectal cancer: Mechanisms of action and clinical applications. Nat Rev Gastroenterol Hepatol. 16:690–704. 2019. View Article : Google Scholar : PubMed/NCBI

25 

Sobhani I, Tap J, Roudot-Thoraval F, Roperch JP, Letulle S, Langella P, Corthier G, Tran Van Nhieu J and Furet JP: Microbial dysbiosis in colorectal cancer (CRC) patients. PLoS One. 6:e163932011. View Article : Google Scholar : PubMed/NCBI

26 

Sears CL: Enterotoxigenic bacteroides fragilis: A rogue among symbiotes. Clin Micobiol Rev. 22:349–369. 2009. View Article : Google Scholar

27 

Ahn J, Sinha R, Pei Z, Dominianni C, Wu J, Shi J, Goedert JJ, Hayes RB and Yang L: Human gut microbiome and risk for colorectal cancer. J Natl Cancer Inst. 105:1907–1911. 2013. View Article : Google Scholar : PubMed/NCBI

28 

Wu N, Yang X, Zhang R, Li J, Xiao X, Hu Y, Chen Y, Yang F, Lu N, Wang Z, et al: Dysbiosis signature of fecal microbiota in colorectal cancer patients. Microb Ecol. 66:462–470. 2013. View Article : Google Scholar : PubMed/NCBI

29 

Bonnet M, Buc E, Sauvanet P, Darcha C, Dubois D, Pereira B, Déchelotte P, Bonnet R, Pezet D and Darfeuille-Michaud A: Colonization of the human gut by E coli and colorectal cancer risk. Clin Cancer Res. 20:859–867. 2014. View Article : Google Scholar

30 

Buc E, Dubois D, Sauvanet P, Raisch J, Delmas J, Darfeuille-Michaud A, Pezet D and Bonnet R: High prevalence of mucosa-associated E coli producing cyclomudulin and genotoxin in colon cancer. PLoS One. 8:e569642013. View Article : Google Scholar

31 

Zhang H, Chang Y, Zheng Q, Zhang R, Hu C and Jia W: Altered intestinal microbiota associated with colorectal cancer. Front Med. 13:461–470. 2019. View Article : Google Scholar : PubMed/NCBI

32 

Marchesi JR, Dutilh BE, Hall N, Peters WHM, Roelofs R, Boleji A and Tjalsma H: Towards the human colorectal cancer microbiome. PLoS One. 6:e204472011. View Article : Google Scholar : PubMed/NCBI

33 

Zou S, Fang L and Lee MH: Dysbiosis of Gut microbiota in promoting the development of colorectal cancer. Gastroenterol Rep (Oxf). 6:1–12. 2018. View Article : Google Scholar

34 

Rubinstein MR, Wang X, Liu W, Hao Y, Cai G and Han YW: Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/β-catenin signaling via its FadA adhesin. Cell Host Microbe. 14:195–206. 2013. View Article : Google Scholar : PubMed/NCBI

35 

Gur C, Ibrahim Y, Isaacson B, Yamin R, Abed J, Gamliel M, Enk J, Bar-On Y, Stanietsky-Kaynan N, Coppenhagen-Glazer S, et al: Binding of the Fap2 protein of Fusobacterium nucleatum to human inhibitory receptor TIGIT protects tumors from immune cell attack. Immunity. 42:344–355. 2015. View Article : Google Scholar : PubMed/NCBI

36 

Abed J, Emgard JE, Zamir G, Faroja M, Almogy G, Grenov A, Sol A, Naor R, Pikarsky E, Atlan KA, et al: Fap2 mediates Fusobacterium nucleatum colorectal adenocarcinoma enrichment by binding to tumor-expressed gal-GalNAc. Cell Host Microbe. 20:215–225. 2016. View Article : Google Scholar : PubMed/NCBI

37 

Ma CT, Luo HS, Gao F, Tang QC and Chen W: Fusobacterium nucleatum promotes the progression of colorectal cancer by interacting with E-cadherin. Oncol Lett. 16:2606–2612. 2018.PubMed/NCBI

38 

Kourtidis A, Lu R, Pence LJ and Anastasiadis PZ: A central role for cadherin signaling in cancer. Exp Cell Res. 358:78–85. 2017. View Article : Google Scholar : PubMed/NCBI

39 

Kim WK, Kwon Y, Jang M, Park M, Kim J, Cho S, Jang DG, Lee WB, Jung SH, Choi HJ, et al: β-catenin activation down-regulates cell-cell junction-related genes and induces epithelial-to-mesenchymal transition in colorectal cancer. Sci Re. 9:184402019.

40 

Yu MR, Kim HJ and Park HRF: Fusobacterium nucleatum accelerates the progression of colitis-associated colorectal cancer by promoting EMT. Cancers (Basel). 12:27282020. View Article : Google Scholar

41 

Guo P, Tian Z, Kong X, Yang L, Shan X, Dong B, Ding X, Jing X, Jiang C, Jiang N and Yu Y: FadA promotes DNA damage and progression of Fusobacterium nucleatum-induced colorectal cancer through up-regulation of chk2. J Exp Clin Cancer Res. 39:2022020. View Article : Google Scholar : PubMed/NCBI

42 

Okita Y, Koi M, Takeda K, Ross R, Mukherjee B, Koeppe E, Stoffel EM, Galanko JA, McCoy AN, Keku TO, et al: Fusobacterium nucleatum infection correlates with two types of microsatellite alterations in colorectal cancer and triggers DNA damage. Gut Pathol. 12:462020. View Article : Google Scholar

43 

Sayed IM, Chakraborty A, Abd El-Hafeez AA, Sharma A, Sahan AZ, Huang WJM, Sahoo D, Ghosh P, Hazra TK and Das S: The DNA Glycosylase NEIL2 suppresses Fusobacterium-infection-induced inflammation and DNA damage in colonic epithelial cells. Cells. 9:19802020. View Article : Google Scholar :

44 

Guo S, Chen J, Chen F, Zeng Q, Liu WL and Zhang G: Exosomes derived from Fusobacterium nucleatum-infected colorectal cancer cells facilitate tumour metastasis by selectively carrying miR-1246/92b-3p/27a-3p and CXCL16. Gut. Nov 10–2020.Epub ahead of print. View Article : Google Scholar

45 

Lin R, Han C, Ding Z, Shi H, He R, Liu J, Qian W, Zhang Q, Fu X, Deng X, et al: Knock down of BMSC-derived Wnt3a or its antagonist analogs attenuate colorectal carcinogenesis induced by chronic Fusobacterium nucleatum infection. Cancer Lett. 495:165–179. 2020. View Article : Google Scholar : PubMed/NCBI

46 

Wang Q, Yu C, Yue C and Liu X and Liu X: Fusobacterium nucleatum produces cancer stem cell characteristics via EMT-resembling variations. Int J Clin Exp Pathol. 13:1819–1828. 2020.PubMed/NCBI

47 

Wu S, Rhee KJ, Zhang M, Franco A and Sears CL: Bacteroides fragilis toxin stimulates intestinal epithelial cell shedding and gamma-secretase dependent E-cadherin cleavage. J Cell Sci. 120:1944–1952. 2007. View Article : Google Scholar : PubMed/NCBI

48 

Tian X, Liu Z, Niu B, Zhang J, Lee SR, Zhao Y, Harris DC and Zheng G: E-cadherin/beta-catenin complex and the epithelial barrier. J Biomed Biotechnol. 2011:5673052011. View Article : Google Scholar

49 

Sears CL, Geis AL and Housseau F: Bacteroides fragilis subverts mucosal biology: From symbiont to colon carcinogenesis. J Clin Invest. 124:4166–4172. 2014. View Article : Google Scholar : PubMed/NCBI

50 

Nistal E, Fernández-Fernández N, Vivas S and Olcoz JL: Factors determining colorectal cancer: The role of the intestinal microbiota. Front Oncol. 5:2202015. View Article : Google Scholar : PubMed/NCBI

51 

Zamani S, Taslimi R, Sarabi A, Jasemi S, Sechi LA and Feizabadi MM: Enterotoxigenic Bacteroides fragilis: A possible etiological candidate for bacterially-induced colorectal precancerous and cancerous lesions. Frontier Cell Infect Microbiol. 9:4492020. View Article : Google Scholar

52 

Liu QQ, Li CM, Fu LN, Wang HL, Tan J, Wang YQ, Sun DF, Gao QY, Chen YX and Fang JY: Enterotoxigenic Bacteroides fragilis induces the stemness in colorectal cancer via upregulating histone demethylase JMJD2B. Gut Microbes. 12:17889002020. View Article : Google Scholar :

53 

Hwang S, Lee CG, Jo M, Park CO, Gwon SY, Hwang S, Yi HC, Lee SY, Eom YB, Karim B and Rhee KJ: Enterotoxigenic Bacteroides fragilis infection exacerbates tumorigenesis in AOM/DSS mouse model. Int J Med Sci. 17:145–152. 2020. View Article : Google Scholar :

54 

Roberti MP, Yonekura S, Duong CPM, Picard M, Ferrere G, Tidjani Alou M, Rauber C, Iebba V, Lehmann CHK, Amon L, et al: Chemotherapy-induced ileal crypt apoptosis and the ileal microbiome shape immunosurveillance and prognosis of proximal colon cancer. Nat Med. 26:919–931. 2020. View Article : Google Scholar : PubMed/NCBI

55 

Bao Y, Tang J, Qian Y, Sun T, Chen H, Chen Z, Sun D, Zhong M, Chen H, Hong J, et al: Long noncoding RNA BFAL1 mediates enterotoxigenic Bacteroides fragilis-related carcinogenesis in colorectal cancer via the RHEB/mTOR pathway. Cell Death Dis. 10:6752019. View Article : Google Scholar : PubMed/NCBI

56 

Arthur JC, Perez-Chanona E, Muhlbauer M, Tomkovich S, Uronis JM, Fan TJ, Campbell BJ, Abujamel T, Dogan B, Rogers AB, et al: Intestinal inflammation targets cancer-inducing activity of the microbiota. Science. 338:120–123. 2012. View Article : Google Scholar : PubMed/NCBI

57 

Tjalsma H, Boleij A, Marchesi JR and Dutilh BE: A bacterial driver-passenger model for colorectal cancer: Beyond the usual suspects. Nat Rev Microbiol. 10:575–582. 2012. View Article : Google Scholar : PubMed/NCBI

58 

Swidsinski A, Khilkin M, Kerjaschki D, Schreiber S, Ortner M, Weber J and Lochs H: Association between intraepithelial Escherichia coli and colorectal cancer. Gastroenterology. 115:281–286. 1998. View Article : Google Scholar : PubMed/NCBI

59 

Martin HM, Campbell BJ, Hart CA, Mpofu C, Nayar M, Singh R, Englyst H, Williams HF and Rhodes JM: Enhanced Escherichia coli adherence and invasion in Crohn's disease and colon cancer. Gastroenterology. 127:80–93. 2004. View Article : Google Scholar : PubMed/NCBI

60 

Darfeuille-Michaud A, Neut C, Barnich N, Lederman E and Di Martino P: Presence of adherent Escherichia coli strains in ileal mucosa of patients with Crohn's disease. Gastroenterology. 115:1405–1413. 1998. View Article : Google Scholar : PubMed/NCBI

61 

Darfeuille-Michaud A, Boudeau J, Bulois P, Neut C, Glasser AL, Barnich N, Bringer MA, Swidsinski A, Beaugerie L and Colombel JF: High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn's disease. Gastroenterology. 127:412–421. 2004. View Article : Google Scholar : PubMed/NCBI

62 

Lax AJ: Opinion: Bacterial toxins and cancer-a case to answer? Nat Rev Microbiol. 3:343–349. 2005. View Article : Google Scholar : PubMed/NCBI

63 

Thelestam M and Frisan T: Cytolethal distending toxins. Rev Physiol Biochem Pharmacol. 152:111–133. 2004. View Article : Google Scholar : PubMed/NCBI

64 

Falzano L, Filippini P, Travaglione S, Miraglia AG, Fabbri A and Fiorentini C: Escherichia coli cytotoxic necrotizing factor 1 blocks cell cycle G2/M transition in uroepithelial cells. Infect Immun. 74:3765–3772. 2006. View Article : Google Scholar : PubMed/NCBI

65 

Malorni W and Fiorentini C: Is the Rac GTPase-activating toxin CNF1 a smart hijacker of host cell fate? FASEB J. 20:606–609. 2006. View Article : Google Scholar : PubMed/NCBI

66 

Jubelin G, Chavez CV, Taieb F, Banfield MJ, Samba-Louaka A, Nobe R, Nougayrède JP, Zumbihl R, Givaudan A, Escoubas JM and Oswald E: Cycle inhibiting factors (CIFs) are a growing family of functional cyclomodulins present in invertebrate and mammal bacterial pathogens. PLoS One. 4:e48552009. View Article : Google Scholar : PubMed/NCBI

67 

Nougayrede JP, Homburg S, Taieb F, Boury M, Brzuszkiewicz E, Gottschalk G, Buchrieser C, Hacker J, Dobrindt U and Oswald E: Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science. 313:848–851. 2006. View Article : Google Scholar : PubMed/NCBI

68 

Cuevas-Ramosa G, Petita CR, Marcqa I, Bourya M, Oswalda E and Nougayrède JP: Escherichia coli induces DNA damage in vivo and triggers genomic instability in mammalian cells. Proc Natl Acad Sci USA. 107:11357–11542. 2010.

69 

Kwong TNY, Wang X, Nakatsu G, Chow TC, Tipoe T, Dai RZW, Tsoi KKK, Wong MCS, Tse G, Chan MTV, et al: Association between bactereia from specific microbes and subsequent diagnosis of colorectal cancer. Gastroenterology. 155:383–390.e8. 2018. View Article : Google Scholar

70 

Tsoi H, Chu ESH, Zhang X, Sheng J, Nakatsu G, Ng SC, Chan AWH, Chan FKL, Sung JJY and Yu J: Peptostreptococcus anaerobius induces intracellular cholesterol biosynthesis in colon cells to induce proliferation and causes dysplasia in mice. Gastroenterology. 152:1419–1433.e5. 2017. View Article : Google Scholar : PubMed/NCBI

71 

Purcell RV, Visnovska M, Biggs PJ, Schmeier S and Frizelle FA: Distinct gut microbiome patterns associate with consensus molecular subtypes of colorectal cancer. Sci Rep. 7:115902017. View Article : Google Scholar : PubMed/NCBI

72 

Long X, Wong CC, Tong L, Chu ESH, Ho Szeto C, Go MYY, Coker OO, Chan AWH, Chan FKL, Sung JJY and Yu J: Peptostreptococcus anaerobius promotes colorectal carcinogenesis and modulates tumour immunity. Nat Microbiol. 4:2319–2330. 2019. View Article : Google Scholar : PubMed/NCBI

73 

Kumar R, Herold JL, Schady D, Davis J, Kopetz S, Martinez-Moczygemba M, Murray BE, Han F, Li Y, Callaway E, et al: Streptococcus gallolyticus Subsp gallolyticus promotes colorectal tumor development. PLoS Pathog. 13:e10064402017. View Article : Google Scholar

74 

Aymeric L, Donnadieu F, Mulet C, du Merle L, Nigro G, Saffarian A, Bérard M, Poyart C, Robine S, Regnault B, et al: Colorect a l ca ncer sp eci f ic cond itions promote Streptococcus gallolyticus gut colonization. Proc Natl Acad Sci USA. 115:E283–E291. 2018. View Article : Google Scholar

75 

Konstantinov SR, Kuipers EJ and Peppelenbosch MP: Functional genomic analysis of Gut microbiota for CRC screening. Nat Rev Gastroenterol Hepatol. 10:741–745. 2013. View Article : Google Scholar : PubMed/NCBI

76 

Gamallat Y, Meyiah A, Kuugbee ED, Hago AM, Chiwala G, Awadasseid A, Bamba D, Zhang X, Shang X, Luo F and Xin Y: Lactobacillus rhamnosus induced epithelial cell apoptosis, ameliorates inflammation and prevents colon cancer development in an animal model. Biomed Pharmacother. 83:536–541. 2016. View Article : Google Scholar : PubMed/NCBI

77 

Wallace BD, Wang H, Lane KT, Scott JE, Orans J, Koo JS, Venkatesh M, Jobin C, Yeh LA, Mani S and Redinbo MR: Alleviating cancer drug toxicity by inhibiting a bacterial enzyme. Science. 330:831–835. 2010. View Article : Google Scholar : PubMed/NCBI

78 

Marchesan J, Jiao YZ, Schaff RA, Hao J, Morelli T, Kinney JS, Gerow E, Sheridan R, Rodrigues V, Paster BJ, et al: TLR4, NOD1 and NOD2 mediate immune recognition of putative newly identified periodontal pathogens. Mol Oral Microbiol. 31:243–258. 2015. View Article : Google Scholar : PubMed/NCBI

79 

Xu J, Yang M, Wang D, Zhang S, Yan S, Zhu Y and Chen W: Alteration of the abundance of Parvimonas micra in the gut along the adenoma-carcinoma sequence. Oncol Lett. 20:1062020. View Article : Google Scholar :

80 

Allali I, Boukhatem N, Bouguenouch L, Hardi H, Boudouaya HA, Cadenas MB, Ouldim K, Amzazi S, Azcarate-Peril MA and Ghazal H: Gut microbiome of Moroccan colorectal cancer patients. Med Microbiol Immunol (Berl). 207:211–225. 2018. View Article : Google Scholar

81 

Yang Y, Cai Q, Shu XO, Steinwandel MD, Blot WJ, Zheng W and Long J: Prospective study of oral microbiome and colorectal cancer risk in low-income and African American populations. Int J Cancer. 144:2381–2389. 2019. View Article : Google Scholar :

82 

Dai Z, Coker OO, Nakatsu G, Wu WKK, Zhao L, Chen Z, Chan FKL, Kristiansen K, Sung JJY, Wong SH and Yu J: Multi-cohort analysis of colorectal cancer metagenome identified altered bacteria across populations and universal bacterial markers. Microbiome. 6:702018. View Article : Google Scholar : PubMed/NCBI

83 

Sobrinho AR: Cytokine production in response to endodontic infection in germ-free mice. Oral Microbiol Immunol. 17:344–353. 2002. View Article : Google Scholar

84 

Lomholt JA and Kilian M: Immunoglobulin A1 protease activity in Gemella haemolysans. J Clin Microbiol. 38:2760–2762. 2000. View Article : Google Scholar : PubMed/NCBI

85 

Montalban-Arques A and Scharl M: Intestinal microbiota and colorectal carcinoma: Implications for pathogenesis, diagnosis, and therapy. EBioMedicine. 48:648–655. 2019. View Article : Google Scholar : PubMed/NCBI

86 

Allen J and Sears CL: Impact of the gut microbiome on the genome and epigenome of colon epithelial cells: Contributions to colorectal cancer development. Genome Med. 11:112019. View Article : Google Scholar : PubMed/NCBI

87 

Xia X, Wu WKK, Wong SH, Liu D, Kwong TNY, Nakatsu G, Yan PS, Chuang YM, Chan MW, Coker OO, et al: Bacteria pathogens drive host colonic epithelial cell promoter hypermethylation of tumor suppressor genes in colorectal cancer. Microbiome. 8:1082020. View Article : Google Scholar : PubMed/NCBI

88 

Sobhani I, Rotkopf H and Khazaie K: Bacteria-related changes in host DNA methylation and risk for CRC. Gut Microbes. 12:e18008982020. View Article : Google Scholar

89 

Gagnière J, Bonnin V, Jarrousse AS, Cardamone E, Agus A, Uhrhammer N, Sauvanet P, Déchelotte P, Barnich N, Bonnet R, et al: Interactions between microsatellite instability and human gut colonization by Escherichia coli in colorectal cancer. Clin Sci (Lond). 131:471–485. 2017. View Article : Google Scholar

90 

Foran E, Garrity-Park MM, Mureau C, Newell J, Smyrk TC, Limburg PJ and Egan LJ: Upregulation of DNA methyltransferase-mediated gene silencing, anchorage-independent growth, and migration of colon cancer cells by interleukin-6. Mol Cancer Res. 8:471–481. 2010. View Article : Google Scholar : PubMed/NCBI

91 

Li Y, Deuring J, Peppelenbosch MP, Kuipers EJ, de Haar C and van der Woude CJ: IL-6-induced DNMT1 activity mediates SOCS3 promoter hypermethylation in ulcerative colitis-related colorectal cancer. Carcinogenesis. 3:1889–1896. 2012. View Article : Google Scholar

92 

Hartnett L and Egan LJ: Inflammation, DNA methylation and colitis-associated cancer. Carcinogenesis. 33:723–731. 2012. View Article : Google Scholar : PubMed/NCBI

93 

Hashemi Goradel N, Heidarzadeh S, Jahangiri S, Farhood B, Mortezaee K, Khanlarkhani N and Neghadari B: Fusobacterium nucleatum and colorectal cancer: A mechanistic overview. J Cell Physiol. 234:2337–2344. 2018. View Article : Google Scholar : PubMed/NCBI

94 

Yu T, Guo F, Yu Y, Sun T, Ma D, Han J, Qian Y, Kryczek I, Sun D, Nagarsheth N, et al: Fusobacterium nucleatum promotes chemoresistance to colorectal cancer by modulating autophagy. Cell. 170:548–563.e16. 2017. View Article : Google Scholar : PubMed/NCBI

95 

Tarallo S, Ferrero G, Gallo G, Francavilla A, Clerico G, Realis Luc A, Manghi P, Thomas AM, Vineis P, Segata N, et al: Altered fecal small RNA profiles in colorectal cancer reflected gut microbiome composition in stool samples. mSystems. 4:200289–19. 2019. View Article : Google Scholar

96 

Yuan C, Steer CJ and Subramanian S: Host-microRNA-Microbiota interaction in colorectal cancer. Genes (Basel). 10:2702019. View Article : Google Scholar

97 

Kang M and Martin A: Microbiome and colorectal cancer: Unraveling host-microbiota interactions in colitis-associated colorectal cancer development. Semin Immunol. 13:3–13. 2017. View Article : Google Scholar

98 

Cooks T, Pateras IS, Tarcic O, Solomon H, Schetter AJ, Wilder S, Lozano G, Pikarsky E, Forshew T, Rosenfeld N, et al: Mutant p53 prolongs NF-κB activation and promotes chronic inflammation and inflammation-associated colorectal cancer. Cancer Cell. 23:634–646. 2013. View Article : Google Scholar : PubMed/NCBI

99 

Lasry A, Zinger A and Ben-Neriah Y: Inflammatory networks underlying colorectal cancer. Nat Immunol. 17:230–240. 2016. View Article : Google Scholar : PubMed/NCBI

100 

Ruskov H, Burcharth J and Pommergaard HC: Linking gut microbiota to colorectal cancer. J Cancer. 8:3378–3395. 2017. View Article : Google Scholar

101 

Grivennikov SI: Inflammation and colorectal cancer: Colitisassociated neoplasia. Semin Immunopathol. 35:229–244. 2013. View Article : Google Scholar

102 

Coussens LM and Pollard JW: Leukocytes in mammary development and cancer. Cold Spring Harb Perspect Biol. 3:a0032852011. View Article : Google Scholar

103 

Chen T, Li Q, Wu J, Wu Y, Peng W, Li H, Wang J, Tang X, Peng Y and Fu X: Fusobacterium nucleatum promotes M2 polarization of macrophages in the microenvironment of colorectal tumours via a TLR4-dependent mechanism. Cancer Immunol Immunother. 67:1635–1646. 2018. View Article : Google Scholar : PubMed/NCBI

104 

Drewes JL, Housseau F and Sears CL: Sporadic colorectal cancer: Microbial contributors to disease prevention, development and therapy. Br J Cancer. 115:273–280. 2016. View Article : Google Scholar : PubMed/NCBI

105 

Dejea CM, Wick EC, Hechenbleikner EM, White JR, Mark Welch JL, Rossetti BJ, Peterson SN, Snesrud EC, Borisy GG, Lazarev M, et al: Microbiota organization is a distinct feature of proximal colorectal cancers. Proc Natl Acad Sci USA. 111:18321–18326. 2014. View Article : Google Scholar : PubMed/NCBI

106 

Villéger R, Lopès A, Veziant J, Gagnière J, Barnich N, Billard E, Boucher D and Bonnet M: Microbial markers in colorectal cancer detection and/or prognosis. World J Gastroenterol. 24:2327–2347. 2018. View Article : Google Scholar : PubMed/NCBI

107 

Kostic AD, Gevers D, Pedamallu CS, Michaud M, Duke F, Earl AM, Ojesina AI, Jung J, Bass AJ, Tabernero J, et al: Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res. 22:292–298. 2012. View Article : Google Scholar :

108 

Yu J, Feng Q, Wong SH, Zhang D, Liang QY, Qin Y, Tang L, Zhao H, Stenvang J, Li Y, et al: Metagenomic analysis of faecal microbiome as a tool towards targeted non-invasive biomarkers for colorectal cancer. Gut. 66:70–78. 2017. View Article : Google Scholar

109 

Wei Z, Cao S, Liu S, Yao Z, Sun T, Li Y, Li J, Zhang D and Zhou Y: Could gut microbiota serve as prognostic biomarker associated with colorectal cancer patients' survival? A pilot study on relevant mechanism. Oncotarget. 7:46158–46170. 2016. View Article : Google Scholar : PubMed/NCBI

110 

Wu Y, Ziao N, Zhu R, Zhang Y, Wu D, Wang AJ, Fang S, Tao L, Li Y, Cheng S, et al: Identification of microbial markers across populations in early detection of colorectal cancer. bioRixv. https://doi.org/10.1101/2020.08.16.253344.

111 

Liu S, da Cunha AP, Rezende RM, Cialic R, Wei Z, Bry L, Comstock LE, Gandhi R and Weiner HL: The host shapes the gut Microbiota via fecal MicroRNA. Cell Host Microbe. 19:32–43. 2016. View Article : Google Scholar : PubMed/NCBI

112 

Yuan C, Burns MB, Subramanian S and Blekhman R: Interaction between Host MicroRNAs and the Gut Microbiota in Colorectal Cancer. mSystems. 3:e00205–17. 2018. View Article : Google Scholar : PubMed/NCBI

113 

Sarshar M, Scribano D, Ambrosi C, Palamara AT and Masotti A: Fecal microRNAs as innovative biomarkers of intestinal diseases and effective players in Host-Microbiome interactions. Cancers (Basel). 12:21742020. View Article : Google Scholar

114 

Yang T, Owen JL, Lightfoot YL, Kladde MP and Mohamadzadeh M: Microbiota impact on the epigenetic regulation of colorectal cancer. Trends Mol Med. 19:714–725. 2013. View Article : Google Scholar : PubMed/NCBI

115 

Li M, Chen WD and Wang YD: The roles of the gut microbiotamiRNA interaction in the host pathophysiology. Mol Med. 26:1012020. View Article : Google Scholar

116 

Geller LT, Barzily-Rokni M, Danino T, Jonas OH, Shental N, Nejman D, Gavert N, Zwang Y, Cooper ZA, Shee K, et al: Potential role of intratumor bacteria in mediating tumor resistance to the chemotherapeutic drug gemcitabine. Science. 357:1156–1160. 2017. View Article : Google Scholar : PubMed/NCBI

117 

Serna G, Ruiz-Pace F, Hernando J, Alonso L, Fasani R, Landolfi S, Comas R, Jimenez J, Elez E, Bullman S, et al: Fusobacterium nucleatum persistance and risk of recurrence after preoperative treatment in locally advanced rectal cancer. Ann Oncol. 31:1366–1375. 2020. View Article : Google Scholar : PubMed/NCBI

118 

Iida N, Dzutsev A, Stewart CA, Smith L, Bouladoux N, Weingarten RA, Molina DA, Salcedo R, Back T, Cramer S, et al: Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science. 342:967–970. 2013. View Article : Google Scholar : PubMed/NCBI

119 

Viaud S, Saccheri F, Mignot G, Yamazaki T, Daillère R, Hannani D, Enot DP, Pfirschke C, Engblom C, Pittet MJ, et al: The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide. Science. 342:971–976. 2013. View Article : Google Scholar : PubMed/NCBI

120 

Xu X and Zhang X: Effects of cyclophosphamide on immune system and gut microbiota in mice. Microbiol Res. 171:97–106. 2015. View Article : Google Scholar : PubMed/NCBI

121 

Sivan A, Corrales L, Hubert N, Williams JB, Aquino-Michaels K, Earley JM, Benyamin FW, Lei YM, Jabri B, Alegre ML, et al: Commensal Bifidobacterium promotes antitumor activity and facilitates anti-PD-L1 efficacy. Science. 350:1084–1089. 2015. View Article : Google Scholar : PubMed/NCBI

122 

Vétizou M, Pitt JM, Daillère R, Lepage P, Waldschmitt N, Flament C, Rusakiewicz S, Routy B, Roberti MP, Duong CP, et al: Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science. 350:1079–1084. 2015. View Article : Google Scholar : PubMed/NCBI

123 

Uribe-Herranz M, Bittinger K, Rafail S, Guedan S, Pierini S, Tanes C, Ganetsky A, Morgan MA, Gill S, Tanyi JL, et al: Gut microbiota modulates adoptive cell therapy via CD8α dendritic cells and IL-12. JCI Insight. 3:e949522018. View Article : Google Scholar

124 

Hold GL: Gastrointestinal microbiota and colon cancer. Dig Dis. 34:244–250. 2016. View Article : Google Scholar : PubMed/NCBI

Related Articles

  • Abstract
  • View
  • Download
  • Twitter
Copy and paste a formatted citation
Spandidos Publications style
Abdulla M, Agarwal D, Singh JK, Traiki TB, Pandey MK, Ahmad R and Srivastava SK: Association of the microbiome with colorectal cancer development (Review). Int J Oncol 58: 17, 2021.
APA
Abdulla, M., Agarwal, D., Singh, J.K., Traiki, T.B., Pandey, M.K., Ahmad, R., & Srivastava, S.K. (2021). Association of the microbiome with colorectal cancer development (Review). International Journal of Oncology, 58, 17. https://doi.org/10.3892/ijo.2021.5197
MLA
Abdulla, M., Agarwal, D., Singh, J. K., Traiki, T. B., Pandey, M. K., Ahmad, R., Srivastava, S. K."Association of the microbiome with colorectal cancer development (Review)". International Journal of Oncology 58.5 (2021): 17.
Chicago
Abdulla, M., Agarwal, D., Singh, J. K., Traiki, T. B., Pandey, M. K., Ahmad, R., Srivastava, S. K."Association of the microbiome with colorectal cancer development (Review)". International Journal of Oncology 58, no. 5 (2021): 17. https://doi.org/10.3892/ijo.2021.5197
Copy and paste a formatted citation
x
Spandidos Publications style
Abdulla M, Agarwal D, Singh JK, Traiki TB, Pandey MK, Ahmad R and Srivastava SK: Association of the microbiome with colorectal cancer development (Review). Int J Oncol 58: 17, 2021.
APA
Abdulla, M., Agarwal, D., Singh, J.K., Traiki, T.B., Pandey, M.K., Ahmad, R., & Srivastava, S.K. (2021). Association of the microbiome with colorectal cancer development (Review). International Journal of Oncology, 58, 17. https://doi.org/10.3892/ijo.2021.5197
MLA
Abdulla, M., Agarwal, D., Singh, J. K., Traiki, T. B., Pandey, M. K., Ahmad, R., Srivastava, S. K."Association of the microbiome with colorectal cancer development (Review)". International Journal of Oncology 58.5 (2021): 17.
Chicago
Abdulla, M., Agarwal, D., Singh, J. K., Traiki, T. B., Pandey, M. K., Ahmad, R., Srivastava, S. K."Association of the microbiome with colorectal cancer development (Review)". International Journal of Oncology 58, no. 5 (2021): 17. https://doi.org/10.3892/ijo.2021.5197
Follow us
  • Twitter
  • LinkedIn
  • Facebook
About
  • Spandidos Publications
  • Careers
  • Cookie Policy
  • Privacy Policy
How can we help?
  • Help
  • Live Chat
  • Contact
  • Email to our Support Team