Systematic Review of Fecal and Mucosa-Associated Microbiota Compositional Shifts in Colorectal Cancer

Document Type : Review Article

Authors

1 Nursing Student, Nursing & Midwifery Faculty, Bushehr Universiity of Medical Sciences, Bushehr, Iran

2 Student Research Committee, Bushehr University of Medical Sciences, Bushehr, Iran

3 Department of English Language, Faculty of Paramedical Sciences, Shiraz University of Medical Sciences, Shiraz, Iran.

4 Department of Epidemiology and Biostatistics, School of Public Health Bushehr University of Medical Sciences; Bushehr, Iran.

Abstract

Introduction:
Gut microbiota is a major component of the intestinal luminal environment and plays important roles in colorectal cancer.
Object:
systematically review all the existing literature on the association of mucosa-associated and fecal microbiota with incidence, location, and stage of colorectal adenoma and carcinoma.
Methods:
The scientific search was done up to July 2018. The search was limited to the English language with predefined and proper keywords. Among 616 articles some of them were eliminated due to some reasons. The inclusion and exclusion criteria were defined. In the next step two reviewers (M.M and Z.K) independently scanned the titles of all retrieved articles, removed duplicates, and identified potentially relevant abstracts for further assessment. The Newcastle-Ottawa Scale (NOS) for assessing the Quality was used for quality control.

Result:
Finally, 54 articles were entered into the study. Fusobacteria 39 (72%), Firmicutes 22(40%), Bacteroidetes 20 (37%), Proteobacteria 15(27%), Actinobacteria 10(18%) was the most prevalent phylum which was found in colorectal cancer patients. Among these taxa some of them were increased in colorectal cancer patients compared to the control; on the other hand, some taxon was declined in colorectal cancer patients. Besides this, in some taxon there were controversies among articles.

Conclusion:
Early detection of CRC is essential because patients whose cancer are detected at an early stage have more chance of survival. Until now there are several studies have demonstrated the potential rule of gut microbiota to be used for detection of CRC, but there is not any predefining protocol for screening. Although we found lots of articles which were published in this area, for defining a precise microbiota profile we need large multicenter case-control studies, where can show the effect of most important confounding factors like nutrition, ethnicity, physical activity, smoking consumption, and genetic background.

Keywords


1.         Kubisch, C.H., A. Crispin, U. Mansmann, B. Göke, and F.T. Kolligs, Screening for colorectal cancer is associated with lower disease stage: a population-based study. Clinical Gastroenterology and Hepatology, 2016. 14(11): p. 1612-1618. e3.
2.         Brenner, H., C. Stock, and M. Hoffmeister, Effect of screening sigmoidoscopy and screening colonoscopy on colorectal cancer incidence and mortality: systematic review and meta-analysis of randomised controlled trials and observational studies. Bmj, 2014. 348: p. g2467.
3.         Syngal, S., Colorectal cancer in young adults. Digestive diseases and sciences, 2015. 60(3): p. 722-733.
4.         Gagnière, J., J. Raisch, J. Veziant, et al., Gut microbiota imbalance and colorectal cancer. World journal of gastroenterology, 2016. 22(2): p. 501.
5.         Wirbel, J., P.T. Pyl, E. Kartal, et al., Meta-analysis of fecal metagenomes reveals global microbial signatures that are specific for colorectal cancer. Nature medicine, 2019. 25(4): p. 679.
6.         Thomas, A.M., P. Manghi, F. Asnicar, et al., Metagenomic analysis of colorectal cancer datasets identifies cross-cohort microbial diagnostic signatures and a link with choline degradation. Nature medicine, 2019. 25(4): p. 667.
7.         Qin, J., R. Li, J. Raes, et al., A human gut microbial gene catalogue established by metagenomic sequencing. nature, 2010. 464(7285): p. 59.
8.         Eckburg, P.B., E.M. Bik, C.N. Bernstein, et al., Diversity of the human intestinal microbial flora. science, 2005. 308(5728): p. 1635-1638.
9.         Kostic, A.D., E. Chun, L. Robertson, et al., Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell host & microbe, 2013. 14(2): p. 207-215.
10.       Shang, F.-M. and H.-L. Liu, Fusobacterium nucleatum and colorectal cancer: A review. World journal of gastrointestinal oncology, 2018. 10(3): p. 71.
11.       Xu, K. and B. Jiang, Analysis of mucosa-associated microbiota in colorectal cancer. Medical science monitor: international medical journal of experimental and clinical research, 2017. 23: p. 4422.
12.       Swidsinski, A., M. Khilkin, D. Kerjaschki, et al., Association between intraepithelial Escherichia coli and colorectal cancer. Gastroenterology, 1998. 115(2): p. 281-286.
13.       Li, Y.-Y., Q.-X. Ge, J. Cao, et al., Association of Fusobacterium nucleatum infection with colorectal cancer in Chinese patients. World journal of gastroenterology, 2016. 22(11): p. 3227.
14.       Zhou, Y., H. He, H. Xu, et al., Association of oncogenic bacteria with colorectal cancer in South China. Oncotarget, 2016. 7(49): p. 80794.
15.       Ohigashi, S., K. Sudo, D. Kobayashi, et al., Changes of the intestinal microbiota, short chain fatty acids, and fecal pH in patients with colorectal cancer. Digestive diseases and sciences, 2013. 58(6): p. 1717-1726.
16.       Alomair, A.O., I. Masoodi, E.J. Alyamani, et al., Colonic mucosal microbiota in colorectal cancer: a single-center metagenomic study in saudi arabia. Gastroenterology research and practice, 2018. 2018.
17.       Yoon, H., N. Kim, J.H. Park, et al., Comparisons of gut microbiota among healthy control, patients with conventional adenoma, sessile serrated adenoma, and colorectal cancer. Journal of cancer prevention, 2017. 22(2): p. 108.
18.       Warren, R.L., D.J. Freeman, S. Pleasance, et al., Co-occurrence of anaerobic bacteria in colorectal carcinomas. Microbiome, 2013. 1(1): p. 16.
19.       Huang, S. and C. Yuan, Detecting Microbiome in Human Colorectal Cancers from High Throughput Sequencing Data. Minnesota Undergraduate Research & Academic Journal, 2018. 1(1).
20.       Wu, N., X. Yang, R. Zhang, et al., Dysbiosis signature of fecal microbiota in colorectal cancer patients. Microbial ecology, 2013. 66(2): p. 462-470.
21.       Liang, Q., J. Chiu, Y. Chen, et al., Fecal bacteria act as novel biomarkers for noninvasive diagnosis of colorectal cancer. Clinical Cancer Research, 2017. 23(8): p. 2061-2070.
22.       Sinha, R., J. Ahn, J.N. Sampson, et al., Fecal microbiota, fecal metabolome, and colorectal cancer interrelations. PloS one, 2016. 11(3): p. e0152126.
23.       McCoy, A.N., F. Araujo-Perez, A. Azcarate-Peril, J.J. Yeh, R.S. Sandler, and T.O. Keku, Fusobacterium is associated with colorectal adenomas. PloS one, 2013. 8(1): p. e53653.
24.       Flanagan, L., J. Schmid, M. Ebert, et al., Fusobacterium nucleatum associates with stages of colorectal neoplasia development, colorectal cancer and disease outcome. European journal of clinical microbiology & infectious diseases, 2014. 33(8): p. 1381-1390.
25.       Sun, Y., Q.-M. An, X.-Y. Tian, et al., Fusobacterium nucleatum infection is correlated with tumor metastasis and postoperative survival of colorectal cancer patients in China. Translational Cancer Research, 2016. 5(5): p. 579-588.
26.       Castellarin, M., R.L. Warren, J.D. Freeman, et al., Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome research, 2012. 22(2): p. 299-306.
27.       Allali, I., S. Delgado, P.I. Marron, et al., Gut microbiome compositional and functional differences between tumor and non-tumor adjacent tissues from cohorts from the US and Spain. Gut Microbes, 2015. 6(3): p. 161-172.
28.       Feng, Q., S. Liang, H. Jia, et al., Gut microbiome development along the colorectal adenoma–carcinoma sequence. Nature communications, 2015. 6: p. 6528.
29.       Allali, I., N. Boukhatem, L. Bouguenouch, et al., Gut microbiome of Moroccan colorectal cancer patients. Medical microbiology and immunology, 2018. 207(3-4): p. 211-225.
30.       Nakatsu, G., X. Li, H. Zhou, et al., Gut mucosal microbiome across stages of colorectal carcinogenesis. Nature communications, 2015. 6: p. 8727.
31.       Sanapareddy, N., R.M. Legge, B. Jovov, et al., Increased rectal microbial richness is associated with the presence of colorectal adenomas in humans. The ISME journal, 2012. 6(10): p. 1858.
32.       Shen, X.J., J.F. Rawls, T.A. Randall, et al., Molecular characterization of mucosal adherent bacteria and associations with colorectal adenomas. Gut microbes, 2010. 1(3): p. 138-147.
33.       Goedert, J.J., Y. Gong, X. Hua, et al., Fecal microbiota characteristics of patients with colorectal adenoma detected by screening: a population-based study. EBioMedicine, 2015. 2(6): p. 597-603.
34.       Lu, Y., J. Chen, J. Zheng, et al., Mucosal adherent bacterial dysbiosis in patients with colorectal adenomas. Scientific reports, 2016. 6: p. 26337.
35.       Geng, J., H. Fan, X. Tang, H. Zhai, and Z. Zhang, Diversified pattern of the human colorectal cancer microbiome. Gut pathogens, 2013. 5(1): p. 2.
36.       Gao, Z., B. Guo, R. Gao, Q. Zhu, and H. Qin, Microbiota disbiosis is associated with colorectal cancer. Frontiers in microbiology, 2015. 6: p. 20.
37.       Gao, Z., B. Guo, R. Gao, Q. Zhu, W. Wu, and H. Qin, Probiotics modify human intestinal mucosa-associated microbiota in patients with colorectal cancer. Molecular medicine reports, 2015. 12(4): p. 6119-6127.
38.       Chen, W., F. Liu, Z. Ling, X. Tong, and C. Xiang, Human intestinal lumen and mucosa-associated microbiota in patients with colorectal cancer. PloS one, 2012. 7(6): p. e39743.
39.       Dejea, C.M., E.C. Wick, E.M. Hechenbleikner, et al., Microbiota organization is a distinct feature of proximal colorectal cancers. Proceedings of the National Academy of Sciences, 2014. 111(51): p. 18321-18326.
40.       Gao, R., C. Kong, L. Huang, et al., Mucosa-associated microbiota signature in colorectal cancer. European Journal of Clinical Microbiology & Infectious Diseases, 2017. 36(11): p. 2073-2083.
41.       Tahara, T., E. Yamamoto, H. Suzuki, et al., Fusobacterium in colonic flora and molecular features of colorectal carcinoma. Cancer research, 2014. 74(5): p. 1311-1318.
42.       Yan, X., L. Liu, H. Li, H. Qin, and Z. Sun, Clinical significance of Fusobacterium nucleatum, epithelial–mesenchymal transition, and cancer stem cell markers in stage III/IV colorectal cancer patients. OncoTargets and therapy, 2017. 10: p. 5031.
43.       Thomas, A.M., E.C. Jesus, A. Lopes, et al., Tissue-associated bacterial alterations in rectal carcinoma patients revealed by 16S rRNA community profiling. Frontiers in cellular and infection microbiology, 2016. 6: p. 179.
44.       Marchesi, J.R., B.E. Dutilh, N. Hall, et al., Towards the human colorectal cancer microbiome. PloS one, 2011. 6(5): p. e20447.
45.       Kasai, C., K. Sugimoto, I. Moritani, et al., Comparison of human gut microbiota in control subjects and patients with colorectal carcinoma in adenoma: Terminal restriction fragment length polymorphism and next-generation sequencing analyses. Oncology reports, 2016. 35(1): p. 325-333.
46.       Wang, T., G. Cai, Y. Qiu, et al., Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers. The ISME journal, 2012. 6(2): p. 320.
47.       Amitay, E.L., S. Werner, M. Vital, et al., Fusobacterium and colorectal cancer: causal factor or passenger? Results from a large colorectal cancer screening study. Carcinogenesis, 2017. 38(8): p. 781-788.
48.       Mira-Pascual, L., R. Cabrera-Rubio, S. Ocon, et al., Microbial mucosal colonic shifts associated with the development of colorectal cancer reveal the presence of different bacterial and archaeal biomarkers. Journal of gastroenterology, 2015. 50(2): p. 167-179.
49.       Wang, X., J. Wang, B. Rao, and L. Deng, Gut flora profiling and fecal metabolite composition of colorectal cancer patients and healthy individuals. Experimental and therapeutic medicine, 2017. 13(6): p. 2848-2854.
50.       Flemer, B., D.B. Lynch, J.M. Brown, et al., Tumour-associated and non-tumour-associated microbiota in colorectal cancer. Gut, 2017. 66(4): p. 633-643.
51.       Yu, J., Q. Feng, S.H. Wong, et al., Metagenomic analysis of faecal microbiome as a tool towards targeted non-invasive biomarkers for colorectal cancer. Gut, 2017. 66(1): p. 70-78.
52.       Wong, S.H., T.N. Kwong, T.-C. Chow, et al., Quantitation of faecal Fusobacterium improves faecal immunochemical test in detecting advanced colorectal neoplasia. Gut, 2017. 66(8): p. 1441-1448.
53.       Ai, L., H. Tian, Z. Chen, H. Chen, J. Xu, and J.-Y. Fang, Systematic evaluation of supervised classifiers for fecal microbiota-based prediction of colorectal cancer. Oncotarget, 2017. 8(6): p. 9546.
54.       Zackular, J.P., M.A. Rogers, M.T. Ruffin, and P.D. Schloss, The human gut microbiome as a screening tool for colorectal cancer. Cancer prevention research, 2014. 7(11): p. 1112-1121.
55.       Zeller, G., J. Tap, A.Y. Voigt, et al., Potential of fecal microbiota for early‐stage detection of colorectal cancer. Molecular systems biology, 2014. 10(11).
56.       Matsuda, K., H. Tsuji, T. Asahara, K. Matsumoto, T. Takada, and K. Nomoto, Establishment of an analytical system for the human fecal microbiota, based on reverse transcription-quantitative PCR targeting of multicopy rRNA molecules. Appl. Environ. Microbiol., 2009. 75(7): p. 1961-1969.