Effects of gut microbiome and obesity on the development, progression and prevention of cancer (Review)

Kumavath,Ranjith; Pavithran,Honey; Paul,Sayan; Anju,V. T.; Busi,Siddhardha; Dyavaiah,Madhu

doi:10.3892/ijo.2023.5592

Effects of gut microbiome and obesity on the development, progression and prevention of cancer (Review)

Authors:
- Ranjith Kumavath
- Honey Pavithran
- Sayan Paul
- V. T. Anju
- Siddhardha Busi
- Madhu Dyavaiah
View Affiliations

Affiliations: Department of Biotechnology, School of Life Sciences, Pondicherry University, Puducherry 605014, India, Department of Genomic Science, School of Biological Sciences, Central University of Kerala, Kasaragod 671320, India, Department of Biochemistry & Molecular Biology, The University of Texas Medical Branch at Galveston, Galveston, TX 77555, USA, Department of Biochemistry and Molecular Biology, School of Life Sciences, Pondicherry University, Puducherry 605014, India, Department of Microbiology, School of Life Sciences, Pondicherry University, Puducherry 605014, India
Published online on: November 23, 2023 https://doi.org/10.3892/ijo.2023.5592
Article Number: 4

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Cancer is one of the leading causes of death worldwide and it is estimated that the mortality rate of cancer will increase in the coming years. The etiology of the development and progression of cancer is multifactorial. Insights have been gained on the association between the human microbiome and tumor cell malignancy. A number of commensal microbe species are present in the human gut. They serve pivotal roles in maintaining several health and disease conditions, such as inflammatory bowel disease, irritable bowel syndrome, obesity and diabetes. Known major factors involved in cancer development include age, hormone levels, alcohol consumption, diet, being overweight, obesity, and infections, regardless of the type of cancer. Therefore, the present review aims to discuss the relationship between the gut microbiome and obesity‑associated malignancies, including colorectal, gastric and liver cancer. Obesity has been reported to contribute to the development of numerous types of cancer primarily caused by high fatty food intake. In addition, obesity‑associated microbiome alterations can lead to cancer and its progression. Dysbiosis of the gut microbiota can alter the metabolite profile, whilst increasing the levels of toxins, such as Bacteroides fragilis toxin and colibactin and cytolethal distending toxin, which are responsible for oncogenesis. The present review provides insights into the impact of gut microbiome dysbiosis on the progression of different types of cancers associated with obesity. It also discusses possible strategies for preserving a healthy gut microbiome. Different pre‑clinical and clinical models are available for studying cancer development downstream of gut microbiome dysbiosis. Furthermore, the role of metabolites or drugs employed in colorectal, gastric and liver cancer therapy would be discussed.

View Figures

View References

1	Deo SVS, Sharma J and Kumar S: GLOBOCAN 2020 report on global cancer burden: Challenges and opportunities for surgical oncologists. Ann Surg Oncol. 29:6497–6500. 2022. View Article : Google Scholar : PubMed/NCBI
2	Siegel RL, Wagle NS, Cercek A, Smith RA and Jemal A: Colorectal cancer statistics, 2023. CA Cancer J Clin. 73:233–254. 2023. View Article : Google Scholar : PubMed/NCBI
3	Hanahan D and Weinberg RA: The hallmarks of cancer. Cell. 100:57–70. 2000. View Article : Google Scholar : PubMed/NCBI
4	Hanahan D and Weinberg RA: Hallmarks of cancer: The next generation. Cell. 144:646–674. 2011. View Article : Google Scholar : PubMed/NCBI
5	Hanahan D: Hallmarks of cancer: New dimensions. Cancer Discov. 12:31–46. 2022. View Article : Google Scholar : PubMed/NCBI
6	Ursell LK, Metcalf JL, Parfrey LW and Knight R: Defining the human microbiome. Nutr Rev. 70:S38–S44. 2012. View Article : Google Scholar : PubMed/NCBI
7	Wang R, Tang R, Li B, Ma X, Schnabl B and Tilg H: Gut microbiome, liver immunology, and liver diseases. Cell Mol Immunol. 18:4–17. 2021. View Article : Google Scholar : PubMed/NCBI
8	Dekaboruah E, Suryavanshi MV, Chettri D and Verma AK: Human microbiome: An academic update on human body site specific surveillance and its possible role. Arch Microbiol. 8:2147–2167. 2020. View Article : Google Scholar : PubMed/NCBI
9	Kuźniar A, Szawica D, Wąsiewicz E, Fularska K and Oleszko M: Human gut microbiome-how intestinal bacteria influence our health. J Educ Health Sport. 1:30–35. 2023. View Article : Google Scholar
10	Zhu X, Li B, Lou P, Dai T, Chen Y, Zhuge A, Yuan Y and Li L: The relationship between the gut microbiome and neurodegenerative diseases. Neurosci Bull. 37:1510–1522. 2021. View Article : Google Scholar : PubMed/NCBI
11	Hoesel B and Schmid JA: The complexity of NF-κB signaling in inflammation and cancer. Mol Cancer. 12:1–15. 2013. View Article : Google Scholar
12	Guinane CM and Cotter PD: Role of the gut microbiota in health and chronic gastrointestinal disease: Understanding a hidden metabolic organ. Ther Adv Gastroenterol. 4:295–308. 2013. View Article : Google Scholar : PubMed/NCBI
13	Meng C, Bai C, Brown TD, Hood LE and Tian Q: Human gut microbiota and gastrointestinal cancer. Genomics Proteomics Bioinformatics. 16:33–49. 2018. View Article : Google Scholar : PubMed/NCBI
14	Bhatt AP, Redinbo MR and Bultman SJ: The role of the microbiome in cancer development and therapy. CA Cancer J Clin. 67:326–344. 2017. View Article : Google Scholar : PubMed/NCBI
15	Boutari C and Mantzoros CS: A 2022 update on the epidemiology of obesity and a call to action: As its twin COVID-19 pandemic appears to be receding, the obesity and dysmetabolism pandemic continues to rage on. Metabolism. 133:1552172022. View Article : Google Scholar : PubMed/NCBI
16	Calle EE, Rodriguez C, Walker-Thurmond K and Thun MJ: Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S adults. N Engl J Med. 17:1625–1638. 2003. View Article : Google Scholar : PubMed/NCBI
17	Martin-Rodriguez E, Guillen-Grima F, Martí A and Brugos-Larumbe A: Comorbidity associated with obesity in a large population: The APNA study. Obes Res Clin Pract. 5:435–447. 2003.PubMed/NCBI
18	Wolin KY, Carson K and Colditz GA: Obesity and cancer. Oncologist. 6:556–565. 2010. View Article : Google Scholar : PubMed/NCBI
19	Amersi F, Agustin M and Ko CY: Colorectal cancer: Epidemiology, risk factors, and health services. Clin Colon Rectal Surg. 3:133–140. 2005. View Article : Google Scholar : PubMed/NCBI
20	Lauby-Secretan B, Scoccianti C, Loomis D, Grosse Y, Bianchini F and Straif K: Body fatness and cancer-viewpoint of the IARC working group. N Engl J Med. 8:794–798. 2016. View Article : Google Scholar
21	Deslypere JP: Obesity and cancer. Metabolism. 44:24–27. 1995. View Article : Google Scholar : PubMed/NCBI
22	Fasshauer M and Blüher M: Adipokines in health and disease. Trends Pharmacol Sci. 7:461–470. 2015. View Article : Google Scholar : PubMed/NCBI
23	Gregor MF and Hotamisligil GS: Inflammatory mechanisms in obesity. Annu Rev Immunol. 29:415–445. 2011. View Article : Google Scholar : PubMed/NCBI
24	Longo M, Zatterale F, Naderi J, Parrillo L, Formisano P, Raciti GA, Beguinot F and Miele C: Adipose tissue dysfunction as determinant of obesity-associated metabolic complications. Int J Mol Sci. 20:23582019. View Article : Google Scholar : PubMed/NCBI
25	Amen OM, Sarker SD, Ghildyal R and Arya A: Endoplasmic reticulum stress activates unfolded protein response signaling and mediates inflammation, obesity, and cardiac dysfunction: Therapeutic and molecular approach. Front Pharmacol. 10:9772019. View Article : Google Scholar : PubMed/NCBI
26	Cnop M, Foufelle F and Velloso LA: Endoplasmic reticulum stress, obesity and diabetes. Trends Mol Med. 18:59–68. 2012. View Article : Google Scholar : PubMed/NCBI
27	Kolb R, Sutterwala FS and Zhang W: Obesity and cancer: Inflammation bridges the two. Curr Opin Pharmacol. 29:77–89. 2016. View Article : Google Scholar : PubMed/NCBI
28	Fenton JI, Hord NG, Lavigne JA, Perkins SN and Hursting SD: Leptin, insulin-like growth factor-1, and insulin-like growth factor-2 are mitogens in ApcMin/+ but not Apc+/+ colonic epithelial cell lines. Cancer Epidemiol Biomarkers Prev. 14:1646–1652. 2005. View Article : Google Scholar : PubMed/NCBI
29	VanSaun MN: Molecular pathways: Adiponectin and leptin signaling in cancer. Clin Cancer Res. 19:1926–1932. 2013. View Article : Google Scholar : PubMed/NCBI
30	Hursting SD, Nunez ND, Varticovski L and Vinson C: The obesity-cancer link: Lessons learned from a fatless mouse. Cancer Res. 67:2391–2393. 2007. View Article : Google Scholar : PubMed/NCBI
31	Cohen DH and LeRoith D: Obesity, type 2 diabetes, and cancer: The insulin and IGF connection. Endocr Relat Cancer. 19:F27–F45. 2012. View Article : Google Scholar : PubMed/NCBI
32	Amin MN, Hussain MS, Sarwar MS, Moghal MM, Das A, Hossain MZ, Chowdhury JA, Millat MS and Islam MS: How the association between obesity and inflammation may lead to insulin resistance and cancer. Diabetes Metab Syndr. 13:1213–1224. 2019. View Article : Google Scholar : PubMed/NCBI
33	Dobbins M, Decorby K and Choi BCK: The association between obesity and cancer risk: A meta-analysis of observational studies from 1985 to 2011. ISRN Prev Med. 2013:1–16. 2013. View Article : Google Scholar : PubMed/NCBI
34	Jiralerspong S and Goodwin PJ: Obesity and breast cancer prognosis: Evidence, challenges, and opportunities. J Clin Oncol. 34:4203–4216. 2016. View Article : Google Scholar : PubMed/NCBI
35	Osman MA and Hennessy BT: Obesity correlation with metastases development and response to first-line metastatic chemotherapy in breast cancer. Clin Med Insights Oncol. 9:105–112. 2015. View Article : Google Scholar : PubMed/NCBI
36	Rumgay H, Arnold M, Ferlay J, Lesi O, Cabasag CJ, Vignat J, Laversanne M, McGlynn KA and Soerjomataram I: Global burden of primary liver cancer in 2020 and predictions to 2040. J Hepatol. 77:1598–1606. 2022. View Article : Google Scholar : PubMed/NCBI
37	El-Serag HB and Mason AC: Risk factors for the rising rates of primary liver cancer in the United States. Arch Intern Med. 160:3227–3230. 2000. View Article : Google Scholar : PubMed/NCBI
38	Ohishi W, Fujiwara S, Cologne JB, Suzuki G, Akahoshi M, Nishi N, Tsuge M and Chayama K: Impact of radiation and hepatitis virus infection on risk of hepatocellular carcinoma. Hepatology. 53:1237–1245. 2011. View Article : Google Scholar : PubMed/NCBI
39	Larsson S and Wolk A: Overweight, obesity and risk of liver cancer: A meta-analysis of cohort studies. Br J Cancer. 97:1005–1008. 2007. View Article : Google Scholar : PubMed/NCBI
40	Chen Y, Wang X, Wang J, Yan Z and Luo J: Excess body weight and the risk of primary liver cancer: An updated meta-analysis of prospective studies. Eur J Cancer. 48:2137–2145. 2012. View Article : Google Scholar : PubMed/NCBI
41	Karczewski J, Begier-Krasińska B, Staszewski R, Popławska E, Gulczynska-Elhadi K and Dobrowolska A: Obesity and the risk of gastrointestinal cancers. Dig Dis Sci. 64:2740–2749. 2019. View Article : Google Scholar : PubMed/NCBI
42	El-Serag HB, Ergun GA, Pandolfino J, Fitzgerald S, Tran T and Kramer JR: Obesity increases oesophageal acid exposure. Gut. 56:749–755. 2007. View Article : Google Scholar : PubMed/NCBI
43	Long E and Beales IL: The role of obesity in oesophageal cancer development. Ther Adv Gastroenterol. 7:247–268. 2014. View Article : Google Scholar : PubMed/NCBI
44	Donohoe CL, O'Farrell NJ, Doyle SL and Reynolds JV: The role of obesity in gastrointestinal cancer: Evidence and opinion. Ther Adv Gastroenterol. 7:38–50. 2014. View Article : Google Scholar : PubMed/NCBI
45	Pati S, Irfan W, Jameel A, Ahmed S and Shahid RK: Obesity and cancer: A current overview of epidemiology, pathogenesis, outcomes, and management. Cancers (Basel). 15:4852023. View Article : Google Scholar : PubMed/NCBI
46	Rawla P, Sunkara T and Barsouk A: Epidemiology of colorectal cancer: Incidence, mortality, survival, and risk factors. Prz Gastroenterology. 14:89–103. 2019.
47	Soltani G, Poursheikhani A, Yassi M, Hayatbakhsh A, Kerachian M and Kerachian MA: Obesity, diabetes and the risk of colorectal adenoma and cancer. BMC Endocr Disord. 19:1132019. View Article : Google Scholar : PubMed/NCBI
48	Hou K, Wu ZX, Chen XY, Wang JQ, Zhang D, Xiao C, Zhu D, Koya JB, Wei L, Li J and Chen ZS: Microbiota in health and diseases. Signal Transduct Target Ther. 7:1352022. View Article : Google Scholar : PubMed/NCBI
49	Barra WF, Sarquis DP, Khayat AS, Khayat BCM, Demachki S, Anaissi AKM, Ishak G, Santos NPC, Dos Santos SEB, Burbano RR, et al: Gastric cancer microbiome. Pathobiology. 88:156–169. 2021. View Article : Google Scholar : PubMed/NCBI
50	Chattopadhyay I, Verma M and Panda M: Role of oral microbiome signatures in diagnosis and prognosis of oral cancer. Technol Cancer Res Treat. 18:15330338198673542019. View Article : Google Scholar : PubMed/NCBI
51	Yang Y, Dai D, Jin W, Huang Y, Zhang Y, Chen Y, Wang W, Lin W, Chen X, Zhang J, et al: Microbiota and metabolites alterations in proximal and distal gastric cancer patients. J Transl Med. 20:4392022. View Article : Google Scholar : PubMed/NCBI
52	Irfan M, Delgado RZR and Frias-Lopez J: The oral microbiome and cancer. Front. Immunol. 11:5910882020.PubMed/NCBI
53	Zhao Y, Liu Y, Li S, Peng Z, Liu X, Chen J and Zheng X: Role of lung and gut microbiota on lung cancer pathogenesis. J Cancer Res Clin Oncol. 147:2177–2186. 2021. View Article : Google Scholar : PubMed/NCBI
54	Ruo SW, Alkayyali T, Win M, Tara A, Joseph C, Kannan A, Srivastava K, Ochuba O, Sandhu JK, Went TR, et al: Role of gut microbiota dysbiosis in breast cancer and novel approaches in prevention, diagnosis, and treatment. Cureus. 26:e174722021.PubMed/NCBI
55	Nicolaro M, Portal DE, Shinder B, Patel HV and Singer EA: The human microbiome and genitourinary malignancies. Ann Transl Med. 8:12452020. View Article : Google Scholar : PubMed/NCBI
56	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. 25:112019. View Article : Google Scholar
57	Collina F, Chiara AD, Renzo AD, Rosa GD, Botti G and Franco R: Chlamydia psittaci in ocular adnexa MALT lymphoma: A possible role in lymphomagenesis and a different geographical distribution. Infect Agent Cancer. 7:82012. View Article : Google Scholar : PubMed/NCBI
58	Tang T, Wu H, Chen X and Chen L, Liu L, Li Z, Bai Q, Chen Y and Chen L: The hypothetical inclusion membrane protein CPSIT_0846 regulates mitochondrial-mediated host cell apoptosis via the ERK/JNK signaling pathway. Front Cell Infect Microbiol. 11:6074222021. View Article : Google Scholar : PubMed/NCBI
59	Olsen I and Yilmaz Ö: Possible role of Porphyromonas gingivalis in orodigestive cancers. J Oral Microbiol. 11:15634102019. View Article : Google Scholar : PubMed/NCBI
60	Cao S, Li J, Lu J, Zhong R and Zhong H: Mycobacterium tuberculosis antigens repress Th1 immune response suppression and promotes lung cancer metastasis through PD-1/PDl-1 signaling pathway. Cell Death Dis. 10:442019. View Article : Google Scholar : PubMed/NCBI
61	Littman AJ, Jackson LA and Vaughan TL: Chlamydia pneumoniae and lung cancer: Epidemiologic evidence. Cancer Epidemiol Biomarkers Prev. 14:773–778. 2005. View Article : Google Scholar : PubMed/NCBI
62	Di Domenico EG, Cavallo I, Pontone M, Toma L and Ensoli F: Biofilm producing Salmonella Typhi: Chronic colonization and development of gallbladder cancer. Int J Mol Sci. 18:18872017. View Article : Google Scholar : PubMed/NCBI
63	Oehmcke-Hecht S, Mandl V, Naatz LT, Dühring L, Köhler J, Kreikemeyer B and Maletzki C: Streptococcus gallolyticus abrogates anti-carcinogenic properties of tannic acid on low-passage colorectal carcinomas. Sci Rep. 10:47142020. View Article : Google Scholar : PubMed/NCBI
64	Abdulamir AS, Hafidh RR and Bakar FA: The association of Streptococcus bovis/gallolyticus with colorectal tumors: The nature and the underlying mechanisms of its etiological role. J Exp Clin Cancer Res. 30:112011. View Article : Google Scholar : PubMed/NCBI
65	Zhou X, Kandalai S, Hossain F and Zheng Q: Tumor microbiome metabolism: A game changer in cancer development and therapy. Front Oncol. 12:9334072022. View Article : Google Scholar : PubMed/NCBI
66	Johansson P, Eckstein A and Küppers R: Biology of ocular adnexal marginal zone lymphomas. Cancers (Basel). 14:12642022. View Article : Google Scholar : PubMed/NCBI
67	Yoo JY, Groer M, Dutra SVO, Sarkar A and McSkimming DI: Gut microbiota and immune system interactions. Microorganisms. 8:15872020. View Article : Google Scholar : PubMed/NCBI
68	Ge Y, Wang X, Guo Y, Yan J, Abuduwaili A, Aximujiang K, Yan J and Wu M: Gut microbiota influence tumor development and Alter interactions with the human immune system. J Exp Clin Cancer Res. 40:422021. View Article : Google Scholar : PubMed/NCBI
69	Kovács T, Mikó E, Ujlaki G, Sári Z and Bai P: The microbiome as a component of the tumor microenvironment. Tumor Microenviron. 2020:137–153. 2020. View Article : Google Scholar
70	Chen Y, Wu FH, Wu PQ, Xing HY and Ma T: The role of the tumor microbiome in tumor development and its treatment. Front Immunol. 13:9358462023. View Article : Google Scholar : PubMed/NCBI
71	He T, Cheng X and Xing C: The gut microbial diversity of colon cancer patients and the clinical significance. Bioengineered. 12:7046–7060. 2021. View Article : Google Scholar : PubMed/NCBI
72	Zheng D, Liwinski T and Elinav E: Interaction between microbiota and immunity in health and disease. Cell Res. 30:492–506. 2020. View Article : Google Scholar : PubMed/NCBI
73	Chénard T, Prévost K, Dubé J and Massé E: Immune system modulations by products of the gut microbiota. Vaccines (Basel). 8:4612020. View Article : Google Scholar : PubMed/NCBI
74	Rawla P and Barsouk A: Epidemiology of gastric cancer: Global trends, risk factors and prevention. Gastroenterol Rev Gastroenterol. 14:26–38. 2018. View Article : Google Scholar
75	Hanus M, Parada-Venegas D, Landskron G, Wielandt AM, Hurtado C, Alvarez K, Hermoso MA, López-Köstner F and la Fuente MD: Immune system, microbiota, and microbial metabolites: The unresolved triad in colorectal cancer microenvironment. Front Immunol. 12:6128262021. View Article : Google Scholar : PubMed/NCBI
76	Ilic M and Ilic I: Epidemiology of stomach cancer. World J Gastroenterol. 28:1187–1203. 2022. View Article : Google Scholar : PubMed/NCBI
77	Lin XJ, Wang CP, Liu XD, Yan KK, Li S, Bao HH, Zhao LY and Liu X: Body mass index and risk of gastric cancer: A meta-analysis. Jpn J Clin Oncol. 44:783–791. 2014. View Article : Google Scholar : PubMed/NCBI
78	Lee HW, Huang D, Shin WK, de la Torre K, Yang JJ, Song M, Shin A, Lee JK and Kang D: Obesity at early adulthood increases risk of gastric cancer from the health Examinees-Gem (HEXA-G) study. PLoS One. 17:e02608262022. View Article : Google Scholar : PubMed/NCBI
79	Cani PD and Jordan BF: Gut microbiota-mediated inflammation in obesity: A link with gastrointestinal cancer. Nat Rev Gastroenterol Hepatol. 15:671–682. 2018. View Article : Google Scholar : PubMed/NCBI
80	Doorakkers E, Lagergren J, Engstrand L and Brusselaers N: Eradication of helicobacter pylori and gastric cancer: A systematic review and meta-analysis of cohort studies. J Natl Cancer Inst. 108:djw1322016. View Article : Google Scholar : PubMed/NCBI
81	Toh JWT and Wilson RB: Pathways of gastric carcinogenesis, helicobacter pylori virulence and interactions with antioxidant systems, vitamin C and phytochemicals. Int J Mol Sci. 21:64512020. View Article : Google Scholar : PubMed/NCBI
82	Colotta F, Allavena A, Sica C, Garlanda C and Mantovani A: Cancer-related inflammation, the seventh hallmark of cancer: Links to genetic instability. Carcinogenesis. 30:1073–1081. 2009. View Article : Google Scholar : PubMed/NCBI
83	Khatoon J, Rai RP and Prasad KN: Role of helicobacter pylori in gastric cancer: Updates. World J Gastrointest Oncol. 8:147–158. 2016. View Article : Google Scholar : PubMed/NCBI
84	Moyat M and Velin D: Immune responses to Helicobacter pylori infection. World J Gastroenterol. 20:5583–5593. 2014. View Article : Google Scholar : PubMed/NCBI
85	Udhayakumar G, Jayanthi V, Devaraj N and Devaraj H: Interaction of MUC1 with β-catenin modulates the Wnt target Gene cyclinD1 in H. pylori-induced gastric cancer. Mol Carcinog. 46:807–817. 2007. View Article : Google Scholar : PubMed/NCBI
86	Hotchin NA, Cover TL and Akhtar N: Cell vacuolation induced by the VacA cytotoxin ofhelicobacter pylori is regulated by the Rac1 GTPase. J Biol Chem. 275:14009–14012. 2000. View Article : Google Scholar : PubMed/NCBI
87	Yahiro K, Akazawa Y, Nakano M, Suzuki H, Hisatune J, Isomoto H, Sap J, Noda M, Moss J and Hirayama T: Helicobacter pylori VacA induces apoptosis by accumulation of connexin 43 in autophagic vesicles via a Rac1/ERK-dependent pathway. Cell Death Discov. 1:150352015. View Article : Google Scholar : PubMed/NCBI
88	Caputo R, Tuccillo C, Manzo BA, Zarrilli R, Tortora G, Blanco CD, Ricci V, Ciardiello F and Romano M: Helicobacter pylori VacA toxin up-regulates vascular endothelial growth factor expression in MKN 28 gastric cells through an epidermal growth factor receptor-, cyclooxygenase-2-dependent mechanism1. Clin Cancer Res. 9:2015–2021. 2003.PubMed/NCBI
89	Song X, Xin N, Wang W and Zhao C: Wnt/β-catenin, an oncogenic pathway targeted by H. pylori in gastric carcinogenesis. Oncotarget. 6:35579–35588. 2015. View Article : Google Scholar : PubMed/NCBI
90	Muhammad JS, Eladl MA and Khoder G: Helicobacter pylori-induced DNA methylation as an epigenetic modulator of gastric cancer: Recent outcomes and future direction. Pathogens. 8:232019. View Article : Google Scholar : PubMed/NCBI
91	Peterson AJ, Menheniott TR, O'Connor L, Walduck AK, Fox JG, Kawakami K, Minamoto T, Ong EK, Wang TC, Judd LM and Giraud AS: Helicobacter pylori infection promotes methylation and silencing of trefoil factor 2, leading to gastric tumor development in mice and humans. Gastroenterology. 139:2005–2017. 2010. View Article : Google Scholar : PubMed/NCBI
92	Sato F and Meltzer SJ: CpG island hypermethylation in progression of esophageal and gastric cancer. Cancer. 106:483–493. 2006. View Article : Google Scholar : PubMed/NCBI
93	Smet A, Kupcinskas J, Link A, Hold GL and Bornschein J: The role of microbiota in gastrointestinal cancer and cancer treatment: Chance or curse? Cell Mol Gastroenterol Hepatol. 13:857–874. 2022. View Article : Google Scholar : PubMed/NCBI
94	Engstrand L and Lindberg M: Helicobacter pylori and the gastric microbiota. Best Pract Res Clin Gastroenterol. 27:39–45. 2013. View Article : Google Scholar : PubMed/NCBI
95	Aviles-Jimenez F, Vazquez-Jimenez F, Medrano-Guzman R, Mantilla A and Torres J: Stomach microbiota composition varies between patients with non-atrophic gastritis and patients with intestinal type of gastric cancer. Sci Rep. 4:42022014. View Article : Google Scholar : PubMed/NCBI
96	Dias-Jácome E, Libânio D, Borges-Canha M, Galaghar A and Pimentel-Nunes P: Gastric microbiota and carcinogenesis: The role of non-Helicobacter pylori bacteria-A systematic review. Rev Esp Enferm Dig. 108:530–540. 2016. View Article : Google Scholar : PubMed/NCBI
97	De Witte C, Schulz C, Smet A, Malfertheiner P and Haesebrouck F: Other Helicobacters and gastric microbiota. Helicobacter. 21:62–68. 2016. View Article : Google Scholar : PubMed/NCBI
98	Tong Y, Gao H, Qi Q, Liu X, Li J, Gao J, Li P, Wang Y, Du L and Wang C: High fat diet, gut microbiome and gastrointestinal cancer. Theranostics. 11:5889–5910. 2021. View Article : Google Scholar : PubMed/NCBI
99	Arita S and Inagaki-Ohara K: High-fat-diet-induced modulations of leptin signaling and gastric microbiota drive precancerous lesions in the stomach. Nutrition. 67–68. 1105562019.
100	Colegio OR, Chu NQ, Szabo AL, Chu T, Rhebergen AM, Jairam V, Cyrus N, Brokowski CE, Eisenbarth SC, Phillips GM, et al: Functional polarization of tumour-associated macrophages by tumour-derived lactic acid. Nature. 513:559–563. 2014. View Article : Google Scholar : PubMed/NCBI
101	He C, Cheng D, Peng C, Li Y, Zhu Y and Lu N: High-fat diet induces dysbiosis of gastric microbiota prior to gut microbiota in association with metabolic disorders in mice. Front Microbiol. 9:6392018. View Article : Google Scholar : PubMed/NCBI
102	Kim KA, Gu W, Lee IA, Joh EH and Kim DH: High fat diet-induced gut microbiota exacerbates inflammation and obesity in mice via the TLR4 signaling pathway. PLoS One. 7:e477132012. View Article : Google Scholar : PubMed/NCBI
103	Xiao S, Fei N, Pang X, Shen J, Wang L, Zhang B, Zhang M, Zhang X, Zhang C, Li M, et al: A gut microbiota-targeted dietary intervention for amelioration of chronic inflammation underlying metabolic syndrome. FEMS Microbiol Ecol. 87:357–367. 2014. View Article : Google Scholar : PubMed/NCBI
104	Li N, Xu H, Ou Y, Feng Z, Zhang Q, Zhu Q and Cai Z: LPS-induced CXCR7 expression promotes gastric Cancer proliferation and migration via the TLR4/MD-2 pathway. Diagn Pathol. 14:32019. View Article : Google Scholar : PubMed/NCBI
105	Zhang XHF, Giuliano M, Trivedi MV, Schiff R and Osborne CK: Metastasis dormancy in estrogen receptor-positive breast cancer. Clin Cancer Res. 19:6389–6397. 2013. View Article : Google Scholar : PubMed/NCBI
106	Bardou M, Barkun AN and Martel M: Obesity and colorectal cancer. Gut. 62:933–947. 2013. View Article : Google Scholar : PubMed/NCBI
107	Pischon T and Nimptsch K: Obesity and risk of cancer: An introductory overview in obesity and cancer. Recent Results Cancer Res. 208:1–15. 2016. View Article : Google Scholar : PubMed/NCBI
108	Torre LA, Siegel RL, Ward EM and Jemal A: Global cancer incidence and mortality rates and trends-an update. Cancer Epidemiol Biomarkers Prev. 25:16–27. 2016. View Article : Google Scholar : PubMed/NCBI
109	Chaplin A, Rodriguez RM, Segura-Sampedro JJ, Ochogavía-Seguí A, Romaguera D and Barceló-Coblijn G: Insights behind the relationship between colorectal cancer and obesity: Is visceral adipose tissue the missing link? Int J Mol Sci. 23:131282022. View Article : Google Scholar : PubMed/NCBI
110	Ma Y, Yang Y, Wang F, Zhang P, Shi C, Zou Y and Qin H: Obesity and risk of colorectal cancer: A systematic review of prospective studies. PLoS One. 8:e539162013. View Article : Google Scholar : PubMed/NCBI
111	Matsuo K, Mizoue T, Tanaka K, Tsuji I, Sugawara Y, Sasazuki S, Nagata C, Tamakoshi A, Wakai K, Inoue M, et al: Association between body mass index and the colorectal cancer risk in Japan: Pooled analysis of population-based cohort studies in Japan. Ann Oncol. 23:479–490. 2012. View Article : Google Scholar : PubMed/NCBI
112	Socol CT, Chira A, Martinez-Sanchez MA, Nuñez-Sanchez MA, Maerescu CM, Mierlita D, Rusu AV, Ruiz-Alcaraz AJ, Trif M and Ramos-Molina B: Leptin signaling in obesity and colorectal cancer. Int J Mol Sci. 23:47132022. View Article : Google Scholar : PubMed/NCBI
113	Milosevic VS, Vukmirovic FC, Krstic MC, Zindovic MM, Stojanovic DL and Jancic SA: Involvement of leptin receptors expression in proliferation and neoangiogenesis in colorectal carcinoma. J BUON. 20:100–108. 2015.PubMed/NCBI
114	Niku M, Pajari AM, Sarantaus L, Päivärinta E, Storvik M, Heiman-Lindh A, Suokas S, Nyström M and Mutanen M: Western diet enhances intestinal tumorigenesis in Min/+ mice, associating with mucosal metabolic and inflammatory stress and loss of Apc heterozygosity. J Nutr Biochem. 39:126–133. 2017. View Article : Google Scholar : PubMed/NCBI
115	Park S, Koh E, Koo JS, Kim SI, Park BW and Kim KS: Lack of both androgen receptor and forkhead box A1 (FOXA1) expression is a poor prognostic factor in estrogen receptor-positive breast cancers. Oncotarget. 8:82940–82955. 2017. View Article : Google Scholar : PubMed/NCBI
116	Gheorghe AS, Negru ȘM, Preda M, Mihăilă RI, Komporaly IA, Dumitrescu EA, Lungulescu CV, Kajanto LA, Georgescu B, Radu EA and Stănculeanu DL: Biochemical and metabolical pathways associated with microbiota-derived butyrate in colorectal cancer and omega-3 fatty acids implications: A narrative review. Nutrients. 14:11522022. View Article : Google Scholar : PubMed/NCBI
117	Mori G, Rampelli S, Orena BS, Rengucci C, De Maio G, Barbieri G, Passardi A, Gardini AC, Frassineti GL, Gaiarsa S, et al: Shifts of faecal microbiota during sporadic colorectal carcinogenesis. Sci Rep. 8:103292018. View Article : Google Scholar : PubMed/NCBI
118	Hannigan GD, Duhaime MB, Ruffin MT IV, Koumpouras CC and Schloss PD: Diagnostic potential and interactive dynamics of the colorectal cancer virome. mBio. 9:e02248–e02218. 2018. View Article : Google Scholar : PubMed/NCBI
119	Fang Y, Yan C, Zhao Q, Xu J, Liu Z, Gao J, Zhu H, Dai Z, Wang D and Tang D: The roles of microbial products in the development of colorectal cancer: A review. Bioengineered. 12:720–735. 2021. View Article : Google Scholar : PubMed/NCBI
120	Sánchez-Alcoholado L, Ramos-Molina B, Otero A, Laborda-Illanes A, Ordóñez R, Medina JA, Gómez-Millán J and Queipo-Ortuño MI: The role of the gut microbiome in colorectal cancer development and therapy response. Cancers (Basel). 12:14062020. View Article : Google Scholar : PubMed/NCBI
121	Schulz MD, Atay C, Heringer J, Romrig FK, Schwitalla S, Aydin B, Ziegler PK, Varga J, Reindl W, Pommerenke C, et al: High-fat-diet-mediated dysbiosis promotes intestinal carcinogenesis independently of obesity. Nature. 514:508–512. 2014. View Article : Google Scholar : PubMed/NCBI
122	Gaines S, van Praagh JB, Williamson AJ, Jacobson RA, Hyoju S, Zaborin A, Mao J, Koo HY, Alpert L, Bissonnette M, et al: Western diet promotes intestinal colonization by collagenolytic microbes and promotes tumor formation after colorectal surgery. Gastroenterology. 158:958–970.e2. 2020. View Article : Google Scholar : PubMed/NCBI
123	Zeng H, Umar S, Rust B, Lazarova D and Bordonaro M: Secondary bile acids and short chain fatty acids in the colon: A focus on colonic microbiome, cell proliferation, inflammation, and cancer. Int J Mol Sci. 20:12142019. View Article : Google Scholar : PubMed/NCBI
124	Schramm C: Bile acids, the microbiome, immunity, and liver tumors. N Engl J Med. 379:888–890. 2018. View Article : Google Scholar : PubMed/NCBI
125	Koh GY, Kane A, Lee K, Xu Q, Wu X, Roper J, Mason JB and Crott JW: Parabacteroides distasonis attenuates toll-like receptor 4 signaling and Akt activation and blocks colon tumor formation in high-fat diet-fed azoxymethane-treated mice. Int J Cancer. 143:1797–1805. 2018. View Article : Google Scholar : PubMed/NCBI
126	Gupta H, Youn GS, Shin MJ and Suk KT: Role of gut microbiota in hepatocarcinogenesis. Microorganisms. 7:1212019. View Article : Google Scholar : PubMed/NCBI
127	Trivedi Y, Bolgarina Z, Desai HN, Senaratne M, Swami SS, Aye SL and Mohammed L: The role of gut microbiome in hepatocellular carcinoma: A systematic review. Cureus. 15:e438622023.PubMed/NCBI
128	Plaza-Díaz J, Solís-Urra P, Rodríguez-Rodríguez F, Olivares-Arancibia J, Navarro-Oliveros M, Abadía-Molina F and Álvarez-Mercado AI: The gut barrier, intestinal microbiota, and liver disease: Molecular mechanisms and strategies to manage. Int J Mol Sci. 21:83512020. View Article : Google Scholar : PubMed/NCBI
129	Schwabe RF and Greten TF: Gut microbiome in HCC-Mechanisms, diagnosis and therapy. J Hepatol. 72:230–238. 2020. View Article : Google Scholar : PubMed/NCBI
130	Chu H, Williams B and Schnabl B: Gut microbiota, fatty liver disease, and hepatocellular carcinoma. Liver Res. 2:43–51. 2018. View Article : Google Scholar : PubMed/NCBI
131	Yoshimoto S, Loo TM, Atarashi K, Kanda H, Sato S, Oyadomari S, Iwakura Y, Oshima K, Morita H, Hattori M, et al: Obesity-induced gut microbial metabolite promotes liver cancer through senescence secretome. Nature. 499:97–101. 2013. View Article : Google Scholar : PubMed/NCBI
132	Roh YS and Seki E: Toll-like receptors in alcoholic liver disease, non-alcoholic steatohepatitis and carcinogenesis. J Gastroenterol Hepatol. 28:38–42. 2013. View Article : Google Scholar : PubMed/NCBI
133	Bartolini I, Risaliti M, Tucci R, Muiesan P, Ringressi MN, Taddei A and Amedei A: Gut microbiota and immune system in liver cancer: Promising therapeutic implication from development to treatment. World J Gastrointest Oncol. 13:1616–1631. 2021. View Article : Google Scholar : PubMed/NCBI
134	Allsopp P, Possemiers S, Campbell D, Gill C and Rowland I: A comparison of the anti-cancer properties of isoxanthohumol and 8-prenylnaringenin using in vitro models of colon cancer. Biofactors. 39:441–447. 2013. View Article : Google Scholar : PubMed/NCBI
135	Higashimura Y, Naito Y, Takagi T, Uchiyama K, Mizushima K, Ushiroda C, Ohnogi H, Kudo Y, Yasui M, Inui S, et al: Protective effect of agaro-oligosaccharides on gut dysbiosis and colon tumorigenesis in high-fat diet-fed mice. Am J Physiol Gastrointest Liver Physiol. 310:G367–G375. 2016. View Article : Google Scholar : PubMed/NCBI
136	Costabile A, Fava F, Röytiö H, Forssten SD, Olli K, Klievink J, Rowland IR, Ouwehand AC, Rastall RA, Gibson GR and Walton GE: Impact of polydextrose on the faecal microbiota: A double-blind, crossover, placebo-controlled feeding study in healthy human subjects. Br J Nutr. 108:471–481. 2012. View Article : Google Scholar : PubMed/NCBI
137	Shields CE, Van Meerbeke SW, Housseau F, Wang H, Huso DL, Casero RA Jr, O'Hagan HM and Sears CL: Reduction of murine colon tumorigenesis driven by enterotoxigenic bacteroides fragilis using cefoxitin treatment. J Infect Dis. 214:122–129. 2016. View Article : Google Scholar
138	Hou H, Chen D, Zhang K, Zhang W, Liu T, Wang S, Dai X, Wang B, Zhong W and Cao H: Gut microbiota-derived short-chain fatty acids and colorectal cancer: Ready for clinical translation? Cancer Lett. 526:225–235. 2022. View Article : Google Scholar : PubMed/NCBI
139	Son MY and Cho HS: Anticancer effects of gut microbiota-derived short-chain fatty acids in cancers. J Microbiol Biotechnol. 33:849–856. 2023. View Article : Google Scholar : PubMed/NCBI
140	Schneider KM, Mohs A, Gui W, Galvez EJC, Candels LS, Hoenicke L, Muthukumarasamy U, Holland CH, Elfers C, Kilic K, et al: Imbalanced gut microbiota fuels hepatocellular carcinoma development by shaping the hepatic inflammatory microenvironment. Nat Commun. 13:39642022. View Article : Google Scholar : PubMed/NCBI
141	Yu LX and Schwabe RF: The gut microbiome and liver cancer: Mechanisms and clinical translation. Nat Rev Gastroenterol Hepatol. 14:527–539. 2017. View Article : Google Scholar : PubMed/NCBI
142	Patel AH, Li Y, Minacapelli CD, Catalano K and Rustgi V: Reduction in gastrointestinal cancers in cirrhotic patients receiving rifaximin vs lactulose only therapy for hepatic encephalopathy. Cureus. 15:e352592023.PubMed/NCBI
143	Ting NLN, Lau HCH and Yu J: Cancer pharmacomicrobiomics: Targeting microbiota to optimise cancer therapy outcomes. Gut. 71:1412–1425. 2022. View Article : Google Scholar : PubMed/NCBI
144	de Clercq NC, van den Ende T, Prodan A, Hemke R, Davids M, Pedersen HK, Nielsen HB, Groen AK, de Vos WM, van Laarhoven HWM and Nieuwdorp M: Fecal microbiota transplantation from overweight or obese donors in cachectic patients with advanced gastroesophageal cancer: A randomized, double-blind, placebo-controlled, phase II study. Clin Cancer Res. 27:3784–3792. 2021. View Article : Google Scholar : PubMed/NCBI
145	Napolitano M and Covasa M: Microbiota transplant in the treatment of obesity and diabetes: Current and future perspectives. Front Microbiol. 11:5903702020. View Article : Google Scholar : PubMed/NCBI
146	Davar D, Dzutsev AK, McCulloch JA, Rodrigues RR, Chauvin JM, Morrison RM, Deblasio RN, Menna C, Ding Q, Pagliano O, et al: Fecal microbiota transplant overcomes resistance to anti-PD-1 therapy in melanoma patients. Science. 371:595–602. 2021. View Article : Google Scholar : PubMed/NCBI
147	Xu H, Cao C, Ren Y, Weng S, Liu L, Guo C, Wang L, Han X, Ren J and Liu Z: Antitumor effects of fecal microbiota transplantation: Implications for microbiome modulation in cancer treatment. Front Immunol. 13:9494902022. View Article : Google Scholar : PubMed/NCBI
148	Zhao LY, Mei JX, Yu G, Lei L, Zhang WH, Liu K, Chen XL, Kołat D, Yang K and Hu JK: Role of the gut microbiota in anticancer therapy: from molecular mechanisms to clinical applications. Signal Transduction Target Ther. 8:2012023. View Article : Google Scholar : PubMed/NCBI