Role of the intestinal microbiota and diet in the onset and progression of colorectal and breast cancers and the interconnection between both types of tumours

Abstract

Colorectal cancer (CRC) is among the leading causes of mortality in adults of both sexes worldwide, while breast cancer (BC) is among the leading causes of death in women. In addition to age, gender, and genetic predisposition, environmental and lifestyle factors exert a strong influence. Global diet, including alcohol consumption, is one of the most important modifiable factors affecting the risk of CRC and BC. Western dietary patterns promoting high intakes of xenobiotics from food processing and ethanol have been associated with increased cancer risk, whereas the Mediterranean diet, generally leading to a higher intake of polyphenols and fibre, has been associated with a protective effect. Gut dysbiosis is a common feature in CRC, where the usual microbiota is progressively replaced by opportunistic pathogens and the gut metabolome is altered. The relationship between microbiota and BC has been less studied. The estrobolome is the collection of genes from intestinal bacteria that can metabolize oestrogens. In a dysbiosis condition, microbial deconjugating enzymes can reactivate conjugated-deactivated oestrogens, increasing the risk of BC. In contrast, intestinal microorganisms can increase the biological activity and bioavailability of dietary phytochemicals through diverse microbial metabolic transformations, potentiating their anticancer activity. Members of the intestinal microbiota can increase the toxicity of xenobiotics through metabolic transformations. However, most of the microorganisms involved in diet-microbiota interactions remain poorly characterized. Here, we provide an overview of the associations between microbiota and diet in BC and CRC, considering the diverse types and heterogeneity of these cancers and their relationship between them and with gut microbiota.

Keywords

Gut microbiota / diet / colorectal cancer / breast cancer / dietary fibre / polyphenol

References

[1] Sung H,Siegel RL.Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.CA Cancer J Clin2021;71:209-49

[2] Key Interdisciplinary Core Program for Colorectal Cancer. Follow-up recommendations in people with a family history of colorectal cancer not associated with hereditary syndromes. (in Spanish) Available from: https://www.astursalud.es/documents/35439/38460/2019%20Actualizaci%C3%B3n%20cribado%20familiar%20CCR%20en%20Asturias_ED03.pdf/c3e8a90d-ddcb-1ad7-7a1f-7a68cdc3903a. [Last accessed on 23 Nov 2023]

[3] Spanish Agency Against Cancer. Anatomy of colon and rectum. (in Spanish) Available from: https://www.contraelcancer.es/es/todo-sobre-cancer/tipos-cancer/cancer-colon. [Last accessed on 23 Nov 2023]

[4] National Cancer Institute. NCI dictionary of cancer terms: adenocarcinoma. Available from: https://www.cancer.gov/publications/dictionaries/cancer-terms/def/adenocarcinoma. [Last accessed on 23 Nov 2023]

[5] Bähr I,Glass M.Characterization of natural killer cells in colorectal tumor tissue of rats fed a control diet or a high-fat diet.Ann Anat2021;233:151586

[6] Dekker E,Vleugels JLA,Wallace MB.Colorectal cancer.Lancet2019;394:1467-80

[7] Carballal S,Balaguer F.Serrated polyps and serrated polyposis syndrome.Cir Esp2013;91:141-8

[8] Anderson WF,Prat A,Sherman ME.How many etiological subtypes of breast cancer: two, three, four, or more?.J Natl Cancer Inst2014;106:dju165 PMCID:PMC4148600

[9] Sawaki M,Iwata H.TNM classification of malignant tumors (Breast Cancer Study Group).Jpn J Clin Oncol2019;49:228-31

[10] Telang N.Preclinical in vitro models from genetically engineered mice for breast and colon cancer (Review).Oncol Rep2011;25:1195-201

[11] Xiao Y,Ruan M.Mixed invasive ductal and lobular carcinoma has distinct clinical features and predicts worse prognosis when stratified by estrogen receptor status.Sci Rep2017;7:10380 PMCID:PMC5583173

[12] Thanikachalam K.Colorectal cancer and nutrition.Nutrients2019;11:164 PMCID:PMC6357054

[13] Zhu JW,Adekunte S.What is known about breast cancer in young women?.Cancers2023;15:1917 PMCID:PMC10047861

[14] Macrae FA. Colorectal cancer: epidemiology, risk factors, and protective factors. Available from: https://www.uptodate.com/contents/colorectal-cancer-epidemiology-risk-factors-and-protective-factors#!. [Last accessed on 23 Nov 2023]

[15] Cicuéndez-Ávila RA. Publication: epidemiology of colon and rectal cancer in public hospitals in the Autonomous Community of Madrid. Survival analysis. University Complutense of Madrid; 2014. p. 1-332. (in Spanish). Available from: https://docta.ucm.es/entities/publication/a4b5cc4d-409c-4b66-a2f3-9cb3913ba072. [Last accessed on 23 Nov 2023]

[16] Alexander DD.Red meat and colorectal cancer: a critical summary of prospective epidemiologic studies.Obes Rev2011;12:e472-93

[17] Tabung FK,Fung TT.Dietary patterns and colorectal cancer risk: a review of 17 years of evidence (2000-2016).Curr Colorectal Cancer Rep2017;13:440-54 PMCID:PMC5794031

[18] World Cancer Research Fund/American Institute for Cancer Research. Continuous update project: diet, nutrition, physical activity and the prevention of cancer. Summary of strong evidence. Available from: https://www.wcrf.org/wp-content/uploads/2021/01/CUP-Strong-Evidence-Matrix.pdf. [Last accessed on 23 Nov 2023]

[19] de Castro ANCL,de Carvalho DC.Polymorphisms of xenobiotic-metabolizing and transporter genes, and the risk of gastric and colorectal cancer in an admixed population from the Brazilian Amazon.Am J Transl Res2020;12:6626-36 PMCID:PMC7653561

[20] Irigaray P,Clapp R.Lifestyle-related factors and environmental agents causing cancer: an overview.Biomed Pharmacother2007;61:640-58

[21] Pericleous M,Caplin ME.Diet and supplements and their impact on colorectal cancer.J Gastrointest Oncol2013;4:409-23 PMCID:PMC3819783

[22] IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Alcohol consumption and ethyl carbamate.IARC Monogr Eval Carcinog Risks Hum2010;96:3-1383 PMCID:PMC4781168

[23] Trama A,Bozovic-Spasojevic I.Cancer burden in adolescents and young adults in Europe.ESMO Open2023;8:100744 PMCID:PMC10024081

[24] Zhang J,Zhang N.Global burden of female breast cancer and its association with socioeconomic development status, 1990-2044.Cancer Rep2023;6:e1827 PMCID:PMC10440843

[25] De Silva S, Tennekoon KH, Karunanayake EH. Interaction of gut microbiome and host microRNAs with the occurrence of colorectal and breast cancer and their impact on patient immunity.Onco Targets Ther2021;14:5115-29 PMCID:PMC8548058

[26] Lu Y,Nordgren A,Frisell J.Increased risk of colorectal cancer in patients diagnosed with breast cancer in women.Cancer Epidemiol2016;41:57-62

[27] Nogacka AM,Suárez A,de Los Reyes-Gavilán CG.Xenobiotics formed during food processing: their relation with the intestinal microbiota and colorectal cancer.Int J Mol Sci2019;20:2051 PMCID:PMC6514608

[28] Ruiz-Saavedra S,Del Rey CG.Dietary xenobiotics derived from food processing: association with fecal mutagenicity and gut mucosal damage.Nutrients2022;14:3482 PMCID:PMC9458229

[29] Zapico A,Ruiz-Saavedra S.Dietary xenobiotics, (poly)phenols and fibers: Exploring associations with gut microbiota in socially vulnerable individuals.Front Nutr2022;9:1000829 PMCID:PMC9597247

[30] Abu-Ghazaleh N,Gopalan V.Intestinal microbiota and its association with colon cancer and red/processed meat consumption.J Gastroenterol Hepatol2021;36:75-88

[31] Kimble R,Ashor A.Effects of a mediterranean diet on the gut microbiota and microbial metabolites: a systematic review of randomized controlled trials and observational studies.Crit Rev Food Sci Nutr2023;63:8698-719

[32] Gantenbein KV.Mediterranean diet as an antioxidant: the impact on metabolic health and overall wellbeing.Nutrients2021;13:1951 PMCID:PMC8227318

[33] Bajic JE,Howarth GS.From the bottom-up: chemotherapy and gut-brain axis dysregulation.Front Behav Neurosci2018;12:104 PMCID:PMC5972222

[34] Subramaniam CB,Gladman MA,Mayo SJ.The microbiota-gut-brain axis: an emerging therapeutic target in chemotherapy-induced cognitive impairment.Neurosci Biobehav Rev2020;116:470-9

[35] Cryan JF,Cowan CSM.The microbiota-gut-brain axis.Physiol Rev2019;99:1877-2013

[36] Martínez-González MÁ,Zazpe I.Transferability of the mediterranean diet to non-mediterranean countries. what is and what is not the mediterranean diet.Nutrients2017;9:1226 PMCID:PMC5707698

[37] Castelló A,Fernández de Larrea N.Adherence to the western, prudent and mediterranean dietary patterns and colorectal cancer risk: findings from the spanish cohort of the european prospective investigation into cancer and nutrition (EPIC-Spain).Nutrients2022;14:3085 PMCID:PMC9370446

[38] Naja F,Itani L,Sibai AM.A Western dietary pattern is associated with overweight and obesity in a national sample of Lebanese adolescents (13-19 years): a cross-sectional study.Br J Nutr2015;114:1909-19 PMCID:PMC4635384

[39] Buja A,Lago L,Baldo V.Breast cancer primary prevention and diet: an umbrella review.Int J Environ Res Public Health2020;17:4731 PMCID:PMC7369836

[40] Yiannakou I,Moore LL.Indices of Mediterranean diet adherence and breast cancer risk in a community-based cohort.Front Nutr2023;10:1148075 PMCID:PMC10070722

[41] Ubago-Guisado E,Ching-López A.Evidence update on the relationship between diet and the most common cancers from the european prospective investigation into cancer and nutrition (EPIC) study: a systematic review.Nutrients2021;13:3582 PMCID:PMC8540388

[42] Torres C, Barrios-Rodríguez R, Muñoz-Bravo C, Toledo E, Dierssen T, Jiménez-Moleón JJ. Mediterranean diet and risk of breast cancer: an umbrella review.Clin Nutr2023;42:600-8

[43] Aranda-olmedo I.Dietary legumes, intestinal microbiota, inflammation and colorectal cancer.J Funct Foods2020;64:103707

[44] van den Brandt PA, Schulpen M. Mediterranean diet adherence and risk of postmenopausal breast cancer: results of a cohort study and meta-analysis.Int J Cancer2017;140:2220-31

[45] Kohls M,Charvat H.Impact of cumulative body mass index and cardiometabolic diseases on survival among patients with colorectal and breast cancer: a multi-centre cohort study.BMC Cancer2022;22:546 PMCID:PMC9107127

[46] McDonald JA,Terry MB.Alcohol intake and breast cancer risk: weighing the overall evidence.Curr Breast Cancer Rep2013;5:208-21 PMCID:PMC3832299

[47] Hamajima N,Tajima K.Alcohol, tobacco and breast cancer - collaborative reanalysis of individual data from 53 epidemiological studies, including 58,515 women with breast cancer and 95,067 women without the disease.Br J Cancer2002;87:1234-45 PMCID:PMC2562507

[48] Smith-Warner SA,Yaun SS.Alcohol and breast cancer in women: a pooled analysis of cohort studies.JAMA1998;279:535-40

[49] Hyun J,Lee C,Jung Y.Pathophysiological aspects of alcohol metabolism in the liver.Int J Mol Sci2021;22:5717 PMCID:PMC8197869

[50] Bosron WF.Genetic polymorphism of human liver alcohol and aldehyde dehydrogenases, and their relationship to alcohol metabolism and alcoholism.Hepatology1986;6:502-10

[51] Crabb DW,Chang D.Overview of the role of alcohol dehydrogenase and aldehyde dehydrogenase and their variants in the genesis of alcohol-related pathology.Proc Nutr Soc2004;63:49-63

[52] Liu Y,Colditz GA.Links between alcohol consumption and breast cancer: a look at the evidence.Womens Health2015;11:65-77 PMCID:PMC4299758

[53] Dumitrescu RG.The etiology of alcohol-induced breast cancer.Alcohol2005;35:213-25

[54] Tosti V,Fontana L.Health benefits of the mediterranean diet: metabolic and molecular mechanisms.J Gerontol A Biol Sci Med Sci2018;73:318-26 PMCID:PMC7190876

[55] Romaguera D,Wark PA.Pre-diagnostic concordance with the WCRF/AICR guidelines and survival in European colorectal cancer patients: a cohort study.BMC Med2015;13:107 PMCID:PMC4423114

[56] Shivappa N,Hurley TG.A population-based dietary inflammatory index predicts levels of C-reactive protein in the Seasonal Variation of Blood Cholesterol Study (SEASONS).Public Health Nutr2014;17:1825-33 PMCID:PMC3983179

[57] Zamora-Ros R,Rothwell JA.Dietary flavonoid intake and colorectal cancer risk in the European prospective investigation into cancer and nutrition (EPIC) cohort.Int J Cancer2017;140:1836-44 PMCID:PMC6241848

[58] Serafini M.Understanding the association between dietary antioxidants, redox status and disease: is the Total Antioxidant Capacity the right tool?.Redox Rep2004;9:145-52

[59] Bouvard V,Guyton KZ.Carcinogenicity of consumption of red and processed meat.Lancet Oncol2015;16:1599-600

[60] Jahurul MH,Ang SJ.Dietary exposure to heterocyclic amines in high-temperature cooked meat and fish in Malaysia.Food Addit Contam Part A Chem Anal Control Expo Risk Assess2010;27:1060-71

[61] de Kok TMCM, van Maanen JM. Evaluation of fecal mutagenicity and colorectal cancer risk.Mutat Res2000;463:53-101

[62] Bastide NM,Nassy G.Red wine and pomegranate extracts suppress cured meat promotion of colonic mucin-depleted foci in carcinogen-induced rats.Nutr Cancer2017;69:289-98

[63] Moorthy B,Carlin DJ.Polycyclic aromatic hydrocarbons: from metabolism to lung cancer.Toxicol Sci2015;145:5-15 PMCID:PMC4408964

[64] Larsson BK,Eriksson AT.Polycyclic aromatic hydrocarbons in grilled food.J Agric Food Chem1983;31:867-73

[65] López GPM,Haza Duaso AI.Polycyclic aromatic hydrocarbons: toxicity, population exposure and foods involved.Rev Complut Cienc Vet2016;10:1-15

[66] Alomirah H,Al-hooti S.Concentrations and dietary exposure to polycyclic aromatic hydrocarbons (PAHs) from grilled and smoked foods.Food Control2011;22:2028-35

[67] Chiavarini M,Minelli L.Dietary intake of meat cooking-related mutagens (HCAs) and risk of colorectal adenoma and cancer: a systematic review and meta-analysis.Nutrients2017;9:514 PMCID:PMC5452244

[68] Martín-Calero A. Development and optimization of new methods for the analysis of heterocyclic amines. University of La Laguna; 2010. p. 1-402. (in Spanish) Available from: https://rebiun.baratz.es/OpacDiscovery/public/catalog/detail/b2FpOmNlbGVicmF0aW9uOmVzLmJhcmF0ei5yZW4vNjM3MDMyNg?tabId=1696324135194. [Last accessed on 23 Nov 2023]

[69] Kondjoyan A,Portanguen S.Relation between crust development and heterocyclic aromatic amine formation when air-roasting a meat cylinder.Food Chem2016;213:641-6

[70] Buła M,Jaworska D.Formation of heterocyclic aromatic amines in relation to pork quality and heat treatment parameters.Food Chem2019;276:511-9

[71] Niehoff N,McCullough LE.Polycyclic aromatic hydrocarbons and postmenopausal breast cancer: an evaluation of effect measure modification by body mass index and weight change.Environ Res2017;152:17-25 PMCID:PMC5135619

[72] Yao Y,Andersson R.Dietary fibre for the prevention of recurrent colorectal adenomas and carcinomas.Cochrane Database Syst Rev2017;1:CD003430 PMCID:PMC6465195

[73] Feng Y,Huang S.Breast cancer development and progression: Risk factors, cancer stem cells, signaling pathways, genomics, and molecular pathogenesis.Genes Dis2018;5:77-106 PMCID:PMC6147049

[74] Jaye K,Bhuyan DJ.The complex interplay of gut microbiota with the five most common cancer types: from carcinogenesis to therapeutics to prognoses.Crit Rev Oncol Hematol2021;165:103429

[75] Tjalsma H,Marchesi JR.A bacterial driver-passenger model for colorectal cancer: beyond the usual suspects.Nat Rev Microbiol2012;10:575-82

[76] Yachida S,Shiroma H.Metagenomic and metabolomic analyses reveal distinct stage-specific phenotypes of the gut microbiota in colorectal cancer.Nat Med2019;25:968-76

[77] Kim M,Ahlquist DA.Fecal metabolomic signatures in colorectal adenoma patients are associated with gut microbiota and early events of colorectal cancer pathogenesis.mBio2020;11:e03186-19 PMCID:PMC7029137

[78] Zhu J,Yao Z.Breast cancer in postmenopausal women is associated with an altered gut metagenome.Microbiome2018;6:136 PMCID:PMC6080540

[79] Ingman WV.The gut microbiome: a new player in breast cancer metastasis.Cancer Res2019;79:3539-41

[80] Mukherjee AG,Bradu P.The crosstalk of the human microbiome in breast and colon cancer: a metabolomics analysis.Crit Rev Oncol Hematol2022;176:103757

[81] Baker JM,Herbst-Kralovetz MM.Estrogen-gut microbiome axis: Physiological and clinical implications.Maturitas2017;103:45-53

[82] Abu-Sbeih H,Ge PS.Patients with breast cancer may be at higher risk of colorectal neoplasia.Ann Gastroenterol2019;32:400-6 PMCID:PMC6595931

[83] Yang J.The association of diet, gut microbiota and colorectal cancer: what we eat may imply what we get.Protein Cell2018;9:474-87 PMCID:PMC5960467

[84] Rothschild D,Barkan E.Environment dominates over host genetics in shaping human gut microbiota.Nature2018;555:210-5

[85] Wong SH.Gut microbiota in colorectal cancer: mechanisms of action and clinical applications.Nat Rev Gastroenterol Hepatol2019;16:690-704

[86] Ternes D,Tsenkova M,Haan S.Microbiome in colorectal cancer: how to get from meta-omics to mechanism?.Trends Microbiol2020;28:401-23

[87] Inamura K.Colorectal cancers: an update on their molecular pathology.Cancers2018;10:26 PMCID:PMC5789376

[88] Gopalakrishnan V,Spencer CN,Wargo JA.The influence of the gut microbiome on cancer, immunity, and cancer immunotherapy.Cancer Cell2018;33:570-80 PMCID:PMC6529202

[89] Pan HW,Li W,Zhang Y.Biodiversity and richness shifts of mucosa-associated gut microbiota with progression of colorectal cancer.Res Microbiol2020;171:107-14

[90] Hibberd AA,Ouwehand AC.Intestinal microbiota is altered in patients with colon cancer and modified by probiotic intervention.BMJ Open Gastroenterol2017;4:e000145 PMCID:PMC5609083

[91] Flemer B,Barrett MP.The oral microbiota in colorectal cancer is distinctive and predictive.Gut2018;67:1454-63 PMCID:PMC6204958

[92] Richard ML,Lamas B.Mucosa-associated microbiota dysbiosis in colitis associated cancer.Gut Microbes2018;9:131-42 PMCID:PMC5989788

[93] Flemer B,Brown JM.Tumour-associated and non-tumour-associated microbiota in colorectal cancer.Gut2017;66:633-43 PMCID:PMC5529966

[94] Gao R,Huang L.Mucosa-associated microbiota signature in colorectal cancer.Eur J Clin Microbiol Infect Dis2017;36:2073-83

[95] Mori G,Orena BS.Shifts of faecal microbiota during sporadic colorectal carcinogenesis.Sci Rep2018;8:10329 PMCID:PMC6037773

[96] Peters BA,Shapiro JA.The gut microbiota in conventional and serrated precursors of colorectal cancer.Microbiome2016;4:69 PMCID:PMC5203720

[97] Liu W,Shu R.Study of the relationship between microbiome and colorectal cancer susceptibility using 16SrRNA sequencing.Biomed Res Int2020;2020:7828392 PMCID:PMC7011317

[98] Hale VL,Johnson S.Shifts in the fecal microbiota associated with adenomatous polyps.Cancer Epidemiol Biomarkers Prev2017;26:85-94 PMCID:PMC5225053

[99] Shen XJ,Randall T.Molecular characterization of mucosal adherent bacteria and associations with colorectal adenomas.Gut Microbes2010;1:138-47 PMCID:PMC2927011

[100] Yang TW,Tu SJ.Enterotype-based analysis of gut microbiota along the conventional adenoma-carcinoma colorectal cancer pathway.Sci Rep2019;9:10923 PMCID:PMC6662695

[101] Zeller G,Voigt AY.Potential of fecal microbiota for early-stage detection of colorectal cancer.Mol Syst Biol2014;10:766 PMCID:PMC4299606

[102] Saito K,Odamaki T.Metagenomic analyses of the gut microbiota associated with colorectal adenoma.PLoS One2019;14:e0212406 PMCID:PMC6386391

[103] Xu J,Yang L.A novel promising diagnosis model for colorectal advanced adenoma and carcinoma based on the progressive gut microbiota gene biomarkers.Cell Biosci2022;12:208 PMCID:PMC9791776

[104] Muguruma N,Nakagawa T.Molecular imaging of aberrant crypt foci in the human colon targeting glutathione S-transferase P1-1.Sci Rep2017;7:6536 PMCID:PMC5529364

[105] Gamallat Y,Walana W.Probiotic Lactobacillus rhamnosus modulates the gut microbiome composition attenuates preneoplastic colorectal Aberrant crypt foci.J Funct Foods2019;53:146-56

[106] Ohkawara S,Nagashima K,Hino T.Oral administration of butyrivibrio fibrisolvens, a butyrate-producing bacterium, decreases the formation of aberrant crypt foci in the colon and rectum of mice.J Nutr2005;135:2878-83

[107] Coker OO,Wu WKK.Altered gut metabolites and microbiota interactions are implicated in colorectal carcinogenesis and can be non-invasive diagnostic biomarkers.Microbiome2022;10:35 PMCID:PMC8862353

[108] Mizutani S,Yachida S.Significance of the gut microbiome in multistep colorectal carcinogenesis.Cancer Sci2020;111:766-73 PMCID:PMC7060472

[109] Yang Y,Liang L.Integrated microbiome and metabolome analysis reveals a novel interplay between commensal bacteria and metabolites in colorectal cancer.Theranostics2019;9:4101-14 PMCID:PMC6592169

[110] Rebersek M.Gut microbiome and its role in colorectal cancer.BMC Cancer2021;21:1325 PMCID:PMC8666072

[111] Sinha R,Sampson JN.Fecal microbiota, fecal metabolome, and colorectal cancer interrelations.PLoS One2016;11:e0152126 PMCID:PMC4807824

[112] Goedert JJ,Hua X.Investigation of the association between the fecal microbiota and breast cancer in postmenopausal women: a population-based case-control pilot study.J Natl Cancer Inst2015;107:djv147 PMCID:PMC4554191

[113] Byrd DA,Wu Z.Associations of fecal microbial profiles with breast cancer and nonmalignant breast disease in the Ghana Breast Health Study.Int J Cancer2021;148:2712-23 PMCID:PMC8386185

[114] Aarnoutse R,Ziemons J.Intestinal microbiota in postmenopausal breast cancer patients and controls.Cancers2021;13:6200 PMCID:PMC8699039

[115] Okubo R,Katsumata N,Xiao J.Impact of chemotherapy on the association between fear of cancer recurrence and the gut microbiota in breast cancer survivors.Brain Behav Immun2020;85:186-91

[116] Luu TH,Bard JM,Nazih H.Intestinal proportion of Blautia sp. is associated with clinical stage and histoprognostic grade in patients with early-stage breast cancer.Nutr Cancer2017;69:267-75

[117] Terrisse S,Iebba V.Intestinal microbiota influences clinical outcome and side effects of early breast cancer treatment.Cell Death Differ2021;28:2778-96 PMCID:PMC8408230

[118] Donnet-Hughes A,Doré J.Potential role of the intestinal microbiota of the mother in neonatal immune education.Proc Nutr Soc2010;69:407-15

[119] Urbaniak C,Brackstone M.Microbiota of human breast tissue.Appl Environ Microbiol2014;80:3007-14 PMCID:PMC4018903

[120] Parida S.The power of small changes: comprehensive analyses of microbial dysbiosis in breast cancer.Biochim Biophys Acta Rev Cancer2019;1871:392-405 PMCID:PMC8769497

[121] Tzeng A,Jia M.Human breast microbiome correlates with prognostic features and immunological signatures in breast cancer.Genome Med2021;13:60 PMCID:PMC8052771

[122] Vitorino M,Vicente R,Santos C.Local breast microbiota: a “new” player on the block.Cancers2022;14:3811 PMCID:PMC9367283

[123] Banerjee S,Wei Z.Distinct microbial signatures associated with different breast cancer types.Front Microbiol2018;9:951 PMCID:PMC5962706

[124] Smith A,Makowski L.Distinct microbial communities that differ by race, stage, or breast-tumor subtype in breast tissues of non-Hispanic Black and non-Hispanic White women.Sci Rep2019;9:11940 PMCID:PMC6697683

[125] Fuhrman BJ,Flores R.Associations of the fecal microbiome with urinary estrogens and estrogen metabolites in postmenopausal women.J Clin Endocrinol Metab2014;99:4632-40 PMCID:PMC4255131

[126] Flores R,Gail MH,Ravel J.Association of fecal microbial diversity and taxonomy with selected enzymatic functions.PLoS One2012;7:e39745 PMCID:PMC3386201

[127] Yang J,Fu Q.Gastrointestinal microbiome and breast cancer: correlations, mechanisms and potential clinical implications.Breast Cancer2017;24:220-8

[128] Bruce E,Urquhart G.Does the gut microbiome environment influence response to systemic breast cancer treatment?.Explor Target Antitumor Ther2021;2:374-84 PMCID:PMC9400737

[129] De Filippis F,Vannini L.High-level adherence to a Mediterranean diet beneficially impacts the gut microbiota and associated metabolome.Gut2016;65:1812-21

[130] Manor O,Kornilov SA.Health and disease markers correlate with gut microbiome composition across thousands of people.Nat Commun2020;11:5206 PMCID:PMC7562722

[131] Asnicar F,Valdes AM.Microbiome connections with host metabolism and habitual diet from 1,098 deeply phenotyped individuals.Nat Med2021;27:321-32 PMCID:PMC8353542

[132] Ibragimova S,Ali FR,Ho SB.Dietary patterns and associated microbiome changes that promote oncogenesis.Front Cell Dev Biol2021;9:725821 PMCID:PMC8633417

[133] Gupta A,Maji A.Association of flavonifractor plautii, a flavonoid-degrading bacterium, with the gut microbiome of colorectal cancer patients in India.mSystems2019;4:e00438-19 PMCID:PMC7407896

[134] Zhang X,Wu D.Tissue-resident Lachnospiraceae family bacteria protect against colorectal carcinogenesis by promoting tumor immune surveillance.Cell Host Microbe2023;31:418-32.e8

[135] Round JL.Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota.Proc Natl Acad Sci U S A2010;107:12204-9 PMCID:PMC2901479

[136] Geuking MB,Lawson MA.Intestinal bacterial colonization induces mutualistic regulatory T cell responses.Immunity2011;34:794-806

[137] Biragyn A.Gut dysbiosis: a potential link between increased cancer risk in ageing and inflammaging.Lancet Oncol2018;19:e295-304 PMCID:PMC6047065

[138] Ríos-Covián D,Margolles A,de Los Reyes-Gavilán CG.Intestinal short chain fatty acids and their link with diet and human health.Front Microbiol2016;7:185 PMCID:PMC4756104

[139] Tao J,Gan RY,Meng X.Targeting gut microbiota with dietary components on cancer: Effects and potential mechanisms of action.Crit Rev Food Sci Nutr2020;60:1025-37

[140] McRae MP.The benefits of dietary fiber intake on reducing the risk of cancer: an umbrella review of meta-analyses.J Chiropr Med2018;17:90-6 PMCID:PMC6112064

[141] Mayo B,Flórez AB.Equol: A bacterial metabolite from the daidzein isoflavone and its presumed beneficial health effects.Nutrients2019;11:2231 PMCID:PMC6770660

[142] Flórez AB,Rodríguez J,Mayo B.Transcriptional regulation of the equol biosynthesis gene cluster in Adlercreutzia equolifaciens DSM19450^T.Nutrients2019;11:993 PMCID:PMC6566806

[143] García-Villalba R,Espín JC,Tomás-Barberán FA.Time course production of urolithins from ellagic acid by human gut microbiota.J Agric Food Chem2013;61:8797-806

[144] Selma MV,Luna MC.Isolation of human intestinal bacteria capable of producing the bioactive metabolite isourolithin a from ellagic acid.Front Microbiol2017;8:1521 PMCID:PMC5545574

[145] Hålldin E,Brunius C.Factors explaining interpersonal variation in plasma enterolactone concentrations in humans.Mol Nutr Food Res2019;63:e1801159 PMCID:PMC7317467

[146] Baldi S,Pallecchi M,Bartolucci G.Interplay between lignans and gut microbiota: nutritional, functional and methodological aspects.Molecules2023;28:343 PMCID:PMC9822457

[147] Adlercreutz H.Lignans and human health.Crit Rev Clin Lab Sci2007;44:483-525

[148] Messina M.Impact of soy foods on the development of breast cancer and the prognosis of breast cancer patients.Forsch Komplementmed2016;23:75-80

[149] van Duursen MBM, Nijmeijer SM, de Morree ES, de Jong PC, van den Berg M. Genistein induces breast cancer-associated aromatase and stimulates estrogen-dependent tumor cell growth in in vitro breast cancer model.Toxicology2011;289:67-73

[150] Fuhrman BJ,Barba M.Equol status modifies the association of soy intake and mammographic density in a sample of postmenopausal women.Cancer Epidemiol Biomarkers Prev2008;17:33-42

[151] Verheus M,Keinan-Boker L,Bingham SA.Plasma phytoestrogens and subsequent breast cancer risk.J Clin Oncol2007;25:648-55

[152] Chi F,Zeng YC,Liu Y.Post-diagnosis soy food intake and breast cancer survival: a meta-analysis of cohort studies.Asian Pac J Cancer Prev2013;14:2407-12

[153] Martino C,Gao B.Acetate reprograms gut microbiota during alcohol consumption.Nat Commun2022;13:4630 PMCID:PMC9359997

[154] Ortega MA,García-Montero C.Microbiota-gut-brain axis mechanisms in the complex network of bipolar disorders: potential clinical implications and translational opportunities.Mol Psychiatry2023;28:2645-73 PMCID:PMC10615769