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Cancer-Promoting Effects of Microbial Dysbiosis

  • Integrative Care (C Lammersfeld, Section Editor)
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Abstract

Humans depend on our commensal bacteria for nutritive, immune-modulating, and metabolic contributions to maintenance of health. However, this commensal community exists in careful balance that, if disrupted, enters dysbiosis; this has been shown to contribute to the pathogenesis of colon, gastric, esophageal, pancreatic, laryngeal, breast, and gallbladder carcinomas. This development is closely tied to host inflammation, which causes and is aggravated by microbial dysbiosis and increases vulnerability to pathogens. Advances in sequencing technology have increased our ability to catalog microbial species associated with various cancer types across the body. However, defining microbial biomarkers as cancer predictors presents multiple challenges, and existing studies identifying cancer-associated bacteria have reported inconsistent outcomes. Combining metabolites and microbiome analyses can help elucidate interactions between gut microbiota, metabolism, and the host. Ultimately, understanding how gut dysbiosis impacts host response and inflammation will be critical to creating an accurate picture of the role of the microbiome in cancer.

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References

Papers of particular interest, published recently, have been highlighted as: • Of importance

  1. Thomas LV, Ockhuizen T. New insights into the impact of the intestinal microbiota on health and disease: a symposium report. Br J Nutr. 2012;107(S1):S1–13.

    Article  CAS  PubMed  Google Scholar 

  2. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486(7402):207–14.

    Article  Google Scholar 

  3. Yang Y, Wang X, Huycke T, Moore DR, Lightfoot SA, Huycke MM. Colon macrophages polarized by commensal bacteria cause colitis and cancer through the bystander effect. Transl Oncol. 2013;6(5):596. This study demonstrates that specific human commensals can polarize macrophages to the M1 phenotype, which then serve as effectors for bacterially induced bystander effects. The authors propose targeting M1 macrophages as a chemopreventive strategy.

  4. Candela M, Turroni S, Biagi E, Carbonero F, Rampelli S, Fiorentini C, et al. Inflammation and colorectal cancer, when microbiota-host mutualism breaks. World J Gastroenterol. 2014;20(4):908–22.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  5. Jobin C. Colorectal cancer: looking for answers in the microbiota. Cancer Discov. 2013;3(4):384–7.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  6. Schwabe RF, Jobin C. The microbiome and cancer. Nat Rev Cancer. 2013;13(11):800–12.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  7. Sears CL, Garrett WS. Microbes, microbiota, and colon cancer. Cell Host Microbe. 2014;15(3):317–28.

    Article  CAS  PubMed  Google Scholar 

  8. Marchesi JR, Dutilh BE, Hall N, Peters WH, Roelofs R, Boleij A, et al. Towards the human colorectal cancer microbiome. PLoS One. 2011;6(5):e20447. This study profiles the colon tumor microbiome in contrast to non-malignant colon mucosa revealing differing microbial colonization patterns between the two sites.

  9. Sobhani I, Tap J, Roudot-Thoraval F, Roperch JP, Letulle S, Langella P, et al. Microbial dysbiosis in colorectal cancer (CRC) patients. PLoS One. 2011;6(1):e16393.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  10. Weir TL, Manter DK, Sheflin AM, Barnett BA, Heuberger AL, Ryan EP. Stool microbiome and metabolome differences between colorectal cancer patients and healthy adults. PLoS One. 2013;8(8):e70803.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  11. Zackular JP, Baxter NT, Iverson KD, Sadler WD, Petrosino JF, Chen GY, et al. The gut microbiome modulates colon tumorigenesis. AmBio. 2013;4(6):e00692–13. This study demonstrates the important role of the microbiome in CRC development using fecal transplants from tumor-bearing mice to conventionalize germ-free animals, which resulted in an increased number of inflammation-induced tumors.

    Google Scholar 

  12. Zhan Y, Chen P-J, Sadler WD, Wang F, Poe S, Núñez G, et al. Gut microbiota protects against gastrointestinal tumorigenesis caused by epithelial injury. Cancer Res. 2013;73(24):7199–210.

    Article  CAS  PubMed  Google Scholar 

  13. Winter SE, Winter MG, Xavier MN, Thiennimitr P, Poon V, Keestra AM, et al. Host-derived nitrate boosts growth of E coli in the inflamed gut. Science. 2013;339(6120):708–11.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  14. Brenchley JM, Douek DC. Microbial translocation across the GI tract. Annu Rev Immunol. 2012;30:149.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  15. Hajishengallis G, Darveau RP, Curtis MA. The keystone-pathogen hypothesis. Nat Rev Microbiol. 2012;10(10):717–25.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Tjalsma H, Boleij A, Marchesi JR, Dutilh BE. A bacterial driver–passenger model for colorectal cancer: beyond the usual suspects. Nat Rev Microbiol. 2012;10(8):575–82. This study proposes the “driver and passenger” hypothesis of bacterially induced tumor formation and progression.

  17. Grivennikov SI, Wang K, Mucida D, Stewart CA, Schnabl B, Jauch D, et al. Adenoma-linked barrier defects and microbial products drive IL-23/IL-17-mediated tumour growth. Nature. 2012;491(7423):254–8.

    CAS  PubMed Central  PubMed  Google Scholar 

  18. Pimentel-Nunes P, Teixeira AL, Pereira C, Gomes M, Brandão C, Rodrigues C, et al. Functional polymorphisms of Toll-like receptors 2 and 4 alter the risk for colorectal carcinoma in Europeans. Dig Liver Dis. 2013;45(1):63–9.

    Article  CAS  PubMed  Google Scholar 

  19. Richmond A. NF-κB, chemokine gene transcription and tumour growth. Nat Rev Immunol. 2002;2(9):664–74.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  20. Schwitalla S, Fingerle AA, Cammareri P, Nebelsiek T, Göktuna SI, Ziegler PK, et al. Intestinal tumorigenesis initiated by dedifferentiation and acquisition of stem-cell-like properties. Cell. 2013;152(1):25–38. This article demonstrates the role of inflammation and outlines signaling pathways involved in the bidirectional conversion of tumor-initiating stem cells and nonstem cells.

    Article  CAS  PubMed  Google Scholar 

  21. Zubair A, Frieri M. Role of nuclear factor-ĸB in breast and colorectal cancer. Curr Allergy Asthma Rep. 2013;13(1):44–9.

    Article  CAS  PubMed  Google Scholar 

  22. Neufert C, Becker C, Türeci Ö, Waldner MJ, Backert I, Floh K, et al. Tumor fibroblast–derived epiregulin promotes growth of colitis-associated neoplasms through ERK. J Clin Investig. 2013;123(4):1428.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. Couturier-Maillard A, Secher T, Rehman A, Normand S, De Arcangelis A, Haesler R, et al. NOD2-mediated dysbiosis predisposes mice to transmissible colitis and colorectal cancer. J Clin Investig. 2013;123(2):700.

    CAS  PubMed Central  PubMed  Google Scholar 

  24. Shanahan MT, Carroll IM, Grossniklaus E, White A, von Furstenberg RJ, Barner R, et al. Mouse Paneth cell antimicrobial function is independent of Nod2. Gut. 2014;63(6):903–10.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  25. Nagi RS, Bhat AS, Kumar H. Cancer: a tale of aberrant PRR response. Front Immunol. 2014;5:161.

    Article  PubMed Central  PubMed  Google Scholar 

  26. Pradere J, Dapito D, Schwabe R. The yin and yang of Toll-like receptors in cancer. Oncogene. 2014;33(27):3485–95.

    Article  CAS  PubMed  Google Scholar 

  27. Collins D, Hogan AM, Winter DC. Microbial and viral pathogens in colorectal cancer. Lancet Oncol. 2011;12(5):504–12.

    Article  CAS  PubMed  Google Scholar 

  28. Buc E, Dubois D, Sauvanet P, Raisch J, Delmas J, Darfeuille-Michaud A, et al. High prevalence of mucosa-associated E. coli producing cyclomodulin and genotoxin in colon cancer. PLoS One. 2013;8(2):e56964.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. Goodwin AC, Shields CED, Wu S, Huso DL, Wu X, Murray-Stewart TR, et al. Polyamine catabolism contributes to enterotoxigenic Bacteroides fragilis-induced colon tumorigenesis. Proc Natl Acad Sci U S A. 2011;108(37):15354–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  30. Kostic AD, Chun E, Robertson L, Glickman JN, Gallini CA, Michaud M, et al. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe. 2013;14(2):207–15.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Bongers G, Pacer ME, Geraldino TH, Chen L, He Z, Hashimoto D, et al. Interplay of host microbiota, genetic perturbations, and inflammation promotes local development of intestinal neoplasms in mice. J Exp Med. 2014;211(3):457–72.

    Article  CAS  PubMed  Google Scholar 

  32. Castellarin M, Warren RL, Freeman JD, Dreolini L, Krzywinski M, Strauss J, et al. Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res. 2012;22(2):299–306.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. Geng J, Fan H, Tang X, Zhai H, Zhang Z. Diversified pattern of the human colorectal cancer microbiome. Gut Pathog. 2013. doi:10.1186/1757-4749-5-2.

    PubMed Central  PubMed  Google Scholar 

  34. Flanagan L, Schmid J, Ebert M, Soucek P, Kunicka T, Liska V, Bruha J, Neary P, Dezeeuw N, Tommasino M. Fusobacterium nucleatum associates with stages of colorectal neoplasia development, colorectal cancer and disease outcome. Eur J Clin Microbiol Infect Dis. 2014;33(8):1381-90. doi:10.1007/s10096-014-2081-3.

  35. Rubinstein MR, Wang X, Liu W, Hao Y, Cai G, Han YW. Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/β-catenin signaling via its FadA adhesin. Cell Host Microbe. 2013;14(2):195–206.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  36. Png CW, Lindén SK, Gilshenan KS, Zoetendal EG, McSweeney CS, Sly LI, et al. Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria. Am J Gastroenterol. 2010;105(11):2420–8.

    Article  CAS  PubMed  Google Scholar 

  37. Ahn J, Sinha R, Pei Z, Dominianni C, Wu J, Shi J, et al. Human gut microbiome and risk for colorectal cancer. J Natl Cancer Inst. 2013;105(24):1907–11. This is the largest comparative study of human stool samples from CRC patients and control subjects and was the first to show decreased microbial community diversity in stool.

    Article  CAS  PubMed  Google Scholar 

  38. Watanabe T, Tada M, Nagai H, Sasaki S, Nakao M. Helicobacter pylori infection induces gastric cancer in Mongolian gerbils. Gastroenterology. 1998;115(3):642–8.

    Article  CAS  PubMed  Google Scholar 

  39. Osaki T, Matsuki T, Asahara T, Zaman C, Hanawa T, Yonezawa H, et al. Comparative analysis of gastric bacterial microbiota in Mongolian gerbils after long-term infection with Helicobacter pylori. Microb Pathog. 2012;53(1):12–8.

    Article  PubMed  Google Scholar 

  40. Zaman C, Osaki T, Hanawa T, Yonezawa H, Kurata S, Kamiya S. Analysis of the microbial ecology between Helicobacter pylori and the gastric microbiota of Mongolian gerbils. J Med Microbiol. 2014;63(Pt 1):129–37.

    Article  CAS  PubMed  Google Scholar 

  41. Aviles-Jimenez F, Vazquez-Jimenez F, Medrano-Guzman R, Mantilla A, Torres J. Stomach microbiota composition varies between patients with non-atrophic gastritis and patients with intestinal type of gastric cancer. Sci Rep. 2014. doi:10.1038/srep04202. As a comprehensive study of microbiota changes in gastric cancer patients, as compared with healthy controls, this study indicates that other microbes are involved in gastric cancer development.

    PubMed Central  PubMed  Google Scholar 

  42. Dicksved J, Lindberg M, Rosenquist M, Enroth H, Jansson JK, Engstrand L. Molecular characterization of the stomach microbiota in patients with gastric cancer and in controls. J Med Microbiol. 2009;58(4):509–16.

    Article  CAS  PubMed  Google Scholar 

  43. Shin CM, Kim N, Lee HS, Park JH, Ahn S, Kang GH, et al. Changes in aberrant DNA methylation after Helicobacter pylori eradication: a long‐term follow‐up study. Int J Cancer. 2013;133(9):2034–42. This study indicates that the eradication of H. pylori, a treatment thought to be effective in reducing the risk of gastric cancer, is not successful in limiting long-term development of gastric cancer. Changes in methylation provide a mechanism for this phenomenon.

    Article  CAS  PubMed  Google Scholar 

  44. Cai X, Carlson J, Stoicov C, Li H, Wang TC, Houghton J. Helicobacter felis eradication restores normal architecture and inhibits gastric cancer progression in C57BL/6 mice. Gastroenterology. 2005;128(7):1937–52.

    Article  CAS  PubMed  Google Scholar 

  45. Wang TC, Goldenring JR, Dangler C, Ito S, Mueller A, Jeon WK, et al. Mice lacking secretory phospholipase A2 show altered apoptosis and differentiation with Helicobacter felis infection. Gastroenterology. 1998;114(4):675–69.

    Article  CAS  PubMed  Google Scholar 

  46. Moen EL, Wen S, Anwar T, Cross-Knorr S, Brilliant K, Birnbaum F, et al. Regulation of RKIP function by Helicobacter pylori in gastric cancer. PLoS One. 2012;7(5):e37819.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  47. Yang L, Chaudhary N, Baghdadi J, Pei Z. Microbiome in reflux disorders and esophageal adenocarcinoma. Cancer J. 2014;20(3):207–10.

    Article  CAS  PubMed  Google Scholar 

  48. Anderson LA, Murphy SJ, Johnston BT, Watson R, Ferguson H, Bamford KB, et al. Relationship between Helicobacter pylori infection and gastric atrophy and the stages of the oesophageal inflammation, metaplasia, adenocarcinoma sequence: results from the FINBAR case–control study. Gut. 2008;57(6):734–9.

    Article  CAS  PubMed  Google Scholar 

  49. Yang L, Lu X, Nossa CW, Francois F, Peek RM, Pei Z. Inflammation and intestinal metaplasia of the distal esophagus are associated with alterations in the microbiome. Gastroenterology. 2009;137(2):588–97.

    Article  PubMed Central  PubMed  Google Scholar 

  50. Narikiyo M, Tanabe C, Yamada Y, Igaki H, Tachimori Y, Kato H, et al. Frequent and preferential infection of Treponema denticola, Streptococcus mitis, and Streptococcus anginosus in esophageal cancers. Cancer Sci. 2004;95(7):569–74.

    Article  CAS  PubMed  Google Scholar 

  51. Farrell JJ, Zhang L, Zhou H, Chia D, Elashoff D, Akin D, et al. Variations of oral microbiota are associated with pancreatic diseases including pancreatic cancer. Gut. 2012;61(4):582–8. This study indicates that changes of the oral microbiota may be useful biomarkers in the detection of pancreatic cancer. It provides an illustration of microbial changes between cancer patients and healthy controls, indicating species that are relevant to the development of pancreatic cancer.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  52. Gong H-L, Shi Y, Zhou L, Wu C-P, Cao P-Y, Tao L, et al. The composition of microbiome in larynx and the throat biodiversity between laryngeal squamous cell carcinoma patients and control population. PLoS One. 2013;8(6):e66476. This study provides a comprehensive depiction of microbial changes between cancer patients and healthy controls, implicating H. pylori and a number of other species in the development of laryngeal carcinoma.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  53. Sharma V, Chauhan VS, Nath G, Kumar A, Shukla VK. Role of bile bacteria in gallbladder carcinoma. Hepatogastroenterology. 2007;54(78):1622.

    CAS  PubMed  Google Scholar 

  54. Shukla V, Tiwari S, Roy S. Biliary bile acids in cholelithiasis and carcinoma of the gall bladder. Eur J Cancer Prev. 1993;2(2):155–60.

    Article  CAS  PubMed  Google Scholar 

  55. Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol. 1999;189(1):12–9.

    Article  CAS  PubMed  Google Scholar 

  56. Mitrani-Rosenbaum S, Tsvieli R, Tur-Kaspa R. Oestrogen stimulates differential transcription of human papillomavirus type 16 in SiHa cervical carcinoma cells. J Gen Virol. 1989;70(8):2227–32.

    Article  CAS  PubMed  Google Scholar 

  57. Riley RR, Duensing S, Brake T, Münger K, Lambert PF, Arbeit JM. Dissection of human papillomavirus E6 and E7 function in transgenic mouse models of cervical carcinogenesis. Cancer Res. 2003;63(16):4862–71.

    CAS  PubMed  Google Scholar 

  58. Chung S-H, Wiedmeyer K, Shai A, Korach KS, Lambert PF. Requirement for estrogen receptor α in a mouse model for human papillomavirus–associated cervical cancer. Cancer Res. 2008;68(23):9928–34.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  59. Elson DA, Riley RR, Lacey A, Thordarson G, Talamantes FJ, Arbeit JM. Sensitivity of the cervical transformation zone to estrogen-induced squamous carcinogenesis. Cancer Res. 2000;60(5):1267–75.

    CAS  PubMed  Google Scholar 

  60. Lombardi P, Goldin B, Boutin E, Gorbach SL. Metabolism of androgens and estrogens by human fecal microorganisms. J Steroid Biochem. 1978;9(8):795–801.

    Article  CAS  PubMed  Google Scholar 

  61. D'Souza G, Kreimer AR, Viscidi R, Pawlita M, Fakhry C, Koch WM, et al. Case–control study of human papillomavirus and oropharyngeal cancer. N Engl J Med. 2007;356(19):1944–56.

    Article  PubMed  Google Scholar 

  62. Coussens LM, Werb Z. Inflammation and cancer. Nature. 2002;420(6917):860–7.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  63. Nugent JL, McCoy AN, Addamo CJ, Jia W, Sandler RS, Keku TO. Altered tissue metabolites correlate with microbial dysbiosis in colorectal adenomas. J Proteome Res. 2014;13(4):1921–9.

    Article  CAS  PubMed  Google Scholar 

  64. Forsythe P, Bienenstock J. Immunomodulation by commensal and probiotic bacteria. Immunol Investig. 2010;39(4–5):429–48.

    Article  CAS  Google Scholar 

  65. Chang PV, Hao L, Offermanns S, Medzhitov R. The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. Proc Natl Acad Sci USA. 2014. doi:10.1073/pnas.1322269111.

    Google Scholar 

  66. Akare S, Jean‐Louis S, Chen W, Wood DJ, Powell AA, Martinez JD. Ursodeoxycholic acid modulates histone acetylation and induces differentiation and senescence. Int J Cancer. 2006;119(12):2958–69.

    Article  CAS  PubMed  Google Scholar 

  67. Miao XP, Ouyang Q, Li HY, Zhao ZQ, Pan Y, Wang ZW. Ursodeoxycholic acid for the prevention of colorectal adenomas and carcinomas. Cochrane Database Syst Rev. 2008;4:CD007377. doi:10.1002/14651858.CD007377.

    Google Scholar 

  68. Eaton JE, Silveira MG, Pardi DS, Sinakos E, Kowdley KV, Luketic VA, et al. High-dose ursodeoxycholic acid is associated with the development of colorectal neoplasia in patients with ulcerative colitis and primary sclerosing cholangitis. Am J Gastroenterol. 2011;106(9):1638–45.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  69. Ajouz H, Mukherji D, Shamseddine A. Secondary bile acids: an underrecognized cause of colon cancer. World J Surg Oncol. 2014;12(1):164.

    Article  PubMed Central  PubMed  Google Scholar 

  70. Yoshimoto S, Loo TM, Atarashi K, Kanda H, Sato S, Oyadomari S, et al. Obesity-induced gut microbial metabolite promotes liver cancer through senescence secretome. Nature. 2013;499(7456):97–101.

    Article  CAS  PubMed  Google Scholar 

  71. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505(7484):559–63.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  72. Wang H, Chen J, Hollister K, Sowers LC, Forman BM. Endogenous bile acids are ligands for the nuclear receptor FXR/BAR. Mol Cell. 1999;3(5):543–53.

    Article  CAS  PubMed  Google Scholar 

  73. Deuschle U, Schüler J, Schulz A, Schlüter T, Kinzel O, Abel U, et al. FXR controls the tumor suppressor NDRG2 and FXR agonists reduce liver tumor growth and metastasis in an orthotopic mouse xenograft model. PLoS One. 2012;7(10):e43044.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  74. Inagaki T, Moschetta A, Lee Y-K, Peng L, Zhao G, Downes M, et al. Regulation of antibacterial defense in the small intestine by the nuclear bile acid receptor. Proc Natl Acad Sci U S A. 2006;103(10):3920–5.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  75. Adlercreutz H, Martin F, Pulkkinen M, Dencker H, Rimer U, Sjoberg N-O, et al. Intestinal metabolism of estrogens 1. J Clin Endocrinol Metab. 1976;43(3):497–505.

    Article  CAS  PubMed  Google Scholar 

  76. Woolcott CG, Shvetsov YB, Stanczyk FZ, Wilkens LR, White KK, Caberto C, et al. Plasma sex hormone concentrations and breast cancer risk in an ethnically diverse population of postmenopausal women: the Multiethnic Cohort Study. Endocr Relat Cancer. 2010;17(1):125–34.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  77. Mackenzie I. The production of mammary cancer in rats using oestrogens. Br J Cancer. 1955;9(2):284.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  78. Hill M, Goddard P, Williams R. Gut bacteria and aetiology of cancer of the breast. Lancet. 1971;298(7722):472–3.

    Article  Google Scholar 

  79. Muti P, Bradlow HL, Micheli A, Krogh V, Freudenheim JL, Schünemann HJ, et al. Estrogen metabolism and risk of breast cancer: a prospective study of the 2: 16α-hydroxyestrone ratio in premenopausal and postmenopausal women. Epidemiology. 2000;11(6):635–40.

    Article  CAS  PubMed  Google Scholar 

  80. Ou J, Carbonero F, Zoetendal EG, DeLany JP, Wang M, Newton K, et al. Diet, microbiota, and microbial metabolites in colon cancer risk in rural Africans and African Americans. Am J Clin Nutr. 2013;98(1):111–20.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  81. Xie G, Zhang S, Zheng X, Jia W. Metabolomics approaches for characterizing metabolic interactions between host and its commensal microbes. Electrophoresis. 2013;34(19):2787–98.

    CAS  PubMed  Google Scholar 

  82. Stecher B, Maier L, Hardt W-D. 'Blooming' in the gut: how dysbiosis might contribute to pathogen evolution. Nat Rev Microbiol. 2013;11(4):277–84.

    Article  CAS  PubMed  Google Scholar 

  83. O'Keefe SJ, Chung D, Mahmoud N, Sepulveda AR, Manafe M, Arch J, et al. Why do African Americans get more colon cancer than Native Africans? J Nutr. 2007;137(1):175S–82S.

    PubMed  Google Scholar 

  84. Keszei AP, Goldbohm RA, Schouten LJ, Jakszyn P, van den Brandt PA. Dietary N-nitroso compounds, endogenous nitrosation, and the risk of esophageal and gastric cancer subtypes in the Netherlands Cohort Study. Am J Clin Nutr. 2013;97(1):135–46.

    Article  CAS  PubMed  Google Scholar 

  85. Giacosa A, Barale R, Bavaresco L, Gatenby P, Gerbi V, Janssens J, et al. Cancer prevention in Europe: the Mediterranean diet as a protective choice. Eur J Cancer Prev. 2013;22(1):90–5.

    Article  CAS  PubMed  Google Scholar 

  86. Vipperla K, Ou J, Wahl E, Ruder E, O'Keefe S. A 14-day in-house dietary modification of a ‘Western’ diet to an ‘African’ diet changes the microbiota, its metabolome, and biomarkers of colon cancer risk (825.5). FASEB J. 2014;28(1 Suppl):825.

    Google Scholar 

  87. Song Y, Garg S, Girotra M, Maddox C, von Rosenvinge EC, Dutta A, et al. Microbiota dynamics in patients treated with fecal microbiota transplantation for recurrent Clostridium difficile infection. PLoS One. 2013;8(11):e81330.

    Article  PubMed Central  PubMed  Google Scholar 

  88. Marzotto M, Maffeis C, Paternoster T, Ferrario R, Rizzotti L, Pellegrino M, et al. Lactobacillus paracasei A survives gastrointestinal passage and affects the fecal microbiota of healthy infants. Res Microbiol. 2006;157(9):857–66.

    Article  CAS  PubMed  Google Scholar 

  89. Matsumoto M, Aranami A, Ishige A, Watanabe K, Benno Y. LKM512 yogurt consumption improves the intestinal environment and induces the T‐helper type 1 cytokine in adult patients with intractable atopic dermatitis. Clin Exp Allergy. 2007;37(3):358–70.

    Article  CAS  PubMed  Google Scholar 

  90. Clarke SF, Murphy EF, O'Sullivan O, Lucey AJ, Humphreys M, Hogan A, et al. Exercise and associated dietary extremes impact on gut microbial diversity. Gut. 2014. doi:10.1136/gutjnl-2013-306541.

    Google Scholar 

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Amy M. Sheflin, Alyssa K. Whitney, and Tiffany L. Weir declare that they have no conflict of interest

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Sheflin, A.M., Whitney, A.K. & Weir, T.L. Cancer-Promoting Effects of Microbial Dysbiosis. Curr Oncol Rep 16, 406 (2014). https://doi.org/10.1007/s11912-014-0406-0

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