Potential Role of the Microbiome in Barrett’s Esophagus and Esophageal Adenocarcinoma

Digestive Diseases and Sciences

Volumn 61, Issue 8, 2016, Pages 2217-2225

  Snider, Erik J ^a   Freedberg, Daniel E ^a   Abrams, Julian A ^a  

^a New York Presbyterian Columbia University Medical Center   (United States)

Author keywords

Barrett s esophagus; Esophageal adenocarcinoma; Gastroesophageal reflux disease; Human microbiome

Indexed keywords

PROTON PUMP INHIBITOR;

ACTINOBACTERIA; BACTEROIDETES; BARRETT ESOPHAGUS; CANCER GROWTH; CANCER RISK; CARCINOGENESIS; CARDIA; DIET; ESOPHAGEAL ADENOCARCINOMA; FIRMICUTES; FUSOBACTERIA; GASTROESOPHAGEAL REFLUX; HELICOBACTER PYLORI; HUMAN; INTESTINE FLORA; MICROBIOME; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEOBACTERIA; REFLUX ESOPHAGITIS; REVIEW; RISK FACTOR; SPIROCHETE; ADENOCARCINOMA; DYSBIOSIS; ESOPHAGEAL NEOPLASMS; ESOPHAGITIS, PEPTIC; ESOPHAGUS; MICROBIOLOGY; MICROFLORA; PRECANCEROUS CONDITIONS;

ADENOCARCINOMA; BARRETT ESOPHAGUS; DYSBIOSIS; ESOPHAGEAL NEOPLASMS; ESOPHAGITIS, PEPTIC; ESOPHAGUS; GASTROESOPHAGEAL REFLUX; HUMANS; MICROBIOTA; OBESITY; PRECANCEROUS CONDITIONS; RISK FACTORS;

EID: 84962828755     PISSN: 01632116     EISSN: 15732568     Source Type: Journal    
DOI: 10.1007/s10620-016-4155-9     Document Type: Review

References (73)

1. Rustgi AK, El-Serag HB. Esophageal carcinoma. N Engl J Med. 2014;371:2499–2509. doi:10.1056/NEJMra1314530.
2. Hvid-Jensen F, Pedersen L, Drewes AM, Sorensen HT, Funch-Jensen P. Incidence of adenocarcinoma among patients with Barrett’s esophagus. N Engl J Med. 2011;365:1375–1383. doi:10.1056/NEJMoa1103042.
3. Bhat S, Coleman HG, Yousef F, et al. Risk of malignant progression in Barrett’s esophagus patients: results from a large population-based study. J Natl Cancer Inst. 2011;103:1049–1057. doi:10.1093/jnci/djr203.
4. Wani S, Falk G, Hall M, et al. Patients with nondysplastic Barrett’s esophagus have low risks for developing dysplasia or esophageal adenocarcinoma. Clin Gastroenterol Hepatol. 2011;9:220–227. doi:10.1016/j.cgh.2010.11.008. (quiz e26).
5. Pohl H, Sirovich B, Welch HG. Esophageal adenocarcinoma incidence: Are we reaching the peak? Cancer Epidemiol Biomarkers Prev. 2010;19:1468–1470. doi:10.1158/1055-9965.EPI-10-0012.
6. Thrift AP, Whiteman DC. The incidence of esophageal adenocarcinoma continues to rise: analysis of period and birth cohort effects on recent trends. Ann Oncol. 2012;23:3155–3162. doi:10.1093/annonc/mds181.
7. Brown LM, Devesa SS, Chow WH. Incidence of adenocarcinoma of the esophagus among white Americans by sex, stage, and age. J Natl Cancer Inst. 2008;100:1184–1187.
8. Abrams JA, Sharaiha RZ, Gonsalves L, Lightdale CJ, Neugut AI. Dating the rise of esophageal adenocarcinoma: analysis of Connecticut Tumor Registry data, 1940–2007. Cancer Epidemiol Biomarkers Prev. 2011;20:183–186. doi:10.1158/1055-9965.EPI-10-0802.
9. Hansson LE, Sparen P, Nyren O. Increasing incidence of both major histological types of esophageal carcinomas among men in Sweden. Int J Cancer. 1993;54:402–407.
10. Post PN, Siersema PD, Van Dekken H. Rising incidence of clinically evident Barrett’s oesophagus in The Netherlands: a nation-wide registry of pathology reports. Scand J Gastroenterol. 2007;42:17–22. doi:10.1080/00365520600815654.
11. Coleman HG, Bhat S, Murray LJ, McManus D, Gavin AT, Johnston BT. Increasing incidence of Barrett’s oesophagus: a population-based study. Eur J Epidemiol. 2011;26:739–745. doi:10.1007/s10654-011-9596-z.
12. van Soest EM, Dieleman JP, Siersema PD, Sturkenboom MC, Kuipers EJ. Increasing incidence of Barrett’s oesophagus in the general population. Gut. 2005;54:1062–1066. doi:10.1136/gut.2004.063685.
13. Petrick JL, Nguyen T, Cook MB. Temporal trends of esophageal disorders by age in the Cerner Health Facts database. Ann Epidemiol. 2016;26:151–154 e4. doi:10.1016/j.annepidem.2015.11.004.
14. Sharma P, Falk GW, Weston AP, Reker D, Johnston M, Sampliner RE. Dysplasia and cancer in a large multicenter cohort of patients with Barrett’s esophagus. Clin Gastroenterol Hepatol. 2006;4:566–572. doi:10.1016/j.cgh.2006.03.001.
15. den Hoed CM, van Blankenstein M, Dees J, Kuipers EJ. The minimal incubation period from the onset of Barrett’s oesophagus to symptomatic adenocarcinoma. Br J Cancer. 2011;105:200–205. doi:10.1038/bjc.2011.214.
16. Engel LS, Chow WH, Vaughan TL, et al. Population attributable risks of esophageal and gastric cancers. J Natl Cancer Inst. 2003;95:1404–1413.
17. El-Serag HB. Time trends of gastroesophageal reflux disease: a systematic review. Clin Gastroenterol Hepatol. 2007;5:17–26. doi:10.1016/j.cgh.2006.09.016.
18. el-Serag HB, Sonnenberg A. Opposing time trends of peptic ulcer and reflux disease. Gut. 1998;43:327–333.
19. Flegal KM, Carroll MD, Kuczmarski RJ, Johnson CL. Overweight and obesity in the United States: prevalence and trends, 1960–1994. Int J Obes Relat Metab Disord. 1998;22:39–47.
20. Kong CY, Nattinger KJ, Hayeck TJ, et al. The impact of obesity on the rise in esophageal adenocarcinoma incidence: estimates from a disease simulation model. Cancer Epidemiol Biomarkers Prev. 2011;20:2450–2456. doi:10.1158/1055-9965.EPI-11-0547.
21. Giovino GA. Epidemiology of tobacco use in the United States. Oncogene. 2002;21:7326–7340. doi:10.1038/sj.onc.1205808.
22. Cook MB, Kamangar F, Whiteman DC, et al. Cigarette smoking and adenocarcinomas of the esophagus and esophagogastric junction: a pooled analysis from the international BEACON consortium. J Natl Cancer Inst. 2010;102:1344–1353. doi:10.1093/jnci/djq289.
23. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2015. CA Cancer J Clin. 2015;65:5–29. doi:10.3322/caac.21254.
24. Lagergren K, Lindam A, Lagergren J. Dietary proportions of carbohydrates, fat, and protein and risk of oesophageal cancer by histological type. PLoS ONE. 2013;8:e54913. doi:10.1371/journal.pone.0054913.
25. Popkin BM, Adair LS, Ng SW. Global nutrition transition and the pandemic of obesity in developing countries. Nutr Rev. 2012;70:3–21. doi:10.1111/j.1753-4887.2011.00456.x.
26. Austin GL, Ogden LG, Hill JO. Trends in carbohydrate, fat, and protein intakes and association with energy intake in normal-weight, overweight, and obese individuals: 1971-2006. Am J Clin Nutr. 2011;93:836–843. doi:10.3945/ajcn.110.000141.
27. Wright JD, Wang CY. Trends in intake of energy and macronutrients in adults from 1999–2000 through 2007–2008. NCHS Data Brief. 2010;49:1–8.
28. Centers for Disease C, Prevention. Trends in intake of energy and macronutrients—United States, 1971–2000. MMWR Morb Mortal Wkly Rep. 2004;53:80–82.
29. Lewis K. Platforms for antibiotic discovery. Nat Rev Drug Discov. 2013;12:371–387. doi:10.1038/nrd3975.
30. Islami F, Kamangar F. Helicobacter pylori and esophageal cancer risk: a meta-analysis. Cancer Prev Res (Phila). 2008;1:329–338. doi:10.1158/1940-6207.CAPR-08-0109.
31. Banatvala N, Mayo K, Megraud F, Jennings R, Deeks JJ, Feldman RA. The cohort effect and Helicobacter pylori. J Infect Dis. 1993;168:219–221.
32. Rehnberg-Laiho L, Rautelin H, Koskela P, et al. Decreasing prevalence of helicobacter antibodies in Finland, with reference to the decreasing incidence of gastric cancer. Epidemiol Infect. 2001;126:37–42.
33. Abreu MT, Peek RM Jr. Gastrointestinal malignancy and the microbiome. Gastroenterology. 2014;146:1534–1546.e3. doi:10.1053/j.gastro.2014.01.001.
34. Schwabe RF, Jobin C. The microbiome and cancer. Nat Rev Cancer. 2013;13:800–812. doi:10.1038/nrc3610.
35. Fraher MH, O’Toole PW, Quigley EM. Techniques used to characterize the gut microbiota: a guide for the clinician. Nat Rev Gastroenterol Hepatol. 2012;9:312–322. doi:10.1038/nrgastro.2012.44.
36. Smith JL, Bayles DO. The contribution of cytolethal distending toxin to bacterial pathogenesis. Crit Rev Microbiol. 2006;32:227–248. doi:10.1080/10408410601023557.
37. Arthur JC, Perez-Chanona E, Muhlbauer M, et al. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science. 2012;338:120–123. doi:10.1126/science.1224820.
38. Rubinstein MR, Wang X, Liu W, Hao Y, Cai G, Han YW. Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/beta-catenin signaling via its FadA adhesin. Cell Host Microbe. 2013;14:195–206. doi:10.1016/j.chom.2013.07.012.
39. Lau WF, Wong J, Lam KH, Ong GB. Oesophageal microbial flora in carcinoma of the oesophagus. Aust N Z J Surg. 1981;51:52–55.
40. Finlay IG, Wright PA, Menzies T, McArdle CS. Microbial flora in carcinoma of oesophagus. Thorax. 1982;37:181–184.
41. Mannell A, Plant M, Frolich J. The microflora of the oesophagus. Ann R Coll Surg Engl. 1983;65:152–154.
42. Pei Z, Bini EJ, Yang L, Zhou M, Francois F, Blaser MJ. Bacterial biota in the human distal esophagus. Proc Natl Acad Sci USA. 2004;101:4250–4255. doi:10.1073/pnas.0306398101.
43. Dewhirst FE, Chen T, Izard J, et al. The human oral microbiome. J Bacteriol. 2010;192:5002–5017. doi:10.1128/JB.00542-10.
44. Osias GL, Bromer MQ, Thomas RM, et al. Esophageal bacteria and Barrett’s esophagus: a preliminary report. Dig Dis Sci. 2004;49:228–236.
45. Macfarlane S, Furrie E, Macfarlane GT, Dillon JF. Microbial colonization of the upper gastrointestinal tract in patients with Barrett’s esophagus. Clin Infect Dis. 2007;45:29–38. doi:10.1086/518578.
46. 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;137:588–597. doi:10.1053/j.gastro.2009.04.046.
47. Liu N, Ando T, Ishiguro K, et al. Characterization of bacterial biota in the distal esophagus of Japanese patients with reflux esophagitis and Barrett’s esophagus. BMC Infect Dis. 2013;13:130. doi:10.1186/1471-2334-13-130.
48. Gall A, Fero J, McCoy C, et al. Bacterial composition of the human upper gastrointestinal tract microbiome is dynamic and associated with genomic instability in a Barrett’s esophagus cohort. PLoS ONE. 2015;10:e0129055. doi:10.1371/journal.pone.0129055.
49. Narikiyo M, Tanabe C, Yamada Y, et al. Frequent and preferential infection of Treponema denticola, Streptococcus mitis, and Streptococcus anginosus in esophageal cancers. Cancer Sci. 2004;95:569–574.
50. Blackett KL, Siddhi SS, Cleary S, et al. Oesophageal bacterial biofilm changes in gastro-oesophageal reflux disease, Barrett’s and oesophageal carcinoma: Association or causality? Aliment Pharmacol Ther. 2013;37:1084–1092. doi:10.1111/apt.12317.
51. Clarke AT, Wirz AA, Seenan JP, Manning JJ, Gillen D, McColl KE. Paradox of gastric cardia: it becomes more acidic following meals while the rest of stomach becomes less acidic. Gut. 2009;58:904–909. doi:10.1136/gut.2008.161927.
52. McDonald SA, Lavery D, Wright NA, Jansen M. Barrett oesophagus: lessons on its origins from the lesion itself. Nat Rev Gastroenterol Hepatol. 2015;12:50–60. doi:10.1038/nrgastro.2014.181.
53. Quante M, Bhagat G, Abrams JA, et al. Bile acid and inflammation activate gastric cardia stem cells in a mouse model of Barrett-like metaplasia. Cancer Cell. 2012;21:36–51. doi:10.1016/j.ccr.2011.12.004.
54. Polk DB, Peek RM Jr. Helicobacter pylori: gastric cancer and beyond. Nat Rev Cancer. 2010;10:403–414. doi:10.1038/nrc2857.
55. Rubenstein JH, Inadomi JM, Scheiman J, et al. Association between Helicobacter pylori and Barrett’s esophagus, erosive esophagitis, and gastroesophageal reflux symptoms. Clin Gastroenterol Hepatol. 2014;12:239–245. doi:10.1016/j.cgh.2013.08.029.
56. Bik EM, Eckburg PB, Gill SR, et al. Molecular analysis of the bacterial microbiota in the human stomach. Proc Natl Acad Sci USA. 2006;103:732–737. doi:10.1073/pnas.0506655103.
57. Tian Z, Yang Z, Gao J, Zhu L, Jiang R, Jiang Y. Lower esophageal microbiota species are affected by the eradication of infection using antibiotics. Exp Ther Med. 2015;9:685–692. doi:10.3892/etm.2015.2169.
58. Andersson AF, Lindberg M, Jakobsson H, Backhed F, Nyren P, Engstrand L. Comparative analysis of human gut microbiota by barcoded pyrosequencing. PLoS ONE. 2008;3:e2836. doi:10.1371/journal.pone.0002836.
59. Li XX, Wong GL, To KF, et al. Bacterial microbiota profiling in gastritis without Helicobacter pylori infection or non-steroidal anti-inflammatory drug use. PLoS ONE. 2009;4:e7985. doi:10.1371/journal.pone.0007985.
60. Stearns JC, Lynch MD, Senadheera DB, et al. Bacterial biogeography of the human digestive tract. Sci Rep. 2011;1:170. doi:10.1038/srep00170.
61. Maldonado-Contreras A, Goldfarb KC, Godoy-Vitorino F, et al. Structure of the human gastric bacterial community in relation to Helicobacter pylori status. ISME J. 2011;5:574–579. doi:10.1038/ismej.2010.149.
62. Jackson MA, Goodrich JK, Maxan ME, et al. Proton pump inhibitors alter the composition of the gut microbiota. Gut. 2015. doi:10.1136/gutjnl-2015-310861.
63. Freedberg DE, Toussaint NC, Chen SP, et al. Proton pump inhibitors alter specific taxa in the human gastrointestinal microbiome: a crossover trial. Gastroenterology. 2015. doi:10.1053/j.gastro.2015.06.043.
64. Rosen R, Amirault J, Liu H, et al. Changes in gastric and lung microflora with acid suppression: acid suppression and bacterial growth. JAMA Pediatr. 2014;168:932–937. doi:10.1001/jamapediatrics.2014.696.
65. David LA, Maurice CF, Carmody RN, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505:559–563. doi:10.1038/nature12820.
66. Albenberg LG, Wu GD. Diet and the intestinal microbiome: associations, functions, and implications for health and disease. Gastroenterology. 2014;146:1564–1572. doi:10.1053/j.gastro.2014.01.058.
67. Schulz MD, Atay C, Heringer J, et al. High-fat-diet-mediated dysbiosis promotes intestinal carcinogenesis independently of obesity. Nature. 2014;514:508–512. doi:10.1038/nature13398.
68. O’Keefe SJ, Li JV, Lahti L, et al. Fat, fibre and cancer risk in African Americans and rural Africans. Nat Commun. 2015;6:6342. doi:10.1038/ncomms7342.
69. Jiang Q, Akashi S, Miyake K, Petty HR. Lipopolysaccharide induces physical proximity between CD14 and toll-like receptor 4 (TLR4) prior to nuclear translocation of NF-kappa B. J Immunol. 2000;165:3541–3544.
70. O’Riordan JM, Abdel-latif MM, Ravi N, et al. Proinflammatory cytokine and nuclear factor kappa-B expression along the inflammation-metaplasia-dysplasia-adenocarcinoma sequence in the esophagus. Am J Gastroenterol. 2005;100:1257–1264. doi:10.1111/j.1572-0241.2005.41338.x.
71. Calatayud S, Garcia-Zaragoza E, Hernandez C, et al. Downregulation of nNOS and synthesis of PGs associated with endotoxin-induced delay in gastric emptying. Am J Physiol Gastrointest Liver Physiol. 2002;283:G1360–G1367. doi:10.1152/ajpgi.00168.2002.
72. Fan YP, Chakder S, Gao F, Rattan S. Inducible and neuronal nitric oxide synthase involvement in lipopolysaccharide-induced sphincteric dysfunction. Am J Physiol Gastrointest Liver Physiol. 2001;280:G32–G42.
73. Suzuki H, Iijima K, Scobie G, Fyfe V, McColl KE. Nitrate and nitrosative chemistry within Barrett’s oesophagus during acid reflux. Gut. 2005;54:1527–1535. doi:10.1136/gut.2005.066043.