The Gut Microbiome in Pancreatic Disease

Clinical Gastroenterology and Hepatology

Volumn 17, Issue 2, 2019, Pages 290-295

  Akshintala, Venkata S ^a   Talukdar, Rupjyoti ^b,c   Singh, Vikesh K ^a   Goggins, Michael ^a  

^a DEPARTMENT OF PATHOLOGY   (United States)

^b ASIAN INSTITUTE OF GASTROENTEROLOGY   (India)

^c Wellcome DBT Laboratories   (India)

Author keywords

Dysbiosis; Intratumoral Bacteria; Microbiome; Pancreatic Cancer; Pancreatitis; Probiotics

Indexed keywords

BACTERIAL DNA; PROBIOTIC AGENT;

ACUTE PANCREATITIS; BACTERIAL GROWTH; BACTEROIDETES; BIFIDOBACTERIUM; CANCER RISK; CANDIDA; CHRONIC PANCREATITIS; DISEASE COURSE; DISEASE EXACERBATION; DYSBIOSIS; ENTEROBACTERIACEAE; ENTEROCOCCUS; FAECALIBACTERIUM PRAUSNITZII; FIRMICUTES; HUMAN; INTESTINE FLORA; INTESTINE MUCOSA; LACTOBACILLUS; MICROBIAL ACTIVITY; MORTALITY; NONHUMAN; PANCREAS CANCER; PANCREAS DISEASE; PATHOGENESIS; REVIEW; STAPHYLOCOCCUS; COMPLICATION; GASTROINTESTINAL TRACT; MICROBIOLOGY;

DYSBIOSIS; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; HOST MICROBIAL INTERACTIONS; HUMANS; PANCREATIC DISEASES;

EID: 85059127500     PISSN: 15423565     EISSN: 15427714     Source Type: Journal    
DOI: 10.1016/j.cgh.2018.08.045     Document Type: Review

References (72)

1. Forbes, J.D., Van Domselaar, G., Bernstein, C.N., The gut microbiota in immune-mediated inflammatory diseases. Front Microbiol, 7, 2016, 1081.
2. Savage, D.C., Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol 31 (1977), 107–133.
3. Lucas Lopez, R., Grande Burgos, M.J., Galvez, A., et al. The human gastrointestinal tract and oral microbiota in inflammatory bowel disease: a state of the science review. APMIS 125 (2017), 3–10.
4. Pagliari, D., Piccirillo, C.A., Larbi, A., et al. The interactions between innate immunity and microbiota in gastrointestinal diseases. J Immunol Res, 2015, 2015, 898297.
5. Jandhyala, S.M., Talukdar, R., Subramanyam, C., et al. Role of the normal gut microbiota. World J Gastroenterol 21 (2015), 8787–8803.
6. Tang, W.H., Wang, Z., Levison, B.S., et al. Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk. N Engl J Med 368 (2013), 1575–1584.
7. Fujisaka, S., Avila-Pacheco, J., Soto, M., et al. Diet, genetics, and the gut microbiome drive dynamic changes in plasma metabolites. Cell Rep 22 (2018), 3072–3086.
8. Zierer, J., Jackson, M.A., Kastenmuller, G., et al. The fecal metabolome as a functional readout of the gut microbiome. Nat Genet 50 (2018), 790–795.
9. Sartor, R.B., Wu, G.D., Roles for intestinal bacteria, viruses, and fungi in pathogenesis of inflammatory bowel diseases and therapeutic approaches. Gastroenterology 152 (2017), 327–339.e4.
10. Greenblum, S., Turnbaugh, P.J., Borenstein, E., Metagenomic systems biology of the human gut microbiome reveals topological shifts associated with obesity and inflammatory bowel disease. Proc Natl Acad Sci U S A 109 (2012), 594–599.
11. Turnbaugh, P.J., Hamady, M., Yatsunenko, T., et al. A core gut microbiome in obese and lean twins. Nature 457 (2009), 480–484.
12. Ridaura, V.K., Faith, J.J., Rey, F.E., et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science, 341, 2013, 1241214.
13. Wang, C., Li, J., Pathogenic microorganisms and pancreatic cancer. Gastrointest Tumors 2 (2015), 41–47.
14. Signoretti, M., Roggiolani, R., Stornello, C., et al. Gut microbiota and pancreatic diseases. Minerva Gastroenterol Dietol 63 (2017), 399–410.
15. Pushalkar, S., Hundeyin, M., Daley, D., et al. The pancreatic cancer microbiome promotes oncogenesis by induction of innate and adaptive immune suppression. Cancer Discov 8 (2018), 403–416.
16. David, L.A., Maurice, C.F., Carmody, R.N., et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505 (2014), 559–563.
17. Wu, G.D., Chen, J., Hoffmann, C., et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 334 (2011), 105–108.
18. Llorente, C., Jepsen, P., Inamine, T., et al. Gastric acid suppression promotes alcoholic liver disease by inducing overgrowth of intestinal Enterococcus. Nat Commun, 8, 2017, 837.
19. Forslund, K., Hildebrand, F., Nielsen, T., et al. Disentangling type 2 diabetes and metformin treatment signatures in the human gut microbiota. Nature 528 (2015), 262–266.
20. Kolde, R., Franzosa, E.A., Rahnavard, G., et al. Host genetic variation and its microbiome interactions within the Human Microbiome Project. Genome Med, 10, 2018, 6.
21. Li, D., Achkar, J.P., Haritunians, T., et al. A pleiotropic missense variant in SLC39A8 is associated with Crohn's disease and human gut microbiome composition. Gastroenterology 151 (2016), 724–732.
22. Imhann, F., Vich Vila, A., Bonder, M.J., et al. Interplay of host genetics and gut microbiota underlying the onset and clinical presentation of inflammatory bowel disease. Gut 67 (2018), 108–119.
23. Yadav, D., Lowenfels, A.B., The epidemiology of pancreatitis and pancreatic cancer. Gastroenterology 144 (2013), 1252–1261.
24. Peery, A.F., Crockett, S.D., Barritt, A.S., et al. Burden of gastrointestinal, liver, and pancreatic diseases in the United States. Gastroenterology 149 (2015), 1731–1741 e3.
25. Lerch, M.M., Gorelick, F.S., Models of acute and chronic pancreatitis. Gastroenterology 144 (2013), 1180–1193.
26. Andersson, R., Wang, X.D., Gut barrier dysfunction in experimental acute pancreatitis. Ann Acad Med Singapore 28 (1999), 141–146.
27. Wu, L.M., Sankaran, S.J., Plank, L.D., et al. Meta-analysis of gut barrier dysfunction in patients with acute pancreatitis. Br J Surg 101 (2014), 1644–1656.
28. Li, Q., Wang, C., Tang, C., et al. Bacteremia in patients with acute pancreatitis as revealed by 16S ribosomal RNA gene-based techniques*. Crit Care Med 41 (2013), 1938–1950.
29. Werge, M., Novovic, S., Schmidt, P.N., et al. Infection increases mortality in necrotizing pancreatitis: a systematic review and meta-analysis. Pancreatology 16 (2016), 698–707.
30. Sahar, N., Kozarek, R.A., Kanji, Z.S., et al. The microbiology of infected pancreatic necrosis in the era of minimally invasive therapy. Eur J Clin Microbiol Infect Dis 37 (2018), 1353–1359.
31. Caldas, C., Hahn, S.A., da Costa, L.T., et al. Frequent somatic mutations and homozygous deletions of the p16 (MTS1) gene in pancreatic adenocarcinoma [published erratum appears in Nat Genet 1994;8:410]. Nat Genet 8 (1994), 27–32.
32. Van Felius, I.D., Akkermans, L.M., Bosscha, K., et al. Interdigestive small bowel motility and duodenal bacterial overgrowth in experimental acute pancreatitis. Neurogastroenterol Motil 15 (2003), 267–276.
33. Fritz, S., Hackert, T., Hartwig, W., et al. Bacterial translocation and infected pancreatic necrosis in acute necrotizing pancreatitis derives from small bowel rather than from colon. Am J Surg 200 (2010), 111–117.
34. Chen, J., Huang, C., Wang, J., et al. Dysbiosis of intestinal microbiota and decrease in Paneth cell antimicrobial peptide level during acute necrotizing pancreatitis in rats. PLoS One, 12, 2017, e0176583.
35. Wong, W., Shaping the gut microbiome from the pancreas. Sci Signal, 10, 2017, 472.
36. Ahuja, M., Schwartz, D.M., Tandon, M., et al. Orai1-mediated antimicrobial secretion from pancreatic acini shapes the gut microbiome and regulates gut innate immunity. Cell Metab 25 (2017), 635–646.
37. Watanabe, T., Sadakane, Y., Yagama, N., et al. Nucleotide-binding oligomerization domain 1 acts in concert with the cholecystokinin receptor agonist, cerulein, to induce IL-33-dependent chronic pancreatitis. Mucosal Immunol 9 (2016), 1234–1249.
38. Tsuji, Y., Watanabe, T., Kudo, M., et al. Sensing of commensal organisms by the intracellular sensor NOD1 mediates experimental pancreatitis. Immunity 37 (2012), 326–338.
39. Tan, C., Ling, Z., Huang, Y., et al. Dysbiosis of intestinal microbiota associated with inflammation involved in the progression of acute pancreatitis. Pancreas 44 (2015), 868–875.
40. Gou, S., Yang, Z., Liu, T., et al. Use of probiotics in the treatment of severe acute pancreatitis: a systematic review and meta-analysis of randomized controlled trials. Crit Care, 18, 2014, R57.
41. Poropat, G., Giljaca, V., Hauser, G., et al. Enteral nutrition formulations for acute pancreatitis. Cochrane Database Syst Rev, 3, 2015, CD010605.
42. Besselink, M.G., Timmerman, H.M., Buskens, E., et al. Probiotic prophylaxis in patients with predicted severe acute pancreatitis (PROPATRIA): design and rationale of a double-blind, placebo-controlled randomised multicenter trial [ISRCTN38327949]. BMC Surg, 4, 2004, 12.
43. Morrow, L.E., Gogineni, V., Malesker, M.A., Synbiotics and probiotics in the critically ill after the PROPATRIA trial. Curr Opin Clin Nutr Metab Care 15 (2012), 147–150.
44. Memba, R., Duggan, S.N., Ni Chonchubhair, H.M., et al. The potential role of gut microbiota in pancreatic disease: a systematic review. Pancreatology 17 (2017), 867–874.
45. Bures, J., Cyrany, J., Kohoutova, D., et al. Small intestinal bacterial overgrowth syndrome. World J Gastroenterol 16 (2010), 2978–2990.
46. Dutta, S.K., Russell, R.M., Iber, F.L., Impaired acid neutralization in the duodenum in pancreatic insufficiency. Dig Dis Sci 24 (1979), 775–780.
47. Ni Chonchubhair, H.M., Bashir, Y., Dobson, M., et al. The prevalence of small intestinal bacterial overgrowth in non-surgical patients with chronic pancreatitis and pancreatic exocrine insufficiency (PEI). Pancreatology 18 (2018), 379–385.
48. Capurso, G., Signoretti, M., Archibugi, L., et al. Systematic review and meta-analysis: small intestinal bacterial overgrowth in chronic pancreatitis. United European Gastroenterol J 4 (2016), 697–705.
49. Jandhyala, S.M., Madhulika, A., Deepika, G., et al. Altered intestinal microbiota in patients with chronic pancreatitis: implications in diabetes and metabolic abnormalities. Sci Rep, 7, 2017, 43640.
50. Wrzosek, L., Miquel, S., Noordine, M.L., et al. Bacteroides thetaiotaomicron and Faecalibacterium prausnitzii influence the production of mucus glycans and the development of goblet cells in the colonic epithelium of a gnotobiotic model rodent. BMC Biol, 11, 2013, 61.
51. Rossi, O., van Berkel, L.A., Chain, F., et al. Faecalibacterium prausnitzii A2-165 has a high capacity to induce IL-10 in human and murine dendritic cells and modulates T cell responses. Sci Rep, 6, 2016, 18507.
52. Rahib, L., Smith, B.D., Aizenberg, R., et al. Projecting cancer incidence and deaths to 2030: the unexpected burden of thyroid, liver, and pancreas cancers in the United States. Cancer Res 74 (2014), 2913–2921.
53. Kirkegard, J., Mortensen, F.V., Cronin-Fenton, D., Chronic pancreatitis and pancreatic cancer risk: a systematic review and meta-analysis. Am J Gastroenterol 112 (2017), 1366–1372.
54. Lowenfels, A.B., Maisonneuve, P., DiMagno, E.P., et al. Hereditary pancreatitis and the risk of pancreatic cancer. International Hereditary Pancreatitis Study Group. J Natl Cancer Inst 89 (1997), 442–446.
55. Duell, E.J., Lucenteforte, E., Olson, S.H., et al. Pancreatitis and pancreatic cancer risk: a pooled analysis in the International Pancreatic Cancer Case-Control Consortium (PanC4). Ann Oncol 23 (2012), 2964–2970.
56. Garrett, W.S., Cancer and the microbiota. Science 348 (2015), 80–86.
57. Maslowski, K.M., Vieira, A.T., Ng, A., et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 461 (2009), 1282–1286.
58. Dejea, C.M., Fathi, P., Craig, J.M., et al. Patients with familial adenomatous polyposis harbor colonic biofilms containing tumorigenic bacteria. Science 359 (2018), 592–597.
59. Dejea, C.M., Wick, E.C., Hechenbleikner, E.M., et al. Microbiota organization is a distinct feature of proximal colorectal cancers. Proc Natl Acad Sci U S A 111 (2014), 18321–18326.
60. Iida, N., Dzutsev, A., Stewart, C.A., et al. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science 342 (2013), 967–970.
61. Sears, C.L., Pardoll, D.M., The intestinal microbiome influences checkpoint blockade. Nat Med 24 (2018), 254–265.
62. Gopalakrishnan, V., Spencer, C.N., Nezi, L., et al. Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science 359 (2018), 97–103.
63. Routy, B., Le Chatelier, E., Derosa, L., et al. Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science 359 (2018), 91–97.
64. Fan, X., Alekseyenko, A.V., Wu, J., et al. Human oral microbiome and prospective risk for pancreatic cancer: a population-based nested case-control study. Gut 67 (2018), 120–127.
65. Michaud, D.S., Izard, J., Wilhelm-Benartzi, C.S., et al. Plasma antibodies to oral bacteria and risk of pancreatic cancer in a large European prospective cohort study. Gut 62 (2013), 1764–1770.
66. Torres, P.J., Fletcher, E.M., Gibbons, S.M., et al. Characterization of the salivary microbiome in patients with pancreatic cancer. PeerJ, 3, 2015, e1373.
67. Chang, J.S., Tsai, C.R., Chen, L.T., et al. Investigating the association between periodontal disease and risk of pancreatic cancer. Pancreas 45 (2016), 134–141.
68. Farrell, J.J., Zhang, L., Zhou, H., et al. Variations of oral microbiota are associated with pancreatic diseases including pancreatic cancer. Gut 61 (2012), 582–588.
69. Geller, L.T., Barzily-Rokni, M., Danino, T., et al. Potential role of intratumor bacteria in mediating tumor resistance to the chemotherapeutic drug gemcitabine. Science 357 (2017), 1156–1160.
70. Sethi, V., Kurtom, S., Tarique, M., et al. Gut microbiota promotes tumor growth in mice by modulating immune response. Gastroenterology 155 (2018), 33–37.e6.
71. Lehouritis, P., Cummins, J., Stanton, M., et al. Local bacteria affect the efficacy of chemotherapeutic drugs. Sci Rep, 5, 2015, 14554.
72. Li, S., Fuhler, G.M., Bn, N., et al. Pancreatic cyst fluid harbors a unique microbiome. Microbiome, 5, 2017, 147.