The microbiome in pancreatic diseases: Recent advances and future perspectives

Christoph Ammer-Herrmenau, Nina Pfisterer, Mark Fj Weingarten, Albrecht Neesse, Christoph Ammer-Herrmenau, Nina Pfisterer, Mark Fj Weingarten, Albrecht Neesse

Abstract

The human microbiota exerts multiple physiological functions such as the regulation of metabolic and inflammatory processes. High-throughput sequencing techniques such as next-generation sequencing have become widely available in preclinical and clinical settings and have exponentially increased our knowledge about the microbiome and its interaction with host cells and organisms. There is now emerging evidence that microorganisms also contribute to inflammatory and neoplastic diseases of the pancreas. This review summarizes current clinical and translational microbiome studies in acute and chronic pancreatitis as well as pancreatic cancer and provides evidence that the microbiome has a high potential for biomarker discovery. Furthermore, the intestinal and pancreas-specific microbiome may also become an integrative part of diagnostic and therapeutic approaches of pancreatic diseases in the near future.

Keywords: 16S rRNA sequencing; Pancreatic cancer; metagenomic sequencing; microbiome; pancreatitis.

Figures

Figure 1.
Figure 1.
Key findings and current perceptions of the orointestinal microbiome in pancreatic ductal adenocarcinoma (PDAC) and acute and chronic pancreatitis.

References

    1. Qin J, Li R, Raes J, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010; 464: 59–65.
    1. Hall AB, Tolonen AC, Xavier RJ. Human genetic variation and the gut microbiome in disease. Nat Rev Genet 2017; 18: 690–699.
    1. Huttenhower C, Gevers D, Knight R, et al. Structure, function and diversity of the healthy human microbiome. Nature 2012; 486: 207–214.
    1. Pushalkar S, Hundeyin M, Daley D, et al. The pancreatic cancer microbiome promotes oncogenesis by induction of innate and adaptive immune suppression. Cancer Discov 2018; 8: 403–416.
    1. Geller LT, Barzily-Rokni M, Danino T, et al. Potential role of intratumor bacteria in mediating tumor resistance to the chemotherapeutic drug gemcitabine. Science 2017; 357: 1156–1160.
    1. Wu LM, Sankaran SJ, Plank LD, et al. Meta-analysis of gut barrier dysfunction in patients with acute pancreatitis. Br J Surg 2014; 101: 1644–1656.
    1. Crockett SD, Wani S, Gardner TB, et al. American Gastroenterological Association Institute guidelines on initial management of acute pancreatitis. Gastroenterol 2018; 154: 1096–1101.
    1. Ding N, Sun Y-H, Wen L-M, et al. Assessment of prophylactic antibiotics administration for acute pancreatitis: A meta-analysis of randomized controlled trials. Chin Med J 2020; 133: 212–220.
    1. Ukai T, Shikata S, Inoue M, et al. Early prophylactic antibiotics administration for acute necrotizing pancreatitis: A meta-analysis of randomized controlled trials. J Hepatobiliary Pancreat Sci 2015; 22: 316–321.
    1. Zhu Y, He C, Li X, et al. Gut microbiota dysbiosis worsens the severity of acute pancreatitis in patients and mice. J Gastroenterol 2019; 54: 347–358.
    1. Werge M, Novovic S, Schmidt PN, et al. Infection increases mortality in necrotizing pancreatitis: A systematic review and meta-analysis. Pancreatology 2016; 16: 698–707.
    1. 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 2010; 200: 111–117.
    1. Aykut B, Pushalkar S, Chen R, et al. The fungal mycobiome promotes pancreatic oncogenesis via activation of MBL. Nature 2019; 574: 264–267.
    1. Sahar N, Kozarek RA, Kanji ZS, et al. The microbiology of infected pancreatic necrosis in the era of minimally invasive therapy. Eur J Clin Microbiol Infect Dis 2018; 37: 1353–1359.
    1. Mowbray NG, Ben-Ismaeil B, Hammoda M, et al. The microbiology of infected pancreatic necrosis. Hepatobiliary Pancreatic Dis Int 2018; 17: 456–460.
    1. Frost F, Kacprowski T, Rühlemann M, et al. Impaired exocrine pancreatic function associates with changes in intestinal microbiota composition and diversity. Gastroenterol 2019; 156: 1010–1015.
    1. Capurso G, Signoretti M, Archibugi L, et al. Systematic review and meta-analysis: Small intestinal bacterial overgrowth in chronic pancreatitis. United European Gastroenterol J 2016; 4: 697–705.
    1. Ní Chonchubhair HM, 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). Pancreatol 2018; 18: 379–385.
    1. Jandhyala SM, Madhulika A, Deepika G, et al. Altered intestinal microbiota in patients with chronic pancreatitis: Implications in diabetes and metabolic abnormalities. Sci Rep 2017; 7: 43640.
    1. Lopez-Siles M, Duncan SH, Garcia-Gil LJ, et al. Faecalibacterium prausnitzii: From microbiology to diagnostics and prognostics. ISME J 2017; 11: 841–852.
    1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2019. CA Cancer J Clin 2019; 69: 7–34.
    1. Rahib L, Smith BD, 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 2014; 74: 2913–2921.
    1. Riquelme E, Zhang Y, Zhang L, et al. Tumor microbiome diversity and composition influence pancreatic cancer outcomes. Cell 2019; 178: 795–806.e12.
    1. Michaud DS, Izard J, Wilhelm-Benartzi CS, et al. Plasma antibodies to oral bacteria and risk of pancreatic cancer in a large European prospective cohort study. Gut 2013; 62: 1764–1770.
    1. Farrell JJ, Zhang L, Zhou H, et al. Variations of oral microbiota are associated with pancreatic diseases including pancreatic cancer. Gut 2012; 61: 582–588.
    1. Fan X, Alekseyenko AV, Wu J, et al. Human oral microbiome and prospective risk for pancreatic cancer: A population-based nested case-control study. Gut 2018; 67: 120–127.
    1. Olson SH, Satagopan J, Xu Y, et al. The oral microbiota in patients with pancreatic cancer, patients with IPMNs, and controls: A pilot study. Cancer Causes Control 2017; 28: 959–969.
    1. Torres PJ, Fletcher EM, Gibbons SM, et al. Characterization of the salivary microbiome in patients with pancreatic cancer. PeerJ 2015; 3: e1373.
    1. Vogtmann E, Han Y, Caporaso JG, et al. Oral microbial community composition is associated with pancreatic cancer: A case-control study in Iran. Cancer Med 2020; 9: 797–806.
    1. Lin I-H, Wu J, Cohen SM, et al. Abstract 101: Pilot study of oral microbiome and risk of pancreatic cancer. In: Epidemiology. American Association for Cancer Research, 2013, p. 101.
    1. Lu H, Ren Z, Li A, et al. Tongue coating microbiome data distinguish patients with pancreatic head cancer from healthy controls. J Oral Microbiol 2019; 11: 1563409.
    1. Nejman D, Livyatan I, Fuks G, et al. The human tumor microbiome is composed of tumor type-specific intracellular bacteria. Science 2020; 368: 973–980.
    1. Knight R, Vrbanac A, Taylor BC, et al. Best practices for analysing microbiomes. Nat Rev Microbiol 2018; 16: 410–422.
    1. Routy B, Le Chatelier E, Derosa L, et al. Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science 2018; 359: 91–97.
    1. Gopalakrishnan V, Spencer CN, Nezi L, et al. Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science 2018; 359: 97–103.
    1. Matson V, Fessler J, Bao R, et al. The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients. Science 2018; 359: 104–108.
    1. Schmitt FCF, Brenner T, Uhle F, et al. Gut microbiome patterns correlate with higher postoperative complication rates after pancreatic surgery. BMC Microbiol 2019; 19: 42.

Source: PubMed

Sponsors et collaborateurs

Les conditions médicales

Interventions en matière de drogue

3
S'abonner