Research progress on the relationship between biliary flora and cholangiocarcinoma_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

XU Tao ¹ , ZHANG Bo ¹ ,  ZHOU Wence ^1,2

1. The First Clinical Medical College, Lanzhou University, Lanzhou 730000, P. R. China;
2. The Second Department of General Surgery, The First Hospital of Lanzhou University, Lanzhou 730000, P. R. China;

Corresponding author：

ZHOU Wence, Email: zhouwc@lzu.edu.cn

Keywords：

cholangiocarcinoma; biliary flora; high-throughput sequencing; review

DOI：

10.7507/1007-9424.202006047

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To summarize the research progress of the relationship between biliary flora and cholangiocarcinoma.Method The literatures on the relationship between biliary flora and cholangiocarcinoma were collected and reviewed.Results Biliary flora was closely related to the occurrence and development of biliary tract diseases. The inflammatory environment of the biliary tract was an important factor in the occurrence and development of cholangiocarcinoma. Microbes might induce chronic inflammation of the host tissue, leading to cell proliferation and genetic mutation, and ultimately leading to the occurrence of cholangiocarcinoma. Bacterial infection might play an important role in the pathogenesis of cholangiocarcinoma.Conclusion The study of the role of biliary flora in the development of cholangiocarcinoma may open up a new direction for the prevention and treatment of cholangiocarcinoma.

Citation： XU Tao, ZHANG Bo, ZHOU Wence. Research progress on the relationship between biliary flora and cholangiocarcinoma. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2021, 28(3): 404-408. doi: 10.7507/1007-9424.202006047 Copy

1.	Rizvi S, Khan SA, Hallemeier CL, et al. Cholangiocarcinoma - evolving concepts and therapeutic strategies. Nat Rev Clin Oncol, 2018, 15(2): 95-111.
2.	Nathan H, Pawlik TM, Wolfgang CL, et al. Trends in survival after surgery for cholangiocarcinoma: a 30-year population-based SEER database analysis. J Gastrointest Surg, 2007, 11(11): 1488-1496.
3.	Saha SK, Zhu AX, Fuchs CS, et al. Forty-year trends in cholangiocarcinoma incidence in the U. S. : intrahepatic disease on the rise. Oncologist, 2016, 21(5): 594-599.
4.	Hu HJ, Mao H, Shrestha A, et al. Prognostic factors and long-term outcomes of hilar cholangiocarcinoma: a single-institution experience in China. World J Gastroenterol, 2016, 22(8): 2601-2610.
5.	Pinto C, Giordano DM, Maroni L, et al. Role of inflammation and proinflammatory cytokines in cholangiocyte pathophysiology. Biochim Biophys Acta Mol Basis Dis, 2018, 1864(4 Pt B): 1270-1278.
6.	Lee H, Lee HK, Min SK, et al. 16S rDNA microbiome composition pattern analysis as a diagnostic biomarker for biliary tract cancer. World J Surg Oncol, 2020, 18(1): 19.
7.	Poore GD, Kopylova E, Zhu Q, et al. Microbiome analyses of blood and tissues suggest cancer diagnostic approach. Nature, 2020, 579(7800): 567-574.
8.	Verdier J, Luedde T, Sellge G. Biliary mucosal barrier and microbiome. Viszeralmedizin, 2015, 31(3): 156-161.
9.	Whiteside SA, Razvi H, Dave S, et al. The microbiome of the urinary tract–a role beyond infection. Nat Rev Urol, 2015, 12(2): 81-90.
10.	Aho VTE, Pereira PAB, Haahtela T, et al. The microbiome of the human lower airways: a next generation sequencing perspective. World Allergy Organ J, 2015, 8(1): 23.
11.	Shen H, Ye F, Xie L, et al. Metagenomic sequencing of bile from gallstone patients to identify different microbial community patterns and novel biliary bacteria. Sci Rep, 2015, 5: 17450.
12.	Sung JY, Shaffer EA, Olson ME, et al. Bacterial invasion of the biliary system by way of the portal-venous system. Hepatology, 1991, 14(2): 313-317.
13.	Scott AJ, Khan GA. Origin of bacteria in bileduct bile. Lancet, 1967, 2(7520): 790-792.
14.	Anderson RE, Priestley JT. Observations on the bacteriology of choledochal bile. Ann Surg, 1951, 133(4): 486-489.
15.	Elkeles G, Mirizzi PL. A study of the bacteriology of the common bile duct in comparison with the other extrahepatic segments of the biliary tract. Ann Surg, 1942, 116(3): 360-366.
16.	Gu XX, Zhang MP, Zhao YF, et al. Clinical and microbiological characteristics of patients with biliary disease. World J Gastroenterol, 2020, 26(14): 1638-1646.
17.	Wu T, Zhang Z, Liu B, et al. Gut microbiota dysbiosis and bacterial community assembly associated with cholesterol gallstones in large-scale study. BMC Genomics, 2013, 14: 669.
18.	Ye F, Shen H, Li Z, et al. Influence of the biliary system on biliary bacteria revealed by bacterial communities of the human biliary and upper digestive tracts. PLoS One, 2016, 11(3): e0150519.
19.	Folseraas T, Melum E, Rausch P, et al. Extended analysis of a genome-wide association study in primary sclerosing cholangitis detects multiple novel risk loci. J Hepatol, 2012, 57(2): 366-375.
20.	Pereira P, Aho V, Arola J, et al. Bile microbiota in primary sclerosing cholangitis: impact on disease progression and development of biliary dysplasia. PLoS One, 2017, 12(8): e0182924.
21.	Jiménez E, Sánchez B, Farina A, et al. Characterization of the bile and gall bladder microbiota of healthy pigs. Microbiologyopen, 2014, 3(6): 937-949.
22.	Molinero N, Ruiz L, Milani C, et al. The human gallbladder microbiome is related to the physiological state and the biliary metabolic profile. Microbiome, 2019, 7(1): 100.
23.	Tyson GL, El-Serag HB. Risk factors for cholangiocarcinoma. Hepatology, 2011, 54(1): 173-184.
24.	Dyson JK, Beuers U, Jones DEJ, et al. Primary sclerosing cholangitis. Lancet, 2018, 391(10139): 2547-2559.
25.	Karlsen TH, Folseraas T, Thorburn D, et al. Primary sclerosing cholangitis–a comprehensive review. J Hepatol, 2017, 67(6): 1298-1323.
26.	Liwinski T, Zenouzi R, John C, et al. Alterations of the bile microbiome in primary sclerosing cholangitis. Gut, 2020, 69(4): 665-672.
27.	Chng KR, Chan SH, Ng AHQ, et al. Tissue microbiome profiling identifies an enrichment of specific enteric bacteria in Opisthorchis viverrini associated cholangiocarcinoma. EBioMedicine, 2016, 8: 195-202.
28.	Avilés-Jiménez F, Guitron A, Segura-López F, et al. Microbiota studies in the bile duct strongly suggest a role for Helicobacter pylori in extrahepatic cholangiocarcinoma. Clin Microbiol Infect, 2016, 22(2): 178. e11-178. e22.
29.	Maki T. Pathogenesis of calcium bilirubinate gallstone: role of E. coli, beta-glucuronidase and coagulation by inorganic ions, polyelectrolytes and agitation. Ann Surg, 1966, 164(1): 90-100.
30.	Kamisawa T, Egawa N, Nakajima H, et al. Origin of the long common channel based on pancreatographic findings in pancreaticobiliary maljunction. Dig Liver Dis, 2005, 37(5): 363-367.
31.	Sugawara H, Yasoshima M, Katayanagi K, et al. Relationship between interleukin-6 and proliferation and differentiation in cholangiocarcinoma. Histopathology, 1998, 33(2): 145-153.
32.	Braconi C, Huang N, Patel T. MicroRNA-dependent regulation of DNA methyltransferase-1 and tumor suppressor gene expression by interleukin-6 in human malignant cholangiocytes. Hepatology, 2010, 51(3): 881-890.
33.	Kobayashi S, Werneburg NW, Bronk SF, et al. Interleukin-6 contributes to Mcl-1 up-regulation and TRAIL resistance via an Akt-signaling pathway in cholangiocarcinoma cells. Gastroenterology, 2005, 128(7): 2054-2065.
34.	Zabron A, Edwards RJ, Khan SA. The challenge of cholangiocarcinoma: dissecting the molecular mechanisms of an insidious cancer. Dis Model Mech, 2013, 6(2): 281-292.
35.	Frampton G, Invernizzi P, Bernuzzi F, et al. Interleukin-6-driven progranulin expression increases cholangiocarcinoma growth by an Akt-dependent mechanism. Gut, 2012, 61(2): 268-277.
36.	Tadlock L, Patel T. Involvement of p38 mitogen-activated protein kinase signaling in transformed growth of a cholangiocarcinoma cell line. Hepatology, 2001, 33(1): 43-51.
37.	Brito AF, Abrantes AM, Encarnação JC, et al. Cholangiocarcinoma: from molecular biology to treatment. Med Oncol, 2015, 32(11): 245.
38.	Komori J, Marusawa H, Machimoto T, et al. Activation-induced cytidine deaminase links bile duct inflammation to human cholangiocarcinoma. Hepatology, 2008, 47(3): 888-896.
39.	You Z, Bei L, Cheng LP, et al. Expression of COX-2 and VEGF-C in cholangiocarcinomas at different clinical and pathological stages. Genet Mol Res, 2015, 14(2): 6239-6246.
40.	Zhang Z, Lai GH, Sirica AE. Celecoxib-induced apoptosis in rat cholangiocarcinoma cells mediated by Akt inactivation and Bax translocation. Hepatology, 2004, 39(4): 1028-1037.
41.	Han C, Leng J, Demetris AJ, et al. Cyclooxygenase-2 promotes human cholangiocarcinoma growth: evidence for cyclooxygenase-2-independent mechanism in celecoxib-mediated induction of p21waf1/cip1 and p27kip1 and cell cycle arrest. Cancer Res, 2004, 64(4): 1369-1376.
42.	Spirlì C, Fabris L, Duner E, et al. Cytokine-stimulated nitric oxide production inhibits adenylyl cyclase and cAMP-dependent secretion in cholangiocytes. Gastroenterology, 2003, 124(3): 737-753.
43.	Jaiswal M, LaRusso NF, Shapiro RA, et al. Nitric oxide-mediated inhibition of DNA repair potentiates oxidative DNA damage in cholangiocytes. Gastroenterology, 2001, 120(1): 190-199.
44.	Wu WR, Zhang R, Shi XD, et al. Notch1 is overexpressed in human intrahepatic cholangiocarcinoma and is associated with its proliferation, invasiveness and sensitivity to 5-fluorouracil in vitro. Oncol Rep, 2014, 31(6): 2515-2524.
45.	Yoon HA, Noh MH, Kim BG, et al. Clinicopathological significance of altered Notch signaling in extrahepatic cholangiocarcinoma and gallbladder carcinoma. World J Gastroenterol, 2011, 17(35): 4023-4030.
46.	Ishimura N, Bronk SF, Gores GJ. Inducible nitric oxide synthase up-regulates Notch-1 in mouse cholangiocytes: implications for carcinogenesis. Gastroenterology, 2005, 128(5): 1354-1368.
47.	Boulter L, Guest RV, Kendall TJ, et al. WNT signaling drives cholangiocarcinoma growth and can be pharmacologically inhibited. J Clin Invest, 2015, 125(3): 1269-1285.
48.	Uemura N, Okamoto S, Yamamoto S, et al. Helicobacter pylori infection and the development of gastric cancer. N Engl J Med, 2001, 345(11): 784-789.
49.	Chen B, Fu SW, Lu L, et al. A preliminary study of biliary microbiota in patients with bile duct stones or distal cholangiocarcinoma. Biomed Res Int, 2019, 2019: 1092563.
50.	Segura-López FK, Avilés-Jiménez F, Güitrón-Cantú A, et al. Infection with Helicobacter bilis but not Helicobacter hepaticus was associated with extrahepatic cholangiocarcinoma. Helicobacter, 2015, 20(3): 223-230.
51.	Murphy G, Michel A, Taylor PR, et al. Association of seropositivity to Helicobacter species and biliary tract cancer in the ATBC study. Hepatology, 2014, 60(6): 1963-1971.
52.	Zhou D, Wang JD, Weng MZ, et al. Infections of Helicobacter spp. in the biliary system are associated with biliary tract cancer: a meta-analysis. Eur J Gastroenterol Hepatol, 2013, 25(4): 447-454.
53.	Shimoyama T, Takahashi R, Abe D, et al. Serological analysis of Helicobacter hepaticus infection in patients with biliary and pancreatic diseases. J Gastroenterol Hepatol, 2010, 25 Suppl 1: S86-S89.
54.	Boonyanugomol W, Chomvarin C, Sripa B, et al. Molecular analysis of Helicobacter pylori virulent-associated genes in hepatobiliary patients. HPB (Oxford), 2012, 14(11): 754-763.
55.	Boonyanugomol W, Chomvarin C, Song JY, et al. Effects of Helicobacter pylori γ-glutamyltranspeptidase on apoptosis and inflammation in human biliary cells. Dig Dis Sci, 2012, 57(10): 2615-2624.
56.	Takayama S, Takahashi H, Matsuo Y, et al. Effect of Helicobacter bilis infection on human bile duct cancer cells. Dig Dis Sci, 2010, 55(7): 1905-1910.
57.	Scanu T, Spaapen RM, Bakker JM, et al. Salmonella manipulation of host signaling pathways provokes cellular transformation associated with gallbladder carcinoma. Cell Host Microbe, 2015, 17(6): 763-774.
58.	Zitvogel L, Daillère R, Roberti MP, et al. Anticancer effects of the microbiome and its products. Nat Rev Microbiol, 2017, 15(8): 465-478.
59.	Honda K, Littman DR. The microbiota in adaptive immune homeostasis and disease. Nature, 2016, 535(7610): 75-84.
60.	Vétizou M, Pitt JM, Daillère R, et al. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science, 2015, 350(6264): 1079-1084.
61.	Sivan A, Corrales L, Hubert N, et al. Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science, 2015, 350(6264): 1084-1089.
62.	Nagino M, Ebata T, Yokoyama Y, et al. Evolution of surgical treatment for perihilar cholangiocarcinoma: a single-center 34-year review of 574 consecutive resections. Ann Surg, 2013, 258(1): 129-140.
63.	Chen X, Sun S, Yan X, et al. Predictive factors and microbial spectrum for infectious complications after hepatectomy with cholangiojejunostomy in perihilar cholangiocarcinoma. Surg Infect (Larchmt), 2020, 21(3): 275-283.
64.	Sugawara G, Nagino M, Nishio H, et al. Perioperative synbiotic treatment to prevent postoperative infectious complications in biliary cancer surgery: a randomized controlled trial. Ann Surg, 2006, 244(5): 706-714.
65.	Kanazawa H, Nagino M, Kamiya S, et al. Synbiotics reduce postoperative infectious complications: a randomized controlled trial in biliary cancer patients undergoing hepatectomy. Langenbecks Arch Surg, 2005, 390(2): 104-113.
66.	Panebianco C, Andriulli A, Pazienza V. Pharmacomicrobiomics: exploiting the drug-microbiota interactions in anticancer therapies. Microbiome, 2018, 6(1): 92.
67.	Lehouritis P, Cummins J, Stanton M, et al. Local bacteria affect the efficacy of chemotherapeutic drugs. Sci Rep, 2015, 5: 14554.
68.	Picardo SL, Coburn B, Hansen AR. The microbiome and cancer for clinicians. Crit Rev Oncol Hematol, 2019, 141: 1-12.
69.	Riquelme E, Zhang Y, Zhang L, et al. Tumor microbiome diversity and composition influence pancreatic cancer outcomes. Cell, 2019, 178(4): 795-806. e12.

1. Rizvi S, Khan SA, Hallemeier CL, et al. Cholangiocarcinoma - evolving concepts and therapeutic strategies. Nat Rev Clin Oncol, 2018, 15(2): 95-111.
2. Nathan H, Pawlik TM, Wolfgang CL, et al. Trends in survival after surgery for cholangiocarcinoma: a 30-year population-based SEER database analysis. J Gastrointest Surg, 2007, 11(11): 1488-1496.
3. Saha SK, Zhu AX, Fuchs CS, et al. Forty-year trends in cholangiocarcinoma incidence in the U. S. : intrahepatic disease on the rise. Oncologist, 2016, 21(5): 594-599.
4. Hu HJ, Mao H, Shrestha A, et al. Prognostic factors and long-term outcomes of hilar cholangiocarcinoma: a single-institution experience in China. World J Gastroenterol, 2016, 22(8): 2601-2610.
5. Pinto C, Giordano DM, Maroni L, et al. Role of inflammation and proinflammatory cytokines in cholangiocyte pathophysiology. Biochim Biophys Acta Mol Basis Dis, 2018, 1864(4 Pt B): 1270-1278.
6. Lee H, Lee HK, Min SK, et al. 16S rDNA microbiome composition pattern analysis as a diagnostic biomarker for biliary tract cancer. World J Surg Oncol, 2020, 18(1): 19.
7. Poore GD, Kopylova E, Zhu Q, et al. Microbiome analyses of blood and tissues suggest cancer diagnostic approach. Nature, 2020, 579(7800): 567-574.
8. Verdier J, Luedde T, Sellge G. Biliary mucosal barrier and microbiome. Viszeralmedizin, 2015, 31(3): 156-161.
9. Whiteside SA, Razvi H, Dave S, et al. The microbiome of the urinary tract–a role beyond infection. Nat Rev Urol, 2015, 12(2): 81-90.
10. Aho VTE, Pereira PAB, Haahtela T, et al. The microbiome of the human lower airways: a next generation sequencing perspective. World Allergy Organ J, 2015, 8(1): 23.
11. Shen H, Ye F, Xie L, et al. Metagenomic sequencing of bile from gallstone patients to identify different microbial community patterns and novel biliary bacteria. Sci Rep, 2015, 5: 17450.
12. Sung JY, Shaffer EA, Olson ME, et al. Bacterial invasion of the biliary system by way of the portal-venous system. Hepatology, 1991, 14(2): 313-317.
13. Scott AJ, Khan GA. Origin of bacteria in bileduct bile. Lancet, 1967, 2(7520): 790-792.
14. Anderson RE, Priestley JT. Observations on the bacteriology of choledochal bile. Ann Surg, 1951, 133(4): 486-489.
15. Elkeles G, Mirizzi PL. A study of the bacteriology of the common bile duct in comparison with the other extrahepatic segments of the biliary tract. Ann Surg, 1942, 116(3): 360-366.
16. Gu XX, Zhang MP, Zhao YF, et al. Clinical and microbiological characteristics of patients with biliary disease. World J Gastroenterol, 2020, 26(14): 1638-1646.
17. Wu T, Zhang Z, Liu B, et al. Gut microbiota dysbiosis and bacterial community assembly associated with cholesterol gallstones in large-scale study. BMC Genomics, 2013, 14: 669.
18. Ye F, Shen H, Li Z, et al. Influence of the biliary system on biliary bacteria revealed by bacterial communities of the human biliary and upper digestive tracts. PLoS One, 2016, 11(3): e0150519.
19. Folseraas T, Melum E, Rausch P, et al. Extended analysis of a genome-wide association study in primary sclerosing cholangitis detects multiple novel risk loci. J Hepatol, 2012, 57(2): 366-375.
20. Pereira P, Aho V, Arola J, et al. Bile microbiota in primary sclerosing cholangitis: impact on disease progression and development of biliary dysplasia. PLoS One, 2017, 12(8): e0182924.
21. Jiménez E, Sánchez B, Farina A, et al. Characterization of the bile and gall bladder microbiota of healthy pigs. Microbiologyopen, 2014, 3(6): 937-949.
22. Molinero N, Ruiz L, Milani C, et al. The human gallbladder microbiome is related to the physiological state and the biliary metabolic profile. Microbiome, 2019, 7(1): 100.
23. Tyson GL, El-Serag HB. Risk factors for cholangiocarcinoma. Hepatology, 2011, 54(1): 173-184.
24. Dyson JK, Beuers U, Jones DEJ, et al. Primary sclerosing cholangitis. Lancet, 2018, 391(10139): 2547-2559.
25. Karlsen TH, Folseraas T, Thorburn D, et al. Primary sclerosing cholangitis–a comprehensive review. J Hepatol, 2017, 67(6): 1298-1323.
26. Liwinski T, Zenouzi R, John C, et al. Alterations of the bile microbiome in primary sclerosing cholangitis. Gut, 2020, 69(4): 665-672.
27. Chng KR, Chan SH, Ng AHQ, et al. Tissue microbiome profiling identifies an enrichment of specific enteric bacteria in Opisthorchis viverrini associated cholangiocarcinoma. EBioMedicine, 2016, 8: 195-202.
28. Avilés-Jiménez F, Guitron A, Segura-López F, et al. Microbiota studies in the bile duct strongly suggest a role for Helicobacter pylori in extrahepatic cholangiocarcinoma. Clin Microbiol Infect, 2016, 22(2): 178. e11-178. e22.
29. Maki T. Pathogenesis of calcium bilirubinate gallstone: role of E. coli, beta-glucuronidase and coagulation by inorganic ions, polyelectrolytes and agitation. Ann Surg, 1966, 164(1): 90-100.
30. Kamisawa T, Egawa N, Nakajima H, et al. Origin of the long common channel based on pancreatographic findings in pancreaticobiliary maljunction. Dig Liver Dis, 2005, 37(5): 363-367.
31. Sugawara H, Yasoshima M, Katayanagi K, et al. Relationship between interleukin-6 and proliferation and differentiation in cholangiocarcinoma. Histopathology, 1998, 33(2): 145-153.
32. Braconi C, Huang N, Patel T. MicroRNA-dependent regulation of DNA methyltransferase-1 and tumor suppressor gene expression by interleukin-6 in human malignant cholangiocytes. Hepatology, 2010, 51(3): 881-890.
33. Kobayashi S, Werneburg NW, Bronk SF, et al. Interleukin-6 contributes to Mcl-1 up-regulation and TRAIL resistance via an Akt-signaling pathway in cholangiocarcinoma cells. Gastroenterology, 2005, 128(7): 2054-2065.
34. Zabron A, Edwards RJ, Khan SA. The challenge of cholangiocarcinoma: dissecting the molecular mechanisms of an insidious cancer. Dis Model Mech, 2013, 6(2): 281-292.
35. Frampton G, Invernizzi P, Bernuzzi F, et al. Interleukin-6-driven progranulin expression increases cholangiocarcinoma growth by an Akt-dependent mechanism. Gut, 2012, 61(2): 268-277.
36. Tadlock L, Patel T. Involvement of p38 mitogen-activated protein kinase signaling in transformed growth of a cholangiocarcinoma cell line. Hepatology, 2001, 33(1): 43-51.
37. Brito AF, Abrantes AM, Encarnação JC, et al. Cholangiocarcinoma: from molecular biology to treatment. Med Oncol, 2015, 32(11): 245.
38. Komori J, Marusawa H, Machimoto T, et al. Activation-induced cytidine deaminase links bile duct inflammation to human cholangiocarcinoma. Hepatology, 2008, 47(3): 888-896.
39. You Z, Bei L, Cheng LP, et al. Expression of COX-2 and VEGF-C in cholangiocarcinomas at different clinical and pathological stages. Genet Mol Res, 2015, 14(2): 6239-6246.
40. Zhang Z, Lai GH, Sirica AE. Celecoxib-induced apoptosis in rat cholangiocarcinoma cells mediated by Akt inactivation and Bax translocation. Hepatology, 2004, 39(4): 1028-1037.
41. Han C, Leng J, Demetris AJ, et al. Cyclooxygenase-2 promotes human cholangiocarcinoma growth: evidence for cyclooxygenase-2-independent mechanism in celecoxib-mediated induction of p21waf1/cip1 and p27kip1 and cell cycle arrest. Cancer Res, 2004, 64(4): 1369-1376.
42. Spirlì C, Fabris L, Duner E, et al. Cytokine-stimulated nitric oxide production inhibits adenylyl cyclase and cAMP-dependent secretion in cholangiocytes. Gastroenterology, 2003, 124(3): 737-753.
43. Jaiswal M, LaRusso NF, Shapiro RA, et al. Nitric oxide-mediated inhibition of DNA repair potentiates oxidative DNA damage in cholangiocytes. Gastroenterology, 2001, 120(1): 190-199.
44. Wu WR, Zhang R, Shi XD, et al. Notch1 is overexpressed in human intrahepatic cholangiocarcinoma and is associated with its proliferation, invasiveness and sensitivity to 5-fluorouracil in vitro. Oncol Rep, 2014, 31(6): 2515-2524.
45. Yoon HA, Noh MH, Kim BG, et al. Clinicopathological significance of altered Notch signaling in extrahepatic cholangiocarcinoma and gallbladder carcinoma. World J Gastroenterol, 2011, 17(35): 4023-4030.
46. Ishimura N, Bronk SF, Gores GJ. Inducible nitric oxide synthase up-regulates Notch-1 in mouse cholangiocytes: implications for carcinogenesis. Gastroenterology, 2005, 128(5): 1354-1368.
47. Boulter L, Guest RV, Kendall TJ, et al. WNT signaling drives cholangiocarcinoma growth and can be pharmacologically inhibited. J Clin Invest, 2015, 125(3): 1269-1285.
48. Uemura N, Okamoto S, Yamamoto S, et al. Helicobacter pylori infection and the development of gastric cancer. N Engl J Med, 2001, 345(11): 784-789.
49. Chen B, Fu SW, Lu L, et al. A preliminary study of biliary microbiota in patients with bile duct stones or distal cholangiocarcinoma. Biomed Res Int, 2019, 2019: 1092563.
50. Segura-López FK, Avilés-Jiménez F, Güitrón-Cantú A, et al. Infection with Helicobacter bilis but not Helicobacter hepaticus was associated with extrahepatic cholangiocarcinoma. Helicobacter, 2015, 20(3): 223-230.
51. Murphy G, Michel A, Taylor PR, et al. Association of seropositivity to Helicobacter species and biliary tract cancer in the ATBC study. Hepatology, 2014, 60(6): 1963-1971.
52. Zhou D, Wang JD, Weng MZ, et al. Infections of Helicobacter spp. in the biliary system are associated with biliary tract cancer: a meta-analysis. Eur J Gastroenterol Hepatol, 2013, 25(4): 447-454.
53. Shimoyama T, Takahashi R, Abe D, et al. Serological analysis of Helicobacter hepaticus infection in patients with biliary and pancreatic diseases. J Gastroenterol Hepatol, 2010, 25 Suppl 1: S86-S89.
54. Boonyanugomol W, Chomvarin C, Sripa B, et al. Molecular analysis of Helicobacter pylori virulent-associated genes in hepatobiliary patients. HPB (Oxford), 2012, 14(11): 754-763.
55. Boonyanugomol W, Chomvarin C, Song JY, et al. Effects of Helicobacter pylori γ-glutamyltranspeptidase on apoptosis and inflammation in human biliary cells. Dig Dis Sci, 2012, 57(10): 2615-2624.
56. Takayama S, Takahashi H, Matsuo Y, et al. Effect of Helicobacter bilis infection on human bile duct cancer cells. Dig Dis Sci, 2010, 55(7): 1905-1910.
57. Scanu T, Spaapen RM, Bakker JM, et al. Salmonella manipulation of host signaling pathways provokes cellular transformation associated with gallbladder carcinoma. Cell Host Microbe, 2015, 17(6): 763-774.
58. Zitvogel L, Daillère R, Roberti MP, et al. Anticancer effects of the microbiome and its products. Nat Rev Microbiol, 2017, 15(8): 465-478.
59. Honda K, Littman DR. The microbiota in adaptive immune homeostasis and disease. Nature, 2016, 535(7610): 75-84.
60. Vétizou M, Pitt JM, Daillère R, et al. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science, 2015, 350(6264): 1079-1084.
61. Sivan A, Corrales L, Hubert N, et al. Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science, 2015, 350(6264): 1084-1089.
62. Nagino M, Ebata T, Yokoyama Y, et al. Evolution of surgical treatment for perihilar cholangiocarcinoma: a single-center 34-year review of 574 consecutive resections. Ann Surg, 2013, 258(1): 129-140.
63. Chen X, Sun S, Yan X, et al. Predictive factors and microbial spectrum for infectious complications after hepatectomy with cholangiojejunostomy in perihilar cholangiocarcinoma. Surg Infect (Larchmt), 2020, 21(3): 275-283.
64. Sugawara G, Nagino M, Nishio H, et al. Perioperative synbiotic treatment to prevent postoperative infectious complications in biliary cancer surgery: a randomized controlled trial. Ann Surg, 2006, 244(5): 706-714.
65. Kanazawa H, Nagino M, Kamiya S, et al. Synbiotics reduce postoperative infectious complications: a randomized controlled trial in biliary cancer patients undergoing hepatectomy. Langenbecks Arch Surg, 2005, 390(2): 104-113.
66. Panebianco C, Andriulli A, Pazienza V. Pharmacomicrobiomics: exploiting the drug-microbiota interactions in anticancer therapies. Microbiome, 2018, 6(1): 92.
67. Lehouritis P, Cummins J, Stanton M, et al. Local bacteria affect the efficacy of chemotherapeutic drugs. Sci Rep, 2015, 5: 14554.
68. Picardo SL, Coburn B, Hansen AR. The microbiome and cancer for clinicians. Crit Rev Oncol Hematol, 2019, 141: 1-12.
69. Riquelme E, Zhang Y, Zhang L, et al. Tumor microbiome diversity and composition influence pancreatic cancer outcomes. Cell, 2019, 178(4): 795-806. e12.

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