The microbiome and hepatobiliary-pancreatic cancers

Cancer Letters

Volumn 402, Issue , 2017, Pages 9-15

  Mima, Kosuke ^a   Nakagawa, Shigeki ^a   Sawayama, Hiroshi ^a   Ishimoto, Takatsugu ^a   Imai, Katsunori ^a   Iwatsuki, Masaaki ^a   Hashimoto, Daisuke ^a   Baba, Yoshifumi ^a   Yamashita, Yo ichi ^a   Yoshida, Naoya ^a   Chikamoto, Akira ^a   Baba, Hideo ^a  

^a KUMAMOTO UNIVERSITY   (Japan)

Author keywords

Bacteria; Cholangiocarcinoma; Gut liver axis; Hepatocellular carcinoma; Pancreatic adenocarcinoma

Indexed keywords

BACTERIUM; BILIARY TRACT CANCER; CANCER GROWTH; CANCER RECURRENCE; CANCER SURVIVAL; CARCINOGENESIS; HUMAN; INTESTINE FLORA; LIVER CANCER; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; SHORT SURVEY; ABDOMINAL SURGERY; ANIMAL; BILIARY TRACT NEOPLASMS; CELL TRANSFORMATION; DRUG EFFECTS; DYSBIOSIS; GASTROINTESTINAL TRACT; HOST PATHOGEN INTERACTION; IMMUNOLOGY; IMMUNOTHERAPY; LIVER NEOPLASMS; MICROBIOLOGY; PANCREATIC NEOPLASMS; PATHOLOGY; PROCEDURES; SURGERY;

ANTINEOPLASTIC AGENT;

ANIMALS; ANTINEOPLASTIC AGENTS; BILIARY TRACT NEOPLASMS; CELL TRANSFORMATION, NEOPLASTIC; DIGESTIVE SYSTEM SURGICAL PROCEDURES; DYSBIOSIS; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNOTHERAPY; LIVER NEOPLASMS; PANCREATIC NEOPLASMS;

EID: 85019666712     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2017.05.001     Document Type: Review

References (126)

1. Llovet, J.M., Zucman-Rossi, J., Pikarsky, E., Sangro, B., Schwartz, M., Sherman, M., et al. Hepatocellular carcinoma. Nat. Rev. Dis. Primers, 2, 2016, 16018.
2. Banales, J.M., Cardinale, V., Carpino, G., Marzioni, M., Andersen, J.B., Invernizzi, P., et al. Expert consensus document: cholangiocarcinoma: current knowledge and future perspectives consensus statement from the European Network for the Study of Cholangiocarcinoma (ENS-CCA). Nat. Rev. Gastroenterol. Hepatol. 13 (2016), 261–280.
3. Kleeff, J., Korc, M., Apte, M., La Vecchia, C., Johnson, C.D., Biankin, A.V., et al. Pancreatic cancer. Nat. Rev. Dis. Primers, 2, 2016, 16022.
4. Fujimoto, A., Totoki, Y., Abe, T., Boroevich, K.A., Hosoda, F., Nguyen, H.H., et al. Whole-genome sequencing of liver cancers identifies etiological influences on mutation patterns and recurrent mutations in chromatin regulators. Nat. Genet. 44 (2012), 760–764.
5. Fujimoto, A., Furuta, M., Totoki, Y., Tsunoda, T., Kato, M., Shiraishi, Y., et al. Whole-genome mutational landscape and characterization of noncoding and structural mutations in liver cancer. Nat. Genet. 48 (2016), 500–509.
6. Nakamura, H., Arai, Y., Totoki, Y., Shirota, T., Elzawahry, A., Kato, M., et al. Genomic spectra of biliary tract cancer. Nat. Genet. 47 (2015), 1003–1010.
7. Bailey, P., Chang, D.K., Nones, K., Johns, A.L., Patch, A.M., Gingras, M.C., et al. Genomic analyses identify molecular subtypes of pancreatic cancer. Nature 531 (2016), 47–52.
8. Wang, J., Jia, H., Metagenome-wide association studies: fine-mining the microbiome. Nat. Rev. Microbiol. 14 (2016), 508–522.
9. Szabo, G., Gut-liver axis in alcoholic liver disease. Gastroenterology 148 (2015), 30–36.
10. Liu, H.X., Rocha, C.S., Dandekar, S., Wan, Y.J., Functional analysis of the relationship between intestinal microbiota and the expression of hepatic genes and pathways during the course of liver regeneration. J. Hepatol. 64 (2016), 641–650.
11. Ahluwalia, V., Betrapally, N.S., Hylemon, P.B., White, M.B., Gillevet, P.M., Unser, A.B., et al. Impaired gut-liver-brain axis in patients with cirrhosis. Sci. Rep., 6, 2016, 26800.
12. Schneider, K.M., Bieghs, V., Heymann, F., Hu, W., Dreymueller, D., Liao, L., et al. CX3CR1 is a gatekeeper for intestinal barrier integrity in mice: limiting steatohepatitis by maintaining intestinal homeostasis. Hepatology 62 (2015), 1405–1416.
13. Le Roy, T., Llopis, M., Lepage, P., Bruneau, A., Rabot, S., Bevilacqua, C., et al. Intestinal microbiota determines development of non-alcoholic fatty liver disease in mice. Gut 62 (2013), 1787–1794.
14. Henao-Mejia, J., Elinav, E., Jin, C., Hao, L., Mehal, W.Z., Strowig, T., et al. Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity. Nature 482 (2012), 179–185.
15. De Minicis, S., Rychlicki, C., Agostinelli, L., Saccomanno, S., Candelaresi, C., Trozzi, L., et al. Dysbiosis contributes to fibrogenesis in the course of chronic liver injury in mice. Hepatology 59 (2014), 1738–1749.
16. Seki, E., De Minicis, S., Osterreicher, C.H., Kluwe, J., Osawa, Y., Brenner, D.A., et al. TLR4 enhances TGF-beta signaling and hepatic fibrosis. Nat. Med. 13 (2007), 1324–1332.
17. Zhu, L., Baker, S.S., Gill, C., Liu, W., Alkhouri, R., Baker, R.D., et al. Characterization of gut microbiomes in nonalcoholic steatohepatitis (NASH) patients: a connection between endogenous alcohol and NASH. Hepatology 57 (2013), 601–609.
18. Mouzaki, M., Comelli, E.M., Arendt, B.M., Bonengel, J., Fung, S.K., Fischer, S.E., et al. Intestinal microbiota in patients with nonalcoholic fatty liver disease. Hepatology 58 (2013), 120–127.
19. Boursier, J., Mueller, O., Barret, M., Machado, M., Fizanne, L., Araujo-Perez, F., et al. The severity of nonalcoholic fatty liver disease is associated with gut dysbiosis and shift in the metabolic function of the gut microbiota. Hepatology 63 (2016), 764–775.
20. Qin, N., Yang, F., Li, A., Prifti, E., Chen, Y., Shao, L., et al. Alterations of the human gut microbiome in liver cirrhosis. Nature 513 (2014), 59–64.
21. Lelouvier, B., Servant, F., Paisse, S., Brunet, A.C., Benyahya, S., Serino, M., et al. Changes in blood microbiota profiles associated with liver fibrosis in obese patients: a pilot analysis. Hepatology 64 (2016), 2015–2027.
22. Chen, Y., Yang, F., Lu, H., Wang, B., Chen, Y., Lei, D., et al. Characterization of fecal microbial communities in patients with liver cirrhosis. Hepatology 54 (2011), 562–572.
23. Sonnenburg, E.D., Smits, S.A., Tikhonov, M., Higginbottom, S.K., Wingreen, N.S., Sonnenburg, J.L., Diet-induced extinctions in the gut microbiota compound over generations. Nature 529 (2016), 212–215.
24. Zhernakova, A., Kurilshikov, A., Bonder, M.J., Tigchelaar, E.F., Schirmer, M., Vatanen, T., et al. Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity. Science 352 (2016), 565–569.
25. Torre, L.A., Siegel, R.L., Ward, E.M., Jemal, A., Global cancer incidence and mortality rates and trends–an update. Cancer Epidemiol. Biomarkers Prev. 25 (2016), 16–27.
26. Amieva, M., Peek, R.M. Jr., Pathobiology of helicobacter pylori-induced gastric cancer. Gastroenterology 150 (2016), 64–78.
27. Ward, J.M., Fox, J.G., Anver, M.R., Haines, D.C., George, C.V., Collins, M.J. Jr., et al. Chronic active hepatitis and associated liver tumors in mice caused by a persistent bacterial infection with a novel Helicobacter species. J. Natl. Cancer Inst. 86 (1994), 1222–1227.
28. Fox, J.G., Feng, Y., Theve, E.J., Raczynski, A.R., Fiala, J.L., Doernte, A.L., et al. Gut microbes define liver cancer risk in mice exposed to chemical and viral transgenic hepatocarcinogens. Gut 59 (2010), 88–97.
29. Huang, Y., Fan, X.G., Wang, Z.M., Zhou, J.H., Tian, X.F., Li, N., Identification of helicobacter species in human liver samples from patients with primary hepatocellular carcinoma. J. Clin. Pathol. 57 (2004), 1273–1277.
30. Rocha, M., Avenaud, P., Menard, A., Le Bail, B., Balabaud, C., Bioulac-Sage, P., et al. Association of Helicobacter species with hepatitis C cirrhosis with or without hepatocellular carcinoma. Gut 54 (2005), 396–401.
31. Kruttgen, A., Horz, H.P., Weber-Heynemann, J., Vucur, M., Trautwein, C., Haase, G., et al. Study on the association of Helicobacter species with viral hepatitis-induced hepatocellular carcinoma. Gut Microbes 3 (2012), 228–233.
32. Rakoff-Nahoum, S., Medzhitov, R., Toll-like receptors and cancer. Nat. Rev. Cancer 9 (2009), 57–63.
33. Yu, L.X., Yan, H.X., Liu, Q., Yang, W., Wu, H.P., Dong, W., et al. Endotoxin accumulation prevents carcinogen-induced apoptosis and promotes liver tumorigenesis in rodents. Hepatology 52 (2010), 1322–1333.
34. Dapito, D.H., Mencin, A., Gwak, G.Y., Pradere, J.P., Jang, M.K., Mederacke, I., et al. Promotion of hepatocellular carcinoma by the intestinal microbiota and TLR4. Cancer Cell 21 (2012), 504–516.
35. Ley, R.E., Turnbaugh, P.J., Klein, S., Gordon, J.I., Microbial ecology: human gut microbes associated with obesity. Nature 444 (2006), 1022–1023.
36. Mittal, S., Sada, Y.H., El-Serag, H.B., Kanwal, F., Duan, Z., Temple, S., et al. Temporal trends of nonalcoholic fatty liver disease-related hepatocellular carcinoma in the veteran affairs population. Clin. Gastroenterol. Hepatol. 13 (2015), 594–601 e591.
37. Mittal, S., El-Serag, H.B., Sada, Y.H., Kanwal, F., Duan, Z., Temple, S., et al. Hepatocellular carcinoma in the absence of cirrhosis in United States Veterans is associated with nonalcoholic fatty liver disease. Clin. Gastroenterol. Hepatol. 14 (2016), 124–131 e121.
38. Xie, G., Wang, X., Huang, F., Zhao, A., Chen, W., Yan, J., et al. Dysregulated hepatic bile acids collaboratively promote liver carcinogenesis. Int. J. Cancer 139 (2016), 1764–1775.
39. Xie, G., Wang, X., Liu, P., Wei, R., Chen, W., Rajani, C., et al. Distinctly altered gut microbiota in the progression of liver disease. Oncotarget 7 (2016), 19355–19366.
40. Laberge, R.M., Sun, Y., Orjalo, A.V., Patil, C.K., Freund, A., Zhou, L., et al. MTOR regulates the pro-tumorigenic senescence-associated secretory phenotype by promoting IL1A translation. Nat. Cell Biol. 17 (2015), 1049–1061.
41. Ruhland, M.K., Loza, A.J., Capietto, A.H., Luo, X., Knolhoff, B.L., Flanagan, K.C., et al. Stromal senescence establishes an immunosuppressive microenvironment that drives tumorigenesis. Nat. Commun., 7, 2016, 11762.
42. Demaria, M., O'Leary, M.N., Chang, J., Shao, L., Liu, S., Alimirah, F., et al. Cellular senescence promotes adverse effects of chemotherapy and cancer relapse. Cancer Discov. 7 (2017), 165–176.
43. Yoshimoto, S., Loo, T.M., Atarashi, K., Kanda, H., Sato, S., Oyadomari, S., et al. Obesity-induced gut microbial metabolite promotes liver cancer through senescence secretome. Nature 499 (2013), 97–101.
44. Niwa, Y., Ishikawa, K., Ishigami, M., Honda, T., Achiwa, K., Izumoto, T., et al. Effect of hyperglycemia on hepatocellular carcinoma development in diabetes. Biochem. Biophys. Res. Commun. 463 (2015), 344–350.
45. Arthur, J.C., Perez-Chanona, E., Muhlbauer, M., Tomkovich, S., Uronis, J.M., Fan, T.J., et al. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 338 (2012), 120–123.
46. Arthur, J.C., Gharaibeh, R.Z., Muhlbauer, M., Perez-Chanona, E., Uronis, J.M., McCafferty, J., et al. Microbial genomic analysis reveals the essential role of inflammation in bacteria-induced colorectal cancer. Nat. Commun., 5, 2014, 4724.
47. Grat, M., Wronka, K.M., Krasnodebski, M., Masior, L., Lewandowski, Z., Kosinska, I., et al. Profile of gut microbiota associated with the presence of hepatocellular cancer in patients with liver cirrhosis. Transpl. Proc. 48 (2016), 1687–1691.
48. Cho, I., Yamanishi, S., Cox, L., Methe, B.A., Zavadil, J., Li, K., et al. Antibiotics in early life alter the murine colonic microbiome and adiposity. Nature 488 (2012), 621–626.
49. Belkaid, Y., Hand, T.W., Role of the microbiota in immunity and inflammation. Cell 157 (2014), 121–141.
50. David, L.A., Maurice, C.F., Carmody, R.N., Gootenberg, D.B., Button, J.E., Wolfe, B.E., et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505 (2014), 559–563.
51. Lukens, J.R., Gurung, P., Vogel, P., Johnson, G.R., Carter, R.A., McGoldrick, D.J., et al. Dietary modulation of the microbiome affects autoinflammatory disease. Nature 516 (2014), 246–249.
52. Desai, M.S., Seekatz, A.M., Koropatkin, N.M., Kamada, N., Hickey, C.A., Wolter, M., et al. A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility. Cell 167 (2016), 1339–1353 e1321.
53. Zhang, H.L., Yu, L.X., Yang, W., Tang, L., Lin, Y., Wu, H., et al. Profound impact of gut homeostasis on chemically-induced pro-tumorigenic inflammation and hepatocarcinogenesis in rats. J. Hepatol. 57 (2012), 803–812.
54. Li, J., Sung, C.Y., Lee, N., Ni, Y., Pihlajamaki, J., Panagiotou, G., et al. Probiotics modulated gut microbiota suppresses hepatocellular carcinoma growth in mice. Proc. Natl. Acad. Sci. U. S. A. 113 (2016), E1306–1315.
55. Toumi, R., Soufli, I., Rafa, H., Belkhelfa, M., Biad, A., Touil-Boukoffa, C., Probiotic bacteria lactobacillus and bifidobacterium attenuate inflammation in dextran sulfate sodium-induced experimental colitis in mice. Int. J. Immunopathol. Pharmacol. 27 (2014), 615–627.
56. Kverka, M., Zakostelska, Z., Klimesova, K., Sokol, D., Hudcovic, T., Hrncir, T., et al. Oral administration of Parabacteroides distasonis antigens attenuates experimental murine colitis through modulation of immunity and microbiota composition. Clin. Exp. Immunol. 163 (2011), 250–259.
57. Arpaia, N., Campbell, C., Fan, X., Dikiy, S., van der Veeken, J., deRoos, P., et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 504 (2013), 451–455.
58. Yang, B., Hagberg, K.W., Chen, J., Sahasrabuddhe, V.V., Graubard, B.I., Jick, S., et al. Associations of antibiotic use with risk of primary liver cancer in the Clinical Practice Research Datalink. Br. J. Cancer 115 (2016), 85–89.
59. Fukuda, K., Kuroki, T., Tajima, Y., Tsuneoka, N., Kitajima, T., Matsuzaki, S., et al. Comparative analysis of Helicobacter DNAs and biliary pathology in patients with and without hepatobiliary cancer. Carcinogenesis 23 (2002), 1927–1931.
60. Bulajic, M., Maisonneuve, P., Schneider-Brachert, W., Muller, P., Reischl, U., Stimec, B., et al. Helicobacter pylori and the risk of benign and malignant biliary tract disease. Cancer 95 (2002), 1946–1953.
61. Zhou, D., Wang, J.D., Weng, M.Z., Zhang, Y., Wang, X.F., Gong, W., et al. Infections of Helicobacter spp. in the biliary system are associated with biliary tract cancer: a meta-analysis. Eur. J. Gastroenterol. Hepatol. 25 (2013), 447–454.
62. Murphy, G., Michel, A., Taylor, P.R., Albanes, D., Weinstein, S.J., Virtamo, J., et al. Association of seropositivity to Helicobacter species and biliary tract cancer in the ATBC study. Hepatology 60 (2014), 1963–1971.
63. Segura-Lopez, F.K., Aviles-Jimenez, F., Guitron-Cantu, A., Valdez-Salazar, H.A., Leon-Carballo, S., Guerrero-Perez, L., et al. Infection with Helicobacter bilis but not Helicobacter hepaticus was Associated with Extrahepatic Cholangiocarcinoma. Helicobacter 20 (2015), 223–230.
64. Shimoyama, T., Takahashi, R., Abe, D., Mizuki, I., Endo, T., Fukuda, S., Serological analysis of Helicobacter hepaticus infection in patients with biliary and pancreatic diseases. J. Gastroenterol. Hepatol. 25:Suppl 1 (2010), S86–S89.
65. Takayama, S., Takahashi, H., Matsuo, Y., Okada, Y., Takeyama, H., Effect of Helicobacter bilis infection on human bile duct cancer cells. Dig. Dis. Sci. 55 (2010), 1905–1910.
66. Chng, K.R., Chan, S.H., Ng, A.H., Li, C., Jusakul, A., Bertrand, D., et al. Tissue microbiome profiling identifies an enrichment of specific enteric bacteria in Opisthorchis viverrini associated cholangiocarcinoma. EBioMedicine 8 (2016), 195–202.
67. Aviles-Jimenez, F., Guitron, A., Segura-Lopez, F., Mendez-Tenorio, A., Iwai, S., Hernandez-Guerrero, A., et al. Microbiota studies in the bile duct strongly suggest a role for Helicobacter pylori in extrahepatic cholangiocarcinoma. Clin. Microbiol. Infect. 22:178 (2016), e111–e122.
68. Nagaraja, V., Eslick, G.D., Systematic review with meta-analysis: the relationship between chronic Salmonella typhi carrier status and gall-bladder cancer. Aliment. Pharmacol. Ther. 39 (2014), 745–750.
69. Koshiol, J., Wozniak, A., Cook, P., Adaniel, C., Acevedo, J., Azocar, L., et al. Salmonella enterica serovar Typhi and gallbladder cancer: a case-control study and meta-analysis. Cancer Med., 5, 2016 3310–3235.
70. Scanu, T., Spaapen, R.M., Bakker, J.M., Pratap, C.B., Wu, L.E., Hofland, I., et al. Salmonella manipulation of host signaling pathways provokes cellular transformation associated with gallbladder carcinoma. Cell Host Microbe 17 (2015), 763–774.
71. Ochi, A., Nguyen, A.H., Bedrosian, A.S., Mushlin, H.M., Zarbakhsh, S., Barilla, R., et al. MyD88 inhibition amplifies dendritic cell capacity to promote pancreatic carcinogenesis via Th2 cells. J. Exp. Med. 209 (2012), 1671–1687.
72. Hujoel, P.P., Drangsholt, M., Spiekerman, C., Weiss, N.S., An exploration of the periodontitis-cancer association. Ann. Epidemiol. 13 (2003), 312–316.
73. Michaud, D.S., Joshipura, K., Giovannucci, E., Fuchs, C.S., A prospective study of periodontal disease and pancreatic cancer in US male health professionals. J. Natl. Cancer Inst. 99 (2007), 171–175.
74. Farrell, J.J., 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 61 (2012), 582–588.
75. Fan, X., Alekseyenko, A.V., Wu, J., Peters, B.A., Jacobs, E.J., Gapstur, S.M., et al. Human oral microbiome and prospective risk for pancreatic cancer: a population-based nested case-control study. Gut, 2016.
76. Michaud, D.S., Izard, J., Wilhelm-Benartzi, C.S., You, D.H., Grote, V.A., Tjonneland, A., et al. Plasma antibodies to oral bacteria and risk of pancreatic cancer in a large European prospective cohort study. Gut 62 (2013), 1764–1770.
77. Mima, K., Sukawa, Y., Nishihara, R., Qian, Z.R., Yamauchi, M., Inamura, K., et al. Fusobacterium nucleatum and T Cells in colorectal carcinoma. JAMA Oncol. 1 (2015), 653–661.
78. Mima, K., Nishihara, R., Qian, Z.R., Cao, Y., Sukawa, Y., Nowak, J.A., et al. Fusobacterium nucleatum in colorectal carcinoma tissue and patient prognosis. Gut 65 (2016), 1973–1980.
79. Mima, K., Cao, Y., Chan, A.T., Qian, Z.R., Nowak, J.A., Masugi, Y., et al. Fusobacterium nucleatum in colorectal carcinoma tissue according to tumor location. Clin. Transl. Gastroenterol., 7, 2016, e200.
80. Yamamura, K., Baba, Y., Nakagawa, S., Mima, K., Miyake, K., Nakamura, K., et al. Human microbiome Fusobacterium nucleatum in esophageal cancer tissue is associated with prognosis. Clin. Cancer Res. 22 (2016), 5574–5581.
81. Sears, C.L., Garrett, W.S., Microbes, microbiota, and colon cancer. Cell Host Microbe 15 (2014), 317–328.
82. Gur, C., Ibrahim, Y., Isaacson, B., Yamin, R., Abed, J., Gamliel, M., et al. Binding of the Fap2 protein of Fusobacterium nucleatum to human inhibitory receptor TIGIT protects tumors from immune cell attack. Immunity 42 (2015), 344–355.
83. Kostic, A.D., Chun, E., Robertson, L., Glickman, J.N., Gallini, C.A., Michaud, M., et al. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe 14 (2013), 207–215.
84. Rubinstein, M.R., Wang, X., Liu, W., Hao, Y., Cai, G., Han, Y.W., Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/beta-catenin signaling via its FadA adhesin. Cell Host Microbe 14 (2013), 195–206.
85. Mitsuhashi, K., Nosho, K., Sukawa, Y., Matsunaga, Y., Ito, M., Kurihara, H., et al. Association of Fusobacterium species in pancreatic cancer tissues with molecular features and prognosis. Oncotarget 6 (2015), 7209–7220.
86. Burris, H.A. 3rd, Moore, M.J., Andersen, J., Green, M.R., Rothenberg, M.L., Modiano, M.R., et al. Improvements in survival and clinical benefit with gemcitabine as first-line therapy for patients with advanced pancreas cancer: a randomized trial. J. Clin. Oncol. 15 (1997), 2403–2413.
87. Von Hoff, D.D., Ervin, T., Arena, F.P., Chiorean, E.G., Infante, J., Moore, M., et al. Increased survival in pancreatic cancer with nab-paclitaxel plus gemcitabine. N. Engl. J. Med. 369 (2013), 1691–1703.
88. Conroy, T., Desseigne, F., Ychou, M., Bouche, O., Guimbaud, R., Becouarn, Y., et al. FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer. N. Engl. J. Med. 364 (2011), 1817–1825.
89. Ozben, T., Oxidative stress and apoptosis: impact on cancer therapy. J. Pharm. Sci. 96 (2007), 2181–2196.
90. Iida, N., Dzutsev, A., Stewart, C.A., Smith, L., Bouladoux, N., Weingarten, R.A., et al. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science 342 (2013), 967–970.
91. Meyerhardt, J.A., Mayer, R.J., Systemic therapy for colorectal cancer. N Engl J Med 352 (2005), 476–487.
92. Stein, A., Voigt, W., Jordan, K., Chemotherapy-induced diarrhea: pathophysiology, frequency and guideline-based management. Ther. Adv. Med. Oncol. 2 (2010), 51–63.
93. Takasuna, K., Hagiwara, T., Hirohashi, M., Kato, M., Nomura, M., Nagai, E., et al. Inhibition of intestinal microflora beta-glucuronidase modifies the distribution of the active metabolite of the antitumor agent, irinotecan hydrochloride (CPT-11) in rats. Cancer Chemother. Pharmacol. 42 (1998), 280–286.
94. Wallace, B.D., Wang, H., Lane, K.T., Scott, J.E., Orans, J., Koo, J.S., et al. Alleviating cancer drug toxicity by inhibiting a bacterial enzyme. Science 330 (2010), 831–835.
95. Vanneman, M., Dranoff, G., Combining immunotherapy and targeted therapies in cancer treatment. Nat. Rev. Cancer 12 (2012), 237–251.
96. Topalian, S.L., Hodi, F.S., Brahmer, J.R., Gettinger, S.N., Smith, D.C., McDermott, D.F., et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N. Engl. J. Med. 366 (2012), 2443–2454.
97. Herbst, R.S., Soria, J.C., Kowanetz, M., Fine, G.D., Hamid, O., Gordon, M.S., et al. Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature 515 (2014), 563–567.
98. Vetizou, M., Pitt, J.M., Daillere, R., Lepage, P., Waldschmitt, N., Flament, C., et al. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science 350 (2015), 1079–1084.
99. Sivan, A., Corrales, L., Hubert, N., Williams, J.B., Aquino-Michaels, K., Earley, Z.M., et al. Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science 350 (2015), 1084–1089.
100. Llovet, J.M., Schwartz, M., Mazzaferro, V., Resection and liver transplantation for hepatocellular carcinoma. Semin. Liver Dis. 25 (2005), 181–200.
101. Sato, M., Tateishi, R., Yasunaga, H., Horiguchi, H., Yoshida, H., Matsuda, S., et al. Mortality and morbidity of hepatectomy, radiofrequency ablation, and embolization for hepatocellular carcinoma: a national survey of 54,145 patients. J. Gastroenterol. 47 (2012), 1125–1133.
102. Nathan, H., Pawlik, T.M., Wolfgang, C.L., Choti, M.A., Cameron, J.L., Schulick, R.D., Trends in survival after surgery for cholangiocarcinoma: a 30-year population-based SEER database analysis. J Gastrointest Surg 11 (2007), 1488–1496 discussion 1496–1487.
103. Nagino, M., Ebata, T., Yokoyama, Y., Igami, T., Sugawara, G., Takahashi, Y., et al. Evolution of surgical treatment for perihilar cholangiocarcinoma: a single-center 34-year review of 574 consecutive resections. Ann. Surg. 258 (2013), 129–140.
104. Amini, N., Spolverato, G., Kim, Y., Pawlik, T.M., Trends in hospital volume and failure to rescue for pancreatic surgery. J. Gastrointest. Surg. 19 (2015), 1581–1592.
105. Kenjo, A., Miyata, H., Gotoh, M., Kitagawa, Y., Shimada, M., Baba, H., et al. Risk stratification of 7,732 hepatectomy cases in 2011 from the National Clinical Database for Japan. J. Am. Coll. Surg. 218 (2014), 412–422.
106. Kimura, W., Miyata, H., Gotoh, M., Hirai, I., Kenjo, A., Kitagawa, Y., et al. A pancreaticoduodenectomy risk model derived from 8575 cases from a national single-race population (Japanese) using a web-based data entry system: the 30-day and in-hospital mortality rates for pancreaticoduodenectomy. Ann. Surg. 259 (2014), 773–780.
107. Chok, K.S., Ng, K.K., Poon, R.T., Lo, C.M., Fan, S.T., Impact of postoperative complications on long-term outcome of curative resection for hepatocellular carcinoma. Br. J. Surg. 96 (2009), 81–87.
108. Zhou, Y.M., Zhang, X.F., Li, B., Sui, C.J., Yang, J.M., Postoperative complications affect early recurrence of hepatocellular carcinoma after curative resection. BMC Cancer, 15, 2015, 689.
109. Spolverato, G., Yakoob, M.Y., Kim, Y., Alexandrescu, S., Marques, H.P., Lamelas, J., et al. Impact of complications on long-term survival after resection of intrahepatic cholangiocarcinoma. Cancer 121 (2015), 2730–2739.
110. Aahlin, E.K., Olsen, F., Uleberg, B., Jacobsen, B.K., Lassen, K., Major postoperative complications are associated with impaired long-term survival after gastro-esophageal and pancreatic cancer surgery: a complete national cohort study. BMC Surg., 16, 2016, 32.
111. Kanazawa, H., Nagino, M., Kamiya, S., Komatsu, S., Mayumi, T., Takagi, K., et al. Synbiotics reduce postoperative infectious complications: a randomized controlled trial in biliary cancer patients undergoing hepatectomy. Langenbecks Arch. Surg. 390 (2005), 104–113.
112. Sugawara, G., Nagino, M., Nishio, H., Ebata, T., Takagi, K., Asahara, T., et al. Perioperative synbiotic treatment to prevent postoperative infectious complications in biliary cancer surgery: a randomized controlled trial. Ann. Surg. 244 (2006), 706–714.
113. Diener, M.K., Fitzmaurice, C., Schwarzer, G., Seiler, C.M., Huttner, F.J., Antes, G., et al. Pylorus-preserving pancreaticoduodenectomy (pp Whipple) versus pancreaticoduodenectomy (classic Whipple) for surgical treatment of periampullary and pancreatic carcinoma. Cochrane Database Syst. Rev., 2014, CD006053.
114. Liou, A.P., Paziuk, M., Luevano, J.M. Jr., Machineni, S., Turnbaugh, P.J., Kaplan, L.M., Conserved shifts in the gut microbiota due to gastric bypass reduce host weight and adiposity. Sci. Transl. Med., 5, 2013 178ra141.
115. Bachmann, J., Heiligensetzer, M., Krakowski-Roosen, H., Buchler, M.W., Friess, H., Martignoni, M.E., Cachexia worsens prognosis in patients with resectable pancreatic cancer. J. Gastrointest. Surg. 12 (2008), 1193–1201.
116. Sato, N., Yamaguchi, K., Chijiiwa, K., Tanaka, M., Risk analysis of pancreatic fistula after pancreatic head resection. Arch. Surg. 133 (1998), 1094–1098.
117. Buchler, M.W., Friess, H., Wagner, M., Kulli, C., Wagener, V., Z'Graggen, K., Pancreatic fistula after pancreatic head resection. Br. J. Surg. 87 (2000), 883–889.
118. Munoz-Bongrand, N., Sauvanet, A., Denys, A., Sibert, A., Vilgrain, V., Belghiti, J., Conservative management of pancreatic fistula after pancreaticoduodenectomy with pancreaticogastrostomy. J. Am. Coll. Surg. 199 (2004), 198–203.
119. Veillette, G., Dominguez, I., Ferrone, C., Thayer, S.P., McGrath, D., Warshaw, A.L., et al. Implications and management of pancreatic fistulas following pancreaticoduodenectomy: the Massachusetts General Hospital experience. Arch. Surg. 143 (2008), 476–481.
120. Ohgi, K., Sugiura, T., Yamamoto, Y., Okamura, Y., Ito, T., Uesaka, K., Bacterobilia may trigger the development and severity of pancreatic fistula after pancreatoduodenectomy. Surgery 160 (2016), 725–730.
121. Rooks, M.G., Garrett, W.S., Gut microbiota, metabolites and host immunity. Nat. Rev. Immunol. 16 (2016), 341–352.
122. Tamburini, S., Shen, N., Wu, H.C., Clemente, J.C., The microbiome in early life: implications for health outcomes. Nat. Med. 22 (2016), 713–722.
123. Wu, G.D., Chen, J., Hoffmann, C., Bittinger, K., Chen, Y.Y., Keilbaugh, S.A., et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 334 (2011), 105–108.
124. Biedermann, L., Zeitz, J., Mwinyi, J., Sutter-Minder, E., Rehman, A., Ott, S.J., et al. Smoking cessation induces profound changes in the composition of the intestinal microbiota in humans. PLoS One, 8, 2013, e59260.
125. Jackson, M.A., Goodrich, J.K., Maxan, M.E., Freedberg, D.E., Abrams, J.A., Poole, A.C., et al. Proton pump inhibitors alter the composition of the gut microbiota. Gut 65 (2016), 749–756.
126. Dethlefsen, L., Huse, S., Sogin, M.L., Relman, D.A., The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol., 6, 2008, e280.