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Published in: European Journal of Medical Research 1/2023

Open Access 01-12-2023 | Research

Variations of bile bacterial community alongside gallstone disease progression and key taxa involved in poor outcomes after endoscopic surgery

Authors: Xunchao Cai, Yao Peng, Yajie Gong, Xiuting Huang, Lu Liu, Yifan Chen, Jingfeng Du, Zhongming Dai, Yun Qian, Long Xu

Published in: European Journal of Medical Research | Issue 1/2023

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Abstract

Gallstone disease is a prevalent biliary disease worldwide, and bacteria play vital roles in the disease development and progression, as well as the prognosis after endoscopic surgery. However, there have been limited studies to explore the key taxa involved. In this study, bile samples from healthy controls (HCs, liver donors without hepatobiliary disease) and three diseased groups, namely patients with gallbladder stones (GBS), patients with common bile duct stones (CBDS), and patients with stricture in the common bile duct (SCBD), were collected and analyzed. Bacterial community characterization based on 16S rRNA amplicon sequencing showed that bacterial diversities did not change significantly alongside gallstone disease development and progression. The predominant phyla in each group were Proteobacteria, Firmicutes, Bacteroidota, and Fusobacteriota, representing over 80% in abundance of the biliary bacteria community. Specifically, the abundance of Proteobacteria decreased greatly while that of Firmicutes and Bacteroidota increased greatly in the diseased groups when compared to that in HCs. Moreover, linear discriminant analysis identified several genera highly represented in the diseased groups. Among them, Klebsiella, Prevotella, Pseudomonas and Veillonella are persistent in both the HCs group and the diseased groups, indicating an enrichment of local bile bacteria in the diseased bile; while Lachnoanerobaculum, Atopobium, Oribacterium, and Stomatobaculum, those aligned to oral cavity taxa, are persistent in the diseased groups but are transient in the HCs group, and their abundances sequentially increased with the disease development and progression (HCs→GBS→CBDS→SCBD), implying a translocation and colonization of the oral cavity bacteria in the diseased bile. Moreover, co-occurrence network analysis revealed that bacterial infection (e.g., Photobacterium and Plesiomonas) from the intestine was developed during endoscopic surgery with reduced bile bacteria diversity. The results of this study revealed that the bile bacterial community is relatively stable and dominated by a few persistent taxa. Moreover, we hypothesized that translocation and colonization of specific bacteria from the oral cavity happens alongside gallstone disease development and progression, and bacterial infection from the intestinal tract results in poor outcomes after endoscopic surgery.
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Literature
1.
go back to reference UK ICGT. Gallstone disease: diagnosis and management of cholelithiasis, cholecystitis and choledocholithiasis. 2014. UK ICGT. Gallstone disease: diagnosis and management of cholelithiasis, cholecystitis and choledocholithiasis. 2014.
2.
go back to reference Lee J, Keane MG, Pereira S. Diagnosis and treatment of gallstone disease. Practitioner. 2015;259 (1783):15–9,2. Lee J, Keane MG, Pereira S. Diagnosis and treatment of gallstone disease. Practitioner. 2015;259 (1783):15–9,2.
3.
go back to reference Shaffer EA. Epidemiology of gallbladder stone disease. Best Pract Res Clin Gastroenterol. 2006;20(6):981–96.PubMed Shaffer EA. Epidemiology of gallbladder stone disease. Best Pract Res Clin Gastroenterol. 2006;20(6):981–96.PubMed
4.
go back to reference Shaffer EA. Epidemiology and risk factors for gallstone disease: has the paradigm changed in the 21st century? Curr Gastroenterol Rep. 2005;7(2):132–40.PubMed Shaffer EA. Epidemiology and risk factors for gallstone disease: has the paradigm changed in the 21st century? Curr Gastroenterol Rep. 2005;7(2):132–40.PubMed
5.
6.
go back to reference Rosenthal RA, Zenilman ME, Katlic MR. Principles and practice of geriatric surgery. Cham: Springer; 2011. Rosenthal RA, Zenilman ME, Katlic MR. Principles and practice of geriatric surgery. Cham: Springer; 2011.
7.
go back to reference Everhart JE, Ruhl CE. Burden of digestive diseases in the United States Part III: Liver, biliary tract, and pancreas. Gastroenterology. 2009;136(4):1134–44.PubMed Everhart JE, Ruhl CE. Burden of digestive diseases in the United States Part III: Liver, biliary tract, and pancreas. Gastroenterology. 2009;136(4):1134–44.PubMed
8.
go back to reference Wang Y, Qi M, Qin C, Hong J. Role of the biliary microbiome in gallstone disease. Expert Rev Gastroenterol Hepatol. 2018;12(12):1193–205.PubMed Wang Y, Qi M, Qin C, Hong J. Role of the biliary microbiome in gallstone disease. Expert Rev Gastroenterol Hepatol. 2018;12(12):1193–205.PubMed
9.
go back to reference Lammert F, Gurusamy K, Ko CW, Miquel J-F, Méndez-Sánchez N, Portincasa P, et al. Gallstones. Nat Rev Dis Primers. 2016;2(1):1–17. Lammert F, Gurusamy K, Ko CW, Miquel J-F, Méndez-Sánchez N, Portincasa P, et al. Gallstones. Nat Rev Dis Primers. 2016;2(1):1–17.
10.
go back to reference Ansaloni L, Pisano M, Coccolini F, Peitzmann A, Fingerhut A, Catena F, et al. 2016 WSES guidelines on acute calculous cholecystitis. World J Emerg Surg. 2016;11(1):1–23. Ansaloni L, Pisano M, Coccolini F, Peitzmann A, Fingerhut A, Catena F, et al. 2016 WSES guidelines on acute calculous cholecystitis. World J Emerg Surg. 2016;11(1):1–23.
11.
go back to reference Luo X, Yang W, Joshi AD, Wu K, Simon TG, Yuan C, et al. Gallstones and risk of cancers of the liver, biliary tract and pancreas: a prospective study within two US cohorts. Br J Cancer. 2022;127(6):1069–75.PubMedPubMedCentral Luo X, Yang W, Joshi AD, Wu K, Simon TG, Yuan C, et al. Gallstones and risk of cancers of the liver, biliary tract and pancreas: a prospective study within two US cohorts. Br J Cancer. 2022;127(6):1069–75.PubMedPubMedCentral
12.
go back to reference Ji CS, Yeseul K, Jehyun J, Ho-Jin G, Mimi K, Kyojin K, et al. Association of microbial dysbiosis with gallbladder diseases identified by bile microbiome profiling. J Korean Med Sci. 2021;36(28):1–15. Ji CS, Yeseul K, Jehyun J, Ho-Jin G, Mimi K, Kyojin K, et al. Association of microbial dysbiosis with gallbladder diseases identified by bile microbiome profiling. J Korean Med Sci. 2021;36(28):1–15.
13.
go back to reference Cai H, Kong W-T, Chen C-B, Shi G-M, Huang C, Shen Y-H, et al. Cholelithiasis and the risk of intrahepatic cholangiocarcinoma: a meta-analysis of observational studies. BMC Cancer. 2015;15(1):1–7. Cai H, Kong W-T, Chen C-B, Shi G-M, Huang C, Shen Y-H, et al. Cholelithiasis and the risk of intrahepatic cholangiocarcinoma: a meta-analysis of observational studies. BMC Cancer. 2015;15(1):1–7.
14.
go back to reference Dangtakot R, Intuyod K, Ahooja A, Wongwiwatchai J, Hanpanich P, Lulitanond A, et al. Profiling of Bile Microbiome Identifies District Microbial Population between Choledocholithiasis and Cholangiocarcinoma Patients. Asian Pacific Journal of Cancer Prevention: APJCP. 2021;22(1):233.PubMedPubMedCentral Dangtakot R, Intuyod K, Ahooja A, Wongwiwatchai J, Hanpanich P, Lulitanond A, et al. Profiling of Bile Microbiome Identifies District Microbial Population between Choledocholithiasis and Cholangiocarcinoma Patients. Asian Pacific Journal of Cancer Prevention: APJCP. 2021;22(1):233.PubMedPubMedCentral
15.
go back to reference Shrikhande S, Barreto S, Singh S, Udwadia T, Agarwal A. Cholelithiasis in gallbladder cancer: coincidence, cofactor, or cause! European journal of surgical oncology (EJSO). 2010;36(6):514–9.PubMed Shrikhande S, Barreto S, Singh S, Udwadia T, Agarwal A. Cholelithiasis in gallbladder cancer: coincidence, cofactor, or cause! European journal of surgical oncology (EJSO). 2010;36(6):514–9.PubMed
16.
go back to reference Fernández L, Langa S, Martín V, Maldonado A, Jiménez E, Martín R, et al. The human milk microbiota: origin and potential roles in health and disease. Pharmacol Res. 2013;69(1):1–10.PubMed Fernández L, Langa S, Martín V, Maldonado A, Jiménez E, Martín R, et al. The human milk microbiota: origin and potential roles in health and disease. Pharmacol Res. 2013;69(1):1–10.PubMed
17.
go back to reference Lelouvier B, Servant F, Païssé S, Brunet AC, Benyahya S, Serino M, et al. Changes in blood microbiota profiles associated with liver fibrosis in obese patients: a pilot analysis. Hepatology. 2016;64(6):2015–27.PubMed Lelouvier B, Servant F, Païssé S, Brunet AC, Benyahya S, Serino M, et al. Changes in blood microbiota profiles associated with liver fibrosis in obese patients: a pilot analysis. Hepatology. 2016;64(6):2015–27.PubMed
18.
go back to reference Stewart L, Grifiss JM, Jarvis GA, Way LW. Biliary bacterial factors determine the path of gallstone formation. The American journal of surgery. 2006;192(5):598–603.PubMed Stewart L, Grifiss JM, Jarvis GA, Way LW. Biliary bacterial factors determine the path of gallstone formation. The American journal of surgery. 2006;192(5):598–603.PubMed
19.
go back to reference Liu J, Yan Q, Luo F, Shang D, Wu D, Zhang H, et al. Acute cholecystitis associated with infection of Enterobacteriaceae from gut microbiota. Clin Microbiol Infect. 2015;21(9):851.e1-e9.PubMed Liu J, Yan Q, Luo F, Shang D, Wu D, Zhang H, et al. Acute cholecystitis associated with infection of Enterobacteriaceae from gut microbiota. Clin Microbiol Infect. 2015;21(9):851.e1-e9.PubMed
20.
go back to reference Lam R, Zakko A, Petrov JC, Kumar P, Duffy AJ, Muniraj T. Gallbladder disorders: a comprehensive review. Dis Mon. 2021;67(7): 101130.PubMed Lam R, Zakko A, Petrov JC, Kumar P, Duffy AJ, Muniraj T. Gallbladder disorders: a comprehensive review. Dis Mon. 2021;67(7): 101130.PubMed
21.
go back to reference Pereira P, Aho V, Arola J, Boyd S, Jokelainen K, Paulin L, et al. Bile microbiota in primary sclerosing cholangitis: Impact on disease progression and development of biliary dysplasia. PLoS ONE. 2017;12(8): e0182924.PubMedPubMedCentral Pereira P, Aho V, Arola J, Boyd S, Jokelainen K, Paulin L, et al. Bile microbiota in primary sclerosing cholangitis: Impact on disease progression and development of biliary dysplasia. PLoS ONE. 2017;12(8): e0182924.PubMedPubMedCentral
23.
go back to reference Molinero N, Ruiz L, Milani C, Gutiérrez-Díaz I, Sánchez B, Mangifesta M, et al. The human gallbladder microbiome is related to the physiological state and the biliary metabolic profile. Microbiome. 2019;7(1):1–17. Molinero N, Ruiz L, Milani C, Gutiérrez-Díaz I, Sánchez B, Mangifesta M, et al. The human gallbladder microbiome is related to the physiological state and the biliary metabolic profile. Microbiome. 2019;7(1):1–17.
24.
go back to reference Salameh H, DiMaio CJ. Endoscopic retrograde cholangiopancreatography and endoscopic ultrasound-guided gallbladder drainage. Gastrointest Endosc Clin. 2019;29(2):293–310. Salameh H, DiMaio CJ. Endoscopic retrograde cholangiopancreatography and endoscopic ultrasound-guided gallbladder drainage. Gastrointest Endosc Clin. 2019;29(2):293–310.
25.
go back to reference Ellis AJ, Chapman RW. Microbiological analysis of bile during cholangiography. Nat Rev Gastroenterol Hepatol. 2010;7(12):655–6.PubMed Ellis AJ, Chapman RW. Microbiological analysis of bile during cholangiography. Nat Rev Gastroenterol Hepatol. 2010;7(12):655–6.PubMed
26.
go back to reference O’Brien PA, Tan S, Yang C, Frade PR, Andreakis N, Smith HA, et al. Diverse coral reef invertebrates exhibit patterns of phylosymbiosis. ISME J. 2020;14(9):2211–22.PubMedPubMedCentral O’Brien PA, Tan S, Yang C, Frade PR, Andreakis N, Smith HA, et al. Diverse coral reef invertebrates exhibit patterns of phylosymbiosis. ISME J. 2020;14(9):2211–22.PubMedPubMedCentral
27.
go back to reference Cohen J. Statistical power analysis for the behavioral sciences. Cambridge: Academic press; 2013. Cohen J. Statistical power analysis for the behavioral sciences. Cambridge: Academic press; 2013.
28.
go back to reference Van Der Gast CJ, Walker AW, Stressmann FA, Rogers GB, Scott P, Daniels TW, et al. Partitioning core and satellite taxa from within cystic fibrosis lung bacterial communities. ISME J. 2011;5(5):780–91.PubMed Van Der Gast CJ, Walker AW, Stressmann FA, Rogers GB, Scott P, Daniels TW, et al. Partitioning core and satellite taxa from within cystic fibrosis lung bacterial communities. ISME J. 2011;5(5):780–91.PubMed
29.
go back to reference Cai X, Mao Y, Xu J, Tian L, Wang Y, Iqbal W, et al. Characterizing community dynamics and exploring bacterial assemblages in two activated sludge systems. Appl Microbiol Biotechnol. 2020;104(4):1795–808.PubMed Cai X, Mao Y, Xu J, Tian L, Wang Y, Iqbal W, et al. Characterizing community dynamics and exploring bacterial assemblages in two activated sludge systems. Appl Microbiol Biotechnol. 2020;104(4):1795–808.PubMed
30.
go back to reference Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics. 2008;9(1):1–13. Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics. 2008;9(1):1–13.
31.
go back to reference Otasek D, Morris JH, Bouças J, Pico AR, Demchak B. Cytoscape automation: empowering workflow-based network analysis. Genome Biol. 2019;20(1):1–15. Otasek D, Morris JH, Bouças J, Pico AR, Demchak B. Cytoscape automation: empowering workflow-based network analysis. Genome Biol. 2019;20(1):1–15.
32.
go back to reference Song X, Wang X, Hu Y, Li H, Ren T, Li Y, et al. A metagenomic study of biliary microbiome change along the cholecystitis-carcinoma sequence. Clin Transl Med. 2020;10(2):e97.PubMedPubMedCentral Song X, Wang X, Hu Y, Li H, Ren T, Li Y, et al. A metagenomic study of biliary microbiome change along the cholecystitis-carcinoma sequence. Clin Transl Med. 2020;10(2):e97.PubMedPubMedCentral
35.
go back to reference Kamada N, Chen GY, Inohara N, Núñez G. Control of pathogens and pathobionts by the gut microbiota. Nat Immunol. 2013;14(7):685–90.PubMedPubMedCentral Kamada N, Chen GY, Inohara N, Núñez G. Control of pathogens and pathobionts by the gut microbiota. Nat Immunol. 2013;14(7):685–90.PubMedPubMedCentral
36.
go back to reference Hu F-L, Chen H-T, Guo F-F, Yang M, Jiang X, Yu J-H, et al. Biliary microbiota and mucin 4 impact the calcification of cholesterol gallstones. Hepatobiliary Pancreat Dis Int. 2021;20(1):61–6.PubMed Hu F-L, Chen H-T, Guo F-F, Yang M, Jiang X, Yu J-H, et al. Biliary microbiota and mucin 4 impact the calcification of cholesterol gallstones. Hepatobiliary Pancreat Dis Int. 2021;20(1):61–6.PubMed
39.
go back to reference Verdier J, Luedde T, Sellge G. Biliary mucosal barrier and microbiome. Visc Med. 2015;31(3):156–61. Verdier J, Luedde T, Sellge G. Biliary mucosal barrier and microbiome. Visc Med. 2015;31(3):156–61.
40.
go back to reference Ye F, Shen H, Li Z, Meng F, Li L, Yang J, 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.PubMedPubMedCentral Ye F, Shen H, Li Z, Meng F, Li L, Yang J, 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.PubMedPubMedCentral
41.
go back to reference Tomazinho LF, Avila-Campos MJ. Detection of Porphyromonas gingivalis, Porphyromonas endodontalis, Prevotella intermedia, and Prevotella nigrescens in chronic endodontic infection. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2007;103(2):285–8.PubMed Tomazinho LF, Avila-Campos MJ. Detection of Porphyromonas gingivalis, Porphyromonas endodontalis, Prevotella intermedia, and Prevotella nigrescens in chronic endodontic infection. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2007;103(2):285–8.PubMed
43.
go back to reference Kummen M, Holm K, Anmarkrud JA, Nygård S, Vesterhus M, Høivik ML, et al. The gut microbial profile in patients with primary sclerosing cholangitis is distinct from patients with ulcerative colitis without biliary disease and healthy controls. Gut. 2017;66(4):611–9.PubMed Kummen M, Holm K, Anmarkrud JA, Nygård S, Vesterhus M, Høivik ML, et al. The gut microbial profile in patients with primary sclerosing cholangitis is distinct from patients with ulcerative colitis without biliary disease and healthy controls. Gut. 2017;66(4):611–9.PubMed
44.
go back to reference Ida Y, Okuyama T, Araki K, Sekiguchi K, Watanabe T, Ohnishi H. First description of Lachnoanaerobaculum orale as a possible cause of human bacteremia. Anaerobe. 2022;73: 102506.PubMed Ida Y, Okuyama T, Araki K, Sekiguchi K, Watanabe T, Ohnishi H. First description of Lachnoanaerobaculum orale as a possible cause of human bacteremia. Anaerobe. 2022;73: 102506.PubMed
45.
go back to reference Poudel SK, Padmanabhan R, Guinta K, Stevens T, Sanaka M, Chahal P, et al. Microbiomic profiles of bile in patients with benign and malignant pancreaticobiliary disease. American Society of Clinical Oncology; 2021 Poudel SK, Padmanabhan R, Guinta K, Stevens T, Sanaka M, Chahal P, et al. Microbiomic profiles of bile in patients with benign and malignant pancreaticobiliary disease. American Society of Clinical Oncology; 2021
47.
go back to reference Bradshaw CS, Tabrizi S, Fairley CK, Morton AN, Rudland E, Garland SM. The association of Atopobium vaginae and Gardnerella vaginalis with bacterial vaginosis and recurrence after oral metronidazole therapy. J Infect Dis. 2006;194(6):828–36.PubMed Bradshaw CS, Tabrizi S, Fairley CK, Morton AN, Rudland E, Garland SM. The association of Atopobium vaginae and Gardnerella vaginalis with bacterial vaginosis and recurrence after oral metronidazole therapy. J Infect Dis. 2006;194(6):828–36.PubMed
48.
go back to reference Lu H, Ren Z, Li A, Li J, Xu S, Zhang H, et al. Tongue coating microbiome data distinguish patients with pancreatic head cancer from healthy controls. J Oral Microbiol. 2019;11(1):1563409.PubMedPubMedCentral Lu H, Ren Z, Li A, Li J, Xu S, Zhang H, et al. Tongue coating microbiome data distinguish patients with pancreatic head cancer from healthy controls. J Oral Microbiol. 2019;11(1):1563409.PubMedPubMedCentral
50.
go back to reference Pence MA. The brief case: wound infection with Plesiomonas shigelloides following a freshwater injury. Am Soc Microbiol; 2016. Pence MA. The brief case: wound infection with Plesiomonas shigelloides following a freshwater injury. Am Soc Microbiol; 2016.
51.
go back to reference Rivas AJ, Lemos ML, Osorio CR. Photobacterium damselae subsp. damselae, a bacterium pathogenic for marine animals and humans. Front Microbiol. 2013;4:283.PubMedPubMedCentral Rivas AJ, Lemos ML, Osorio CR. Photobacterium damselae subsp. damselae, a bacterium pathogenic for marine animals and humans. Front Microbiol. 2013;4:283.PubMedPubMedCentral
52.
go back to reference Maciejewska A, Bednarczyk B, Lugowski C, Lukasiewicz J. Structural studies of the lipopolysaccharide isolated from Plesiomonas shigelloides O22: H3 (CNCTC 90/89). Int J Mol Sci. 2020;21(18):6788.PubMedPubMedCentral Maciejewska A, Bednarczyk B, Lugowski C, Lukasiewicz J. Structural studies of the lipopolysaccharide isolated from Plesiomonas shigelloides O22: H3 (CNCTC 90/89). Int J Mol Sci. 2020;21(18):6788.PubMedPubMedCentral
Metadata
Title
Variations of bile bacterial community alongside gallstone disease progression and key taxa involved in poor outcomes after endoscopic surgery
Authors
Xunchao Cai
Yao Peng
Yajie Gong
Xiuting Huang
Lu Liu
Yifan Chen
Jingfeng Du
Zhongming Dai
Yun Qian
Long Xu
Publication date
01-12-2023
Publisher
BioMed Central
Published in
European Journal of Medical Research / Issue 1/2023
Electronic ISSN: 2047-783X
DOI
https://doi.org/10.1186/s40001-023-01308-y

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