Causal relationship between intestinal flora and esophageal cancer: A Mendelian randomization analysis_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

WANG Mengmeng ¹ , GAO Mingjun ¹ , ZHOU Siding ² , TIAN Shuyu ¹ ,  SHU Yusheng ³ ,  WANG Xiaolin ³

1. Dalian Medical University, Dalian, 116000, Liaoning, P. R. China;
2. Yangzhou University, Yangzhou, 225000, Jiangsu, P. R. China;
3. Department of Thoracic Surgery, Northern Jiangsu People's Hospital, Yangzhou, 225000, Jiangsu, P. R. China;

Corresponding author：

SHU Yusheng, Email: 18051061999@yzu.edu.cn; WANG Xiaolin, Email: 18051063909@yzu.edu.cn

Keywords：

Esophageal cancer; intestinal flora; causal association; Mendelian randomization

DOI：

10.7507/1007-4848.202403016

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To explore whether there is a causal relationship between intestinal flora and esophageal cancer. Methods Summary statistics of intestinal flora and esophageal cancer were obtained from the genome-wide association studies (GWAS) database. Five methods, including inverse variance weighted (IVW), weighted median estimation, Mendelian randomization (MR)-Egger regression, single mode, and weighted mode, were used for analysis, with IVW as the main analysis method. Sensitivity analysis was used to evaluate the reliability of MR results. Results In the IVW method, Oxalobacteraceae [OR=1.001, 95%CI (1.000, 1.002), P=0.023], Faecalibacterium [OR=1.001, 95%CI (1.000, 1.002), P=0.028], Senegalimassilia [OR=1.002, 95%CI (1.000, 1.003), P=0.006] and Veillonella [OR=1.001, 95%CI (1.000, 1.002), P=0.018] were positively correlated with esophageal cancer, while Burkholderiales [OR=0.999, 95%CI (0.998, 1.001), P=0.002], Eubacterium oxidoreducens [OR=0.998, 95%CI (0.997, 0.999), P=0.038], Romboutsia [OR=0.999, 95%CI (0.998, 1.000), P=0.048] and Turicibacter[OR=0.998, 95%CI (0.997, 0.999), P=0.013] were negatively correlated with esophageal cancer. Sensitivity analysis showed no evidence of heterogeneity, horizontal pleiotropy and reverse causality. Conclusion Oxalobacteraceae, Faecalibacterium, Senegalimassilia and Veillonella increase the risk of esophageal cancer, while Burkholderiales, Eubacterium oxidoreducens, Romboutsia and Turicibacter decrease the risk of esophageal cancer. Further studies are needed to explore how these bacteria affect the progression of esophageal cancer.

1.	Liu CQ, Ma YL, Qin Q, et al. Epidemiology of esophageal cancer in 2020 and projections to 2030 and 2040. Thorac Cancer, 2023, 14(1): 3-11.
2.	Kelly RJ. Emerging multimodality approaches to treat localized esophageal cancer. J Natl Compr Canc Netw, 2019, 17(8): 1009-1014.
3.	Asombang AW, Chishinga N, Nkhoma A, et al. Systematic review and meta-analysis of esophageal cancer in Africa: Epidemiology, risk factors, management and outcomes. World J Gastroenterol, 2019, 25(31): 4512-4533.
4.	Kitagawa Y, Uno T, Oyama T, et al. Esophageal cancer practice guidelines 2017 edited by the Japan Esophageal Society: Part 1. Esophagus, 2019, 16(1): 1-24.
5.	Sewram V, Sitas F, O'Connell D, et al. Tobacco and alcohol as risk factors for oesophageal cancer in a high incidence area in South Africa. Cancer Epidemiol, 2016, 41: 113-21.
6.	Thrift AP. Global burden and epidemiology of Barrett oesophagus and oesophageal cancer. Nat Rev Gastroenterol Hepatol, 2021, 18(6): 432-443.
7.	Zhou J, Sun K, Wang S, et al. Associations between cancer family history and esophageal cancer and precancerous lesions in high-risk areas of China. Chin Med J (Engl), 2022, 135(7): 813-819.
8.	Cai Y, Lin J, Wei W, et al. Burden of esophageal cancer and its attributable risk factors in 204 countries and territories from 1990 to 2019. Front Public Health, 2022, 10: 952087.
9.	Qin X, Jia G, Zhou X, et al. Diet and esophageal cancer risk: An umbrella review of systematic reviews and meta-analyses of observational studies. Adv Nutr, 2022, 13(6): 2207-2216.
10.	Kawasaki M, Ikeda Y, Ikeda E, et al. Oral infectious bacteria in dental plaque and saliva as risk factors in patients with esophageal cancer. Cancer, 2021, 127(4): 512-519.
11.	Wang L, Han H, Wang Z, et al. Targeting the microenvironment in esophageal cancer. Front Cell Dev Biol, 2021, 9: 684966.
12.	Kho ZY, Lal SK. The human gut microbiome: A potential controller of wellness and disease. Front Microbiol, 2018, 9: 1835.
13.	Yuan S, Chen J, Ruan X, et al. Smoking, alcohol consumption, and 24 gastrointestinal diseases: Mendelian randomization analysis. Elife, 2023, 12: e84051.
14.	Mima K, Ogino S, Nakagawa S, et al. The role of intestinal bacteria in the development and progression of gastrointestinal tract neoplasms. Surg Oncol, 2017, 26(4): 368-376.
15.	Zhou J, Shrestha P, Qiu Z, et al. Distinct microbiota dysbiosis in patients with non-erosive reflux disease and esophageal adenocarcinoma. J Clin Med, 2020, 9(7): 2162.
16.	Münch NS, Fang HY, Ingermann J, et al. High-fat diet accelerates carcinogenesis in a mouse model of Barrett's esophagus via interleukin 8 and alterations to the gut microbiome. Gastroenterology, 2019, 157(2): 492-506.
17.	Muszyński D, Kudra A, Sobocki BK, et al. Esophageal cancer and bacterial part of gut microbiota: A multidisciplinary point of view. Front Cell Infect Microbiol, 2022, 12: 1057668.
18.	Dan YL, Wang P, Cheng Z, et al. Circulating adiponectin levels and systemic lupus erythematosus: A two-sample Mendelian randomization study. Rheumatology (Oxford), 2021, 60(2): 940-946.
19.	Long Y, Tang L, Zhou Y, et al. Causal relationship between gut microbiota and cancers: A two-sample Mendelian randomisation study. BMC Med, 2023, 21(1): 66.
20.	Xiang K, Wang P, Xu Z, et al. Causal effects of gut microbiome on systemic lupus erythematosus: A two-sample Mendelian randomization study. Front Immunol, 2021, 12: 667097.
21.	Sanna S, van Zuydam NR, Mahajan A, et al. Causal relationships among the gut microbiome, short-chain fatty acids and metabolic diseases. Nat Genet, 2019, 51(4): 600-605.
22.	Kurilshikov A, Medina-Gomez C, Bacigalupe R, et al. Large-scale association analyses identify host factors influencing human gut microbiome composition. Nat Genet, 2021, 53(2): 156-165.
23.	Yin L, Yan H, Chen K, et al. Diet-derived circulating antioxidants and risk of digestive system tumors: A Mendelian randomization study. Nutrients, 2022, 14(16): 3274.
24.	Zhang X, Yang X, Zhang T, et al. Association of educational attainment with esophageal cancer, Barrett's esophagus, and gastroesophageal reflux disease, and the mediating role of modifiable risk factors: A Mendelian randomization study. Front Public Health, 2023, 11: 1022367.
25.	Lv WQ, Lin X, Shen H, et al. Human gut microbiome impacts skeletal muscle mass via gut microbial synthesis of the short-chain fatty acid butyrate among healthy menopausal women. J Cachexia Sarcopenia Muscle, 2021, 12(6): 1860-1870.
26.	Luo M, Cai J, Luo S, et al. Causal effects of gut microbiota on the risk of chronic kidney disease: A Mendelian randomization study. Front Cell Infect Microbiol, 2023, 13: 1142140.
27.	Larsson SC, Spyrou N, Mantzoros CS. Body fatness associations with cancer: Evidence from recent epidemiological studies and future directions. Metabolism, 2022, 137: 155326.
28.	Li C, Liu C, Li N. Causal associations between gut microbiota and adverse pregnancy outcomes: A two-sample Mendelian randomization study. Front Microbiol, 2022, 13: 1059281.
29.	Gao N, Kong M, Li X, et al. Systemic lupus erythematosus and cardiovascular disease: A Mendelian randomization study. Front Immunol, 2022, 13: 908831.
30.	Chen JH, Zeng LY, Zhao YF, et al. Causal effects of gut microbiota on sepsis: A two-sample Mendelian randomization study. Front Microbiol, 2023, 14: 1167416.
31.	Boehm FJ, Zhou X. Statistical methods for Mendelian randomization in genome-wide association studies: A review. Comput Struct Biotechnol J, 2022, 20: 2338-2351.
32.	Zhang D, Hu Y, Guo W, et al. Mendelian randomization study reveals a causal relationship between rheumatoid arthritis and risk for pre-eclampsia. Front Immunol, 2022, 13: 1080980.
33.	Burgess S, Thompson SG. Interpreting findings from Mendelian randomization using the MR-Egger method. Eur J Epidemiol, 2017, 32(5): 377-389.
34.	Park CH, Lee SK. Exploring esophageal microbiomes in esophageal diseases: A systematic review. J Neurogastroenterol Motil, 2020, 26(2): 171-179.
35.	Lv J, Guo L, Liu JJ, et al. Alteration of the esophageal microbiota in Barrett's esophagus and esophageal adenocarcinoma. World J Gastroenterol, 2019, 25(18): 2149-2161.
36.	Li M, Shao D, Zhou J, et al. Signatures within esophageal microbiota with progression of esophageal squamous cell carcinoma. Chin J Cancer Res, 2020, 32(6): 755-767.
37.	Yang L, Francois F, Pei Z. Molecular pathways: Pathogenesis and clinical implications of microbiome alteration in esophagitis and Barrett esophagus. Clin Cancer Res, 2012, 18(8): 2138-2144.
38.	Baghdadi J, Chaudhary N, Pei Z, et al. Microbiome, innate immunity, and esophageal adenocarcinoma. Clin Lab Med, 2014, 34(4): 721-732.
39.	Neto AG, Whitaker A, Pei Z. Microbiome and potential targets for chemoprevention of esophageal adenocarcinoma. Semin Oncol, 2016, 43(1): 86-96.
40.	Sheflin AM, Whitney AK, Weir TL. Cancer-promoting effects of microbial dysbiosis. Curr Oncol Rep, 2014, 16(10): 406.
41.	Schwabe RF, Jobin C. The microbiome and cancer. Nat Rev Cancer, 2013, 13(11): 800-812.
42.	Di Pilato V, Freschi G, Ringressi MN, et al. The esophageal microbiota in health and disease. Ann N Y Acad Sci, 2016, 1381(1): 21-33.
43.	Wang X, Huycke MM. Extracellular superoxide production by Enterococcus faecalis promotes chromosomal instability in mammalian cells. Gastroenterology, 2007, 132(2): 551-561.
44.	Donia MS, Fischbach MA. HUMAN MICROBIOTA. Small molecules from the human microbiota. Science, 2015, 349(6246): 1254766.
45.	Guerra L, Guidi R, Frisan T. Do bacterial genotoxins contribute to chronic inflammation, genomic instability and tumor progression? FEBS J, 2011, 278(23): 4577-4588.
46.	Lopetuso LR, Severgnini M, Pecere S, et al. Esophageal microbiome signature in patients with Barrett's esophagus and esophageal adenocarcinoma. PLoS One, 2020, 15(5): e0231789.
47.	Duncan SH, Hold GL, Barcenilla A, et al. Roseburia intestinalis sp. nov. , a novel saccharolytic, butyrate-producing bacterium from human faeces. Int J Syst Evol Microbiol, 2002, 52(Pt 5): 1615-1620.
48.	Cheung MK, Yue GGL, Lauw S, et al. Alterations in gut microbiota of esophageal squamous cell carcinoma patients. J Gastroenterol Hepatol, 2022, 37(10): 1919-1927.
49.	Zhang T, Zhang W, Feng C, et al. Stronger gut microbiome modulatory effects by postbiotics than probiotics in a mouse colitis model. NPJ Sci Food, 2022, 6(1): 53.
50.	Deng Y, Tang D, Hou P, et al. Dysbiosis of gut microbiota in patients with esophageal cancer. Microb Pathog, 2021, 150: 104709.
51.	Nie X, Geng Z, Liu J, et al. Chinese herbal medicine anticancer cocktail soup activates immune cells to kill colon cancer cells by regulating the gut microbiota-Th17 axis. Front Pharmacol, 2022, 13: 963638.
52.	Pan F, Zhang LL, Luo HJ, et al. Dietary riboflavin deficiency induces ariboflavinosis and esophageal epithelial atrophy in association with modification of gut microbiota in rats. Eur J Nutr, 2021, 60(2): 807-820.
53.	Zhang X, Li C, Cao W, et al. Alterations of gastric microbiota in gastric cancer and precancerous stages. Front Cell Infect Microbiol, 2021, 11: 559148.
54.	Jeong JY, Kim TB, Kim J, et al. Diversity in the extracellular vesicle-derived microbiome of tissues according to tumor progression in pancreatic cancer. Cancers (Basel), 2020, 12(9): 2346.
55.	Hao X, Zhang J, Shang X, et al. Exercise modifies the disease-relevant gut microbial shifts in post-traumatic osteoarthritis rats. Bone Joint Res, 2022, 11(4): 214-225.
56.	Garcia-Beltran C, Malpique R, Carbonetto B, et al. Gut microbiota in adolescent girls with polycystic ovary syndrome: Effects of randomized treatments. Pediatr Obes, 2021, 16(4): e12734.
57.	Wang Q, Wang Q, Zhao L, et al. Blood bacterial 16S rRNA gene alterations in women with polycystic ovary syndrome. Front Endocrinol (Lausanne), 2022, 13: 814520.
58.	Zhang M, Lv Y, Hou S, et al. Differential mucosal microbiome profiles across stages of human colorectal cancer. Life (Basel), 2021, 11(8): 831.
59.	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.
60.	Liu M, Devlin JC, Hu J, et al. Microbial genetic and transcriptional contributions to oxalate degradation by the gut microbiota in health and disease. Elife, 2021, 10: e63642.

1. Liu CQ, Ma YL, Qin Q, et al. Epidemiology of esophageal cancer in 2020 and projections to 2030 and 2040. Thorac Cancer, 2023, 14(1): 3-11.
2. Kelly RJ. Emerging multimodality approaches to treat localized esophageal cancer. J Natl Compr Canc Netw, 2019, 17(8): 1009-1014.
3. Asombang AW, Chishinga N, Nkhoma A, et al. Systematic review and meta-analysis of esophageal cancer in Africa: Epidemiology, risk factors, management and outcomes. World J Gastroenterol, 2019, 25(31): 4512-4533.
4. Kitagawa Y, Uno T, Oyama T, et al. Esophageal cancer practice guidelines 2017 edited by the Japan Esophageal Society: Part 1. Esophagus, 2019, 16(1): 1-24.
5. Sewram V, Sitas F, O'Connell D, et al. Tobacco and alcohol as risk factors for oesophageal cancer in a high incidence area in South Africa. Cancer Epidemiol, 2016, 41: 113-21.
6. Thrift AP. Global burden and epidemiology of Barrett oesophagus and oesophageal cancer. Nat Rev Gastroenterol Hepatol, 2021, 18(6): 432-443.
7. Zhou J, Sun K, Wang S, et al. Associations between cancer family history and esophageal cancer and precancerous lesions in high-risk areas of China. Chin Med J (Engl), 2022, 135(7): 813-819.
8. Cai Y, Lin J, Wei W, et al. Burden of esophageal cancer and its attributable risk factors in 204 countries and territories from 1990 to 2019. Front Public Health, 2022, 10: 952087.
9. Qin X, Jia G, Zhou X, et al. Diet and esophageal cancer risk: An umbrella review of systematic reviews and meta-analyses of observational studies. Adv Nutr, 2022, 13(6): 2207-2216.
10. Kawasaki M, Ikeda Y, Ikeda E, et al. Oral infectious bacteria in dental plaque and saliva as risk factors in patients with esophageal cancer. Cancer, 2021, 127(4): 512-519.
11. Wang L, Han H, Wang Z, et al. Targeting the microenvironment in esophageal cancer. Front Cell Dev Biol, 2021, 9: 684966.
12. Kho ZY, Lal SK. The human gut microbiome: A potential controller of wellness and disease. Front Microbiol, 2018, 9: 1835.
13. Yuan S, Chen J, Ruan X, et al. Smoking, alcohol consumption, and 24 gastrointestinal diseases: Mendelian randomization analysis. Elife, 2023, 12: e84051.
14. Mima K, Ogino S, Nakagawa S, et al. The role of intestinal bacteria in the development and progression of gastrointestinal tract neoplasms. Surg Oncol, 2017, 26(4): 368-376.
15. Zhou J, Shrestha P, Qiu Z, et al. Distinct microbiota dysbiosis in patients with non-erosive reflux disease and esophageal adenocarcinoma. J Clin Med, 2020, 9(7): 2162.
16. Münch NS, Fang HY, Ingermann J, et al. High-fat diet accelerates carcinogenesis in a mouse model of Barrett's esophagus via interleukin 8 and alterations to the gut microbiome. Gastroenterology, 2019, 157(2): 492-506.
17. Muszyński D, Kudra A, Sobocki BK, et al. Esophageal cancer and bacterial part of gut microbiota: A multidisciplinary point of view. Front Cell Infect Microbiol, 2022, 12: 1057668.
18. Dan YL, Wang P, Cheng Z, et al. Circulating adiponectin levels and systemic lupus erythematosus: A two-sample Mendelian randomization study. Rheumatology (Oxford), 2021, 60(2): 940-946.
19. Long Y, Tang L, Zhou Y, et al. Causal relationship between gut microbiota and cancers: A two-sample Mendelian randomisation study. BMC Med, 2023, 21(1): 66.
20. Xiang K, Wang P, Xu Z, et al. Causal effects of gut microbiome on systemic lupus erythematosus: A two-sample Mendelian randomization study. Front Immunol, 2021, 12: 667097.
21. Sanna S, van Zuydam NR, Mahajan A, et al. Causal relationships among the gut microbiome, short-chain fatty acids and metabolic diseases. Nat Genet, 2019, 51(4): 600-605.
22. Kurilshikov A, Medina-Gomez C, Bacigalupe R, et al. Large-scale association analyses identify host factors influencing human gut microbiome composition. Nat Genet, 2021, 53(2): 156-165.
23. Yin L, Yan H, Chen K, et al. Diet-derived circulating antioxidants and risk of digestive system tumors: A Mendelian randomization study. Nutrients, 2022, 14(16): 3274.
24. Zhang X, Yang X, Zhang T, et al. Association of educational attainment with esophageal cancer, Barrett's esophagus, and gastroesophageal reflux disease, and the mediating role of modifiable risk factors: A Mendelian randomization study. Front Public Health, 2023, 11: 1022367.
25. Lv WQ, Lin X, Shen H, et al. Human gut microbiome impacts skeletal muscle mass via gut microbial synthesis of the short-chain fatty acid butyrate among healthy menopausal women. J Cachexia Sarcopenia Muscle, 2021, 12(6): 1860-1870.
26. Luo M, Cai J, Luo S, et al. Causal effects of gut microbiota on the risk of chronic kidney disease: A Mendelian randomization study. Front Cell Infect Microbiol, 2023, 13: 1142140.
27. Larsson SC, Spyrou N, Mantzoros CS. Body fatness associations with cancer: Evidence from recent epidemiological studies and future directions. Metabolism, 2022, 137: 155326.
28. Li C, Liu C, Li N. Causal associations between gut microbiota and adverse pregnancy outcomes: A two-sample Mendelian randomization study. Front Microbiol, 2022, 13: 1059281.
29. Gao N, Kong M, Li X, et al. Systemic lupus erythematosus and cardiovascular disease: A Mendelian randomization study. Front Immunol, 2022, 13: 908831.
30. Chen JH, Zeng LY, Zhao YF, et al. Causal effects of gut microbiota on sepsis: A two-sample Mendelian randomization study. Front Microbiol, 2023, 14: 1167416.
31. Boehm FJ, Zhou X. Statistical methods for Mendelian randomization in genome-wide association studies: A review. Comput Struct Biotechnol J, 2022, 20: 2338-2351.
32. Zhang D, Hu Y, Guo W, et al. Mendelian randomization study reveals a causal relationship between rheumatoid arthritis and risk for pre-eclampsia. Front Immunol, 2022, 13: 1080980.
33. Burgess S, Thompson SG. Interpreting findings from Mendelian randomization using the MR-Egger method. Eur J Epidemiol, 2017, 32(5): 377-389.
34. Park CH, Lee SK. Exploring esophageal microbiomes in esophageal diseases: A systematic review. J Neurogastroenterol Motil, 2020, 26(2): 171-179.
35. Lv J, Guo L, Liu JJ, et al. Alteration of the esophageal microbiota in Barrett's esophagus and esophageal adenocarcinoma. World J Gastroenterol, 2019, 25(18): 2149-2161.
36. Li M, Shao D, Zhou J, et al. Signatures within esophageal microbiota with progression of esophageal squamous cell carcinoma. Chin J Cancer Res, 2020, 32(6): 755-767.
37. Yang L, Francois F, Pei Z. Molecular pathways: Pathogenesis and clinical implications of microbiome alteration in esophagitis and Barrett esophagus. Clin Cancer Res, 2012, 18(8): 2138-2144.
38. Baghdadi J, Chaudhary N, Pei Z, et al. Microbiome, innate immunity, and esophageal adenocarcinoma. Clin Lab Med, 2014, 34(4): 721-732.
39. Neto AG, Whitaker A, Pei Z. Microbiome and potential targets for chemoprevention of esophageal adenocarcinoma. Semin Oncol, 2016, 43(1): 86-96.
40. Sheflin AM, Whitney AK, Weir TL. Cancer-promoting effects of microbial dysbiosis. Curr Oncol Rep, 2014, 16(10): 406.
41. Schwabe RF, Jobin C. The microbiome and cancer. Nat Rev Cancer, 2013, 13(11): 800-812.
42. Di Pilato V, Freschi G, Ringressi MN, et al. The esophageal microbiota in health and disease. Ann N Y Acad Sci, 2016, 1381(1): 21-33.
43. Wang X, Huycke MM. Extracellular superoxide production by Enterococcus faecalis promotes chromosomal instability in mammalian cells. Gastroenterology, 2007, 132(2): 551-561.
44. Donia MS, Fischbach MA. HUMAN MICROBIOTA. Small molecules from the human microbiota. Science, 2015, 349(6246): 1254766.
45. Guerra L, Guidi R, Frisan T. Do bacterial genotoxins contribute to chronic inflammation, genomic instability and tumor progression? FEBS J, 2011, 278(23): 4577-4588.
46. Lopetuso LR, Severgnini M, Pecere S, et al. Esophageal microbiome signature in patients with Barrett's esophagus and esophageal adenocarcinoma. PLoS One, 2020, 15(5): e0231789.
47. Duncan SH, Hold GL, Barcenilla A, et al. Roseburia intestinalis sp. nov. , a novel saccharolytic, butyrate-producing bacterium from human faeces. Int J Syst Evol Microbiol, 2002, 52(Pt 5): 1615-1620.
48. Cheung MK, Yue GGL, Lauw S, et al. Alterations in gut microbiota of esophageal squamous cell carcinoma patients. J Gastroenterol Hepatol, 2022, 37(10): 1919-1927.
49. Zhang T, Zhang W, Feng C, et al. Stronger gut microbiome modulatory effects by postbiotics than probiotics in a mouse colitis model. NPJ Sci Food, 2022, 6(1): 53.
50. Deng Y, Tang D, Hou P, et al. Dysbiosis of gut microbiota in patients with esophageal cancer. Microb Pathog, 2021, 150: 104709.
51. Nie X, Geng Z, Liu J, et al. Chinese herbal medicine anticancer cocktail soup activates immune cells to kill colon cancer cells by regulating the gut microbiota-Th17 axis. Front Pharmacol, 2022, 13: 963638.
52. Pan F, Zhang LL, Luo HJ, et al. Dietary riboflavin deficiency induces ariboflavinosis and esophageal epithelial atrophy in association with modification of gut microbiota in rats. Eur J Nutr, 2021, 60(2): 807-820.
53. Zhang X, Li C, Cao W, et al. Alterations of gastric microbiota in gastric cancer and precancerous stages. Front Cell Infect Microbiol, 2021, 11: 559148.
54. Jeong JY, Kim TB, Kim J, et al. Diversity in the extracellular vesicle-derived microbiome of tissues according to tumor progression in pancreatic cancer. Cancers (Basel), 2020, 12(9): 2346.
55. Hao X, Zhang J, Shang X, et al. Exercise modifies the disease-relevant gut microbial shifts in post-traumatic osteoarthritis rats. Bone Joint Res, 2022, 11(4): 214-225.
56. Garcia-Beltran C, Malpique R, Carbonetto B, et al. Gut microbiota in adolescent girls with polycystic ovary syndrome: Effects of randomized treatments. Pediatr Obes, 2021, 16(4): e12734.
57. Wang Q, Wang Q, Zhao L, et al. Blood bacterial 16S rRNA gene alterations in women with polycystic ovary syndrome. Front Endocrinol (Lausanne), 2022, 13: 814520.
58. Zhang M, Lv Y, Hou S, et al. Differential mucosal microbiome profiles across stages of human colorectal cancer. Life (Basel), 2021, 11(8): 831.
59. 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.
60. Liu M, Devlin JC, Hu J, et al. Microbial genetic and transcriptional contributions to oxalate degradation by the gut microbiota in health and disease. Elife, 2021, 10: e63642.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Latest ArticlesCausal relationship between intestinal flora and esophageal cancer: A Mendelian randomization analysis

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