Research progress of effect of gut microbiota on non-small cell lung cancer_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

WANG Mengmeng ¹ , CHEN Yong ¹ , WANG Xiaolin ² ,  SHU Yusheng ²

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

Corresponding author：

SHU Yusheng, Email: 18051061999@yzu.edu.cn

Keywords：

Gut microbiota; non-small cell lung cancer; biomarkers; nosogenesis; therapeutic targets; review

DOI：

10.7507/1007-4848.202204087

Video：

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Abstract Full text Figures/Tables Video References Cited by

The human gut microbiota regulates many host pathophysiological processes including metabolic, inflammatory, immune and cellular responses. In recent years, the incidence and mortality of lung cancer have increased rapidly, which is one of the biggest challenges in the field of cancer treatment today, especially in non-small cell lung cancer. Animal models and clinical studies have found that the gut microbiota of non-small cell lung cancer patients is significantly changed compared with the healthy people. The gut microbiota and metabolites can not only play a pro-cancer or tumor suppressor role by regulating immune, inflammatory responses and so on, but also be related with radiotherapy and chemotherapy of non-small cell lung cancer and the resistance of immunotherapy. Therefore, gut microbiota and related metabolites can be both potential markers for early diagnosis and prognosis in patients with non-small cell lung cancer and novel therapeutic targets for targeted drugs. This study will review the latest research progress of effect of gut microbiota on non-small cell lung cancer, and provide a new diagnosis and treatment ideas for non-small cell lung cancer.

Citation： WANG Mengmeng, CHEN Yong, WANG Xiaolin, SHU Yusheng. Research progress of effect of gut microbiota on non-small cell lung cancer. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2023, 30(5): 753-760. doi: 10.7507/1007-4848.202204087 Copy

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2.	Zhuang H, Cheng L, Wang Y, et al. Dysbiosis of the gut microbiome in lung cancer. Front Cell Infect Microbiol, 2019, 9: 112.
3.	The Lancet. Lung cancer: Some progress, but still a lot more to do. Lancet, 2019, 394(10212): 1880.
4.	Gao S, Li N, Wang S, et al. Lung cancer in People's Republic of China. J Thorac Oncol, 2020, 15(10): 1567-1576.
5.	Thai AA, Solomon BJ, Sequist LV, et al. Lung cancer. Lancet, 2021, 398(10299): 535-554.
6.	Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2021, 71(3): 209-249.
7.	Nicholson AG, Tsao MS, Beasley MB, et al. The 2021 WHO classification of lung tumors: Impact of advances since 2015. J Thorac Oncol, 2022, 17(3): 362-387.
8.	Szalontai K, Gémes N, Furák J, et al. Chronic obstructive pulmonary disease: Epidemiology, biomarkers, and paving the way to lung cancer. J Clin Med, 2021, 10(13): 2889.
9.	Zappa C, Mousa SA. Non-small cell lung cancer: Current treatment and future advances. Transl Lung Cancer Res, 2016, 5(3): 288-300.
10.	Barta JA, Powell CA, Wisnivesky JP. Global epidemiology of lung cancer. Ann Glob Health, 2019, 85(1): 8.
11.	Stapelfeld C, Dammann C, Maser E. Sex-specificity in lung cancer risk. Int J Cancer, 2020, 146(9): 2376-2382.
12.	Wang M, Herbst RS, Boshoff C. Toward personalized treatment approaches for non-small-cell lung cancer. Nat Med, 2021, 27(8): 1345-1356.
13.	Kang J, Zhang C, Zhong WZ. Neoadjuvant immunotherapy for non-small cell lung cancer: State of the art. Cancer Commun (Lond), 2021, 41(4): 287-302.
14.	Doroshow DB, Sanmamed MF, Hastings K, et al. Immunotherapy in non-small cell lung cancer: Facts and hopes. Clin Cancer Res, 2019, 25(15): 4592-4602.
15.	Hong T, Wang R, Wang X, et al. Interplay between the intestinal microbiota and acute graft-versus-host disease: Experimental evidence and clinical significance. Front Immunol, 2021, 12: 644982.
16.	Bhatt AP, Redinbo MR, Bultman SJ. The role of the microbiome in cancer development and therapy. CA Cancer J Clin, 2017, 67(4): 326-344.
17.	Bingula R, Filaire M, Radosevic-Robin N, et al. Desired turbulence? Gut-lung axis, immunity, and lung cancer. J Oncol, 2017, 2017: 5035371.
18.	Kho ZY, Lal SK. The human gut microbiome—A potential controller of wellness and disease. Front Microbiol, 2018, 9: 1835.
19.	Cani PD. Human gut microbiome: Hopes, threats and promises. Gut, 2018, 67(9): 1716-1725.
20.	Zheng Y, Fang Z, Xue Y, et al. Specific gut microbiome signature predicts the early-stage lung cancer. Gut Microbes, 2020, 11(4): 1030-1042.
21.	Nagasaka M, Sexton R, Alhasan R, et al. Gut microbiome and response to checkpoint inhibitors in non-small cell lung cancer—A review. Crit Rev Oncol Hematol, 2020, 145: 102841.
22.	Lim MY, Hong S, Hwang KH, et al. Diagnostic and prognostic potential of the oral and gut microbiome for lung adenocarcinoma. Clin Transl Med, 2021, 11(9): e508.
23.	Gui QF, Lu HF, Zhang CX, et al. Well-balanced commensal microbiota contributes to anti-cancer response in a lung cancer mouse model. Genet Mol Res, 2015, 14(2): 5642-5651.
24.	Zhang WQ, Zhao SK, Luo JW, et al. Alterations of fecal bacterial communities in patients with lung cancer. Am J Transl Res, 2018, 10(10): 3171-3185.
25.	Heshiki Y, Vazquez-Uribe R, Li J, et al. Predictable modulation of cancer treatment outcomes by the gut microbiota. Microbiome, 2020, 8(1): 28.
26.	Hakozaki T, Richard C, Elkrief A, et al. The gut microbiome associates with immune checkpoint inhibition outcomes in patients with advanced non-small cell lung cancer. Cancer Immunol Res, 2020, 8(10): 1243-1250.
27.	Huang J, Liu D, Wang Y, et al. Ginseng polysaccharides alter the gut microbiota and kynurenine/tryptophan ratio, potentiating the antitumour effect of antiprogrammed cell death 1/programmed cell death ligand 1 (anti-PD-1/PD-L1) immunotherapy. Gut, 2022, 71(4): 734-745.
28.	Altorki NK, Markowitz GJ, Gao D, et al. The lung microenvironment: An important regulator of tumour growth and metastasis. Nat Rev Cancer, 2019, 19(1): 9-31.
29.	Yang Q, Ouyang J, Sun F, et al. Short-chain fatty acids: A soldier fighting against inflammation and protecting from tumorigenesis in people with diabetes. Front Immunol, 2020, 11: 590685.
30.	Vernocchi P, Gili T, Conte F, et al. Network analysis of gut microbiome and metabolome to discover microbiota-linked biomarkers in patients affected by non-small cell lung cancer. Int J Mol Sci, 2020, 21(22): 8730.
31.	Xiao X, Cao Y, Chen H. Profiling and characterization of microRNAs responding to sodium butyrate treatment in A549 cells. J Cell Biochem, 2018, 119(4): 3563-3573.
32.	Kim K, Kwon O, Ryu TY, et al. Propionate of a microbiota metabolite induces cell apoptosis and cell cycle arrest in lung cancer. Mol Med Rep, 2019, 20(2): 1569-1574.
33.	Liu X, Chen B, You W, et al. The membrane bile acid receptor TGR5 drives cell growth and migration via activation of the JAK2/STAT3 signaling pathway in non-small cell lung cancer. Cancer Lett, 2018, 412: 194-207.
34.	Liu CH, Chen Z, Chen K, et al. Lipopolysaccharide-mediated chronic inflammation promotes tobacco carcinogen-induced lung cancer and determines the efficacy of immunotherapy. Cancer Res, 2021, 81(1): 144-157.
35.	Zhao J, Wang X, Mi Z, et al. STAT3/miR-135b/NF-κB axis confers aggressiveness and unfavorable prognosis in non-small-cell lung cancer. Cell Death Dis, 2021, 12(5): 493.
36.	Liu KT, Yeh IJ, Chou SK, et al. Regulatory mechanism of fatty acid-CoA metabolic enzymes under endoplasmic reticulum stress in lung cancer. Oncol Rep, 2018, 40(5): 2674-2682.
37.	Qu Z, Zhang L, Hou R, et al. Exposure to a mixture of cigarette smoke carcinogens disturbs gut microbiota and influences metabolic homeostasis in A/J mice. Chem Biol Interact, 2021, 344: 109496.
38.	Zhao Y, Liu Y, Li S, et al. Role of lung and gut microbiota on lung cancer pathogenesis. J Cancer Res Clin Oncol, 2021, 147(8): 2177-2186.
39.	Ramakrishna C, Kujawski M, Chu H, et al. Bacteroides fragilis polysaccharide A induces IL-10 secreting B and T cells that prevent viral encephalitis. Nat Commun, 2019, 10(1): 2153.
40.	Ladinsky MS, Araujo LP, Zhang X, et al. Endocytosis of commensal antigens by intestinal epithelial cells regulates mucosal T cell homeostasis. Science, 2019, 363(6431): eaat4042.
41.	Khosravi N, Caetano MS, Cumpian AM, et al. IL22 promotes kras-mutant lung cancer by induction of a protumor immune response and protection of stemness properties. Cancer Immunol Res, 2018, 6(7): 788-797.
42.	Jin C, Lagoudas GK, Zhao C, et al. Commensal microbiota promote lung cancer development via γδ T cells. Cell, 2019, 176(5): 998-1013.
43.	Thibeault C, Suttorp N, Opitz B. The microbiota in pneumonia: From protection to predisposition. Sci Transl Med, 2021, 13(576): eaba0501.
44.	Wypych TP, Pattaroni C, Perdijk O, et al. Microbial metabolism of L-tyrosine protects against allergic airway inflammation. Nat Immunol, 2021, 22(3): 279-286.
45.	Sarate PJ, Srutkova D, Geissler N, et al. Pre- and neonatal imprinting on immunological homeostasis and epithelial barrier integrity by escherichia coli nissle 1917 prevents allergic poly-sensitization in mice. Front Immunol, 2021, 11: 612775.
46.	Guzior DV, Quinn RA. Review: Microbial transformations of human bile acids. Microbiome, 2021, 9(1): 140.
47.	Dalal N, Jalandra R, Bayal N, et al. Gut microbiota-derived metabolites in CRC progression and causation. J Cancer Res Clin Oncol, 2021, 147(11): 3141-3155.
48.	Wang RP, Wang XH, Li ZM, et al. Changes in serum inflammatory factors, adiponectin, intestinal flora and immunity in patients with non-small cell lung cancer. Eur Rev Med Pharmacol Sci, 2020, 24(20): 10566-10572.
49.	Cvetkovic L, Régis C, Richard C, et al. Physiologic colonic uptake of 18 F-FDG on PET/CT is associated with clinical response and gut microbiome composition in patients with advanced non-small cell lung cancer treated with immune checkpoint inhibitors. Eur J Nucl Med Mol Imaging, 2021, 48(5): 1550-1559.
50.	Shaikh FY, Gills JJ, Sears CL. Impact of the microbiome on checkpoint inhibitor treatment in patients with non-small cell lung cancer and melanoma. EBioMedicine, 2019, 48: 642-647.
51.	Topalian SL, Hodi FS, Brahmer JR, et al. Five-year survival and correlates among patients with advanced melanoma, renal cell carcinoma, or non-small cell lung cancer treated with nivolumab. JAMA Oncol, 2019, 5(10): 1411-1420.
52.	Socinski MA, Jotte RM, Cappuzzo F, et al. Atezolizumab for first-line treatment of metastatic nonsquamous NSCLC. N Engl J Med, 2018, 378(24): 2288-2301.
53.	Pakkala S, Ramalingam SS. Personalized therapy for lung cancer: Striking a moving target. JCI Insight, 2018, 3(15): e120858.
54.	Song P, Yang D, Wang H, et al. Relationship between intestinal flora structure and metabolite analysis and immunotherapy efficacy in Chinese NSCLC patients. Thorac Cancer, 2020, 11(6): 1621-1632.
55.	Routy B, Gopalakrishnan V, Daillère R, et al. The gut microbiota influences anticancer immunosurveillance and general health. Nat Rev Clin Oncol, 2018, 15(6): 382-396.
56.	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.
57.	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.
58.	Gori S, Inno A, Belluomini L, et al. Gut microbiota and cancer: How gut microbiota modulates activity, efficacy and toxicity of antitumoral therapy. Crit Rev Oncol Hematol, 2019, 143: 139-147.
59.	Daillère R, Vétizou M, Waldschmitt N, et al. Enterococcus hirae and barnesiella intestinihominis facilitate cyclophosphamide-induced therapeutic immunomodulatory effects. Immunity, 2016, 45(4): 931-943.
60.	Zhang M, Liu D, Zhou H, et al. Intestinal flora characteristics of advanced non-small cell lung cancer in China and their role in chemotherapy based on metagenomics: A prospective exploratory cohort study. Thorac Cancer, 2021, 12(24): 3293-3303.
61.	Badgeley A, Anwar H, Modi K, et al. Effect of probiotics and gut microbiota on anti-cancer drugs: Mechanistic perspectives. Biochim Biophys Acta Rev Cancer, 2021, 1875(1): 188494.
62.	Qiu Y, Zhang J, Ji R, et al. Preventative effects of selenium-enriched Bifidobacterium longum on irinotecan-induced small intestinal mucositis in mice. Benef Microbes, 2019, 10(5): 569-577.
63.	Hsiao YP, Chen HL, Tsai JN, et al. Administration of lactobacillus reuteri combined with clostridium butyricum attenuates cisplatin-induced renal damage by gut microbiota reconstitution, increasing butyric acid production, and suppressing renal inflammation. Nutrients, 2021, 13(8): 2792.
64.	Yang WC, Hsu FM, Yang PC. Precision radiotherapy for non-small cell lung cancer. J Biomed Sci, 2020, 27(1): 82.
65.	Vinod SK, Hau E. Radiotherapy treatment for lung cancer: Current status and future directions. Respirology, 2020, 25 Suppl 2: 61-71.
66.	Gerassy-Vainberg S, Blatt A, Danin-Poleg Y, et al. Radiation induces proinflammatory dysbiosis: Transmission of inflammatory susceptibility by host cytokine induction. Gut, 2018, 67(1): 97-107.
67.	Sokol H, Adolph TE. The microbiota: An underestimated actor in radiation-induced lesions? Gut, 2018, 67(1): 1-2.
68.	Yang J, Wu Z, Chen Y, et al. Pre-treatment with bifidobacterium infantis and its specific antibodies enhance targeted radiosensitization in a murine model for lung cancer. J Cancer Res Clin Oncol, 2021, 147(2): 411-422.
69.	Nie X, Li L, Yi M, et al. The intestinal microbiota plays as a protective regulator against radiation pneumonitis. Radiat Res, 2020, 194(1): 52-60.

1. Xia Q, Chen G, Ren Y, et al. Investigating efficacy of "microbiota modulation of the gut-lung axis" combined with chemotherapy in patients with advanced NSCLC: Study protocol for a multicenter, prospective, double blind, placebo controlled, randomized trial. BMC Cancer, 2021, 21(1): 721.
2. Zhuang H, Cheng L, Wang Y, et al. Dysbiosis of the gut microbiome in lung cancer. Front Cell Infect Microbiol, 2019, 9: 112.
3. The Lancet. Lung cancer: Some progress, but still a lot more to do. Lancet, 2019, 394(10212): 1880.
4. Gao S, Li N, Wang S, et al. Lung cancer in People's Republic of China. J Thorac Oncol, 2020, 15(10): 1567-1576.
5. Thai AA, Solomon BJ, Sequist LV, et al. Lung cancer. Lancet, 2021, 398(10299): 535-554.
6. Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2021, 71(3): 209-249.
7. Nicholson AG, Tsao MS, Beasley MB, et al. The 2021 WHO classification of lung tumors: Impact of advances since 2015. J Thorac Oncol, 2022, 17(3): 362-387.
8. Szalontai K, Gémes N, Furák J, et al. Chronic obstructive pulmonary disease: Epidemiology, biomarkers, and paving the way to lung cancer. J Clin Med, 2021, 10(13): 2889.
9. Zappa C, Mousa SA. Non-small cell lung cancer: Current treatment and future advances. Transl Lung Cancer Res, 2016, 5(3): 288-300.
10. Barta JA, Powell CA, Wisnivesky JP. Global epidemiology of lung cancer. Ann Glob Health, 2019, 85(1): 8.
11. Stapelfeld C, Dammann C, Maser E. Sex-specificity in lung cancer risk. Int J Cancer, 2020, 146(9): 2376-2382.
12. Wang M, Herbst RS, Boshoff C. Toward personalized treatment approaches for non-small-cell lung cancer. Nat Med, 2021, 27(8): 1345-1356.
13. Kang J, Zhang C, Zhong WZ. Neoadjuvant immunotherapy for non-small cell lung cancer: State of the art. Cancer Commun (Lond), 2021, 41(4): 287-302.
14. Doroshow DB, Sanmamed MF, Hastings K, et al. Immunotherapy in non-small cell lung cancer: Facts and hopes. Clin Cancer Res, 2019, 25(15): 4592-4602.
15. Hong T, Wang R, Wang X, et al. Interplay between the intestinal microbiota and acute graft-versus-host disease: Experimental evidence and clinical significance. Front Immunol, 2021, 12: 644982.
16. Bhatt AP, Redinbo MR, Bultman SJ. The role of the microbiome in cancer development and therapy. CA Cancer J Clin, 2017, 67(4): 326-344.
17. Bingula R, Filaire M, Radosevic-Robin N, et al. Desired turbulence? Gut-lung axis, immunity, and lung cancer. J Oncol, 2017, 2017: 5035371.
18. Kho ZY, Lal SK. The human gut microbiome—A potential controller of wellness and disease. Front Microbiol, 2018, 9: 1835.
19. Cani PD. Human gut microbiome: Hopes, threats and promises. Gut, 2018, 67(9): 1716-1725.
20. Zheng Y, Fang Z, Xue Y, et al. Specific gut microbiome signature predicts the early-stage lung cancer. Gut Microbes, 2020, 11(4): 1030-1042.
21. Nagasaka M, Sexton R, Alhasan R, et al. Gut microbiome and response to checkpoint inhibitors in non-small cell lung cancer—A review. Crit Rev Oncol Hematol, 2020, 145: 102841.
22. Lim MY, Hong S, Hwang KH, et al. Diagnostic and prognostic potential of the oral and gut microbiome for lung adenocarcinoma. Clin Transl Med, 2021, 11(9): e508.
23. Gui QF, Lu HF, Zhang CX, et al. Well-balanced commensal microbiota contributes to anti-cancer response in a lung cancer mouse model. Genet Mol Res, 2015, 14(2): 5642-5651.
24. Zhang WQ, Zhao SK, Luo JW, et al. Alterations of fecal bacterial communities in patients with lung cancer. Am J Transl Res, 2018, 10(10): 3171-3185.
25. Heshiki Y, Vazquez-Uribe R, Li J, et al. Predictable modulation of cancer treatment outcomes by the gut microbiota. Microbiome, 2020, 8(1): 28.
26. Hakozaki T, Richard C, Elkrief A, et al. The gut microbiome associates with immune checkpoint inhibition outcomes in patients with advanced non-small cell lung cancer. Cancer Immunol Res, 2020, 8(10): 1243-1250.
27. Huang J, Liu D, Wang Y, et al. Ginseng polysaccharides alter the gut microbiota and kynurenine/tryptophan ratio, potentiating the antitumour effect of antiprogrammed cell death 1/programmed cell death ligand 1 (anti-PD-1/PD-L1) immunotherapy. Gut, 2022, 71(4): 734-745.
28. Altorki NK, Markowitz GJ, Gao D, et al. The lung microenvironment: An important regulator of tumour growth and metastasis. Nat Rev Cancer, 2019, 19(1): 9-31.
29. Yang Q, Ouyang J, Sun F, et al. Short-chain fatty acids: A soldier fighting against inflammation and protecting from tumorigenesis in people with diabetes. Front Immunol, 2020, 11: 590685.
30. Vernocchi P, Gili T, Conte F, et al. Network analysis of gut microbiome and metabolome to discover microbiota-linked biomarkers in patients affected by non-small cell lung cancer. Int J Mol Sci, 2020, 21(22): 8730.
31. Xiao X, Cao Y, Chen H. Profiling and characterization of microRNAs responding to sodium butyrate treatment in A549 cells. J Cell Biochem, 2018, 119(4): 3563-3573.
32. Kim K, Kwon O, Ryu TY, et al. Propionate of a microbiota metabolite induces cell apoptosis and cell cycle arrest in lung cancer. Mol Med Rep, 2019, 20(2): 1569-1574.
33. Liu X, Chen B, You W, et al. The membrane bile acid receptor TGR5 drives cell growth and migration via activation of the JAK2/STAT3 signaling pathway in non-small cell lung cancer. Cancer Lett, 2018, 412: 194-207.
34. Liu CH, Chen Z, Chen K, et al. Lipopolysaccharide-mediated chronic inflammation promotes tobacco carcinogen-induced lung cancer and determines the efficacy of immunotherapy. Cancer Res, 2021, 81(1): 144-157.
35. Zhao J, Wang X, Mi Z, et al. STAT3/miR-135b/NF-κB axis confers aggressiveness and unfavorable prognosis in non-small-cell lung cancer. Cell Death Dis, 2021, 12(5): 493.
36. Liu KT, Yeh IJ, Chou SK, et al. Regulatory mechanism of fatty acid-CoA metabolic enzymes under endoplasmic reticulum stress in lung cancer. Oncol Rep, 2018, 40(5): 2674-2682.
37. Qu Z, Zhang L, Hou R, et al. Exposure to a mixture of cigarette smoke carcinogens disturbs gut microbiota and influences metabolic homeostasis in A/J mice. Chem Biol Interact, 2021, 344: 109496.
38. Zhao Y, Liu Y, Li S, et al. Role of lung and gut microbiota on lung cancer pathogenesis. J Cancer Res Clin Oncol, 2021, 147(8): 2177-2186.
39. Ramakrishna C, Kujawski M, Chu H, et al. Bacteroides fragilis polysaccharide A induces IL-10 secreting B and T cells that prevent viral encephalitis. Nat Commun, 2019, 10(1): 2153.
40. Ladinsky MS, Araujo LP, Zhang X, et al. Endocytosis of commensal antigens by intestinal epithelial cells regulates mucosal T cell homeostasis. Science, 2019, 363(6431): eaat4042.
41. Khosravi N, Caetano MS, Cumpian AM, et al. IL22 promotes kras-mutant lung cancer by induction of a protumor immune response and protection of stemness properties. Cancer Immunol Res, 2018, 6(7): 788-797.
42. Jin C, Lagoudas GK, Zhao C, et al. Commensal microbiota promote lung cancer development via γδ T cells. Cell, 2019, 176(5): 998-1013.
43. Thibeault C, Suttorp N, Opitz B. The microbiota in pneumonia: From protection to predisposition. Sci Transl Med, 2021, 13(576): eaba0501.
44. Wypych TP, Pattaroni C, Perdijk O, et al. Microbial metabolism of L-tyrosine protects against allergic airway inflammation. Nat Immunol, 2021, 22(3): 279-286.
45. Sarate PJ, Srutkova D, Geissler N, et al. Pre- and neonatal imprinting on immunological homeostasis and epithelial barrier integrity by escherichia coli nissle 1917 prevents allergic poly-sensitization in mice. Front Immunol, 2021, 11: 612775.
46. Guzior DV, Quinn RA. Review: Microbial transformations of human bile acids. Microbiome, 2021, 9(1): 140.
47. Dalal N, Jalandra R, Bayal N, et al. Gut microbiota-derived metabolites in CRC progression and causation. J Cancer Res Clin Oncol, 2021, 147(11): 3141-3155.
48. Wang RP, Wang XH, Li ZM, et al. Changes in serum inflammatory factors, adiponectin, intestinal flora and immunity in patients with non-small cell lung cancer. Eur Rev Med Pharmacol Sci, 2020, 24(20): 10566-10572.
49. Cvetkovic L, Régis C, Richard C, et al. Physiologic colonic uptake of 18 F-FDG on PET/CT is associated with clinical response and gut microbiome composition in patients with advanced non-small cell lung cancer treated with immune checkpoint inhibitors. Eur J Nucl Med Mol Imaging, 2021, 48(5): 1550-1559.
50. Shaikh FY, Gills JJ, Sears CL. Impact of the microbiome on checkpoint inhibitor treatment in patients with non-small cell lung cancer and melanoma. EBioMedicine, 2019, 48: 642-647.
51. Topalian SL, Hodi FS, Brahmer JR, et al. Five-year survival and correlates among patients with advanced melanoma, renal cell carcinoma, or non-small cell lung cancer treated with nivolumab. JAMA Oncol, 2019, 5(10): 1411-1420.
52. Socinski MA, Jotte RM, Cappuzzo F, et al. Atezolizumab for first-line treatment of metastatic nonsquamous NSCLC. N Engl J Med, 2018, 378(24): 2288-2301.
53. Pakkala S, Ramalingam SS. Personalized therapy for lung cancer: Striking a moving target. JCI Insight, 2018, 3(15): e120858.
54. Song P, Yang D, Wang H, et al. Relationship between intestinal flora structure and metabolite analysis and immunotherapy efficacy in Chinese NSCLC patients. Thorac Cancer, 2020, 11(6): 1621-1632.
55. Routy B, Gopalakrishnan V, Daillère R, et al. The gut microbiota influences anticancer immunosurveillance and general health. Nat Rev Clin Oncol, 2018, 15(6): 382-396.
56. 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.
57. 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.
58. Gori S, Inno A, Belluomini L, et al. Gut microbiota and cancer: How gut microbiota modulates activity, efficacy and toxicity of antitumoral therapy. Crit Rev Oncol Hematol, 2019, 143: 139-147.
59. Daillère R, Vétizou M, Waldschmitt N, et al. Enterococcus hirae and barnesiella intestinihominis facilitate cyclophosphamide-induced therapeutic immunomodulatory effects. Immunity, 2016, 45(4): 931-943.
60. Zhang M, Liu D, Zhou H, et al. Intestinal flora characteristics of advanced non-small cell lung cancer in China and their role in chemotherapy based on metagenomics: A prospective exploratory cohort study. Thorac Cancer, 2021, 12(24): 3293-3303.
61. Badgeley A, Anwar H, Modi K, et al. Effect of probiotics and gut microbiota on anti-cancer drugs: Mechanistic perspectives. Biochim Biophys Acta Rev Cancer, 2021, 1875(1): 188494.
62. Qiu Y, Zhang J, Ji R, et al. Preventative effects of selenium-enriched Bifidobacterium longum on irinotecan-induced small intestinal mucositis in mice. Benef Microbes, 2019, 10(5): 569-577.
63. Hsiao YP, Chen HL, Tsai JN, et al. Administration of lactobacillus reuteri combined with clostridium butyricum attenuates cisplatin-induced renal damage by gut microbiota reconstitution, increasing butyric acid production, and suppressing renal inflammation. Nutrients, 2021, 13(8): 2792.
64. Yang WC, Hsu FM, Yang PC. Precision radiotherapy for non-small cell lung cancer. J Biomed Sci, 2020, 27(1): 82.
65. Vinod SK, Hau E. Radiotherapy treatment for lung cancer: Current status and future directions. Respirology, 2020, 25 Suppl 2: 61-71.
66. Gerassy-Vainberg S, Blatt A, Danin-Poleg Y, et al. Radiation induces proinflammatory dysbiosis: Transmission of inflammatory susceptibility by host cytokine induction. Gut, 2018, 67(1): 97-107.
67. Sokol H, Adolph TE. The microbiota: An underestimated actor in radiation-induced lesions? Gut, 2018, 67(1): 1-2.
68. Yang J, Wu Z, Chen Y, et al. Pre-treatment with bifidobacterium infantis and its specific antibodies enhance targeted radiosensitization in a murine model for lung cancer. J Cancer Res Clin Oncol, 2021, 147(2): 411-422.
69. Nie X, Li L, Yi M, et al. The intestinal microbiota plays as a protective regulator against radiation pneumonitis. Radiat Res, 2020, 194(1): 52-60.

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