Efficacy of antibiotics on the outcomes of patients with non-small cell lung cancer treated with immune checkpoint inhibitors: a meta-analysis_Chinese Journal of Evidence-Based Medicine

Authors：

LIN Guihua ^1,2 , YAN Lidong ^1,2 , ZHANG Ying ^1,2 ,  LIN Qunying ^1,2

1. The Third Clinical Medical College, Fujian Medical University, Fuzhou 350004, P. R. China;
2. Department of Pulmonary and Critical Care Medicine, Affiliated Hospital of Putian University, Putian 351100, P. R. China;

Corresponding author：

LIN Qunying, Email: linqyin@126.com

Keywords：

Non-small cell lung cancer; Immunotherapy; Antibiotic; Meta-analysis; Systematic review; Cohort study

DOI：

10.7507/1672-2531.202109104

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To systematically review the efficacy of antibiotics on the outcomes of patients with non-small cell lung cancer (NSCLC) treated with immune checkpoint inhibitors. Methods PubMed, EMbase, Web of Science, The Cochrane Library, CNKI, WanFang Data, VIP and CBM databases were electronically searched to collect cohort studies on efficacy of antibiotics on the outcomes of patients with NSCLC treated with immune checkpoint inhibitors from inception to August 1^st, 2021. Two reviewers independently screened literature, extracted data, and evaluated the risk of bias of the included studies. Meta-analysis was then performed by using RevMan 5.3 software. Results A total of 27 cohort studies involving 7 087 patients were included. The results of meta-analysis showed that antibiotic use was associated with poor overall survival (OS) (HR=2.04, 95%CI 1.68 to 2.49, P<0.000 01) and progression free survival (PFS) (HR=1.63, 95%CI 1.35 to 1.99, P<0.000 01). Conclusion Current evidence shows that antibiotic use is associated with poor OS and PFS. Due to the limited quality and quantity of the included studies, more high-quality studies are needed to verify the above conclusion.

Citation： LIN Guihua, YAN Lidong, ZHANG Ying, LIN Qunying. Efficacy of antibiotics on the outcomes of patients with non-small cell lung cancer treated with immune checkpoint inhibitors: a meta-analysis. Chinese Journal of Evidence-Based Medicine, 2022, 22(3): 309-315. doi: 10.7507/1672-2531.202109104 Copy

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2.	Arbour KC, Mezquita L, Long N, et al. Impact of baseline steroids on efficacy of programmed cell death-1 and programmed death-ligand 1 blockade in patients with non-small-cell lung cancer. J Clin Oncol, 2018, 36(28): 2872-2878.
3.	Drakaki A, Luhn P, Wakelee H, et al. Association of systemic corticosteroids with overall survival in patients receiving cancer immunotherapy for advanced melanoma, non-small cell lung cancer or urothelial cancer in routine clinical practice. Ann Oncol, 2019, 30(1): i16-i17.
4.	Martínez Bernal G, Mezquita L, Auclin E, et al. Baseline corticosteroids (CS) could be associated with absence of benefit to immune checkpoint inhibitors (ICI) in advanced non-small cell lung cancer (NSCLC) patients. Ann Oncol, 2017, 28: v472.
5.	Ricciuti B, Dahlberg SE, Adeni A, et al. Immune checkpoint inhibitor outcomes for patients with non-small-cell lung cancer receiving baseline corticosteroids for palliative versus nonpalliative indications. J Clin Oncol, 2019, 37(22): 1927-1934.
6.	Skribek M, Rounis K, Afshar S, et al. Effect of corticosteroids on the outcome of patients with advanced non-small cell lung cancer treated with immune-checkpoint inhibitors. Eur J Cancer, 2021, 145: 245-254.
7.	Buti S, Bersanelli M, Perrone F, et al. Effect of concomitant medications with immune-modulatory properties on the outcomes of patients with advanced cancer treated with immune checkpoint inhibitors: development and validation of a novel prognostic index. Eur J Cancer, 2021, 142: 18-28.
8.	Kostine M, Mauric E, Barnetche T, et al. Commonly used drugs in rheumatology may alter anti-tumoral response to immune checkpoint inhibitors. Ann Rheum Dis, 2019, 78: 251.
9.	Trabolsi A, Winter M, Rodriguez E. Proton pump inhibitors and response to immune check-point inhibitors: single center study. J Clin Oncol, 2019, 37(15_suppl): e14092.
10.	Takada K, Shimokawa M, Takamori S, et al. Clinical impact of probiotics on the efficacy of anti-PD-1 monotherapy in patients with nonsmall cell lung cancer: a multicenter retrospective survival analysis study with inverse probability of treatment weighting. Int J Cancer, 2021, 149(2): 473-482.
11.	Tomita Y, Ikeda T, Sakata S, et al. Association of probiotic clostridium butyricum therapy with survival and response to immune checkpoint blockade in patients with lung cancer. Cancer Immunol Res, 2020, 8(10): 1236-1242.
12.	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.
13.	McQuade JL, Daniel CR, Helmink BA, et al. Modulating the microbiome to improve therapeutic response in cancer. Lancet Oncol, 2019, 20(2): e77-e91.
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15.	Gopalakrishnan V, Helmink BA, Spencer CN, et al. The influence of the gut microbiome on cancer, immunity, and cancer immunotherapy. Cancer Cell, 2018, 33(4): 570-580.
16.	Li W, Deng Y, Chu Q, et al. Gut microbiome and cancer immunotherapy. Cancer Lett, 2019, 447: 41-47.
17.	Routy B, Le Chatelier E, Derosa L, et al. Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science, 2018, 359(6371): 91-97.
18.	Blaser MJ. Antibiotic use and its consequences for the normal microbiome. Science, 2016, 352(6285): 544-545.
19.	Jernberg C, Löfmark S, Edlund C, et al. Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. ISME J, 2007, 1(1): 56-66.
20.	Schwabe RF, Jobin C. The microbiome and cancer. Nat Rev Cancer, 2013, 13(11): 800-812.
21.	Castello A, Rossi S, Toschi L, et al. Impact of antibiotic therapy and metabolic parameters in non-small cell lung cancer patients receiving checkpoint inhibitors. J Clin Med, 2021, 10(6): 1251.
22.	Derosa L, Hellmann MD, Spaziano M, et al. Negative association of antibiotics on clinical activity of immune checkpoint inhibitors in patients with advanced renal cell and non-small-cell lung cancer. Ann Oncol, 2018, 29(6): 1437-1444.
23.	Kim H, Lee JE, Hong SH, et al. The effect of antibiotics on the clinical outcomes of patients with solid cancers undergoing immune checkpoint inhibitor treatment: a retrospective study. BMC Cancer, 2019, 19(1): 1100.
24.	Hossain T, Htut S, Pathmanathan S, et a1. Do antibiotics reduce survival in patients with advanced non-small cell lung cancer treated with immunotherapy? Asia-Pac J Clin Onco, 2020, 16(Suppl 2): 37-38.
25.	Kulkarni A, Patel M, Wang Y, et a1. Antibiotic use and clinical outcomes of PD-1 antagonists in advanced non-small cell lung cancers. J Immuno Ther Cancer, 2018, 6(Suppl 1): 573.
26.	Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 2010, 25(9): 603-605.
27.	Ahmed Y, Calvert P. Antibiotics and response to immunotherapy: real-world experience. J ImmunoTher Cancer, 2020, 8(Suppl 3): A435-A436.
28.	Bagley SJ, Dhopeshwarkar N, Narayan V, et al. Impact of antibiotics (ABX) on overall survival (OS) in patients (pts) with advanced non-small-cell lung cancer (aNSCLC) and melanoma (aMel) treated with first-line immune checkpoint inhibition (ICI). J Clin Oncol, 2019, 37(15_suppl): e20643.
29.	Barrón F, Arrieta OG, Cardona AF, et al. EP1. 04-45 relevance of antibiotic use on clinical activity of immune checkpoint inhibitors in Hispanic patients with advanced NSCLC (CLICAP-ABs). J Thorac Oncol, 2019, 14(10): S972.
30.	Castro BA, Tourís LM, Álvarez SR, et al. Association of antibiotics and proton pump inhibitors on clinical activity of firstline pembrolizumab for non-small cell lung cancer: 2 years of real world data. Eur J Hosp Pharm, 2021, 28(Suppl 1): A65.
31.	Chalabi M, Cardona A, Nagarkar DR, et al. Efficacy of chemotherapy and atezolizumab in patients with non-small-cell lung cancer receiving antibiotics and proton pump inhibitors: pooled post hoc analyses of the OAK and POPLAR trials. Ann Oncol, 2020, 31(4): 525-531.
32.	Cortellini A, Di Maio M, Nigro O, et al. Differential influence of antibiotic therapy and other medications on oncological outcomes of patients with non-small cell lung cancer treated with first-line pembrolizumab versus cytotoxic chemotherapy. J Immunother Cancer, 2021, 9(4): e002421.
33.	Do TP, Hegde AM, Cherry CR, et al. Antibiotic use and overall survival in lung cancer patients receiving nivolumab. J Clin Oncol, 2018, 36(15_suppl): e15109.
34.	Forde C, Gregory R, Scott JA, et al. Antibiotic use in advanced non-small cell lung cancer (NSCLC) patients receiving immune checkpoint inhibitors across the Northern Ireland Cancer Network. Lung Cancer, 2020, 139: S54.
35.	Geum MJ, Kim C, Kang JE, et al. Broad-spectrum antibiotic regimen affects survival in patients receiving nivolumab for non-small cell lung cancer. Pharmaceuticals (Basel), 2021, 14(5): 445.
36.	Hakozaki T, Okuma Y, Omori M, et al. Impact of prior antibiotic use on the efficacy of nivolumab for non-small cell lung cancer. Oncol Lett, 2019, 17(3): 2946-2952.
37.	Hogue C, Kuzel T, Borgia J, et al. Impact of antibiotic usage on survival during checkpoint inhibitor treatment of non-small cell lung cancer (NSCLC). J Thorac Oncol, 2019, 14(S10): S735.
38.	Huemer F, Lang D, Westphal T, et al. Baseline absolute lymphocyte count and ECOG performance score are associated with survival in advanced non-small cell lung cancer undergoing PD-1/PD-L1 blockade. J Clin Med, 2019, 8(7): 1014.
39.	Lu PH, Tsai TC, Chang JW, et al. Association of prior fluoroquinolone treatment with survival outcomes of immune checkpoint inhibitors in Asia. J Clin Pharm Ther, 2021, 46(2): 408-414.
40.	Mielgo Rubio X, Aguado C, Sereno M, et al. Early antibiotic use affects the efficacy of first line immunotherapy in lung cancer patients but route of administration seems to be decisive. J Thorac Oncol, 2019, 14(S10): S445.
41.	Ochi N, Ichihara E, Takigawa N, et al. The effects of antibiotics on the efficacy of immune checkpoint inhibitors in patients with non-small-cell lung cancer differ based on PD-L1 expression. Eur J Cancer, 2021, 149: 73-81.
42.	Ouaknine Krief J, Helly de Tauriers P, Dumenil C, et al. Role of antibiotic use, plasma citrulline and blood microbiome in advanced non-small cell lung cancer patients treated with nivolumab. J Immunother Cancer, 2019, 7(1): 176.
43.	Pinato DJ, Howlett S, Ottaviani D, et al. Association of prior antibiotic treatment with survival and response to immune checkpoint inhibitor therapy in patients with cancer. JAMA Oncol, 2019, 5(12): 1774-1778.
44.	Rounis K, Papadaki C, Makrakis D, et al. Correlation of various clinical, imaging and laboratory parameters with outcome in patients with metastatic non-small cell lung cancer (NSCLC) treated with immune checkpoint inhibitors (ICIs): results from a prospective, observational, single institution study. Ann Oncol, 2019, 30: i61.
45.	Zhao S, Gao G, Li W, et al. Antibiotics are associated with attenuated efficacy of anti-PD-1/PD-L1 therapies in Chinese patients with advanced non-small cell lung cancer. Lung Cancer, 2019, 130: 10-17.
46.	Schett A, Rothschild SI, Curioni-Fontecedro A, et al. Predictive impact of antibiotics in patients with advanced non small-cell lung cancer receiving immune checkpoint inhibitors: antibiotics immune checkpoint inhibitors in advanced NSCLC. Cancer Chemother Pharmacol, 2020, 85(1): 121-131.
47.	Thompson J, Szabo A, Arce-Lara C, et al. Microbiome & immunotherapy: antibiotic use is associated with inferior survival for lung cancer patients receiving PD-1 inhibitors. J Thorac Oncol, 2017, 12(11): S1998.
48.	WHO. Latest global cancer data: Cancer burden rises to 19.3 million new cases and 10.0 million cancer deaths in 2020-IARC. Available at: https://www.iarc.who.int/news-events/latest-global-cancer-data-cancer-burden-rises-to-19-3-million-new-cases-and-10-0-million-cancer-deaths-in-2020/.
49.	Golay J, Andrea AE. Combined anti-cancer strategies based on anti-checkpoint inhibitor antibodies. Antibodies (Basel), 2020, 9(2): 17.
50.	Lurienne L, Cervesi J, Duhalde L, et al. NSCLC immunotherapy efficacy and antibiotic use: a systematic review and meta-analysis. J Thorac Oncol, 2020, 15(7): 1147-1159.
51.	Wilson BE, Routy B, Nagrial A, et al. The effect of antibiotics on clinical outcomes in immune-checkpoint blockade: a systematic review and meta-analysis of observational studies. Cancer Immunol Immunother, 2020, 69(3): 343-354.
52.	Cortellini A, Ricciuti B, Facchinetti F, et al. Antibiotic-exposed patients with non-small-cell lung cancer preserve efficacy outcomes following first-line chemo-immunotherapy. Ann Oncol, 2021, 32(11): 1391-1399.
53.	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.

1. Pardoll D. Cancer and the immune system: basic concepts and targets for intervention. Semin Oncol, 2015, 42(4): 523-538.
2. Arbour KC, Mezquita L, Long N, et al. Impact of baseline steroids on efficacy of programmed cell death-1 and programmed death-ligand 1 blockade in patients with non-small-cell lung cancer. J Clin Oncol, 2018, 36(28): 2872-2878.
3. Drakaki A, Luhn P, Wakelee H, et al. Association of systemic corticosteroids with overall survival in patients receiving cancer immunotherapy for advanced melanoma, non-small cell lung cancer or urothelial cancer in routine clinical practice. Ann Oncol, 2019, 30(1): i16-i17.
4. Martínez Bernal G, Mezquita L, Auclin E, et al. Baseline corticosteroids (CS) could be associated with absence of benefit to immune checkpoint inhibitors (ICI) in advanced non-small cell lung cancer (NSCLC) patients. Ann Oncol, 2017, 28: v472.
5. Ricciuti B, Dahlberg SE, Adeni A, et al. Immune checkpoint inhibitor outcomes for patients with non-small-cell lung cancer receiving baseline corticosteroids for palliative versus nonpalliative indications. J Clin Oncol, 2019, 37(22): 1927-1934.
6. Skribek M, Rounis K, Afshar S, et al. Effect of corticosteroids on the outcome of patients with advanced non-small cell lung cancer treated with immune-checkpoint inhibitors. Eur J Cancer, 2021, 145: 245-254.
7. Buti S, Bersanelli M, Perrone F, et al. Effect of concomitant medications with immune-modulatory properties on the outcomes of patients with advanced cancer treated with immune checkpoint inhibitors: development and validation of a novel prognostic index. Eur J Cancer, 2021, 142: 18-28.
8. Kostine M, Mauric E, Barnetche T, et al. Commonly used drugs in rheumatology may alter anti-tumoral response to immune checkpoint inhibitors. Ann Rheum Dis, 2019, 78: 251.
9. Trabolsi A, Winter M, Rodriguez E. Proton pump inhibitors and response to immune check-point inhibitors: single center study. J Clin Oncol, 2019, 37(15_suppl): e14092.
10. Takada K, Shimokawa M, Takamori S, et al. Clinical impact of probiotics on the efficacy of anti-PD-1 monotherapy in patients with nonsmall cell lung cancer: a multicenter retrospective survival analysis study with inverse probability of treatment weighting. Int J Cancer, 2021, 149(2): 473-482.
11. Tomita Y, Ikeda T, Sakata S, et al. Association of probiotic clostridium butyricum therapy with survival and response to immune checkpoint blockade in patients with lung cancer. Cancer Immunol Res, 2020, 8(10): 1236-1242.
12. 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.
13. McQuade JL, Daniel CR, Helmink BA, et al. Modulating the microbiome to improve therapeutic response in cancer. Lancet Oncol, 2019, 20(2): e77-e91.
14. Picardo SL, Coburn B, Hansen AR. The microbiome and cancer for clinicians. Crit Rev Oncol Hematol, 2019, 141: 1-12.
15. Gopalakrishnan V, Helmink BA, Spencer CN, et al. The influence of the gut microbiome on cancer, immunity, and cancer immunotherapy. Cancer Cell, 2018, 33(4): 570-580.
16. Li W, Deng Y, Chu Q, et al. Gut microbiome and cancer immunotherapy. Cancer Lett, 2019, 447: 41-47.
17. Routy B, Le Chatelier E, Derosa L, et al. Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science, 2018, 359(6371): 91-97.
18. Blaser MJ. Antibiotic use and its consequences for the normal microbiome. Science, 2016, 352(6285): 544-545.
19. Jernberg C, Löfmark S, Edlund C, et al. Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. ISME J, 2007, 1(1): 56-66.
20. Schwabe RF, Jobin C. The microbiome and cancer. Nat Rev Cancer, 2013, 13(11): 800-812.
21. Castello A, Rossi S, Toschi L, et al. Impact of antibiotic therapy and metabolic parameters in non-small cell lung cancer patients receiving checkpoint inhibitors. J Clin Med, 2021, 10(6): 1251.
22. Derosa L, Hellmann MD, Spaziano M, et al. Negative association of antibiotics on clinical activity of immune checkpoint inhibitors in patients with advanced renal cell and non-small-cell lung cancer. Ann Oncol, 2018, 29(6): 1437-1444.
23. Kim H, Lee JE, Hong SH, et al. The effect of antibiotics on the clinical outcomes of patients with solid cancers undergoing immune checkpoint inhibitor treatment: a retrospective study. BMC Cancer, 2019, 19(1): 1100.
24. Hossain T, Htut S, Pathmanathan S, et a1. Do antibiotics reduce survival in patients with advanced non-small cell lung cancer treated with immunotherapy? Asia-Pac J Clin Onco, 2020, 16(Suppl 2): 37-38.
25. Kulkarni A, Patel M, Wang Y, et a1. Antibiotic use and clinical outcomes of PD-1 antagonists in advanced non-small cell lung cancers. J Immuno Ther Cancer, 2018, 6(Suppl 1): 573.
26. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 2010, 25(9): 603-605.
27. Ahmed Y, Calvert P. Antibiotics and response to immunotherapy: real-world experience. J ImmunoTher Cancer, 2020, 8(Suppl 3): A435-A436.
28. Bagley SJ, Dhopeshwarkar N, Narayan V, et al. Impact of antibiotics (ABX) on overall survival (OS) in patients (pts) with advanced non-small-cell lung cancer (aNSCLC) and melanoma (aMel) treated with first-line immune checkpoint inhibition (ICI). J Clin Oncol, 2019, 37(15_suppl): e20643.
29. Barrón F, Arrieta OG, Cardona AF, et al. EP1. 04-45 relevance of antibiotic use on clinical activity of immune checkpoint inhibitors in Hispanic patients with advanced NSCLC (CLICAP-ABs). J Thorac Oncol, 2019, 14(10): S972.
30. Castro BA, Tourís LM, Álvarez SR, et al. Association of antibiotics and proton pump inhibitors on clinical activity of firstline pembrolizumab for non-small cell lung cancer: 2 years of real world data. Eur J Hosp Pharm, 2021, 28(Suppl 1): A65.
31. Chalabi M, Cardona A, Nagarkar DR, et al. Efficacy of chemotherapy and atezolizumab in patients with non-small-cell lung cancer receiving antibiotics and proton pump inhibitors: pooled post hoc analyses of the OAK and POPLAR trials. Ann Oncol, 2020, 31(4): 525-531.
32. Cortellini A, Di Maio M, Nigro O, et al. Differential influence of antibiotic therapy and other medications on oncological outcomes of patients with non-small cell lung cancer treated with first-line pembrolizumab versus cytotoxic chemotherapy. J Immunother Cancer, 2021, 9(4): e002421.
33. Do TP, Hegde AM, Cherry CR, et al. Antibiotic use and overall survival in lung cancer patients receiving nivolumab. J Clin Oncol, 2018, 36(15_suppl): e15109.
34. Forde C, Gregory R, Scott JA, et al. Antibiotic use in advanced non-small cell lung cancer (NSCLC) patients receiving immune checkpoint inhibitors across the Northern Ireland Cancer Network. Lung Cancer, 2020, 139: S54.
35. Geum MJ, Kim C, Kang JE, et al. Broad-spectrum antibiotic regimen affects survival in patients receiving nivolumab for non-small cell lung cancer. Pharmaceuticals (Basel), 2021, 14(5): 445.
36. Hakozaki T, Okuma Y, Omori M, et al. Impact of prior antibiotic use on the efficacy of nivolumab for non-small cell lung cancer. Oncol Lett, 2019, 17(3): 2946-2952.
37. Hogue C, Kuzel T, Borgia J, et al. Impact of antibiotic usage on survival during checkpoint inhibitor treatment of non-small cell lung cancer (NSCLC). J Thorac Oncol, 2019, 14(S10): S735.
38. Huemer F, Lang D, Westphal T, et al. Baseline absolute lymphocyte count and ECOG performance score are associated with survival in advanced non-small cell lung cancer undergoing PD-1/PD-L1 blockade. J Clin Med, 2019, 8(7): 1014.
39. Lu PH, Tsai TC, Chang JW, et al. Association of prior fluoroquinolone treatment with survival outcomes of immune checkpoint inhibitors in Asia. J Clin Pharm Ther, 2021, 46(2): 408-414.
40. Mielgo Rubio X, Aguado C, Sereno M, et al. Early antibiotic use affects the efficacy of first line immunotherapy in lung cancer patients but route of administration seems to be decisive. J Thorac Oncol, 2019, 14(S10): S445.
41. Ochi N, Ichihara E, Takigawa N, et al. The effects of antibiotics on the efficacy of immune checkpoint inhibitors in patients with non-small-cell lung cancer differ based on PD-L1 expression. Eur J Cancer, 2021, 149: 73-81.
42. Ouaknine Krief J, Helly de Tauriers P, Dumenil C, et al. Role of antibiotic use, plasma citrulline and blood microbiome in advanced non-small cell lung cancer patients treated with nivolumab. J Immunother Cancer, 2019, 7(1): 176.
43. Pinato DJ, Howlett S, Ottaviani D, et al. Association of prior antibiotic treatment with survival and response to immune checkpoint inhibitor therapy in patients with cancer. JAMA Oncol, 2019, 5(12): 1774-1778.
44. Rounis K, Papadaki C, Makrakis D, et al. Correlation of various clinical, imaging and laboratory parameters with outcome in patients with metastatic non-small cell lung cancer (NSCLC) treated with immune checkpoint inhibitors (ICIs): results from a prospective, observational, single institution study. Ann Oncol, 2019, 30: i61.
45. Zhao S, Gao G, Li W, et al. Antibiotics are associated with attenuated efficacy of anti-PD-1/PD-L1 therapies in Chinese patients with advanced non-small cell lung cancer. Lung Cancer, 2019, 130: 10-17.
46. Schett A, Rothschild SI, Curioni-Fontecedro A, et al. Predictive impact of antibiotics in patients with advanced non small-cell lung cancer receiving immune checkpoint inhibitors: antibiotics immune checkpoint inhibitors in advanced NSCLC. Cancer Chemother Pharmacol, 2020, 85(1): 121-131.
47. Thompson J, Szabo A, Arce-Lara C, et al. Microbiome & immunotherapy: antibiotic use is associated with inferior survival for lung cancer patients receiving PD-1 inhibitors. J Thorac Oncol, 2017, 12(11): S1998.
48. WHO. Latest global cancer data: Cancer burden rises to 19.3 million new cases and 10.0 million cancer deaths in 2020-IARC. Available at: https://www.iarc.who.int/news-events/latest-global-cancer-data-cancer-burden-rises-to-19-3-million-new-cases-and-10-0-million-cancer-deaths-in-2020/.
49. Golay J, Andrea AE. Combined anti-cancer strategies based on anti-checkpoint inhibitor antibodies. Antibodies (Basel), 2020, 9(2): 17.
50. Lurienne L, Cervesi J, Duhalde L, et al. NSCLC immunotherapy efficacy and antibiotic use: a systematic review and meta-analysis. J Thorac Oncol, 2020, 15(7): 1147-1159.
51. Wilson BE, Routy B, Nagrial A, et al. The effect of antibiotics on clinical outcomes in immune-checkpoint blockade: a systematic review and meta-analysis of observational studies. Cancer Immunol Immunother, 2020, 69(3): 343-354.
52. Cortellini A, Ricciuti B, Facchinetti F, et al. Antibiotic-exposed patients with non-small-cell lung cancer preserve efficacy outcomes following first-line chemo-immunotherapy. Ann Oncol, 2021, 32(11): 1391-1399.
53. 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.

Chinese Journal of Evidence-Based Medicine

Efficacy of antibiotics on the outcomes of patients with non-small cell lung cancer treated with immune checkpoint inhibitors: a meta-analysis

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