Real-world effectiveness of nivolumab in patients with non-small-cell lung cancer: a systematic review and meta-analysis

Papers of special note have been highlighted as: • of interest; •• of considerable interest

References

• 1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2019. CA Cancer J. Clin. 69(1), 7–34 (2019).
  MedlineGoogle Scholar
• 2. Howlader N, Noone AM, Krapcho M et al. SEER Cancer Statistics Review, 1975-2016 National Cancer Institute, Bethesda, MD, USA (2019). https://seer.cancer.gov/csr/1975_2016/
  Google Scholar
• 3. Walters S, Maringe C, Coleman MP et al. Lung cancer survival and stage at diagnosis in Australia, Canada, Denmark, Norway, Sweden and the UK: a population-based study, 2004–2007. Thorax 68(6), 551–564 (2013).
  MedlineGoogle Scholar
• 4. Kim BJ, Kim JH, Kim HS. Survival benefit of immune checkpoint inhibitors according to the histology in non-small-cell lung cancer: a meta-analysis and review. Oncotarget 8(31), 51779–51785 (2017).
  MedlineGoogle Scholar
• 5. Khan M, Lin J, Liao G et al. Comparative analysis of immune checkpoint inhibitors and chemotherapy in the treatment of advanced non-small cell lung cancer. Medicine. 97(33), e11936 (2018).
  Medline CASGoogle Scholar
• 6. Nixon NA, Blais N, Ernst S et al. Current landscape of immunotherapy in the treatment of solid tumours, with future opportunities and challenges. Curr. Oncol. 25(5), e373–e384 (2018).
  Medline CASGoogle Scholar
• 7. Brahmer J, Reckamp KL, Baas P et al. Nivolumab versus docetaxel in advanced squamous-cell non-small-cell lung cancer. N. Engl. J. Med. 373(2), 123–135 (2015).
  Medline CASGoogle Scholar
• 8. Borghaei H, Paz-Ares L, Horn L et al. Nivolumab versus docetaxel in advanced nonsquamous non-small-cell lung cancer. N. Engl. J. Med. 373(17), 1627–1639 (2015).
  Medline CASGoogle Scholar
• 9. Carbone DP, Reck M, Paz-Ares L et al. First-line nivolumab in stage IV or recurrent non-small-cell lung cancer. N. Engl. J. Med. 376(25), 2415–2426 (2017).
  Medline CASGoogle Scholar
• 10. Moher D, Liberati A, Tetzlaff J et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 6(7), e1000097 (2009).
  MedlineGoogle Scholar
• 11. Wells GA, Shea B, O'Connell D et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses (2019). www.ohri.ca/programs/clinical_epidemiology/oxford.asp
  Google Scholar
• 12. Dijkers M. Introducing GRADE: a systematic approach to rating evidence in systematic reviews and to guideline development. KT Update 1(5), 1–9 (2013).
  Google Scholar
• 13. McGrath S, Zhao X, Qin ZZ et al. One-sample aggregate data meta-analysis of medians. Stat. Med. 38(6), 969–984 (2019).
  MedlineGoogle Scholar
• 14. McGrath S, Sohn H, Steele R et al. Meta-analysis of the difference of medians. Biom J. 62(1), 69–98 (2020).
  MedlineGoogle Scholar
• 15. Ksienski D, Wai ES, Croteau N et al. Efficacy of nivolumab and pembrolizumab in patients with advanced non-small-cell lung cancer needing treatment interruption because of adverse events: a retrospective multicenter analysis. Clin. Lung Cancer 20(1), e97–e106 (2019). • Nivolumab was associated with 9.2 and 5.7 months for OS and PFS, respectively. Pembrolizumab was associated with 13.5 and 13.5 months for overall survival (OS) and progression-free survival (PFS), respectively.
  Medline CASGoogle Scholar
• 16. Calpe-Armero P, Ferriols-Lisart R, Ferriols- Lisart F et al. Effectiveness of nivolumab versus docetaxel as second-line treatment in non-small cell lung cancer patients in clinical practice. Chemotherapy 62(6), 374–380 (2017). • The median PFS was 2.7 and 2.0 months for nivolumab and docetaxel, respectively.
  Medline CASGoogle Scholar
• 17. Yoo SH, Keam B, Kim M et al. Low-dose nivolumab can be effective in non-small cell lung cancer: alternative option for financial toxicity. ESMO Open 3(5), e000332 (2018). • Reports higher effectiveness for low-dose nivolumab therapy over standard-dose nivolumab therapy with 12.5 and 8.2 months for OS and 3.0 and 1.0 months for PFS, respectively.
  MedlineGoogle Scholar
• 18. Areses Manrique MC, Mosquera Martinez J, Garcia Gonzalez J et al. Real world data of nivolumab for previously treated non-small cell lung cancer patients: a Galician lung cancer group clinical experience. Transl. Lung Cancer Res. 7(3), 404–415 (2018).
  MedlineGoogle Scholar
• 19. Bagley SJ, Kothari S, Aggarwal C et al. Pretreatment neutrophil-to-lymphocyte ratio as a marker of outcomes in nivolumab-treated patients with advanced non-small-cell lung cancer. Lung Cancer 106, 1–7 (2017).
  MedlineGoogle Scholar
• 20. Brustugun OT, Sprauten M, Helland A. Real-world data on nivolumab treatment of non-small cell lung cancer. Acta Oncol. 56(3), 438–440 (2017).
  Medline CASGoogle Scholar
• 21. Costantini A, Corny J, Fallet V et al. Efficacy of next treatment received after nivolumab progression in patients with advanced non-small cell lung cancer. ERJ Open Res. 4(2), 00120–02017 (2018).
  MedlineGoogle Scholar
• 22. Crino L, Bronte G, Bidoli P et al. Nivolumab and brain metastases in patients with advanced non-squamous non-small cell lung cancer. Lung Cancer 129, 35–40 (2019).
  MedlineGoogle Scholar
• 23. Diem S, Schmid S, Krapf M et al. Neutrophil-to-lymphocyte ratio (NLR) and platelet-to-lymphocyte (PLR) as prognostic markers in patients with non-small cell lung cancer (NSCLC) treated with nivolumab. Lung Cancer 111, 176–181 (2017).
  MedlineGoogle Scholar
• 24. Dudnik E, Moskovitz M, Daher S et al. Effectiveness and safety of nivolumab in advanced non-small cell lung cancer: the real-life data. Lung Cancer 126, 217–223 (2018).
  MedlineGoogle Scholar
• 25. Dumenil C, Massiani MA, Dumoulin J et al. Clinical factors associated with early progression and grade 3–4 toxicity in patients with advanced non-small-cell lung cancers treated with nivolumab. PLoS ONE 13(4), e0195945 (2018).
  MedlineGoogle Scholar
• 26. Facchinetti F, Veneziani M, Buti S et al. Clinical and hematologic parameters address the outcomes of non-small-cell lung cancer patients treated with nivolumab. Immunotherapy 10(8), 681–694 (2018).
  CASGoogle Scholar
• 27. Fiorica F, Belluomini L, Stefanelli A et al. Immune checkpoint inhibitor nivolumab and radiotherapy in pretreated lung cancer patients: efficacy and safety of combination. Am. J. Clin. Oncol. 41(11), 1101–1105 (2018).
  Medline CASGoogle Scholar
• 28. Fujimoto D, Yoshioka H, Kataoka Y et al. Pseudoprogression in previously treated patients with non-small cell lung cancer who received nivolumab monotherapy. J. Thorac. Oncol. 14(3), 468–474 (2019).
  Medline CASGoogle Scholar
• 29. Fukui T, Okuma Y, Nakahara Y et al. Activity of nivolumab and utility to neutrophil-to-lymphocyte ratio as a predictive biomarker for advanced non-small-cell lung cancer: a prospective observational study. Clin. Lung Cancer 20(3), 2018–2214 (2019).
  Google Scholar
• 30. Garde-Noguera J, Martin-Martorell P, De Julian M et al. Predictive and prognostic clinical and pathological factors of nivolumab efficacy in non-small-cell lung cancer patients. Clin. Transl. Oncol. 20(8), 1072–1079 (2018).
  Medline CASGoogle Scholar
• 31. Garassino MC, Crino L, Catino A et al. Nivolumab in never-smokers with advanced squamous non-small cell lung cancer: results from the Italian cohort of an expanded access program. Tumour Biol. 40(11), 1010428318815047 (2018).
  Google Scholar
• 32. Grossi F, Crino L, Logroscino A et al. Use of nivolumab in elderly patients with advanced squamous non-small-cell lung cancer: results from the Italian cohort of an expanded access programme. Eur. J. Cancer 100, 126–134 (2018).
  Medline CASGoogle Scholar
• 33. Haratani K, Hayashi H, Tanaka T et al. Tumor immune microenvironment and nivolumab efficacy in EGFR mutation-positive non-small-cell lung cancer based on T790M status after disease progression during EGFR-TKI treatment. Ann. Oncol. 28(7), 1532–1539 (2017). •• Higher effectiveness associated with nivolumab was observed for T790M-negative patients with EGFR mutation-positive non-small-cell lung cancer over T790M-positive patients.
  Medline CASGoogle Scholar
• 34. Juergens RA, Mariano C, Jolivet J et al. Real-world benefit of nivolumab in a Canadian non-small-cell lung cancer cohort. Curr. Oncol. 25(6), 384–392 (2018).
  Medline CASGoogle Scholar
• 35. Kataoka Y, Hirano K, Narabayashi T et al. Carcinoembryonic antigen as a predictive biomarker of response to nivolumab in non-small cell lung cancer. Anticancer Res. 38(1), 559–563 (2018).
  Medline CASGoogle Scholar
• 36. Kiriu T, Yamamoto M, Nagano T et al. The time-series behavior of neutrophil-to-lymphocyte ratio is useful as a predictive marker in non-small-cell lung cancer. PLoS ONE 13(2), e0193018 (2018).
  MedlineGoogle Scholar
• 37. Kobayashi K, Nakachi I, Naoki K et al. Real-world efficacy and safety of nivolumab for advanced non-small-cell lung cancer: a retrospective multicenter analysis. Clin. Lung Cancer 19(3), e349–e358 (2018).
  Medline CASGoogle Scholar
• 38. Lesueur P, Escande A, Thariat J et al. Safety of combined PD-1 pathway inhibition and radiation therapy for non-small-cell lung cancer: a multicentric retrospective study from the GFPC. Cancer Med. 7(11), 5505–5513 (2018).
  Medline CASGoogle Scholar
• 39. Merino Almazan M, Duarte Perez JM, Marin Pozo JF et al. A multicentre observational study of the effectiveness, safety and economic impact of nivolumab on non-small-cell lung cancer in real clinical practice. Int. J. Clin. Pharm. 41(1), 272–279 (2019).
  MedlineGoogle Scholar
• 40. Montana M, Garcia ME, Ausias N et al. Efficacy and safety of nivolumab in patients with non-small cell lung cancer: a retrospective study in clinical practice. J. Chemother. 31(2), 90–94 (2019).
  Medline CASGoogle Scholar
• 41. Sabatier R, Nicolas E, Paciencia M et al. Nivolumab in routine practice for older patients with advanced or metastatic non-small cell lung cancer. J. Geriatr. Oncol. 9(5), 494–500 (2018).
  MedlineGoogle Scholar
• 42. Sato K, Akamatsu H, Murakami E et al. Correlation between immune-related adverse events and efficacy in non-small cell lung cancer treated with nivolumab. Lung Cancer 115, 71–74 (2018).
  MedlineGoogle Scholar
• 43. Schmid S, Diem S, Li Q et al. Organ-specific response to nivolumab in patients with non-small cell lung cancer (NSCLC). Cancer Immunol. Immunother. 67(12), 1825–1832 (2018).
  Medline CASGoogle Scholar
• 44. Schouten RD, Muller M, de Gooijer CJ et al. Real life experience with nivolumab for the treatment of non-small cell lung carcinoma: data from the expanded access program and routine clinical care in a tertiary cancer centre-The Netherlands Cancer Institute. Lung Cancer 126, 210–216 (2018).
  MedlineGoogle Scholar
• 45. Sekine K, Kanda S, Goto Y et al. Change in the lymphocyte-to-monocyte ratio is an early surrogate marker of the efficacy of nivolumab monotherapy in advanced non-small-cell lung cancer. Lung Cancer 124, 179–188 (2018).
  MedlineGoogle Scholar
• 46. Shamai S, Merimsky O. Efficacy and safety of nivolumab in non-small cell lung cancer patients in Tel-Aviv tertiary medical center: facing the reality. Mol. Clin. Oncol. 9(4), 419–422 (2018).
  Medline CASGoogle Scholar
• 47. Shiroyama T, Suzuki H, Tamiya M et al. Pretreatment advanced lung cancer inflammation index (ALI) for predicting early progression in nivolumab-treated patients with advanced non-small cell lung cancer. Cancer Med. 7(1), 13–20 (2018).
  Medline CASGoogle Scholar
• 48. Takeda T, Takeuchi M, Saitoh M et al. Neutrophil-to-lymphocyte ratio after four weeks of nivolumab administration as a predictive marker in patients with pretreated non-small-cell lung cancer. Thorac. Cancer 9(10), 1291–1299 (2018).
  Medline CASGoogle Scholar
• 49. Tiu AC, Potdar R, Djibo DA et al. Clinical outcomes of African American patients with advanced or metastatic non-small cell lung cancer on nivolumab in a single community-based cancer center. Med. Oncol. 35(7), 109 (2018). •• Reports the highest median OS and PFS where the majority of the population were African Americans.
  MedlineGoogle Scholar
• 50. Tournoy KG, Thomeer M, Germonpre P et al. Does nivolumab for progressed metastatic lung cancer fulfill its promises? An efficacy and safety analysis in 20 general hospitals. Lung Cancer 115, 49–55 (2018).
  MedlineGoogle Scholar
• 51. Horn L, Spigel DR, Vokes EE et al. Nivolumab versus docetaxel in previously treated patients with advanced non-small-cell lung cancer: two-year outcomes from two randomized, open-label, phase III trials (CheckMate 017 and CheckMate 057). J. Clin. Oncol. 35(35), 3924–3933 (2017).
  Medline CASGoogle Scholar
• 52. Vokes EE, Ready N, Felip E et al. Nivolumab versus docetaxel in previously treated advanced non-small-cell lung cancer (CheckMate 017 and CheckMate 057): 3-year update and outcomes in patients with liver metastases. Ann. Oncol. 29(4), 959–965 (2018).
  Medline CASGoogle Scholar
• 53. Barlesi F, Dixmier A, Debieuvre D et al. Effectiveness and safety of nivolumab in the treatment of lung cancer patients in France: preliminary results from the real-world EVIDENS study. Oncoimmunology 9(1), 1744898 (2020).
  MedlineGoogle Scholar