PD-L1 expression testing in non-small cell lung cancer

Therapeutic Advances in Medical Oncology

Volumn 10, Issue , 2018, Pages

  Teixidó, Cristina ^a,b   Vilariño, Noelia ^a,b   Reyes, Roxana ^a   Reguart, Noemí ^a  

^a HOSPITAL CLÍNIC   (Spain)

^b INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

Author keywords

immunohistochemistry (IHC); immunotherapy; non small cell lung cancer (NSCLC); PD L1 expression testing; predictive biomarker

Indexed keywords

EID: 85048835703     PISSN: 17588340     EISSN: 17588359     Source Type: Journal    
DOI: 10.1177/1758835918763493     Document Type: Review

References (83)

1. Schreiber RD, Old LJ, Smyth MJ., Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion. Science 2011; 331: 1565–1570
2. Chen DS, Mellman I., Elements of cancer immunity and the cancer-immune set point. Nature 2017; 541: 321–330
3. McGranahan N, Furness AJ, Rosenthal R. Clonal neoantigens elicit T cell immunoreactivity and sensitivity to immune checkpoint blockade. Science 2016; 351: 1463–1469
4. Topalian SL, Hodi FS, Brahmer JR. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012; 366: 2443–2454
5. Pardoll DM., The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 2012; 12: 252–264
6. González-Cao M, Karachaliou N, Viteri S. Targeting PD-1/PD-L1 in lung cancer: current perspectives. Lung Cancer 2015; 6: 55–70
7. Fehrenbacher L, Spira A, Ballinger M. Atezolizumab versus docetaxel for patients with previously treated non-small-cell lung cancer (POPLAR): a multicentre, open-label, phase 2 randomised controlled trial. Lancet 2016; 387: 1837–1846
8. Rebelatto MC, Midha A, Mistry A. Development of a programmed cell death ligand-1 immunohistochemical assay validated for analysis of non-small cell lung cancer and head and neck squamous cell carcinoma. Diagn Pathol 2016; 11: 95
9. Dong H, Zhu G, Tamada K. B7-H1, a third member of the B7 family, co-stimulates T-cell proliferation and interleukin-10 secretion. Nat Med 1999; 5: 1365–1369
10. Yu H, Boyle TA, Zhou C. PD-L1 expression in lung cancer. J Thorac Oncol 2016; 11: 964–975
11. Sharpe AH, Wherry EJ, Ahmed R. The function of programmed cell death 1 and its ligands in regulating autoimmunity and infection. Nat Immunol 2007; 8: 239–245
12. Sun Y, Wang Y, Zhao J. B7-H3 and B7-H4 expression in non-small-cell lung cancer. Lung Cancer 2006; 53: 143–151
13. Garon EB, Rizvi NA, Hui R. Pembrolizumab for the treatment of non-small-cell lung cancer. N Engl J Med 2015; 372: 2018–2028
14. Brahmer J, Reckamp KL, Baas P. Nivolumab versus docetaxel in advanced squamous-cell non-small-cell lung cancer. N Engl J Med 2015; 373: 123–135
15. Carbone DP, Reck M, Paz-Ares L. First-line nivolumab in stage IV or recurrent non-small-cell lung cancer. N Engl J Med 2017; 376: 2415–2426
16. Reck M, Rodríguez-Abreu D, Robinson AG. Pembrolizumab versus chemotherapy for PD-L1-positive non-small-cell lung cancer. N Engl J Med 2016; 375: 1823–1833
17. Borghaei H, Paz-Ares L, Horn L. Nivolumab versus docetaxel in advanced nonsquamous non-small-cell lung cancer. N Engl J Med 2015; 373: 1627–1639
18. Herbst RS, Baas P, Kim DW. Pembrolizumab versus docetaxel for previously treated, PD-L1-positive, advanced non-small-cell lung cancer (KEYNOTE-010): a randomised controlled trial. Lancet 2016; 387: 1540–1550
19. Rittmeyer A, Barlesi F, Waterkamp D. Atezolizumab versus docetaxel in patients with previously treated non-small-cell lung cancer (OAK): a phase 3, open-label, multicentre randomised controlled trial. Lancet 2017; 389: 255–265
20. Antonia SJ, Villegas A, Daniel D. Durvalumab after chemoradiotherapy in stage III non-small-cell lung cancer. N Engl J Med 2017; 377: 1919–1929
21. Milne CP, Bryan C, Garafalo S. Complementary versus companion diagnostics: apples and oranges? Biomark Med 2015; 9: 25–34
22. Sznol M, Chen L., Antagonist antibodies to PD-1 and B7-H1 (PD-L1) in the treatment of advanced human cancer. Clin Cancer Res 2013; 19: 1021–1034
23. US Food and Drug Administration. Dako PD-L1 IHC 22C3 pharmDx, http://www.accessdata.fda.gov/cdrh_docs/pdf15/P150013c.pdf (accessed 1 October 2017)
24. US Food and Drug Administration. Dako PD-L1 IHC 28–8 pharmDx, http://www.accessdata.fda.gov/cdrh_docs/pdf15/P150025c.pdf (accessed 1 October 2017)
25. Phillips T, Simmons P, Inzunza HD. Development of an automated PD-L1 immunohistochemistry (IHC) assay for non-small cell lung cancer. Appl Immunohistochem Mol Morphol 2015; 23: 541–549
26. Ventana Medical Systems. Media release. Roche announces FDA approval for VENTANA PD-L1 (SP142) Assay to support immunotherapy treatment decisions in lung cancer, http://www.ventana.com/roche-receives-fda-approval-for-pd-l1-assay-for-nsclc (accessed 1 October 2017)
27. Ventana Medical Systems, Inc. Ventana PD-L1 (SP142) Assay Staining of Non-Small Cell Lung Cancer Interpretation Guide 2017, http://productlibrary.ventana.com/ventana_portal/OpenOverlayServlet?launchIndex=1&objectId=741–48601015703EN (accessed 25 January 2018)
28. Quon C, Xia X, Smith M. VENTANA anti-PD-L1 (SP263) rabbit monoclonal antibody: a high specificity and sensitivity anti-human PD-L1 antibody. J Clin Oncol 2016; 34(Suppl. 15): e14509
29. Ventana Medical Systems, Inc. Ventana PD-L1 (SP263) Assay Staining of Non-Small Cell Lung Cancer Interpretation Guide 2016, http://www.roche-diagnostics.ch/content/dam/corporate/roche-dia_ch/documents/broschueren/tissue_diagnostics/Parameter/lung-pathology/PDF_VENTANAPD-L1SP263StainingofNSCLCInterpretationGuide.pdf (accessed 7 October 2017)
30. US Food and Drug Administration. VENTANA PD-L1 (SP263) Assay, https://www.accessdata.fda.gov/cdrh_docs/pdf16/p160046c.pdf (accessed 20 October 2017)
31. Ratcliffe MJ, Sharpe A, Midha A. Agreement between programmed cell death ligand-1 diagnostic assays across multiple protein expression cutoffs in non-small cell lung cancer. Clin Cancer Res 2017; 23: 3585–3591
32. Tsao MS, Kerr KM, Dacic S. IASLC atlas of PD-L1 immunohistochemistry testing in lung cancer. North Fort Myers, FL: Editorial Rx Press, 2017
33. Kerr KM, Bubendorf L, Edelman MJ. Second ESMO consensus conference on lung cancer: pathology and molecular biomarkers for non-small-cell lung cancer. Ann Oncol 2014; 25: 1681–1690
34. Cree IA, Booton R, Cane P. PD-L1 testing for lung cancer in the UK: recognizing the challenges for implementation. Histopathology 2016; 69: 177–186
35. Calles A, Liao X, Sholl LM. Expression of PD-1 and its ligands, PD-L1 and PD-L2, in smokers and never smokers with KRAS-mutant lung cancer. J Thorac Oncol 2015; 10: 1726–1735
36. Giunchi F, Degiovanni A, Daddi N. Fading with time of PD-L1 immunoreactivity in non-small cells lung cancer tissues: a methodological study. Appl Immunohistochem Mol Morphol. Epub ahead of print 31 October 2016. DOI: 10.1097/PAI.0000000000000458
37. Hirsch FR, McElhinny A, Stanforth D. PD-L1 immunohistochemistry assays for lung cancer: results from phase 1 of the blueprint PD-L1 IHC assay comparison project. J Thorac Oncol 2017; 12: 208–222
38. Rimm DL, Han G, Taube JM. A prospective, multi-institutional, pathologist-based assessment of 4 immunohistochemistry assays for PD-L1 expression in non-small cell lung cancer. JAMA Oncol 2017; 3: 1051–1058
39. Scheel AH, Dietel M, Heukamp LC. Harmonized PD-L1 immunohistochemistry for pulmonary squamous-cell and adenocarcinomas. Mod Pathol 2016; 29: 1165–1172
40. Fujimoto D, Sato Y, Uehara K. Predictive performance of four programmed cell death ligand 1 assay systems on nivolumab response in previously treated patients with non-small cell lung cancer. J Thorac Oncol 2017; 12: 1654–1663
41. Hendry S, Byrne DJ, Wright GM. Comparison of four PD-L1 immunohistochemical assays in lung cancer. J Thorac Oncol. Epub ahead of print 23 November 2017. DOI: 10.1016/j.jtho.2017.11.112
42. Marchetti A, Barberis M, Franco R. Multicenter comparison of 22c3 pharmDx (Agilent) and SP263 (Ventana) assays to test PD-L1 expression for NSCLC patients to be treated with immune checkpoint inhibitors. J Thorac Oncol 2017; 12: 1654–1663
43. Brunnström H, Johansson A, Westbom-Fremer S. PD-L1 immunohistochemistry in clinical diagnostics of lung cancer: inter-pathologist variability is higher than assay variability. Mod Pathol 2017; 30: 1411–1421
44. Adam J, Rouquette I, Damotte D. PL04a.04: multicentric French harmonization study for PD-L1 IHC testing in NSCLC. J Thorac Oncol 2017; 12: S11–S12
45. Røge R, Vyberg M, Nielsen S., Accurate PD-L1 protocols for non-small cell lung cancer can be developed for automated staining platforms with clone 22C3. Appl Immunohistochem Mol Morphol 2017; 25: 381–385
46. Ilie M, Khambata-Ford S, Copie-Bergman C. Use of the 22C3 anti-PD-L1 antibody to determine PD-L1 expression in multiple automated immunohistochemistry platforms. PLoS One 2017; 12: e0183023
47. Neuman T, London M, Kania-Almog J. A harmonization study for the use of 22C3 PD-L1 immunohistochemical staining on ventana’s platform. J Thorac Oncol 2016; 11: 1863–1868
48. Tsao MS, Kerr KM, Yatabe Y. PL 03.03 Blueprint 2: PD-L1 Immunohistochemistry comparability study in real-life clinical samples (BLUEPRINT 2). J Thorac Oncol 2017; 12: S1606
49. Skov BG, Skov T., Paired comparison of PD-L1 expression on cytologic and histologic specimens from malignancies in the lung assessed with PD-L1 IHC 28–8pharmDx and PD-L1 IHC 22C3pharmDx. Appl Immunohistochem Mol Morphol 2017; 25: 453–459
50. Novello S, Barlesi F, Califano R. Metastatic non-small-cell lung cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol 2016; 27: v1–v27
51. Ettinger DS, Wood DE, Aisner DL. Non-small cell lung cancer, version 5.2017, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw 2017; 15: 504–535
52. Peters S, Gettinger S, Johnson ML. Phase II trial of atezolizumab as first-line or subsequent therapy for patients with programmed death-ligand 1-selected advanced non-small-cell lung cancer (BIRCH). J Clin Oncol 2017; 35: 2781–2789
53. Reck M, Rabe KF., Precision diagnosis and treatment for advanced non–small-cell lung cancer. N Engl J Med 2017; 377: 849–861
54. Kim M-Y, Koh J, Kim S. Clinicopathological analysis of PD-L1 and PD-L2 expression in pulmonary squamous cell carcinoma: comparison with tumor-infiltrating T cells and the status of oncogenic drivers. Lung Cancer 2015; 88: 24–33
55. Ilie M, Long-Mira E, Bence C. Comparative study of the PD-L1 status between surgically resected specimens and matched biopsies of NSCLC patients reveal major discordances: a potential issue for anti-PD-L1 therapeutic strategies. Ann Oncol 2016; 27: 147–153
56. McLaughlin J, Han G, Schalper KA. Quantitative assessment of the heterogeneity of PD-L1 expression in non-small-cell lung cancer. JAMA Oncol 2016; 2: 46–54
57. Uruga H, Bozkurtlar E, Huynh TG. Programmed cell death ligand (PD-L1) expression in stage II and III lung adenocarcinomas and nodal metastases. J Thorac Oncol 2017; 12: 458–466
58. Paulsen EE, Kilvaer TK, Khanehkenari MR. Assessing PDL-1 and PD-1 in non-small cell lung cancer: a novel immunoscore approach. Clin Lung Cancer 2017; 18: 220–233.e8
59. Takamori S, Toyokawa G, Okamoto I. Discrepancy in programmed cell death-ligand 1 between primary and metastatic non-small cell lung cancer. Anticancer Res 2017; 37: 4223–4228
60. Twyman-Saint Victor C, Rech AJ, Maity A. Radiation and dual checkpoint blockade activate non-redundant immune mechanisms in cancer. Nature 2015; 520: 373–377
61. Sheng J, Fang W, Yu J. Erratum: expression of programmed death ligand-1 on tumor cells varies pre and post chemotherapy in non-small cell lung cancer. Sci Rep 2016; 6: 23850
62. Chaft JE, Chao B, Akerley WL. Evaluation of PD-L1 expression in metachronous tumor samples and FDG-PET as a predictive biomarker in Ph2 study (FIR) of atezolizumab (MPDL3280A). J Thorac Oncol 2015; 10(Suppl. 2): S176
63. Aggarwal C, Abreu DR, Felip E. Prevalence of PD-L1 expression in patients with non-small cell lung cancer screened for enrollment in KEYNOTE-001, -010, and -024. Ann Oncol 2016; 27(Suppl. 6): 1060P
64. Rehman JA, Han G, Carvajal-Hausdorf DE. Quantitative and pathologist-read comparison of the heterogeneity of programmed death-ligand 1 (PD-L1) expression in non-small cell lung cancer. Mod Pathol 2017; 30: 340–349
65. Cho JH, Sorensen SF, Choi YL. Programmed death ligand 1 expression in paired non-small cell lung cancer tumor samples. Clin Lung Cancer 2015; 16: 385–390
66. Kitazono S, Fujiwara Y, Tsuta K. Reliability of small biopsy samples compared with resected specimens for the determination of programmed death-ligand 1 expression in non–small-cell lung cancer. Clin Lung Cancer 2015; 16: 385–390
67. Heymann JJ, Bulman WA, Swinarski D. Programmed death-ligand 1 expression in non-small cell lung carcinoma: comparison among cytology, small biopsy, and surgical resection specimens. Cancer 2017; 125: 896–907
68. Lawrence MS, Stojanov P, Mermel CH. Discovery and saturation analysis of cancer genes across 21 tumour types. Nature 2014; 505: 495–501
69. Govindan R, Ding L, Griffith M. Genomic landscape of non-small cell lung cancer in smokers and never-smokers. Cell 2012; 150: 1121–1134
70. Peters S, Creelan B, Hellmann MD. Abstract CT082: impact of tumor mutation burden on the efficacy of first-line nivolumab in stage IV or recurrent non-small cell lung cancer: an exploratory analysis of CheckMate 026. Cancer Res 2017; 77: CT082
71. Spigel DR, Schrock AB, Fabrizio D. Total mutation burden (TMB) in lung cancer (LC) and relationship with response to PD-1/PD-L1 targeted therapies. J Clin Oncol 2016; 34: 9017
72. Le DT, Durham JN, Smith KN. Mismatch repair deficiency predicts response of solid tumors to PD-1 blockade. Science 2017; 357: 409–413
73. Rizvi NA, Hellmann MD, Snyder A. Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science 2015; 348: 124–128
74. Atmaca A. OA 07.03a Impact of tumor mutation burden on the efficacy of nivolumab or nivolumab + ipilimumab in small cell lung cancer: an exploratory analysis of CheckMate 032. In: IASLC 18th world conference on lung cancer, 2017
75. Cristescu R, Mogg R, Ayers M. Mutational load (ML) and T-cell-inflamed microenvironment as predictors of response to pembrolizumab. ASCO-SITC clinical immuno-oncology symposium. J Clin Oncol 2017; 35: S7S
76. Kowanetz M, Zou W, Shames D. OA20.01 Tumor Mutation Burden (TMB) is associated with improved efficacy of atezolizumab in 1L and 2L+ NSCLC patients. J Thorac Oncol 2017; 12: S321–S322
77. Campbell JD, Alexandrov A, Kim J. Distinct patterns of somatic genome alterations in lung adenocarcinomas and squamous cell carcinomas. Nat Genet 2016; 48: 607–616
78. Alexandrov LB, Ju YS, Haase K. Mutational signatures associated with tobacco smoking in human cancer. Science 2016; 354: 618–622
79. Zehir A, Benayed R, Shah RH. Erratum: mutational landscape of metastatic cancer revealed from prospective clinical sequencing of 10,000 patients. Nat Med 2017; 23: 1004
80. Rieke DT, Messerschmidt C, Ochsenreither S. Abstract e14613: association of an APOBEC mutational signature, mutational load, and BRCAness with inflammation and PD-L1 expression in HNSCC. J Clin Oncol 2017; 35: e14613
81. Schumacher TN, Schreiber RD., Neoantigens in cancer immunotherapy. Science 2015; 348: 69–74
82. Gandara DR, Kowanetz M, Mok TSK. Blood-based biomarkers for cancer immunotherapy: tumor mutational burden in blood (bTMB) is associated with improved atezolizumab (atezo) efficacy in 2L+ NSCLC (POPLAR and OAK) ESMO congress. Ann Oncol 2017; 28(Suppl. 5): v460–v496
83. Routy B, Le Chatelier E, Derosa L. Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science 2018; 359: 91–97