Developments in predictive biomarker testing and targeted therapy in advanced stage non-small cell lung cancer and their application across European countries
Status PubMed-not-MEDLINE Jazyk angličtina Země Anglie, Velká Británie Médium electronic-ecollection
Typ dokumentu časopisecké články, přehledy
PubMed
38476742
PubMed Central
PMC10928289
DOI
10.1016/j.lanepe.2024.100838
PII: S2666-7762(24)00004-8
Knihovny.cz E-zdroje
- Klíčová slova
- Europe, Non-small cell lung cancer, Predictive biomarker testing, Targeted therapy,
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
In the past two decades, the treatment of metastatic non-small cell lung cancer (NSCLC), has undergone significant changes due to the introduction of targeted therapies and immunotherapy. These advancements have led to the need for predictive molecular tests to identify patients eligible for targeted therapy. This review provides an overview of the development and current application of targeted therapies and predictive biomarker testing in European patients with advanced stage NSCLC. Using data from eleven European countries, we conclude that recommendations for predictive testing are incorporated in national guidelines across Europe, although there are differences in their comprehensiveness. Moreover, the availability of recently EMA-approved targeted therapies varies between European countries. Unfortunately, routine assessment of national/regional molecular testing rates is limited. As a result, it remains uncertain which proportion of patients with metastatic NSCLC in Europe receive adequate predictive biomarker testing. Lastly, Molecular Tumor Boards (MTBs) for discussion of molecular test results are widely implemented, but national guidelines for their composition and functioning are lacking. The establishment of MTB guidelines can provide a framework for interpreting rare or complex mutations, facilitating appropriate treatment decision-making, and ensuring quality control.
Centre for Cancer Society and Public Health King's College London London United Kingdom
Charles University and Thomayer Hospital Prague Czech Republic
Department of Oncology University Hospital Antwerp University of Antwerp Edegem Belgium
Department of Pathology University Hospital Antwerp University of Antwerp Edegem Belgium
Department of Radiation Sciences Oncology Umeå University Umeå Sweden
Diagnostic and Research Institute of Pathology Medical University of Graz Graz Austria
IHU RespirERA FHU OncoAge Nice University Hospital Côte d'Azur University Nice France
Institute of Medical Genetics and Applied Genomics University of Tuebingen Tuebingen Germany
Institute of Molecular Pathology and Immunology of the University of Porto Porto Portugal
Karl Landsteiner Institute of Lung Research and Pulmonary Oncology Klinik Floridsdorf Vienna Austria
Laboratory for Cytology and Pathology University Clinic Golnik Golnik Slovenia
Lung Unit Royal Marsden NHS Trust London United Kingdom
National Disease Registration Service NHS England London United Kingdom
Oncostat U1018 Inserm Paris Saclay University Gustave Roussy Villejuif France
Pulmonology Department Centro Hospitalar Universitário de São João Porto Portugal
University Clinic of Respiratory and Allergic Diseases Golnik Slovenia
Zobrazit více v PubMed
Sung H., Ferlay J., Siegel R.L., 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. PubMed
Malvezzi M., Santucci C., Boffetta P., et al. European cancer mortality predictions for the year 2023 with focus on lung cancer. Ann Oncol. 2023;34(4):410–419. PubMed
Gregor A., Inage T., Hwangbo B., Yasufuku K. Lung cancer staging: state of the art in the era of ablative therapies and surgical segmentectomy. Respirology. 2020;25(9):924–932. PubMed
Howlader N., Forjaz G., Mooradian M.J., et al. The effect of advances in lung-cancer treatment on population mortality. N Engl J Med. 2020;383(7):640–649. PubMed PMC
Hendriks L.E., Kerr K.M., Menis J., et al. Oncogene-addicted metastatic non-small-cell lung cancer: ESMO clinical practice guideline for diagnosis, treatment and follow-up. Ann Oncol. 2023;34(4):339–357. PubMed
Thunnissen E., Weynand B., Udovicic-Gagula D., et al. Lung cancer biomarker testing: perspective from Europe. Transl Lung Cancer Res. 2020;9(3):887–897. PubMed PMC
Ryska A., Berzinec P., Brcic L., et al. NSCLC molecular testing in Central and Eastern European countries. BMC Cancer. 2018;18(1):269. PubMed PMC
Kerr K.M., Bibeau F., Thunnissen E., et al. The evolving landscape of biomarker testing for non-small cell lung cancer in Europe. Lung Cancer. 2021;154:161–175. PubMed
Normanno N., Apostolidis K., Wolf A., et al. Access and quality of biomarker testing for precision oncology in Europe. Eur J Cancer. 2022;176:70–77. PubMed
Bayle A., Bonastre J., Chaltiel D., et al. ESMO study on the availability and accessibility of biomolecular technologies in oncology in Europe. Ann Oncol. 2023;34(10):934–945. PubMed
de Jager V.D., Timens W., Bayle A., et al. Future perspective for the application of predictive biomarker testing in advanced stage non-small cell lung cancer. Lancet Reg Health Eur. 2024;38:100839. doi: 10.1016/j.lanepe.2024.100839. PubMed DOI PMC
Houda I., Dickhoff C., Uyl-de Groot C.A., et al. New systemic treatment paradigms in resectable non-small cell lung cancer and variations in patient access across Europe. Lancet Reg Health Eur. 2024;38:100840. doi: 10.1016/j.lanepe.2024.100840. PubMed DOI PMC
Adib E., Nassar A.H., Abou Alaiwi S., et al. Variation in targetable genomic alterations in non-small cell lung cancer by genetic ancestry, sex, smoking history, and histology. Genome Med. 2022;14(1):39. PubMed PMC
Koopman B., Cajiao Garcia B.N., Kuijpers C., et al. A nationwide study on the impact of routine testing for EGFR mutations in advanced NSCLC reveals distinct survival patterns based on EGFR mutation subclasses. Cancers. 2021;13(14):3641. PubMed PMC
Soria J.C., Ohe Y., Vansteenkiste J., et al. Osimertinib in untreated EGFR-mutated advanced non-small-cell lung cancer. N Engl J Med. 2018;378(2):113–125. PubMed
Yang J.C., Sequist L.V., Geater S.L., et al. Clinical activity of afatinib in patients with advanced non-small-cell lung cancer harbouring uncommon EGFR mutations: a combined post-hoc analysis of LUX-Lung 2, LUX-Lung 3, and LUX-Lung 6. Lancet Oncol. 2015;16(7):830–838. PubMed
Elamin Y.Y., Robichaux J.P., Carter B.W., et al. Poziotinib for EGFR exon 20-mutant NSCLC: clinical efficacy, resistance mechanisms, and impact of insertion location on drug sensitivity. Cancer Cell. 2022;40(7):754–767.e6. PubMed PMC
Zhou C., Ramalingam S.S., Kim T.M., et al. Treatment outcomes and safety of mobocertinib in platinum-pretreated patients with EGFR Exon 20 insertion-positive metastatic non-small cell lung cancer: a phase 1/2 open-label nonrandomized clinical trial. JAMA Oncol. 2021;7(12) PubMed PMC
Park K., Haura E.B., Leighl N.B., et al. Amivantamab in EGFR exon 20 insertion-mutated non-small-cell lung cancer progressing on platinum chemotherapy: initial results from the CHRYSALIS phase I study. J Clin Oncol. 2021;39(30):3391–3402. PubMed PMC
Duke E.S., Stapleford L., Drezner N., et al. FDA approval summary: mobocertinib for metastatic non-small cell lung cancer with EGFR exon 20 insertion mutations. Clin Cancer Res. 2023;29(3):508–512. PubMed PMC
Chon K., Larkins E., Chatterjee S., et al. FDA approval summary: amivantamab for the treatment of patients with non-small cell lung cancer with EGFR exon 20 insertion mutations. Clin Cancer Res. 2023;29(17):3262–3266. PubMed PMC
Wang C., Zhao K., Hu S., Dong W., Gong Y., Xie C. Clinical outcomes of afatinib versus osimertinib in patients with non-small cell lung cancer with uncommon EGFR mutations: a pooled analysis. Oncologist. 2023;28(6):e397–e405. PubMed PMC
Robichaux J.P., Le X., Vijayan R.S.K., et al. Structure-based classification predicts drug response in EGFR-mutant NSCLC. Nature. 2021;597(7878):732–737. PubMed PMC
Wu Y.L., Tsuboi M., He J., et al. Osimertinib in resected EGFR-mutated non-small-cell lung cancer. N Engl J Med. 2020;383(18):1711–1723. PubMed
Houda I., Dickhoff C., Uyl-de Groot C.A., et al. Challenges and controversies in resectable non-small cell lung cancer: a clinician’s perspective. Lancet Reg Health Eur. 2024;38:100841. doi: 10.1016/j.lanepe.2024.100841. PubMed DOI PMC
Koopman B., Groen H.J.M., Schuuring E., et al. Actionability of on-target ALK resistance mutations in patients with non-small cell lung cancer: local experience and review of the literature. Clin Lung Cancer. 2022;23(2):e104–e115. PubMed
Ariyasu R., Kakuto S., Miyadera K., et al. Real-world outcome analysis of patients with stage IV NSCLC treated with tyrosine kinase and immune checkpoint inhibitors. JTO Clin Res Rep. 2023;4(6) PubMed PMC
Ou S.I., Nagasaka M., Brazel D., Hou Y., Zhu V.W. Will the clinical development of 4th-generation "double mutant active" ALK TKIs (TPX-0131 and NVL-655) change the future treatment paradigm of ALK+NSCLC? Transl Oncol. 2021;14(11) PubMed PMC
Shaw A.T., Ou S.H., Bang Y.J., et al. Crizotinib in ROS1-rearranged non-small-cell lung cancer. N Engl J Med. 2014;371(21):1963–1971. PubMed PMC
Drilon A., Siena S., Dziadziuszko R., et al. Entrectinib in ROS1 fusion-positive non-small-cell lung cancer: integrated analysis of three phase 1-2 trials. Lancet Oncol. 2020;21(2):261–270. PubMed PMC
Ou S.I., Zhu V.W. CNS metastasis in ROS1+ NSCLC: an urgent call to action, to understand, and to overcome. Lung Cancer. 2019;130:201–207. PubMed
Dankner M., Rose A.A.N., Rajkumar S., Siegel P.M., Watson I.R. Classifying BRAF alterations in cancer: new rational therapeutic strategies for actionable mutations. Oncogene. 2018;37(24):3183–3199. PubMed
Lim G.H.T., Balbi K.J., Poskitt B., Bennett P., Moore D.A. Prevalence and breakdown of non-small cell lung cancer BRAF driver mutations in a large UK cohort. Lung Cancer. 2022;173:71–74. PubMed
Dankner M., Wang Y., Fazelzad R., et al. Clinical activity of mitogen-activated protein kinase-targeted therapies in patients with non-V600 BRAF-mutant tumors. JCO Precis Oncol. 2022;6 PubMed PMC
Forsythe A., Zhang W., Phillip Strauss U., Fellous M., Korei M., Keating K. A systematic review and meta-analysis of neurotrophic tyrosine receptor kinase gene fusion frequencies in solid tumors. Ther Adv Med Oncol. 2020;12 PubMed PMC
Hong D.S., DuBois S.G., Kummar S., et al. Larotrectinib in patients with TRK fusion-positive solid tumours: a pooled analysis of three phase 1/2 clinical trials. Lancet Oncol. 2020;21(4):531–540. PubMed PMC
Drilon A., Siena S., Ou S.I., et al. Safety and antitumor activity of the multitargeted pan-TRK, ROS1, and ALK inhibitor entrectinib: combined results from two phase I trials (ALKA-372-001 and STARTRK-1) Cancer Discov. 2017;7(4):400–409. PubMed PMC
Drilon A., Tan D.S.W., Lassen U.N., et al. Efficacy and safety of larotrectinib in patients with tropomyosin receptor kinase fusion-positive lung cancers. JCO Precis Oncol. 2022;6 PubMed PMC
Doebele R.C., Drilon A., Paz-Ares L., et al. Entrectinib in patients with advanced or metastatic NTRK fusion-positive solid tumours: integrated analysis of three phase 1-2 trials. Lancet Oncol. 2020;21(2):271–282. PubMed PMC
Drilon A., Oxnard G.R., Tan D.S.W., et al. Efficacy of selpercatinib in RET fusion-positive non-small-cell lung cancer. N Engl J Med. 2020;383(9):813–824. PubMed PMC
Gainor J.F., Curigliano G., Kim D.W., et al. Pralsetinib for RET fusion-positive non-small-cell lung cancer (ARROW): a multi-cohort, open-label, phase 1/2 study. Lancet Oncol. 2021;22(7):959–969. PubMed
Hobbs G.A., Der C.J., Rossman K.L. RAS isoforms and mutations in cancer at a glance. J Cell Sci. 2016;129(7):1287–1292. PubMed PMC
Terrenato I., Ercolani C., Di Benedetto A., et al. A real-world systematic analysis of driver mutations' prevalence in early- and advanced-stage NSCLC: implications for targeted therapies in the adjuvant setting. Cancers. 2022;14(12):2971. PubMed PMC
Garcia B.N.C., van Kempen L.C., Kuijpers C., Schuuring E., Willems S.M., van der Wekken A.J. Prevalence of KRAS p.(G12C) in stage IV NSCLC patients in the Netherlands; a nation-wide retrospective cohort study. Lung Cancer. 2022;167:1–7. PubMed
Isaksson J., Berglund A., Louie K., et al. KRAS G12C mutant non-small cell lung cancer linked to female sex and high risk of CNS metastasis: population-based demographics and survival data from the National Swedish Lung Cancer Registry. Clin Lung Cancer. 2023;24(6):507–518. PubMed
Cox A.D., Fesik S.W., Kimmelman A.C., Luo J., Der C.J. Drugging the undruggable RAS: mission possible? Nat Rev Drug Discov. 2014;13(11):828–851. PubMed PMC
Ostrem J.M., Peters U., Sos M.L., Wells J.A., Shokat K.M. K-Ras(G12C) inhibitors allosterically control GTP affinity and effector interactions. Nature. 2013;503(7477):548–551. PubMed PMC
Lanman B.A., Allen J.R., Allen J.G., et al. Discovery of a covalent inhibitor of KRAS(G12C) (AMG 510) for the treatment of solid tumors. J Med Chem. 2020;63(1):52–65. PubMed
Skoulidis F., Li B.T., Dy G.K., et al. Sotorasib for lung cancers with KRAS p.G12C mutation. N Engl J Med. 2021;384(25):2371–2381. PubMed PMC
de Langen A.J., Johnson M.L., Mazieres J., et al. Sotorasib versus docetaxel for previously treated non-small-cell lung cancer with KRAS(G12C) mutation: a randomised, open-label, phase 3 trial. Lancet. 2023;401(10378):733–746. PubMed
Fujino T., Suda K., Mitsudomi T. Lung cancer with MET exon 14 skipping mutation: genetic feature, current treatments, and future challenges. Lung Cancer. 2021;12:35–50. PubMed PMC
Awad M.M., Oxnard G.R., Jackman D.M., et al. MET exon 14 mutations in non-small-cell lung cancer are associated with advanced age and stage-dependent MET genomic amplification and c-met overexpression. J Clin Oncol. 2016;34(7):721–730. PubMed
Remon J., Hendriks L.E.L., Mountzios G., et al. MET alterations in NSCLC-current perspectives and future challenges. J Thorac Oncol. 2023;18(4):419–435. PubMed
Wolf J., Seto T., Han J.Y., et al. Capmatinib in MET exon 14-mutated or MET-amplified non-small-cell lung cancer. N Engl J Med. 2020;383(10):944–957. PubMed
Paik P.K., Felip E., Veillon R., et al. Tepotinib in non-small-cell lung cancer with MET exon 14 skipping mutations. N Engl J Med. 2020;383(10):931–943. PubMed PMC
Planchard D., Popat S., Kerr K., et al. Metastatic non-small cell lung cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2018;29(Suppl 4):iv192–iv237. PubMed
NHS England National genomic test directory (version June 2023) https://www.england.nhs.uk/publication/national-genomic-test-directories/
Lung cancer: diagnosis and management (NICE guideline [NG122]) 2023. https://www.nice.org.uk/guidance/ng122 PubMed
Teixeira M.E., Oliveira J., Borralho P., et al. Portuguese consensus recommendations for next-generation sequencing of lung cancer, rare tumors, and cancers of unknown primary origin in clinical practice. Acta Med Port. 2022;35(9):677–690. PubMed
Popper H.H., Gruber-Mosenbacher U., Pall G., et al. The 2020 update of the recommendations of the Austrian working group on lung pathology and oncology for the diagnostic workup of non-small cell lung cancer with focus on predictive biomarkers. Memo. 2020;13(1):11–26.
Janžič U. 2022. POROČILO BOLNIŠNIČNEGA REGISTRA TUMORJEV PRSNEGA KOŠA KLINIKE GOLNIK ZA LETA 2010 – 2020.https://www.klinika-golnik.si/dejavnost-klinike/onkoloska-dejavnost/klinicni-register-bolnikov-z-rakom-pljuc
Oncologie: Terugbetaling van de moleculair biologische testen met “next generation sequencing” (NGS) https://www.riziv.fgov.be/nl/professionals/verzorgingsinstellingen/laboratoria/Paginas/oncologie-terugbetaling-moleculair-biologische-ngs.aspx
Griesinger F., Absenger G., Bleckmann A., et al. 2022. Lungenkarzinom, nicht-kleinzellig (NSCLC)https://www.onkopedia.com/de/onkopedia/guidelines/lungenkarzinom-nicht-kleinzellig-nsclc/@@guideline/html/index.html
Patients atteints d'un cancer bronchique non à petites cellules: indications des tests moléculaires en vue de la prescription de traitements de précision. 2023. https://www.e-cancer.fr/Expertises-et-publications/Catalogue-des-publications/Patients-atteints-d-un-cancer-bronchique-non-a-petites-cellules-indications-des-tests-moleculaires-en-vue-de-la-prescription-de-traitements-de-precision
Federatie Medisch Specialisten (FMS) - Richtlijn Niet-kleincellig longcarcinoom. 2020. https://richtlijnendatabase.nl/richtlijn/niet_kleincellig_longcarcinoom/startpagina_-_niet-kleincellig_longcarcinoom.html
Lungcancer - Nationellt vårdprogram (v7.0) 2023. https://kunskapsbanken.cancercentrum.se/globalassets/cancerdiagnoser/lunga-och-lungsack/vardprogram/nationellt-vardprogram-lungcancer.pdf
Isla D., Lozano M.D., Paz-Ares L., et al. [New update to the guidelines on testing predictive biomarkers in non-small-cell lung cancer: a National Consensus of the Spanish Society of Pathology and the Spanish Society of Medical Oncology] Rev Esp Patol. 2023;56(2):97–112. PubMed
Direção-Geral da Saúde (DGS) - Diagnóstico e Tratamento do Carcinoma de Não Pequenas Células do Pulmão. 2013. https://normas.dgs.min-saude.pt/wp-content/uploads/2019/09/diagnostico-e-tratamento-do-carcinoma-de-nao-pequenas-celulas-do-pulmao.pdf
Drilon A., Duruisseaux M., Han J.Y., et al. Clinicopathologic features and response to therapy of NRG1 fusion-driven lung cancers: the eNRGy1 global multicenter registry. J Clin Oncol. 2021;39(25):2791–2802. PubMed PMC
Burghuber O.C., Kirchbacher K., Mohn-Staudner A., et al. Results of the Austrian national lung cancer audit. Clin Med Insights Oncol. 2020;14 PubMed PMC
Adizie J.B., Tweedie J., Khakwani A., et al. Biomarker testing for people with advanced lung cancer in England. JTO Clin Res Rep. 2021;2(6) PubMed PMC
Lamy T., Cabarrou B., Planchard D., et al. Biomarker testing in older patients treated for an advanced or metastatic non-squamous non-small-cell lung cancer: the French ESME real-life multicenter cohort experience. Cancers. 2021;14(1):92. PubMed PMC
Griesinger F., Eberhardt W., Nusch A., et al. Biomarker testing in non-small cell lung cancer in routine care: analysis of the first 3,717 patients in the German prospective, observational, nation-wide CRISP registry (AIO-TRK-0315) Lung Cancer. 2021;152:174–184. PubMed
Steeghs E.M.P., Groen H.J.M., Schuuring E., et al. Mutation-tailored treatment selection in non-small cell lung cancer patients in daily clinical practice. Lung Cancer. 2022;167:87–97. PubMed
Salas C., Martin-Lopez J., Martinez-Pozo A., et al. Real-world biomarker testing rate and positivity rate in NSCLC in Spain: prospective central lung cancer biomarker testing registry (LungPath) from the Spanish Society of Pathology (SEAP) J Clin Pathol. 2022;75(3):193–200. PubMed PMC
Kuijpers C., van den Heuvel M.M., Overbeek L.I.H., et al. [National variation in molecular diagnostics in metastatic lung cancer] Ned Tijdschr Geneeskd. 2018;162 PubMed
Eide I.J.Z., Nilssen Y., Stensland E.M., Brustugun O.T. Real-world data on EGFR and ALK testing and TKI usage in Norway-a nation-wide population study. Cancers. 2023;15(5):1505. PubMed PMC
Baijal S., Crosbie P., Fenemore J., Desai K. Variations in genomic testing in non-small cell lung carcinoma: a healthcare professional survey of current practices in the UK. Oncologist. 2023;28(8):e699–e702. PubMed PMC
Fox A.H., Jett J.R., Roy U.B., et al. Knowledge and practice patterns among pulmonologists for molecular biomarker testing in advanced non-small cell lung cancer. Chest. 2021;160(6):2293–2303. PubMed PMC
Roberts T.J., Kehl K.L., Brooks G.A., et al. Practice-level variation in molecular testing and use of targeted therapy for patients with non-small cell lung cancer and colorectal cancer. JAMA Netw Open. 2023;6(4) PubMed PMC
Cox S., Powell C., Morgan S. Implementing genomic testing for lung cancer into routine clinical practice - the Welsh experience. Clin Oncol. 2022;34(11):716–723. PubMed
de Jager V.D., Cajiao Garcia B.N., ter Elst A., et al. Optimalisatie van de zorgketen moleculaire diagnostiek bij niet-kleincellig longcarcinoom in Noord-Nederland. Ned Tijdschr Oncol. 2023;20:70–76.
Ossowski S., Neeman E., Borden C., et al. Improving time to molecular testing results in patients with newly diagnosed, metastatic non-small-cell lung cancer. JCO Oncol Pract. 2022;18(11):e1874–e1884. PubMed
Navani N., Butler R., Ibrahimo S., et al. Optimising tissue acquisition and the molecular testing pathway for patients with non-small cell lung cancer: a UK expert consensus statement. Lung Cancer. 2022;172:142–153. PubMed
Deans Z.C., Costa J.L., Cree I., et al. Integration of next-generation sequencing in clinical diagnostic molecular pathology laboratories for analysis of solid tumours; an expert opinion on behalf of IQN Path ASBL. Virchows Arch. 2017;470(1):5–20. PubMed PMC
Koopman B., van der Wekken A.J., Ter Elst A., et al. Relevance and effectiveness of molecular tumor board recommendations for patients with non-small-cell lung cancer with rare or complex mutational profiles. JCO Precis Oncol. 2020;4:393–410. PubMed
Koopman B., Groen H.J.M., Ligtenberg M.J.L., et al. Multicenter comparison of molecular tumor boards in the Netherlands: definition, composition, methods, and targeted therapy recommendations. Oncologist. 2021;26(8):e1347–e1358. PubMed PMC
Stenzinger A., Moltzen E.K., Winkler E., et al. Implementation of precision medicine in healthcare-a European perspective. J Intern Med. 2023;294(4):437–454. PubMed
Hofman P., Calabrese F., Kern I., et al. Real-world EGFR testing practices for non-small-cell lung cancer by thoracic pathology laboratories across Europe. ESMO Open. 2023;8(5) PubMed PMC