417
Views
5
CrossRef citations to date
0
Altmetric
Review

Pharmacotherapeutic advances with anaplastic lymphoma kinase inhibitors for the treatment of non-small cell lung cancer

, , , , , , , , & show all
Pages 931-940 | Received 10 Dec 2019, Accepted 02 Mar 2020, Published online: 12 Mar 2020

References

  • Chia PL, John T, Dobrovic A, et al. Prevalence and natural history of ALK positive non-small-cell lung cancer and the clinical impact of targeted therapy with ALK inhibitors. Clin Epidemiol. 2014;6:423–432.
  • Rodig SJ, Mino-Kenudson M, Dacic S, et al. Unique clinicopathologic features characterize ALK-rearranged lung adenocarcinoma in the Western population. Clin Cancer Res. 2009;15(16):5216–5223.
  • Pikor LA, Ramnarine VR, Lam S, et al. Genetic alterations defining NSCLC subtypes and their therapeutic implications. Lung Cancer. 2013;82(2):179–189.
  • Hallberg B, Palmer RH. Mechanistic insight into ALK receptor tyrosine kinase in human cancer biology. Nat Rev Cancer. 2013;13(10):685–700.
  • Hallberg B, Palmer RH. The role of the ALK receptor in cancer biology. Ann Oncol. 2016;27:iii4–iii15.
  • von Laffert M, Warth A, Penzel R, et al. Multicenter immunohistochemical ALK-testing of non-small-cell lung cancer shows high concordance after harmonization of techniques and interpretation criteria. J Thorac Oncol. 2014;9(11):1685–1692.
  • McCusker MG, Russo A, Scilla KA, et al. How I treat ALK positive non-small cell lung cancer. ESMO Open. 2019;4(Suppl 2):e000524.
  • Friedlaender A, Banna G, Patel S, et al. Diagnosis and treatment of ALK aberrations in metastatic NSCLC. Curr Treat Options Oncol. 2019;20(10):79.
  • Xalkori® (crizotinib) [prescribing information]. Pfizer, Inc; Revised: 7/2019.
  • Kwak EL, Bang YJ, Camidge DR, et al. Anaplastic lymphoma kinase inhibition in non–small-cell lung cancer. N Engl J Med. 2010;363(18):1693–1703.
  • Camidge DR, Bang YJ, Kwak EL, et al. Activity and safety of crizotinib in patients with ALK-positive non-small-cell lung cancer: updated results from a phase 1 study. Lancet Oncol. 2012;13(10):1011–1019.
  • Kim D-W, Ahn M-J, Shi Y, et al. Results of a global phase II study with crizotinib in advanced ALK-positive non-small cell lung cancer (NSCLC). J Clin Oncol. 2012;30(16):e147–e150.
  • Shaw AT, Kim DW, Nakagawa K, et al. Crizotinib versus chemotherapy in advanced ALK-positive lung cancer. N Engl J Med. 2013;368(25):2385–2394.
  • Blackhall F, Ross Camidge D, Shaw AT, et al. Final results of the large-scale multinational trial PROFILE 1005: efficacy and safety of crizotinib in previously treated patients with advanced/metastatic ALK-positive non-small cell lung cancer. ESMO Open. 2017;2(3):e000219.
  • Solomon BJ, Mok T, Kim D-W, et al. First-line crizotinib versus chemotherapy in ALK-positive lung cancer. N Engl J Med. 2014;371(23):2167–2177.
  • Solomon BJ, Kim D-W, Wu Y-L, et al. Final overall survival analysis from a study comparing first-line crizotinib versus chemotherapy in ALK-mutation-positive non–small-cell lung cancer. J Clin Oncol. 2018;36(22):2251–2258.
  • Kassem L, Shohdy KS, Lasheen S, et al. Safety issues with the ALK inhibitors in the treatment of NSCLC: a systematic review. Crit Rev Oncol Hematol. 2019;134:56–64.
  • Okimoto T, Tsubata Y, Hotta T, et al. A low crizotinib concentration in the cerebrospinal fluid causes ineffective treatment of anaplastic lymphoma kinase-positive non-small cell lung cancer with carcinomatous meningitis. Intern Med. 2019;58(5):703–705.
  • Costa DB, Kobayashi S, Pandya SS, et al. CSF concentration of the anaplastic lymphoma kinase inhibitor crizotinib. J Clin Oncol. 2011;29(15):e443–5.
  • Metro G, Lunardi G, Floridi P, et al. CSF concentration of crizotinib in two ALK-positive non-small-cell lung cancer patients with CNS metastases deriving clinical benefit from treatment. J Thorac Oncol. 2015 May;10(5):e26–7.
  • Weickhardt AJ, Scheier B, Burke JM, et al. Local ablative therapy of oligoprogressive disease prolongs disease control by tyrosine kinase inhibitors in oncogene-addicted non-small-cell lung cancer. J Thorac Oncol. 2012;7(12):1807–1814.
  • Gainor JF, Dardaei L, Yoda S, et al. Molecular mechanisms of resistance to first- and second-generation ALK inhibitors in ALK-rearranged lung cancer. Cancer Discov. 2016;6(10):1118–1133.
  • NCT02201992. Crizotinib in treating patients with stage IB-IIIA non-small cell lung cancer that has been removed by surgery and ALK fusion mutations (an ALCHEMIST treatment trial). [cited 2019 Dec 7]. Available from: https://clinicaltrials.gov/ct2/show/NCT02201992?term=NCT02201992&draw=1&rank=1
  • NCT03088930. Evaluating crizotinib in the neoadjuvant setting in patients with non-small cell lung cancer. [cited 2019 Dec 7]. Available from: https://clinicaltrials.gov/ct2/show/NCT03088930?term=NCT03088930&draw=1&rank=1
  • Zykadia® (ceritinib) [prescribing information]. Novartis, Inc; Revised: 5/2017.
  • Friboulet L, Li N, Katayama R, et al. The ALK inhibitor ceritinib overcomes crizotinib resistance in non-small cell lung cancer. Cancer Discov. 2014;4(6):662–673.
  • Kim DW, Mehra R, Tan DS, et al. Activity and safety of ceritinib in patients with ALK-rearranged non-small-cell lung cancer (ASCEND-1): updated results from the multicentre, open-label, phase 1 trial. Lancet Oncol. 2016;17(4):452–463.
  • Crino L, Ahn MJ, De Marinis F, et al. Multicenter phase II study of whole-body and intracranial activity with ceritinib in patients with ALK-rearranged non-small-cell lung cancer previously treated with chemotherapy and crizotinib: results from ASCEND-2. J Clin Oncol. 2016;34(24):2866–2873.
  • Soria JC, Tan DSW, Chiari R, et al. First-line ceritinib versus platinum-based chemotherapy in advanced ALK-rearranged non-small-cell lung cancer (ASCEND-4): a randomized, open-label, phase 3 study. Lancet. 2017;389(10072):917–929.
  • Tan DS, Araújo A, Zhang J, et al. Comparative efficacy of ceritinib and crizotinib as initial ALK-targeted therapies in previously treated advanced NSCLC: an adjusted comparison with external controls. J Thorac Oncol. 2016;11(9):1550–1557.
  • Novartis Europharm Limited. Zykadia hard capsules: EU summary of product characteristics. 2015. [Cited 2019 Dec 1]. Available from: http://www.ema.europa.eu
  • NCT03087448. Ceritinib + trametinib in patients with advanced ALK-positive non-small cell lung cancer (NSCLC). Available from: https:/clinicaltrials.gov/ct2/show/NCT03087448?cond=NCT03087448&draw=1&rank=1
  • NCT02292550. Study of safety and efficacy of LEE011 and ceritinib in patients with ALK-positive non-small cell lung cancer. Available from: https://clinicaltrials.gov/ct2/show/NCT02292550?term=NCT02292550&draw=1&rank=1
  • NCT01772797. Phase Ib study of LDK378 and AUY922 in ALK-rearranged non-small cell lung cancer. [cited 2019 Dec 7]. Available from: https://clinicaltrials.gov/ct2/show/NCT01772797?term=NCT01772797&draw=1&rank=1
  • Alecensa® (alectinib) tablets. [Prescribing Information]. Genentech USA, Inc.
  • Seto T, Kiura K, Nishio M, et al. CH5424802 (RO5424802) for patients with ALK-rearranged advanced non-small-cell lung cancer (AF-001JP study): a single-arm, open-label, phase 1–2 study. Lancet Oncol. 2013;14(7):590–598.
  • Gadgeel SM, Gandhi L, Riely GJ, et al. Safety and activity of alectinib against systemic disease and brain metastases in patients with crizotinib-resistant ALK-rearranged non-small-cell lung cancer (AF-002JG): results from the dose-finding portion of a phase 1/2 study. Lancet Oncol. 2014;15(10):1119–1128.
  • Shaw AT, Gandhi L, Gadgeel S, et al. Alectinib in ALK-positive, crizotinib-resistant, non-small-cell lung cancer: a single-group,multicentre, phase 2 trial. Lancet Oncol. 2016;17(2):234–242.
  • Ou SH, Ahn JS, De Petris L, et al. Alectinib in crizotinib-refractory ALK-rearranged non-small-cell lung cancer: a phase II global study. J Clin Oncol. 2016;34(7):661–668.
  • Hida T, Nokihara H, Kondo M, et al. Alectinib versus crizotinib in patients with ALK-positive non-small-cell lung cancer (J-ALEX): an open-label, randomised phase 3 trial. Lancet. 2017;390(10089):29–39.
  • Seto T, Nishio M, Hida T. Final PFS analysis and safety data from the phase III J-ALEX study of alectinib (ALC) vs. crizotinib (CRZ) in ALK-inhibitor naïve ALK-positive non-small cell lung cancer (ALK+ NSCLC). J Clin Oncol. 2019;37(Suppl): abstract 9092.
  • Peters S, Camidge DR, Shaw AT, et al. Alectinib versus crizotinib in untreated ALK-positive non-small-cell lung cancer. N Engl J Med. 2017;377(9):829–838.
  • Camidge DR, Dziadziuszko R, Peters S, et al. Updated efficacy and safety data and impact of the EML4-ALK fusion variant on the efficacy of alectinib in untreated ALK-positive advanced non-small cell lung cancer in the global phase III ALEX study. J Thorac Oncol. 2019;14(7):1233–1243.
  • Solomon BJ, Ahn JS, Barlesi F, et al. ALINA: a phase III study of alectinib versus chemotherapy as adjuvant therapy in patients with stage IB–IIIA anaplastic lymphoma kinase-positive (ALK+) non-small cell lung cancer (NSCLC). J Clin Oncol. 2019;37(Suppl): abstract TPS8569.
  • Uchibori K, Inase N, Araki M, et al. Brigatinib combined with anti-EGFR antibody overcomes osimertinib resistance in EGFR-mutated non-small-cell lung cancer. Nat Commun. 2017;8(1):14768.
  • Zhang S, Anjum R, Squillace R, et al. The potent ALK inhibitor brigatinib (AP26113) overcomes mechanisms of resistance to first- and second-generation ALK inhibitors in preclinical models. Clin Cancer Res. 2016;22(22):5527–5538.
  • Alunbrig® (brigatinib) tablets. [Prescribing Information]. ARIAD Pharmaceuticals, Inc.
  • Gettinger SN, Bazhenova LA, Langer CJ, et al. Activity and safety of brigatinib in ALK-rearranged non-small-cell lung cancer and other malignancies: a single-arm, open-label,phase 1/2 trial. Lancet Oncol. 2016;17(12):1683–1696.
  • Kim DW, Tiseo M, Ahn MJ, et al. Brigatinib in patients with crizotinib-refractory anaplastic lymphoma kinase-positive non-small-cell lung cancer: a randomized, multicenter phase II trial. J Clin Oncol. 2017;35(22):2490–2498.
  • Huber RM, Hansen KH, Paz-Ares Rodríguez L, et al. Brigatinib in crizotinib-refractory ALK+ non-small cell lung cancer: 2-year follow-up on systemic and intracranial outcomes in the phase 2 ALTA trial. J Thorac Oncol. 2020;15(3):404–415. Epub ahead of print.
  • Camidge DR, Kim HR, Ahn MJ, et al. Brigatinib versus crizotinib in ALK-positive non-small-cell lung cancer. N Engl J Med. 2018;379(21):2027–2039.
  • Camidge R, Kim HR, Ahn M, et al. Brigatinib vs crizotinib in patients with ALK inhibitor-naive advanced ALK+ NSCLC: updated results from the phase III ALTA-1L trial. Ann Oncol. 2019;30(suppl_9):ix183–ix202.
  • Stinchcombe T, Doebele RC, Wang XF, et al. Preliminary results of single arm phase 2 trial of brigatinib in patients (pts) with progression disease (PD) after next-generation (NG) anaplastic lymphoma kinase (ALK) tyrosine kinase inhibitors (TKIs) in ALK + non-small cell lung cancer (NSCLC). J Clin Oncol 2019;37(Suppl): abstract 9027..
  • NCT03535740. A study of brigatinib in participants with anaplastic lymphoma kinase-positive (ALK+), advanced non-small cell lung cancer (NSCLC) progressed on alectinib or ceritinib (ALTA-2). [cited 2019 Dec 7]. Available from: https://clinicaltrials.gov/ct2/show/NCT03535740?term=brigatinib&cond=nsclc&draw=1&rank=2
  • NCT03596866. An efficacy study comparing brigatinib versus alectinib in advanced anaplastic lymphoma kinase-positive (ALK+) non-small cell lung cancer (NSCLC) participants who have progressed on crizotinib (ALTA-3). [cited 2019 Dec 7]. Available from: https://clinicaltrials.gov/ct2/show/NCT03596866?term=brigatinib&cond=nsclc&draw=1&rank=3
  • Lorbrena® (lorlatinib) tablets. [Prescribing Information]. Pfizer Labs.
  • Patel M, Chen J, McGrory S, et al. The effect of itraconazole on the pharmacokinetics of lorlatinib: results of a phase I, open-label, crossover study in healthy participants. Invest New Drugs. 2020;38(1):131–39. Epub ahead of print.
  • Shaw AT, Felip E, Bauer TM, et al. Lorlatinib in non-small-cell lung cancer with ALK or ROS1 rearrangement: an international, multicentre, open-label, single-arm first-in-man phase 1 trial. Lancet Oncol. 2017;18(12):1590–1599.
  • Solomon BJ, Besse B, Bauer TM, et al. Lorlatinib in patients with ALK-positive non-small-cell lung cancer: results from a global phase 2 study. Lancet Oncol. 2018;19(12):1654–1667.
  • LiverTox: Clinical and Research Information on Drug-Induced Liver Injury [Internet]. Bethesda (MD): National Institute of Diabetes and Digestive and Kidney Diseases; 2012. Available from: http://www.ncbi.nlm.nih.gov/books/NBK548564/
  • Shaw AT, Solomon BJ, Besse B, et al. ALK resistance mutations and efficacy of lorlatinib in advanced anaplastic lymphoma kinase-positive non-small-cell lung cancer. J Clin Oncol. 2019;37(16):1370–1379.
  • NCT03052608. A study of lorlatinb versus crizotinib in first line treatment of patients with ALK-positive NSCLC. [cited 2019 Dec 7]. Available from: https://clinicaltrials.gov/ct2/show/NCT03052608?term=lorlatinib&cond=nsclc&draw=1&rank=9
  • Horn L, Infante JR, Reckamp KL, et al. Ensartinib (X-396) in ALK-positive non-small cell lung cancer: results from a first-in-human PhaseI/II, multicenter study. Clin Cancer Res. 2018;24(12):2771–2779.
  • Yang Y, Zhou J, Zhou J, et al. Efficacy, safety, and biomarker analysis of ensartinib in crizotinib-resistant,ALK-positive non-small-cell lung cancer: a multicentre, phase 2 trial. Lancet Respir Med. 2020;8(1):45–53. Epub ahead of print.
  • NCT02767804. eXalt3: phase 3 randomized study comparing ensartinib to crizotinib in anaplastic lymphoma kinase (ALK) positive non-small cell lung cancer (NSCLC) patients. [cited 2019 Dec 7]. Available from: https://clinicaltrials.gov/ct2/show/NCT02767804?term=nsclc&cond=ensartinib&draw=1
  • Pacheco JM, Gao D, Smith D, et al. Natural history and factors associated with overall survival in stage IV ALK-rearranged non-small cell lung cancer. J Thorac Oncol. 2019;14(4):691–700.
  • Sharma GG, Cortinovis D, Agustoni F, et al. A compound L1196M/G1202R ALK mutation in a patient with ALK-positive lung cancer with acquired resistance to brigatinib also confers primary resistance to lorlatinib. J Thorac Oncol. 2019;14(11):e257–e259.
  • JJ, Schoenfeld AJ Zhu VW, et al. Efficacy of platinum/pemetrexed combination chemotherapy in ALK-positive Non-small cell lung cancer refractory to second-generation ALK inhibitors. J Thorac Oncol. 2020;15(2):258–265.
  • NCT03737994. Biomarker/ALK inhibitor combinations in treating patients with stage IV ALK positive non-squamous non-small cell lung cancer (The NCI-NRG ALK protocol). [cited 2019 Dec 7]. Available from: https://clinicaltrials.gov/ct2/show/NCT03737994?term=NRG-LU003&draw=1&rank=1
  • Mazières J, Drilon A, Lusque A, et al. Immune checkpoint inhibitors for patients with advanced lung cancer and oncogenic driver alterations: results from the IMMUNOTARGET registry. Ann Oncol. 2019;30(8):1321–1328. Epub ahead of print.
  • Gainor JF, Shaw AT, Sequist LV, et al. EGFR mutations and ALK rearrangements are associated with low response rates to PD-1 pathway blockade in non-small cell lung cancer: a retrospective analysis. Clin Cancer Res. 2016;22(18):4585–4593.
  • Spigel DR, Reynolds C, Waterhouse D, et al. Phase ½ study of the safety and tolerability of nivolumab plus crizotinib for the first-line treatment of anaplastic lymphoma kinase translocation-positive advanced non-small cell lung cancer (Checkmate 370). J Thorac Oncol. 2018;13(5):682–688.
  • Chalmers AW, Patel S, Boucher K, et al. Phase I trial of targeted EGFR or ALK therapy with ipilimumab in metastatic NSCLC with long-term follow-up. Target Oncol. 2019;14(4):417–421.
  • Kim D-W, Gadgeel SM, Gettinger SN, et al. Safety and clinical activity results from a phase Ib study of alectinib plus atezolizumab in ALK + advanced NSCLC (aNSCLC). J Clin Oncol. 2018;36(15_suppl):9009.
  • Shaw AT, Lee S-H, Ramalingam SS, et al. Avelumab (anti–PD-L1) in combination with crizotinib or lorlatinib in patients with previously treated advanced NSCLC: phase 1B results from javelin lung 101. J Clin Oncol. 2018;36(15_suppl):9008.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.