Abstract
Purpose
Immune checkpoint inhibitors are associated with clinical benefit in lung cancer. However, response patterns to immunotherapy, including pseudoprogression and hyperprogression, are difficult to diagnose, and their mechanisms remain unclear. This review aimed to describe two response patterns observed in lung cancer, namely pseudoprogression and hyperprogression, including their epidemiology, diagnostic characteristics, and plausible mechanisms.
Methods
We performed a comprehensive literature search in the PubMed database, using keywords “pseudoprogression”, “hyperprogression”, and “lung cancer”, among others. The literature was examined for pseudoprogression and hyperprogression characteristics and plausible mechanisms.
Results
Pseudoprogression manifests in multiple forms; however, the immune system-related response criteria and biopsy data are helpful to make accurate diagnosis. Serological biomarkers, such as neutrophil-to-lymphocyte ratio (NLR) and circulating tumor DNA (ctDNA), might help distinguish pseudoprogression from true progression. The incidence of hyperprogression ranges within 5–19.2%, depending on definition. The unique response pattern of rapid progression is observed not only with immunotherapy, but also with other treatment regimens. Molecular mutations and amplifications may result in hyperprogression; however, the exact mechanism remains unclear.
Conclusion
Atypical response patterns, such as pseudoprogression and hyperprogression, are increasingly common in clinical practice. Immune-related response criteria can help diagnose pseudoprogression. Molecular mechanisms of hyperprogression remain unclear. Biomarkers for pseudoprogression and hyperprogression are required.
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References
Albert NL, Weller M, Suchorska B et al (2016) Response Assessment in Neuro-Oncology working group and European Association for Neuro-Oncology recommendations for the clinical use of PET imaging in gliomas. Neuro Oncol 18(9):1199–1208. https://doi.org/10.1093/neuonc/now058
Alexander JL, Gillespie PJ, Edelstyn GA (1976) Serial bone scanning using technetium 99m diphosphonate in patients undergoing cyclical combination chemotherapy for advanced breast cancer. Clin Nucl Med 1:13–17. https://doi.org/10.1097/00003072-197606000-00004
Bagley SJ, Kothari S, Aggarwal C et al (2017) 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. https://doi.org/10.1016/j.lungcan.2017.01.013
Barrón F, Cardona AF, Corrales L et al (2018) Characteristics of progression to tyrosine kinase inhibitors predict overall survival in patients with advanced non-small cell lung cancer harboring an EGFR mutation. J Thorac Dis 10:2166–2178. https://doi.org/10.21037/jtd.2018.03.106
Beer L, Hochmair M, Prosch H (2018) Pitfalls in the radiological response assessment of immunotherapy. Memo 11(2):138–143. https://doi.org/10.1007/s12254-018-0389-x
Bellmunt J, de Wit R, Vaughn DJ et al (2017) Pembrolizumab as second-line therapy for advanced urothelial carcinoma. N Engl J Med 376(11):1015–1026. https://doi.org/10.1056/nejmoa1613683
Bensch F, van der Veen EL, Lub-de Hooge MN et al (2018) Zr-atezolizumab imaging as a non-invasive approach to assess clinical response to PD-L1 blockade in cancer. Nat Med 24(12):1852–1858. https://doi.org/10.1038/s41591-018-0255-8
Berghoff AS, Preusser M (2018) New developments in brain metastases. Ther Adv Neurol Disord 11:1756286418785502. https://doi.org/10.1177/1756286418785502
Bohnsack O, Hoos A, Ludajic K (1070P) 1070P Adaptation of the immune-related response criteria: irRECIST. Ann Oncol 25(Supplement 4):iv361–iv372. https://doi.org/10.1093/annonc/mdu342.23
Borcoman E, Kanjanapan Y, Champiat S et al (2019) Novel patterns of response under immunotherapy. Ann Oncol 30(3):385–396. https://doi.org/10.1093/annonc/mdz003
Borghaei H, Paz-Ares L, Horn L et al (2015) Nivolumab versus docetaxel in advanced nonsquamous non-small-cell lung cancer. N Engl J Med 373:1627–1639. https://doi.org/10.1056/NEJMoa1507643
Brahmer J, Reckamp KL, Baas P et al (2015) Nivolumab versus docetaxel in advanced squamous-cell non-small-cell lung cancer. N Engl J Med 373:123–135. https://doi.org/10.1056/NEJMoa1504627
Champiat S, Dercle L, Ammari S et al (2017) Hyperprogressive disease is a new pattern of progression in cancer patients treated by anti-PD-1/PD-L1. Clin Cancer Res 23(8):1920–1928. https://doi.org/10.1158/1078-0432.ccr-16-1741
Champiat S, Ferrar R, Massard C et al (2018) Hyperprogressive disease: recognizing a novel pattern to improve patient management. Nat Rev Clin Oncol 15(12):748–762. https://doi.org/10.1038/s41571-018-0111-2
Chao HS, Chang CP, Chiu CH et al (2009) Bone scan flare phenomenon in nonsmall-cell lung cancer patients treated with gefitinib. Clin Nucl Med 34:346–349. https://doi.org/10.1097/rlu.0b013e3181a344df
Chiou VL, Burotto M (2015) Pseudoprogression and immune-related response in solid tumors. J Clin Oncol 33:3541–3543. https://doi.org/10.1200/JCO.2015.61.6870
Curioni-Fontecedro A, Ickenberg C, Franzen D et al (2018) Diffuse pseudoprogression in a patient with metastatic non-small-cell lung cancer treated with Nivolumab. Ann Oncol 28:2040–2041. https://doi.org/10.1093/annonc/mdx233
De Cecco CN, Darnell A, Rengo M et al (2012) Dual-energy CT: oncologic applications. AJR Am J Roentgenol 199:S98–S105. https://doi.org/10.2214/AJR.12.9207
Desar IM, Mulder SF, Stillebroer AB et al (2009) The reverse side of the victory: flare up of symptoms after discontinuation of sunitinib or sorafenib in renal cell cancer patients. A report of three cases. Acta Oncol 48:927–931. https://doi.org/10.1080/02841860902974167
Di Giacomo AM, Danielli R, Guidoboni M et al (2009) Therapeutic efficacy of ipilimumab, an anti-CTLA-4 monoclonal antibody, in patients with metastatic melanoma unresponsive to prior systemic treatments: clinical and immunological evidence from three patient cases. Cancer Immunol Immunother 58:1297–1306. https://doi.org/10.1007/s00262-008-0642-y
Doherty MK, Jao K, Shepherd FA et al (2015) Central nervous system pseudoprogression in a patient treated with PD-1 checkpoint inhibitor. J Thorac Oncol 10:e100–101. https://doi.org/10.1097/JTO.0000000000000587
Dulos J, Carven GJ, van Boxtel SJ et al (2012) PD-1 blockade augments Th1 and Th17 and suppresses Th2 responses in peripheral blood from patients with prostate and advanced melanoma cancer. J Immunother 35:169–178. https://doi.org/10.1097/CJI.0b013e318247a4e7
Ellestad KK, Thangavelu G, Ewen CL et al (2014) PD-1 is not required for natural or peripherally induced regulatory T cells: severe autoimmunity despite normal production of regulatory T cells. Eur J Immunol 44:3560–3572. https://doi.org/10.1002/eji.201444688
Erasmus JJ, Gladish GW, Broemeling L et al (2003) Interobserver and intraobserver variability in measurement of non-small-cell carcinoma lung lesions: implications for assessment of tumor response. J Clin Oncol 21(13):2574–2582. https://doi.org/10.1200/jco.2003.01.144
Ferrara R, Mezquita L, Texier M et al (2018) Hyperprogressive Disease in patients with advanced non-small cell lung cancer treated with PD-1/PD-L1 inhibitors or with single-agent chemotherapy. JAMA Oncol 4(11):1543–1552. https://doi.org/10.1001/jamaoncol.2018.3676
Ferris RL, Blumenschein G Jr, Fayette J et al (2016) Nivolumab for recurrent squamous-cell carcinoma of the head and neck. N Engl J Med 375(19):1856–1867. https://doi.org/10.1038/sj.bdj.2016.860
Galldiks N, Kocher M, Ceccon G et al (2020) Imaging challenges of immunotherapy and targeted therapy in patients with brain metastases: response, progression, and pseudoprogression. Neuro-oncology 22(1):17–30. https://doi.org/10.1093/neuonc/noz147
Gandara DR, von Pawel J, Mazieres J et al (2018) Atezolizumab treatment beyond progression in advanced NSCLC: results from the randomized, phase III OAK study. J Thorac Oncol 13:1906–1918. https://doi.org/10.1016/j.jtho.2018.08.2027
Garassino M, Cho BC, Kim JH et al (2018) Durvalumab as third-line or later treatment for advanced non-small-cell lung cancer (ATLANTIC): an open-label, single-arm, phase 2 study. Lancet Oncol 19(4):521–536. https://doi.org/10.1016/s1470-2045(18)30144-x
Guibert N, Mazieres J, Delaunay M et al (2017) Monitoring of KRAS-mutated ctDNA to discriminate pseudo-progression from true progression during anti-PD-1 treatment of lung adenocarcinoma. Oncotarget 8(23):38056–38060. https://doi.org/10.18632/oncotarget.16935
Guthrie GJ, Charles KA, Roxburgh CS et al (2013) The systemic inflammation-based neutrophil-lymphocyte ratio: experience in patients with cancer. Crit Re Oncol Hematol 88:218–230. https://doi.org/10.1016/j.critrevonc.2013.03.010
Hammer M, Bagley S, Aggarwal C et al (2019) Thoracic imaging of non-small cell lung cancer treated with anti-programmed death receptor-1 therapy. Curr Probl Diagn Radiol 48(2):142–147. https://doi.org/10.1067/j.cpradiol.2018.01.005
Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144:646–674. https://doi.org/10.1016/j.cell.2011.02.013
Hendriks LEL, Henon C, Auclin E et al (2019) Outcome of patients with non-small cell lung cancer and brain metastases treated with checkpoint inhibitors. J Thorac Oncol 14(7):1244–1254. https://doi.org/10.1016/j.jtho.2019.02.009
Herbst RS, Baas P, Kim DW et al (2016) Pembrolizumab versus docetaxel for previously treated, PD-L1-positive, advanced non-small-cell lung cancer: a randomised controlled trial. Lancet 387:1540–1550. https://doi.org/10.1016/S0140-6736(15)01281-7
Hodi FS, Oble DA, Drappatz J et al (2008) CTLA-4 blockade with ipilimumab induces signifificant clinical benefifit in a female with melanoma metastases to the CNS. Nat Clin Pract Oncol 5(9):557–561. https://doi.org/10.1038/ncponc1183
Hodi FS, Hwu WJ, Kefford R et al (2016) Evaluation of immune-related response criteria and RECIST v1.1 in patients with advanced melanoma treated with Pembrolizumab. J Clin Oncol 34:1510–1517. https://doi.org/10.1200/JCO.2015.64.0391
Huang B, Pan PY, Li Q et al (2006) Gr-1+CD115+immature myeloid suppressor cells mediate the development of tumorinduced T regulatory cells and T cell anergy in tumor-bearing host. Cancer Res 66:1123–1131. https://doi.org/10.1158/0008-5472.can-05-1299
Huang RY, Francois A, McGray AR et al (2017) Compensatory upregulation of PD-1, LAG-3, and CTLA-4 limits the efficacy of single-agent checkpoint blockade in metastatic ovarian cancer. Oncoimmunology 6:e1249561. https://doi.org/10.1080/2162402x.2016.1249561
Iacovelli R, Massari F, Albiges L et al (2015) Evidence and clinical relevance of tumor flare in patients who discontinue tyrosine kinase inhibitors for treatment of metastatic renal cell carcinoma. Eur Urol 68:154–160. https://doi.org/10.1016/j.eururo.2014.10.034
Jensen TJ, Goodman AM, Kato S et al (2019) Genome-wide sequencing of cell-free DNA identifies copy-number alterations that can be used for monitoring response to immunotherapy in cancer patients. Mol Cancer Ther 18(2):448–458. https://doi.org/10.1158/1535-7163.mct-18-0535
Kang MH, Go SI, Song HN et al (2014) The prognostic impact of the neutrophil-to-lymphocyte ratio in patients with small-cell lung cancer. Br J Cancer 111:452–460. https://doi.org/10.1038/bjc.2014.317
Kas B, Talbot H, Ferrara R et al (2020) Clarification of definitions of hyperprogressive disease during immunotherapy for non-small cell lung cancer. JAMA Oncol 6(7):1039–1046. https://doi.org/10.1001/jamaoncol.2020.1634
Kato R, Hayashi H, Tanizaki J et al (2017a) Peritumoural ground-glass opacity associated with tumour pseudoprogression in a patient with non-small cell lung cancer treated with nivolumab. ESMO Open 2:e000145. https://doi.org/10.1136/esmoopen-2016-000145
Kato S, Goodman A, Walavalkar V et al (2017b) Hyperprogressors after immunotherapy: analysis of genomic alterations associated with accelerated growth rate. Clin Cancer Res 23:4242–4250. https://doi.org/10.1158/1078-0432.ccr-16-3133
Kazandjian D, Keegan P, Suzman DL et al (2017) Characterization of outcomes in patients with metastatic non-small cell lung cancer treated with programmed cell death protein 1 inhibitors past RECIST version1.1-defined disease progression in clinical trials. Semin Oncol 44:3–7. https://doi.org/10.1053/j.seminoncol.2017.01.001
Kim HK, Heo MH, Lee HS et al (2017) Comparison of RECIST to immune-related response criteria in patients with non-small cell lung cancer treated with immune-checkpoint inhibitors. Cancer Chemother Pharmacol 80(3):591–598. https://doi.org/10.1007/s00280-017-3396-4
Kim EY, Park I, Kim YS (2019a) Unusual radiologic manifestation of pseudoprogression in pulmonary metastases after durvalumab treatment in metastatic bladder urothelial cancer. Thorac Cancer 10(4):1016–1018. https://doi.org/10.1111/1759-7714.12994
Kim HK, Baek SW, Jeong Y et al (2019b) Pseudoprogression presenting as intestinal perforation in non-small cell lung cancer treated with anti-PD-1: a case report. Mol Clin Oncol 11(2):132–134. https://doi.org/10.3892/mco.2019.1871
Kim CG, Kim KH, Pyo K-H et al (2019c) Hyperprogressive disease during PD-1/PD-L1 blockade in patients with non-small-cell lung cancer. Ann Oncol 30(7):1104–1113. https://doi.org/10.1093/annonc/mdz123
Kim SH, Choi CM, Lee DH et al (2020) Clinical outcomes of nivolumab in patients with advanced non-small cell lung cancer in real-world practice, with an emphasis on hyper-progressive disease. J Cancer Res Clin Oncol. https://doi.org/10.1007/s00432-020-03293-9
Krupitskaya Y, Eslamy HK, Nguyen DD et al (2009) Osteoblastic bone flare on F18-FDG PET in non-small cell lung cancer (NSCLC) patients receiving bevacizumab in addition to standard chemotherapy. J Thorac Oncol 4(3):429–431. https://doi.org/10.1097/jto.0b013e3181989e12
Kuriyama Y, Kim YH, Nagai H et al (2013) Disease flare after discontinuation of crizotinib in anaplastic lymphoma kinase-positive lung cancer. Case Rep Oncol 6:430–433. https://doi.org/10.1159/000354756
Kurra V, Sullivan RJ, Gainor JF et al (2016) Pseudoprogression in cancer immunotherapy: Rates, time course and patient outcomes. J Clin Oncol 34(15_suppl):6580–6580. https://doi.org/10.1200/JCO.2016.34.15_suppl.6580
Lamichhane P, Karyampudi L, Shreeder B et al (2017) IL-10 release upon PD-1 blockade sustains immunosuppression in ovarian cancer. Cancer Res 77:6667–6678. https://doi.org/10.1158/0008-5472.CAN-17-0740
Langen KJ, Galldiks N, Hattingen E et al (2017) Advances in neuro-oncology imaging. Nat Rev Neurol 13(5):279–289. https://doi.org/10.1038/nrneurol.2017.44
Lau SCM, Leighl NB (2019) Hyperprogressive disease with immunotherapy: new directions. J Thorac Dis 11:S1877–S1880. https://doi.org/10.21037/jtd.2019.08.88
Lee JH, Long GV, Menzies AM et al (2018) Association between circulating tumor DNA and pseudoprogression in patients with metastatic melanoma treated with anti-programmed cell death 1 antibodies. JAMA Oncol 4(5):717–721. https://doi.org/10.1001/jamaoncol.2017.5332
Lemieux J, Guimond J, Laberge F et al (2002) The bone scan flare phenomenon in nonsmall-cell lung cancer. Clin Nucl Med 27:486–489. https://doi.org/10.1097/00003072-200207000-00004
Lin X, Lu T, Xie Z et al (2019) Extracranial abscopal effect induced by combining immunotherapy with brain radiotherapy in a patient with lung adenocarcinoma: a case report and literature review. Thorac Cancer 10(5):1272–1275. https://doi.org/10.1111/1759-7714.13048
Liu G, Chen T, Li R et al (2018) Well-controlled pleural effusion indicated pseudoprogression after immunotherapy in lung cancer: a case report. Thorac Cancer 9(9):1190–1193. https://doi.org/10.1111/1759-7714.12799
Lo Russo G, Moro M, Sommariva M et al (2019) AntibodyFc/FcR interaction on macrophages as a mechanism for hyperprogressive disease in non-small cell lung cancer subsequent to PD-1/PD-L1 blockade. Clin Cancer Res 25:989–999. https://doi.org/10.1158/1078-0432.CCR-18-1390
Mantovani A, Sica A (2010) Macrophages, innate immunity and cancer: balance, tolerance, and diversity. Curr Opin Immunol 22:231–237. https://doi.org/10.1016/j.coi.2010.01.009
Masaki K, Ryuya E, Hiroyuki K et al (2018) Hyperprogressive disease in patients with non-small cell lung cancer treated with nivolumab: a case series. Thorac Cancer 9:1782–1787. https://doi.org/10.1111/1759-7714.12894
Matos I, Martin-Liberal J, Hierro C et al (2018) Incidence and clinical implications of a new definition of hyperprogression(HPD) with immune checkpoint inhibitors (ICIs) in patients treated in phase 1 (Ph1)trials. J Clin Oncol 36(15 suppl):3032–3032. https://doi.org/10.1200/jco.2018.36.15_suppl.3032
Matsuo N, Azuma K, Hattori S et al (2019) Association between soluble immune mediators and tumor responses in patients with nonsmall cell lung cancer treated with anti-PD-1 inhibitor. Int J Cancer 144(5):1170–1179. https://doi.org/10.1002/ijc.31923
Melian M, Lorente D, Aparici F et al (2018) Lung brain metastasis pseudoprogression after nivolumab and ipilimumab combination treatment. Thorac Cancer 9(12):1770–1773. https://doi.org/10.1111/1759-7714.12873
Mellema WW, Burgers SA, Smit EF (2015) Tumor flare after start of RAF inhibition in KRAS mutated NSCLC: a case report. Lung Cancer 87:201–203. https://doi.org/10.1016/j.lungcan.2014.11.014
Mezquita L, Auclin E, Ferrara R et al (2018) Association of the lung immune prognostic index with immune checkpoint inhibitor outcomes in patients with advanced non-small cell lung cancer. JAMA Oncol 4:351–357. https://doi.org/10.1001/jamaoncol.2017.4771
Molina JR, Yang P, Cassivi SD, Schild SE, Adjei AA (2008) Non-small cell lung cancer: epidemiology, risk factors, treatment, and survivorship. Mayo Clin Proc 83(5):584–594. https://doi.org/10.4065/83.5.584
Nishino M, Guo M, Jackman DM et al (2011) CT tumor volume measurement in advanced non-small-cell lung cancer: performance characteristics of an emerging clinical tool. Acad radiol 18(1):54–62. https://doi.org/10.1016/j.acra.2010.08.021
Nishino M, Giobbie-Hurder A, Gargano M et al (2013) Developing a common language for tumor response to immunotherapy: immune related response criteria using unidimensional measurements. Clin Cancer Res 19(14):3936–3943. https://doi.org/10.1158/1078-0432.ccr-13-0895
Nishino M, Ramaiya NH, Chambers ES et al (2016) Immune-related response assessment during PD-1 inhibitor therapy in advanced non-small-cell lung cancer patients. J Immunother Cancer 4:84–93. https://doi.org/10.1186/s40425-016-0193-2
Pop O, Pirvu A, Toffart AC et al (2012) Disease flare after treatment discontinuation in a patient with EML4-ALK lung cancer and acquired resistance to crizotinib. J Thorac Oncol 7:e1–e2. https://doi.org/10.1097/jto.0b013e318257fc1d
Popat V, Gerber DE (2019) Hyperprogressive disease: a distinct effect of immunotherapy? J Thorac Dis 11:S262–S265. https://doi.org/10.21037/jtd.2019.01.97
Powles T, Kayani I, Sharpe K et al (2013) A prospective evaluation of VEGF targeted treatment cessation in metastatic clear cell renal cancer. Ann Oncol 24:2098–2103. https://doi.org/10.1093/annonc/mdt130
Powles T, Duran I, van der Heijden MS et al (2018) Atezolizumab versus chemotherapy in patients with platinum-treated locally advanced or metastatic urothelial carcinoma (IMvigor211): a multicentre, open-label, phase 3 randomised controlled trial. Lancet 391(10122):748–757. https://doi.org/10.1016/s0140-6736(17)33297-x
Raez LE, Cassileth PA, Schlesselman JJ, Sridhar K, Padmanabhan S, Fisher EZ, Baldie PA, Podack ER (2004) Allogeneic vaccination with a B7.1 HLA-A gene-modified adenocarcinoma cell line in patients with advanced non-small-cell lung cancer. J Clin Oncol 22(14):2800–2807. https://doi.org/10.1200/JCO.2004.10.197
Ricciuti B, Genova C, Bassanelli M et al (2019) Safety and efficacy of nivolumab in patients with advanced non-small-cell lung cancer treated beyond progression. Clin Lung Cancer 20:178.e2–185.e2. https://doi.org/10.1016/j.cllc.2019.02.001
Riely GJ, Kris MG, Zhao B et al (2007) Prospective assessment of discontinuation and reinitiation of erlotinib or gefitinib in patients with acquired resistance to erlotinib or gefitinib followed by the addition of everolimus. Clin Cancer Res 13:5150–5155. https://doi.org/10.1158/1078-0432.ccr-07-0560
Rittmeyer A, Barlesi F, Waterkamp D et al (2017) Atezolizumab versus docetaxel in patients with previously treated nonsmall cell lung cancer (OAK): a phase 3, open-label, multicentre randomised controlled trial. Lancet 389:255–265. https://doi.org/10.1016/s0140-6736(16)32517-x
Saada-Bouzid E, Defaucheux C, Karabajakian A et al (2017) Hyperprogression during anti-PD-1/PD-L1 therapy in patients with recurrent and/or metastatic head and neck squamous cell carcinoma. Ann Oncol 28(7):1605–1611. https://doi.org/10.1093/annonc/mdx178
Saenger YM, Wolchok JD (2008) The heterogeneity of the kinetics of response to ipilimumab in metastatic melanoma: patient cases. Cancer Immun 8:1
Sage PT, Francisco LM, Carman CV et al (2013) The receptor PD-1 controls follicular regulatory T cells in the lymph nodes and blood. Nat Immunol 14:152–161. https://doi.org/10.1038/ni.2496
Sanmamed MF, Perez-Gracia JL, Schalper KA et al (2017) Changes in serum interleukin-8 (IL-8) levels reflect and predict response to anti-PD-1 treatment in melanoma and non-small cell lung cancer patients. Ann Oncol 28(8):1988–1995. https://doi.org/10.1093/annonc/mdx190
Sarfaty M, Moore A, Dudnik E et al (2017) Not only for melanoma. Subcutaneous pseudoprogression in lung squamous-cell carcinoma treated with nivolumab: a case report. Medicine (Baltimore) 96:e5951. https://doi.org/10.1097/MD.0000000000005951
Seymour L, Bogaerts J, Perrone A et al (2017) iRECIST: guidelines for response criteria for use in trials testing immunotherapeutics. Lancet Oncol 18:e143–e152. https://doi.org/10.1016/s1470-2045(17)30074-8
Shepherd FA, Papadimitrakopoulou V, Mok T et al (2018) Early clearance of plasma EGFR mutations as a predictor of response to osimertinib in the AURA3 trial. J Clin Oncol 36:abstr 9027. https://doi.org/10.1200/jco.2018.36.15_suppl.9027
Siegel RL, Miller KD, Jemal A (2018) Cancer statistics. CA Cancer J Clin 68(1):7–30. https://doi.org/10.3322/caac.21442
Siegel RL, Miller KD, Jemal A (2020) Cancer statistics. CA Cancer J Clin 70(1):7–30. https://doi.org/10.3322/caac.21590
Singavi AK, Menon S, Kilari D et al (1140PD) Predictive biomarkers for hyper-progression (HP) in response to immune checkpoint inhibitors (ICI)—analysis of somatic alterations (SAs). Ann Oncol 28:1140PD. https://doi.org/10.1093/annonc/mdx376.006
Skoulidis F, Goldberg ME, Greenawalt DM et al (2018) STK11/LKB1 mutations and PD-1 inhibitor resistance in KRAS-mutant lung adenocarcinoma. Cancer Discov 8:822–835. https://doi.org/10.1158/2159-8290.CD-18-0099
Skoulidis F, Arbour KC, Hellmann MD et al (2019) Association of STK11/LKB1 genomic alterations with lack of benefit from the addition of pembrolizumab to platinum doublet chemotherapy in non-squamous non-small cell lung cancer. J Clin Oncol 37:abstr 102. https://doi.org/10.1200/jco.2019.37.15_suppl.102
Solinas C, Porcu M, Hlavata Z et al (2017) Critical features and challenges associated with imaging in patients undergoing cancer immunotherapy. Crit Rev Oncol Hematol 120:13–21. https://doi.org/10.1016/j.critrevonc.2017.09.017
Song P, Zhang J, Shang C et al (2019) Curative effect assessment of immunotherapy for non-small cell lung cancer: the “blind area” of immune response evaluation criteria in solid tumors (iRECIST). Thoracic Cancer 10(4):587–592. https://doi.org/10.1111/1759-7714.13010
Taniguchi Y, Tamiya A, Isa S et al (2017) Predictive factors for poor progression-free survival in patients with non-small cell lung cancer treated with nivolumab. Anticancer Res 37(10):5857–5862. https://doi.org/10.21873/anticanres.12030
Tanizaki J, Hayashi H, Kimura M et al (2016) Report of two cases of pseudoprogression in patients with non-small cell lung cancer treated with nivolumab-including histological analysis of one case after tumor regression. Lung Cancer 102:44–48. https://doi.org/10.1016/j.lungcan.2016.10.014
Tazdait M, Mezquita L, Lahmar J et al (2018) Patterns of responses in metastatic NSCLC during PD-1 or PDL-1 inhibitor therapy: comparison of RECIST 1.1, irRECIST and iRECIST criteria. Eur J Cancer 88:38–47. https://doi.org/10.1016/j.ejca.2017.10.017
Templeton AJ, McNamara MG, Šeruga B et al (2014) Prognostic role of neutrophil-to-lymphocyte ratio in solid tumors: a systematic review and meta-analysis. J Natl Cancer Inst 106:dju124. https://doi.org/10.1093/jnci/dju124
Vrankar M, Unk M (2018) Immune RECIST criteria and symptomatic pseudoprogression in non-small cell lung cancer patients treated with immunotherapy. Radiol Oncol 52(4):365–369. https://doi.org/10.2478/raon-2018-0037
Wang Q, Gao J, Wu X et al (2018) Pseudoprogression and hyperprogression after checkpoint blockade. Int Immunopharmacol 58:125–135. https://doi.org/10.1016/j.intimp.2018.03.018
Weiss GJ, Beck J, Braun DP et al (2017) Tumor cell-free DNA copy number instability predicts therapeutic response to immunotherapy. Clin Cancer Res 23(17):5074–5081. https://doi.org/10.1158/1078-0432.ccr-17-0231
Wolchok JD, Hoos A, O’Day S et al (2009) Guidelines for the evaluation of immune therapy activity in solid tumors: immunerelated response criteria. Clin Cancer Res 15:7412–7420. https://doi.org/10.1158/1078-0432.CCR-09-1624
Wolter P, Beuselinck B, Pans S et al (2009) Flare-up: an often unreported phenomenon nevertheless familiar to oncologists prescribing tyrosine kinase inhibitors. Acta Oncol 48:621–624. https://doi.org/10.1080/02841860802609574
Xiong D, Wang Y, Singavi AK et al (2018) Immunogenomic landscape contributes to hyperprogressive disease after Anti-PD-1 immunotherapy for cancer. iScience 9:258–277. https://doi.org/10.1016/j.isci.2018.10.021
Yang JJ, Chen HJ, Yan HH et al (2013) Clinical modes of EGFR tyrosine kinase inhibitor failure and subsequent management in advanced non-small cell lung cancer. Lung Cancer 79:33–39. https://doi.org/10.1016/s0923-7534(20)33797-2
Yang K, Blanco DB, Neale G et al (2017) Homeostatic control of metabolic and functional fitness of Treg cells by LKB1 signalling. Nature 548:602–606. https://doi.org/10.1038/nature23665
Zer A, Sung MR, Walia P et al (2018) Correlation of neutrophil to lymphocyte ratio and absolute neutrophil count with outcomes with PD-1 axis inhibitors in patients with advanced non-small-cell lung cancer. Clin Lung Cancer 19(5):426–434.e1. https://doi.org/10.1016/j.cllc.2018.04.008
Zhao B, James LP, Moskowitz CS et al (2009) Evaluating variability in tumor measurements from same-day repeat CT scans of patients with non-small cell lung cancer. Radiology 252(1):263–272. https://doi.org/10.1148/radiol.2522081593
Zhou C, Imamura F, Cheng Y et al (2019) Early clearance of plasma EGFR mutations as a predictor of response to osimertinib and comparator EGFR-TKIs in the FLAURA trial. J Clin Oncol 37:abstr 9020. https://doi.org/10.1200/jco.2019.37.15_suppl.9020
Acknowledgements
The work was sponsored by National Key Research and Development Program of China (No. 2018YFC1311400/2018YFC1311402); National Natural Science Foundation of China (Grants 81672982, 81872478).
Funding
This work was supported by National Key Research and Development Program of China (No. 2018YFC1311400/2018YFC1311402); National Natural Science Foundation of China (Grants 81672982, 81872478).
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Zhou, L., Zhang, M., Li, R. et al. Pseudoprogression and hyperprogression in lung cancer: a comprehensive review of literature. J Cancer Res Clin Oncol 146, 3269–3279 (2020). https://doi.org/10.1007/s00432-020-03360-1
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DOI: https://doi.org/10.1007/s00432-020-03360-1