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Combinatorial Chemistry & High Throughput Screening

Editor-in-Chief

ISSN (Print): 1386-2073
ISSN (Online): 1875-5402

Meta-Analysis

Anti-Angiogenic Agents Combined with Immunotherapy for Advanced Non-Small Cell Lung Cancer: A Systematic Review and Meta-Analysis

Author(s): Heng Lin, Chenhui Ma, Aihong Zhong, Huanping Zang, Wenxin Chen, Lixiu Li, Yuyin Le and Qiang Xie*

Volume 27, Issue 7, 2024

Published on: 25 August, 2023

Page: [1081 - 1091] Pages: 11

DOI: 10.2174/1386207326666230808112656

Price: $65

Abstract

Background: Anti-angiogenic agents could enhance tumor immunity response, and anti- angiogenesis plus immunotherapy has become a novel treatment option for advanced non-small cell lung cancer (NSCLC). The efficacy of this combination therapy remains controversial and obscure.

Aim: We conducted a meta-analysis to evaluate the clinical efficacy and safety of this therapeutic strategy in patients with advanced NSCLC and provide more guidance for treating NSCLC clinically.

Methods: A systematic literature search was performed in PubMed, Embase, Web of Science, CNKI, and Wanfang databases to identify relevant studies published up to December 2021. The primary endpoint was the objective response rate (ORR). Second endpoints were progression-free survival (PFS), overall survival (OS), and grade ≥3 AEs adverse events (AEs). The sensitivity analysis was conducted to confirm the stability of the results. STATA 15.0 was utilized for all pooled analyses.

Results: Eleven studies were eventually included in the meta-analysis, involving 533 patients with advanced NSCLC. The pooled ORR rate was 27% (95% CI 18% to 35%; I2 =84.2%; p<0.001), while the pooled median PFS and OS was 5.84 months (95% CI 4.66 to 7.03 months; I2=78.4%; p<0.001) and 14.20 months (95% CI 11.08 to 17.32 months; I2=82.2%; p=0.001), respectively. Most common grade ≥3 AEs included hypertension, hand-foot syndrome, diarrhea, adrenal insufficiency, hyponatremia, proteinuria, rash, thrombocytopenia, and fatigue.

Conclusion: Anti-angiogenesis combined with immunotherapy demonstrated satisfactory antitumor activity and an acceptable toxicity profile in patients with advanced NSCLC. The pooled results of our meta-analysis provided further evidence supporting the favorable efficacy and safety of this therapeutic strategy.

Keywords: Anti-angiogenesis, immunotherapy, combination therapy, non-small cell lung cancer (NSCLC), adverse events (AEs), overall survival (OS).

Graphical Abstract
[1]
Sung, H.; Ferlay, J.; Siegel, RL. 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.
[2]
Herbst, R.S.; Morgensztern, D.; Boshoff, C. The biology and management of non-small cell lung cancer. Nature., 2018, 553(7689), 446-454.
[http://dx.doi.org/10.1038/nature25183] [PMID: 29364287]
[3]
Siegel, RL; Miller, KD Cancer statistics, 2023. CA Cancer J. Clin., 2023, 73(1), 17-48.
[4]
Arbour, K.C.; Riely, G.J. Systemic therapy for locally advanced and metastatic non–small cell lung cancer. JAMA, 2019, 322(8), 764-774.
[http://dx.doi.org/10.1001/jama.2019.11058] [PMID: 31454018]
[5]
Bray, F.; Ferlay, J.; Soerjomataram, I.; Siegel, R.L.; Torre, L.A.; Jemal, A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin., 2018, 68(6), 394-424.
[http://dx.doi.org/10.3322/caac.21492] [PMID: 30207593]
[6]
Doroshow, D.B.; Sanmamed, M.F.; Hastings, K.; Politi, K.; Rimm, D.L.; Chen, L.; Melero, I.; Schalper, K.A.; Herbst, R.S. Immunotherapy in Non–Small Cell Lung Cancer: Facts and Hopes. Clin. Cancer Res., 2019, 25(15), 4592-4602.
[http://dx.doi.org/10.1158/1078-0432.CCR-18-1538] [PMID: 30824587]
[7]
Lim, S.M.; Hong, M.H.; Kim, H.R. Immunotherapy for non-small cell lung cancer: Current landscape and future perspectives. Immune Netw., 2020, 20(1), e10.
[http://dx.doi.org/10.4110/in.2020.20.e10] [PMID: 32158598]
[8]
Mok, T.S.K.; Wu, Y.L.; Kudaba, I.; Kowalski, D.M.; Cho, B.C.; Turna, H.Z.; Castro, G., Jr; Srimuninnimit, V.; Laktionov, K.K.; Bondarenko, I.; Kubota, K.; Lubiniecki, G.M.; Zhang, J.; Kush, D.; Lopes, G.; Adamchuk, G.; Ahn, M-J.; Alexandru, A.; Altundag, O.; Alyasova, A.; Andrusenko, O.; Aoe, K.; Araujo, A.; Aren, O.; Arrieta Rodriguez, O.; Ativitavas, T.; Avendano, O.; Barata, F.; Barrios, C.H.; Beato, C.; Bergstrom, P.; Betticher, D.; Bolotina, L.; Bondarenko, I.; Botha, M.; Buddu, S.; Caglevic, C.; Cardona, A.; Castro, G., Jr; Castro, H.; Cay Senler, F.; Cerny, C.A.S.; Cesas, A.; Chan, G-C.; Chang, J.; Chen, G.; Chen, X.; Cheng, S.; Cheng, Y.; Cherciu, N.; Chiu, C-H.; Cho, B.C.; Cicenas, S.; Ciurescu, D.; Cohen, G.; Costa, M.A.; Danchaivijitr, P.; De Angelis, F.; de Azevedo, S.J.; Dediu, M.; Deliverski, T.; De Marchi, P.R.M.; de The Bustamante Valles, F.; Ding, Z.; Doganov, B.; Dreosti, L.; Duarte, R.; Edusma-Dy, R.; Emelyanov, S.; Erman, M.; Fan, Y.; Fein, L.; Feng, J.; Fenton, D.; Fernandes, G.; Ferreira, C.; Franke, F.A.; Freitas, H.; Fujisaka, Y.; Galindo, H.; Galvez, C.; Ganea, D.; Gil, N.; Girotto, G.; Goker, E.; Goksel, T.; Gomez Aubin, G.; Gomez Wolff, L.; Griph, H.; Gumus, M.; Hall, J.; Hart, G.; Havel, L.; He, J.; He, Y.; Hernandez Hernandez, C.; Hespanhol, V.; Hirashima, T.; Ho, C.M.J.; Horiike, A.; Hosomi, Y.; Hotta, K.; Hou, M.; How, S.H.; Hsia, T-C.; Hu, Y.; Ichiki, M.; Imamura, F.; Ivashchuk, O.; Iwamoto, Y.; Jaal, J.; Jassem, J.; Jordaan, C.; Juergens, R.A.; Kaen, D.; Kalinka-Warzocha, E.; Karaseva, N.; Karaszewska, B.; Kazarnowicz, A.; Kasahara, K.; Katakami, N.; Kato, T.; Kawaguchi, T.; Kim, J.H.; Kishi, K.; Kolek, V.; Koleva, M.; Kolman, P.; Koubkova, L.; Kowalyszyn, R.; Kowalski, D.; Koynov, K.; Ksienski, D.; Kubota, K.; Kudaba, I.; Kurata, T.; Kuusk, G.; Kuzina, L.; Laczo, I.; Ladrera, G.E.I.; Laktionov, K.; Landers, G.; Lazarev, S.; Lerzo, G.; Lesniewski Kmak, K.; Li, W.; Liam, C.K.; Lifirenko, I.; Lipatov, O.; Liu, X.; Liu, Z.; Lo, S.H.; Lopes, V.; Lopez, K.; Lu, S.; Martinengo, G.; Mas, L.; Matrosova, M.; Micheva, R.; Milanova, Z.; Miron, L.; Mok, T.; Molina, M.; Murakami, S.; Nakahara, Y.; Nguyen, T.Q.; Nishimura, T.; Ochsenbein, A.; Ohira, T.; Ohman, R.; Ong, C.K.; Ostoros, G.; Ouyang, X.; Ovchinnikova, E.; Ozyilkan, O.; Petruzelka, L.; Pham, X.D.; Picon, P.; Piko, B.; Poltoratsky, A.; Ponomarova, O.; Popelkova, P.; Purkalne, G.; Qin, S.; Ramlau, R.; Rappaport, B.; Rey, F.; Richardet, E.; Roubec, J.; Ruff, P.; Rusyn, A.; Saka, H.; Salas, J.; Sandoval, M.; Santos, L.; Sawa, T.; Seetalarom, K.; Seker, M.; Seki, N.; Seolwane, F.; Shepherd, L.; Shevnya, S.; Shimada, A.K.; Shparyk, Y.; Sinielnikov, I.; Sirbu, D.; Smaletz, O.; Soares, J.P.H.; Sookprasert, A.; Speranza, G.; Srimuninnimit, V.; Sriuranpong, V.; Stara, Z.; Su, W-C.; Sugawara, S.; Szpak, W.; Takahashi, K.; Takigawa, N.; Tanaka, H.; Tan Chun Bing, J.; Tang, Q.; Taranov, P.; Tejada, H.; Tho, L.M.; Torii, Y.; Trukhyn, D.; Turdean, M.; Turna, H.; Ursol, G.; Vanasek, J.; Varela, M.; Vallejo, M.; Vera, L.; Victorino, A-P.; Vlasek, T.; Vynnychenko, I.; Wang, B.; Wang, J.; Wang, K.; Wu, Y.; Yamada, K.; Yang, C-H.; Yokoyama, T.; Yokoyama, T.; Yoshioka, H.; Yumuk, F.; Zambrano, A.; Zarba, J.J.; Zarubenkov, O.; Zemaitis, M.; Zhang, L.; Zhang, L.; Zhang, X.; Zhao, J.; Zhou, C.; Zhou, J.; Zhou, Q.; Zippelius, A. Pembrolizumab versus chemotherapy for previously untreated, PD-L1-expressing, locally advanced or metastatic non-small-cell lung cancer (KEYNOTE-042): A randomised, open-label, controlled, phase 3 trial. Lancet, 2019, 393(10183), 1819-1830.
[http://dx.doi.org/10.1016/S0140-6736(18)32409-7] [PMID: 30955977]
[9]
Sezer, A.; Kilickap, S.; Gümüş, M.; Bondarenko, I.; Özgüroğlu, M.; Gogishvili, M.; Turk, H.M.; Cicin, I.; Bentsion, D.; Gladkov, O.; Clingan, P.; Sriuranpong, V.; Rizvi, N.; Gao, B.; Li, S.; Lee, S.; McGuire, K.; Chen, C.I.; Makharadze, T.; Paydas, S.; Nechaeva, M.; Seebach, F.; Weinreich, D.M.; Yancopoulos, G.D.; Gullo, G.; Lowy, I.; Rietschel, P. Cemiplimab monotherapy for first-line treatment of advanced non-small-cell lung cancer with PD-L1 of at least 50%: A multicentre, open-label, global, phase 3, randomised, controlled trial. Lancet, 2021, 397(10274), 592-604.
[http://dx.doi.org/10.1016/S0140-6736(21)00228-2] [PMID: 33581821]
[10]
Reck, M.; Rodríguez-Abreu, D.; Robinson, A.G.; Hui, R.; Csőszi, T.; Fülöp, A.; Gottfried, M.; Peled, N.; Tafreshi, A.; Cuffe, S.; O’Brien, M.; Rao, S.; Hotta, K.; Leiby, M.A.; Lubiniecki, G.M.; Shentu, Y.; Rangwala, R.; Brahmer, J.R. Pembrolizumab versus chemotherapy for PD-L1–positive non–small-cell lung cancer. N. Engl. J. Med., 2016, 375(19), 1823-1833.
[http://dx.doi.org/10.1056/NEJMoa1606774] [PMID: 27718847]
[11]
Hellmann, M.D.; Paz-Ares, L.; Bernabe Caro, R.; Zurawski, B.; Kim, S.W.; Carcereny Costa, E.; Park, K.; Alexandru, A.; Lupinacci, L.; de la Mora Jimenez, E.; Sakai, H.; Albert, I.; Vergnenegre, A.; Peters, S.; Syrigos, K.; Barlesi, F.; Reck, M.; Borghaei, H.; Brahmer, J.R.; O’Byrne, K.J.; Geese, W.J.; Bhagavatheeswaran, P.; Rabindran, S.K.; Kasinathan, R.S.; Nathan, F.E.; Ramalingam, S.S. Nivolumab plus Ipilimumab in advanced non–small-cell lung cancer. N. Engl. J. Med., 2019, 381(21), 2020-2031.
[http://dx.doi.org/10.1056/NEJMoa1910231] [PMID: 31562796]
[12]
Herbst, R.S.; Giaccone, G.; de Marinis, F.; Reinmuth, N.; Vergnenegre, A.; Barrios, C.H.; Morise, M.; Felip, E.; Andric, Z.; Geater, S.; Özgüroğlu, M.; Zou, W.; Sandler, A.; Enquist, I.; Komatsubara, K.; Deng, Y.; Kuriki, H.; Wen, X.; McCleland, M.; Mocci, S.; Jassem, J.; Spigel, D.R. Atezolizumab for First-Line Treatment of PD-L1–Selected Patients with NSCLC. N. Engl. J. Med., 2020, 383(14), 1328-1339.
[http://dx.doi.org/10.1056/NEJMoa1917346] [PMID: 32997907]
[13]
Antonia, S.J.; Villegas, A.; Daniel, D.; Vicente, D.; Murakami, S.; Hui, R.; Kurata, T.; Chiappori, A.; Lee, K.H.; de Wit, M.; Cho, B.C.; Bourhaba, M.; Quantin, X.; Tokito, T.; Mekhail, T.; Planchard, D.; Kim, Y.C.; Karapetis, C.S.; Hiret, S.; Ostoros, G.; Kubota, K.; Gray, J.E.; Paz-Ares, L.; de Castro Carpeño, J.; Faivre-Finn, C.; Reck, M.; Vansteenkiste, J.; Spigel, D.R.; Wadsworth, C.; Melillo, G.; Taboada, M.; Dennis, P.A.; Özgüroğlu, M. Overall survival with durvalumab after chemoradiotherapy in stage III NSCLC. N. Engl. J. Med., 2018, 379(24), 2342-2350.
[http://dx.doi.org/10.1056/NEJMoa1809697] [PMID: 30280658]
[14]
Reck, M.; Rodríguez-Abreu, D.; Robinson, A.G.; Hui, R.; Csőszi, T.; Fülöp, A.; Gottfried, M.; Peled, N.; Tafreshi, A.; Cuffe, S.; O´Brien, M.; Rao, S.; Hotta, K.; Vandormael, K.; Riccio, A.; Yang, J.; Pietanza, M.C.; Brahmer, J.R. Updated Analysis of KEYNOTE-024: Pembrolizumab versus Platinum-Based Chemotherapy for Advanced Non–Small-Cell Lung Cancer With PD-L1 Tumor Proportion Score of 50% or Greater. J. Clin. Oncol., 2019, 37(7), 537-546.
[http://dx.doi.org/10.1200/JCO.18.00149] [PMID: 30620668]
[15]
Lu, S.; Wang, J.; Cheng, Y.; Mok, T.; Chang, J.; Zhang, L.; Feng, J.; Tu, H.Y.; Wu, L.; Zhang, Y.; Luft, A.; Zhou, J.; Ma, Z.; Lu, Y.; Hu, C.; Shi, Y.; Ying, K.; Zhong, H.; Poddubskaya, E.; Soo, R.A.; Chia, Y.H.; Li, A.; Li, A.; Wu, Y.L. Nivolumab versus docetaxel in a predominantly Chinese patient population with previously treated advanced non-small cell lung cancer: 2-year follow-up from a randomized, open-label, phase 3 study (CheckMate 078). Lung Cancer, 2021, 152, 7-14.
[http://dx.doi.org/10.1016/j.lungcan.2020.11.013] [PMID: 33321441]
[16]
Park, SE; Lee, SH; Ahn, JS; Ahn, MJ; Park, K; Sun, JM Increased response rates to salvage chemotherapy administered after PD-1/PD-L1 inhibitors in patients with non-small cell lung cancer. J Thorac Oncol., 2018, 13(1), 106-111.
[17]
Herbst, R.S.; Bendell, J.C.; Isambert, N.; Calvo, E.; Santana-Davila, R.; Cassier, P.; Perez-Gracia, J.L.; Yang, J.; Rege, J.; Ferry, D. A phase 1 study of ramucirumab (R) plus pembrolizumab (P) in patients (pts) with advanced gastric or gastroesophageal junction (G/GEJ) adenocarcinoma, non-small cell lung cancer (NSCLC), or urothelial carcinoma (UC): Phase 1a results. Am. Soc Clin Oncol., 2016, 32, 15.
[http://dx.doi.org/10.1200/JCO.2016.34.15_suppl.3056]
[18]
Rizvi, N.A.; Antonia, S.J.; Shepherd, F.A.; Chow, L.Q.; Goldman, J.; Shen, Y.; Chen, A.C.; Gettinger, S. Nivolumab (Anti-PD-1; BMS-936558, ONO-4538) maintenance as monotherapy or in combination with bevacizumab (BEV) for non-small cell lung cancer (NSCLC) previously treated with chemotherapy: Metastatic non-small cell lung cancer. Int. J. Radiat. Oncol. Biol. Phys., 2014, 90(5), S32.
[http://dx.doi.org/10.1016/j.ijrobp.2014.08.206]
[19]
Abdelazeem, B.; Abbas, K.S.; Labieb, F.; Arida, A.K.; El-Shahat, N.A.; Shehata, J.; Kandah, E.; Malik, B.; Akanbi, M.; Rafae, A.; Wahab, A.; Ehsan, H. The role of immunotherapy plus chemotherapy versus chemotherapy alone as first-line treatment for advanced non-small cell lung cancer: An updated systematic review and meta-analysis of randomized controlled trials. Expert Rev. Anticancer Ther., 2022, 22(10), 1127-1140.
[http://dx.doi.org/10.1080/14737140.2022.2116005] [PMID: 35993418]
[20]
Paz-Ares, L.; Luft, A.; Vicente, D.; Tafreshi, A.; Gümüş, M.; Mazières, J.; Hermes, B.; Çay Şenler, F.; Csőszi, T.; Fülöp, A.; Rodríguez-Cid, J.; Wilson, J.; Sugawara, S.; Kato, T.; Lee, K.H.; Cheng, Y.; Novello, S.; Halmos, B.; Li, X.; Lubiniecki, G.M.; Piperdi, B.; Kowalski, D.M. Pembrolizumab plus Chemotherapy for Squamous Non–Small-Cell Lung Cancer. N. Engl. J. Med., 2018, 379(21), 2040-2051.
[http://dx.doi.org/10.1056/NEJMoa1810865] [PMID: 30280635]
[21]
Gandhi, L.; Rodríguez-Abreu, D.; Gadgeel, S.; Esteban, E.; Felip, E.; De Angelis, F.; Domine, M.; Clingan, P.; Hochmair, M.J.; Powell, S.F.; Cheng, S.Y.S.; Bischoff, H.G.; Peled, N.; Grossi, F.; Jennens, R.R.; Reck, M.; Hui, R.; Garon, E.B.; Boyer, M.; Rubio-Viqueira, B.; Novello, S.; Kurata, T.; Gray, J.E.; Vida, J.; Wei, Z.; Yang, J.; Raftopoulos, H.; Pietanza, M.C.; Garassino, M.C. Pembrolizumab plus Chemotherapy in Metastatic Non–Small-Cell Lung Cancer. N. Engl. J. Med., 2018, 378(22), 2078-2092.
[http://dx.doi.org/10.1056/NEJMoa1801005] [PMID: 29658856]
[22]
Zondor, S.D.; Medina, P.J. Bevacizumab: An angiogenesis inhibitor with efficacy in colorectal and other malignancies. Ann. Pharmacother., 2004, 38(7-8), 1258-1264.
[http://dx.doi.org/10.1345/aph.1D470] [PMID: 15187215]
[23]
Tian, W.; Cao, C.; Shu, L.; Wu, F. Anti-Angiogenic therapy in the treatment of non-small cell lung cancer. OncoTargets Ther., 2020, 13, 12113-12129.
[http://dx.doi.org/10.2147/OTT.S276150] [PMID: 33262610]
[24]
Manegold, C.; Dingemans, A.C.; Gray, J.E.; Nakagawa, K.; Nicolson, M.; Peters, S.; Reck, M.; Wu, Y.L.; Brustugun, O.T.; Crinò, L. The potential of combined immunotherapy and antiangiogenesis for the synergistic treatment of advanced NSCLC. J. Thorac. Oncol., 2017, 12(2), 194-207.
[25]
Li, B.; Lalani, A.S.; Harding, T.C.; Luan, B.; Koprivnikar, K.; Huan Tu, G.; Prell, R.; VanRoey, M.J.; Simmons, A.D.; Jooss, K. Vascular endothelial growth factor blockade reduces intratumoral regulatory T cells and enhances the efficacy of a GM-CSF-secreting cancer immunotherapy. Clin. Cancer Res., 2006, 12(22), 6808-6816.
[http://dx.doi.org/10.1158/1078-0432.CCR-06-1558] [PMID: 17121902]
[26]
Huang, Y.; Kim, B.Y.S.; Chan, C.K.; Hahn, S.M.; Weissman, I.L.; Jiang, W. Improving immune–vascular crosstalk for cancer immunotherapy. Nat. Rev. Immunol., 2018, 18(3), 195-203.
[http://dx.doi.org/10.1038/nri.2017.145] [PMID: 29332937]
[27]
Tian, L.; Goldstein, A.; Wang, H.; Ching Lo, H.; Sun Kim, I.; Welte, T.; Sheng, K.; Dobrolecki, L.E.; Zhang, X.; Putluri, N.; Phung, T.L.; Mani, S.A.; Stossi, F.; Sreekumar, A.; Mancini, M.A.; Decker, W.K.; Zong, C.; Lewis, M.T.; Zhang, X.H.F. Mutual regulation of tumour vessel normalization and immunostimulatory] reprogramming. Nature, 2017, 544(7649), 250-254.
[http://dx.doi.org/10.1038/nature21724] [PMID: 28371798]
[28]
Rini, B.I.; Plimack, E.R.; Stus, V.; Gafanov, R.; Hawkins, R.; Nosov, D.; Pouliot, F.; Alekseev, B.; Soulières, D.; Melichar, B.; Vynnychenko, I.; Kryzhanivska, A.; Bondarenko, I.; Azevedo, S.J.; Borchiellini, D.; Szczylik, C.; Markus, M.; McDermott, R.S.; Bedke, J.; Tartas, S.; Chang, Y.H.; Tamada, S.; Shou, Q.; Perini, R.F.; Chen, M.; Atkins, M.B.; Powles, T. Pembrolizumab plus axitinib versus sunitinib for advanced renal-cell carcinoma. N. Engl. J. Med., 2019, 380(12), 1116-1127.
[http://dx.doi.org/10.1056/NEJMoa1816714] [PMID: 30779529]
[29]
Liu, J.F.; Herold, C.; Gray, K.P.; Penson, R.T.; Horowitz, N.; Konstantinopoulos, P.A.; Castro, C.M.; Hill, S.J.; Curtis, J.; Luo, W.; Matulonis, U.A.; Cannistra, S.A.; Dizon, D.S. Assessment of combined nivolumab and bevacizumab in relapsed ovarian cancer. JAMA Oncol., 2019, 5(12), 1731-1738.
[http://dx.doi.org/10.1001/jamaoncol.2019.3343] [PMID: 31600397]
[30]
Herbst, R.S.; Arkenau, H.T.; Santana-Davila, R.; Calvo, E.; Paz-Ares, L.; Cassier, P.A.; Bendell, J.; Penel, N.; Krebs, M.G.; Martin-Liberal, J.; Isambert, N.; Soriano, A.; Wermke, M.; Cultrera, J.; Gao, L.; Widau, R.C.; Mi, G.; Jin, J.; Ferry, D.; Fuchs, C.S.; Petrylak, D.P.; Chau, I. Ramucirumab plus pembrolizumab in patients with previously treated advanced non-small-cell lung cancer, gastro- oesophageal cancer, or urothelial carcinomas (JVDF): A multicohort, non-randomised, open-label, phase 1a/b trial. Lancet Oncol., 2019, 20(8), 1109-1123.
[http://dx.doi.org/10.1016/S1470-2045(19)30458-9] [PMID: 31301962]
[31]
Chu, T; Zhong, R; Zhong, H; Zhang, B; Zhang, W; Shi, C; Qian, J; Zhang, Y; Chang, Q; Zhang, X Phase 1b Study of Sintilimab Plus Anlotinib as First-line Therapy in Patients With Advanced NSCLC J Thorac Oncol., 2021, 16(4), 643-652.
[32]
Ren, S.; He, J.; Fang, Y.; Chen, G.; Ma, Z.; Chen, J.; Guo, R.; Lin, X.; Yao, Y.; Wu, G.; Wang, Q.; Zhou, C. MA13.01 camrelizumab plus apatinib in treatment-naive patients with advanced non-squamous NSCLC: A Multicenter, Open-Label, Single-Arm, Phase 2 Trial. J. Thorac. Oncol., 2021, 16(10), S924.
[http://dx.doi.org/10.1016/j.jtho.2021.08.175]
[33]
Bang, YJ; Golan, T; Dahan, L; Fu, S; Moreno, V; Park, K; Geva, R; De Braud, F; Wainberg, ZA; Reck, M Ramucirumab and durvalumab for previously treated, advanced non–small-cell lung cancer, gastric/gastro-oesophageal junction adenocarcinoma, or hepatocellular carcinoma: An open-label, phase Ia/b study (JVDJ). Eur J. Cancer., 2020, 137(15 suppl), 272-284.
[34]
Zhou, N.; Jiang, M.; Li, T.; Zhu, J.; Liu, K.; Hou, H.; Zhang, X. Anlotinib combined with anti-PD-1 antibody, camrelizumab for advanced NSCLCs after multiple lines treatment: An open-label, dose escalation and expansion study. Lung Cancer, 2021, 160, 111-117.
[http://dx.doi.org/10.1016/j.lungcan.2021.08.006] [PMID: 34482102]
[35]
Zhai, C.; Zhang, X.; Ren, L.; You, L.; Pan, Q.; Pan, H.; Han, W. The efficacy and safety of anlotinib combined with PD-1 antibody for third-line or further-line treatment of patients with advanced non-small-cell lung cancer. Front. Oncol., 2021, 10, 619010.
[http://dx.doi.org/10.3389/fonc.2020.619010] [PMID: 33680942]
[36]
Page, M.J.; McKenzie, J.E.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Akl, E.A.; Brennan, S.E.; Chou, R.; Glanville, J.; Grimshaw, J.M.; Hróbjartsson, A.; Lalu, M.M.; Li, T.; Loder, E.W.; Mayo-Wilson, E.; McDonald, S.; McGuinness, L.A.; Stewart, L.A.; Thomas, J.; Tricco, A.C.; Welch, V.A.; Whiting, P.; Moher, D. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. BMJ, 2021, 372(71), n71.
[http://dx.doi.org/10.1136/bmj.n71] [PMID: 33782057]
[37]
Slim, K.; Nini, E.; Forestier, D.; Kwiatkowski, F.; Panis, Y.; Chipponi, J. Methodological index for non-randomized studies (MINORS): Development and validation of a new instrument. ANZ J. Surg., 2003, 73(9), 712-716.
[http://dx.doi.org/10.1046/j.1445-2197.2003.02748.x] [PMID: 12956787]
[38]
Wang, P.; Fang, X.; Yin, T.; Tian, H.; Yu, J.; Teng, F. Efficacy and Safety of Anti-PD-1 Plus Anlotinib in Patients With Advanced Non–Small-Cell Lung Cancer After Previous Systemic Treatment Failure—A Retrospective Study. Front. Oncol., 2021, 11, 628124.
[http://dx.doi.org/10.3389/fonc.2021.628124] [PMID: 33791214]
[39]
Chen, Y.; Li, X.; Liu, G.; Chen, S.; Xu, M.; Song, L.; Wang, Y. ctDNA concentration, MIKI67 mutations and hyper-progressive disease related gene mutations are prognostic markers for camrelizumab and apatinib combined multiline treatment in advanced NSCLC. Front. Oncol., 2020, 10, 1706.
[http://dx.doi.org/10.3389/fonc.2020.01706] [PMID: 33014846]
[40]
Yao, J.; Wang, Z.; Sheng, J.; Wang, H.; You, L.; Zhu, X.; Pan, H.; Han, W. Efficacy and safety of combined immunotherapy and antiangiogenic therapy for advanced non-small cell lung cancer: A two-center retrospective study. Int. Immunopharmacol., 2020, 89(Pt A), 107033.
[http://dx.doi.org/10.1016/j.intimp.2020.107033]
[41]
Jin, Y.; Weng, Y.M.; Wei, J.Y.; Peng, M. Clinical efficacy and safety of immune checkpoint inhibitors combined with antiangiogenic agents in the treatment of advanced non-small cell lung] cancer. J. Oncol., 2021, 27(9), 6.
[42]
Yang, S.; Zhang, W.; Chen, Q.; Guo, Q. Clinical investigation of the efficacy and safety of anlotinib with immunotherapy in advanced non-small cell lung cancer as third-line therapy: A retrospective study. Cancer Manag. Res., 2020, 12, 10333-10340.
[http://dx.doi.org/10.2147/CMAR.S280096] [PMID: 33116888]
[43]
Xiong, Q.; Qin, B.; Xin, L.; Yang, B.; Song, Q.; Wang, Y.; Zhang, S.; Hu, Y. Real-world efficacy and safety of anlotinib with and without immunotherapy in advanced non-small cell lung cancer. Front. Oncol., 2021, 11, 659380.
[http://dx.doi.org/10.3389/fonc.2021.659380] [PMID: 34395243]
[44]
Dhiman, A.; Sharma, R.; Singh, R.K. Target-based anticancer indole derivatives and insight into structure‒activity relationship: A mechanistic review update (2018–2021). Acta Pharm. Sin. B, 2022, 12(7), 3006-3027.
[http://dx.doi.org/10.1016/j.apsb.2022.03.021] [PMID: 35865090]
[45]
Sethi, N.S.; Prasad, D.N.; Singh, R.K. Synthesis, Anticancer, and Antibacterial Studies of Benzylidene Bearing 5-substituted and 3,5-disubstituted-2,4-Thiazolidinedione Derivatives. Med. Chem., 2021, 17(4), 369-379.
[http://dx.doi.org/10.2174/1573406416666200512073640] [PMID: 32394843]
[46]
Singh, R.K. Key heterocyclic cores for smart anticancer drug–design Part II; Bentham Science Publishers: Sharjah, 2022.
[http://dx.doi.org/10.2174/97898150400741220101]
[47]
Singh, R.K.; Kumar, S.; Prasad, D.N.; Bhardwaj, T.R. Therapeutic journery of nitrogen mustard as alkylating anticancer agents: Historic to future perspectives. Eur. J. Med. Chem., 2018, 151, 401-433.
[http://dx.doi.org/10.1016/j.ejmech.2018.04.001] [PMID: 29649739]
[48]
Felip Font, E.; Gettinger, S.N.; Burgio, M.A.; Antonia, S.J.; Holgado, E.; Spigel, D.R.; Arrieta, O.; Domine Gomez, M.; Aren Frontera, O.; Brahmer, J.; Chow, L.Q.; Crinò, L.; Butts, C.; Coudert, B.; Horn, L.; Steins, M.; Geese, W.J.; Li, A.; Healey, D.; Vokes, E.E. Three-year follow-up from CheckMate 017/057: Nivolumab versus docetaxel in patients with previously treated advanced non-small cell lung cancer (NSCLC). Ann. Oncol., 2017, 28, v462.
[http://dx.doi.org/10.1093/annonc/mdx380.004]
[49]
ASCO annual meeting. Pembrolizumab vs. platinum-based chemotherapy as first-line therapy for advanced/metastatic NSCLC with a PD-L1 TPS≥ 1 %: Open-label, phase 3 KEYNOTE-042 study. 2018. Available From: https://meetinglibrary.asco.org/browse-meetings/2018%20ASCO%20Annual%20Meeting
[50]
Rittmeyer, A.; Barlesi, F.; Waterkamp, D.; Park, K.; Ciardiello, F.; von Pawel, J.; Gadgeel, S.M.; Hida, T.; Kowalski, D.M.; Dols, M.C.; Cortinovis, D.L.; Leach, J.; Polikoff, J.; Barrios, C.; Kabbinavar, F.; Frontera, O.A.; De Marinis, F.; Turna, H.; Lee, J.S.; Ballinger, M.; Kowanetz, M.; He, P.; Chen, D.S.; Sandler, A.; Gandara, D.R. 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(10066), 255-265.
[http://dx.doi.org/10.1016/S0140-6736(16)32517-X] [PMID: 27979383]
[51]
Yi, M.; Jiao, D.; Qin, S.; Chu, Q.; Wu, K.; Li, A. Synergistic effect of immune checkpoint blockade and anti-angiogenesis in cancer treatment. Mol. Cancer, 2019, 18(1), 60.
[http://dx.doi.org/10.1186/s12943-019-0974-6] [PMID: 30925919]
[52]
Shi, S.; Wang, R.; Chen, Y.; Song, H.; Chen, L.; Huang, G. Combining antiangiogenic therapy with adoptive cell immunotherapy exerts better antitumor effects in non-small cell lung cancer models. PLoS One, 2013, 8(6), e65757.
[http://dx.doi.org/10.1371/journal.pone.0065757] [PMID: 23799045]
[53]
Han, Y.; Liu, D.; Li, L. PD-1/PD-L1 pathway: Current researches in cancer. Am. J. Cancer Res., 2020, 10(3), 727-742.
[PMID: 32266087]
[54]
Liu, J.; Chen, Z.; Li, Y.; Zhao, W.; Wu, J.; Zhang, Z. PD-1/PD-L1 checkpoint inhibitors in tumor immunotherapy. Front. Pharmacol., 2021, 12, 731798.
[http://dx.doi.org/10.3389/fphar.2021.731798] [PMID: 34539412]
[55]
Goel, S.; Duda, D.G.; Xu, L.; Munn, L.L.; Boucher, Y.; Fukumura, D.; Jain, R.K. Normalization of the vasculature for treatment of cancer and other diseases. Physiol. Rev., 2011, 91(3), 1071-1121.
[http://dx.doi.org/10.1152/physrev.00038.2010] [PMID: 21742796]
[56]
Wu, J.; Tang, Y.; Liang, X. Targeting VEGF pathway to normalize the vasculature: An emerging insight in cancer therapy. OncoTargets Ther., 2018, 11, 6901-6909.
[http://dx.doi.org/10.2147/OTT.S172042] [PMID: 30410348]
[57]
Allen, E.; Jabouille, A.; Rivera, L.B.; Lodewijckx, I.; Missiaen, R.; Steri, V.; Feyen, K.; Tawney, J.; Hanahan, D.; Michael, I.P.; Bergers, G. Combined antiangiogenic and anti–PD-L1 therapy stimulates tumor immunity through HEV formation. Sci. Transl. Med., 2017, 9(385), eaak9679.
[http://dx.doi.org/10.1126/scitranslmed.aak9679] [PMID: 28404866]
[58]
Han, B.; Chu, T.; Zhong, R.; Zhong, H.; Zhang, B.; Zhang, W.; Shi, C.; Qian, J.; Han, Y. P1. 04-02 efficacy and safety of sintilimab with anlotinib as first-line therapy for advanced non-small cell lung cancer (NSCLC). J. Thorac. Oncol., 2019, 14(10), S439.
[http://dx.doi.org/10.1016/j.jtho.2019.08.905]

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