Pneumonitis With Combined Immune Checkpoint Inhibitors and Chemoradiotherapy in Locally Advanced Non-Small-Cell Lung Cancer: a Systematic Review and Meta-Analysis

References

• Bobbili P , RyanK, DuhMSet al. Treatment patterns and overall survival among patients with unresectable, stage III non-small-cell lung cancer. Future Oncol.15(29), 3381–3393 (2019).
   PubMed Web of Science ®Google Scholar
• Chansky K , DetterbeckFC, NicholsonAGet al. The IASLC Lung Cancer Staging Project: external validation of the revision of the TNM stage groupings in the Eighth Edition of the TNM Classification of Lung Cancer. J. Thorac. Oncol.12(7), 1109–1121 (2017).
   PubMed Web of Science ®Google Scholar
• Curran WJ Jr , PaulusR, LangerCJet al. Sequential vs. concurrent chemoradiation for stage III non-small cell lung cancer: randomized phase III trial RTOG 9410. J. Natl Cancer Inst.103(19), 1452–1460 (2011).
   PubMedGoogle Scholar
• Bradley JD , PaulusR, KomakiRet al. Standard-dose versus high-dose conformal radiotherapy with concurrent and consolidation carboplatin plus paclitaxel with or without cetuximab for patients with stage IIIA or IIIB non-small-cell lung cancer (RTOG 0617): a randomised, two-by-two factorial phase 3 study. Lancet Oncol.16(2), 187–199 (2015).
   PubMed Web of Science ®Google Scholar
• Spigel DR , Faivre-FinnC, GrayJEet al. Five-year survival outcomes from the PACIFIC trial: durvalumab after chemoradiotherapy in stage III non-small-cell lung cancer. J. Clin. Oncol.40(12), 1301–1311 (2022).
   PubMed Web of Science ®Google Scholar
• Ko EC , RabenD, FormentiSC. The integration of radiotherapy with immunotherapy for the treatment of non-small cell lung cancer. Clin. Cancer Res.24(23), 5792–5806 (2018).
   PubMed Web of Science ®Google Scholar
• Theelen W , ChenD, VermaVet al. Pembrolizumab with or without radiotherapy for metastatic non-small-cell lung cancer: a pooled analysis of two randomised trials. Lancet Respir. Med.9(5), 467–475 (2021).
   PubMed Web of Science ®Google Scholar
• Barker HE , PagetJT, KhanAA, HarringtonKJ. The tumour microenvironment after radiotherapy: mechanisms of resistance and recurrence. Nat. Rev. Cancer15(7), 409–425 (2015).
   PubMed Web of Science ®Google Scholar
• Santivasi WL , XiaF. Ionizing radiation-induced DNA damage, response, and repair. Antioxid. Redox Signal.21(2), 251–259 (2014).
   PubMed Web of Science ®Google Scholar
• Rodríguez-Ruiz ME , Vanpouille-BoxC, MeleroI, FormentiSC, DemariaS. Immunological mechanisms responsible for radiation-induced abscopal effect. Trends Immunol.39(8), 644–655 (2018).
   PubMed Web of Science ®Google Scholar
• Kaur P , AseaA. Radiation-induced effects and the immune system in cancer. Front. Oncol.2, 191 (2012).
   PubMedGoogle Scholar
• Daly ME , MonjazebAM, KellyK. Clinical trials integrating immunotherapy and radiation for non-small-cell lung cancer. J. Thorac. Oncol.10(12), 1685–1693 (2015).
   PubMed Web of Science ®Google Scholar
• Shaverdian N , LisbergAE, BornazyanKet al. Previous radiotherapy and the clinical activity and toxicity of pembrolizumab in the treatment of non-small-cell lung cancer: a secondary analysis of the KEYNOTE-001 phase 1 trial. Lancet Oncol.18(7), 895–903 (2017).
   PubMed Web of Science ®Google Scholar
• Shaverdian N , BeattieJ, ThorMet al. Safety of thoracic radiotherapy in patients with prior immune-related adverse events from immune checkpoint inhibitors. Ann. Oncol.31(12), 1719–1724 (2020).
   PubMed Web of Science ®Google Scholar
• Hanania AN , MainwaringW, GhebreYT, HananiaNA, LudwigM. Radiation-induced lung injury: assessment and management. Chest156(1), 150–162 (2019).
   PubMed Web of Science ®Google Scholar
• Weber JS , YangJC, AtkinsMB, DisisML. Toxicities of immunotherapy for the practitioner. J. Clin. Oncol.33(18), 2092–2099 (2015).
   PubMed Web of Science ®Google Scholar
• Li M , GanL, SongA, XueJ, LuY. Rethinking pulmonary toxicity in advanced non-small cell lung cancer in the era of combining anti-PD-1/PD-L1 therapy with thoracic radiotherapy. Biochim. Biophys. Acta Rev. Cancer1871(2), 323–330 (2019).
   PubMed Web of Science ®Google Scholar
• Page MJ , MoherD, BossuytPMet al. PRISMA 2020 explanation and elaboration: updated guidance and exemplars for reporting systematic reviews. BMJ372, n160 (2021).
   PubMed Web of Science ®Google Scholar
• Page MJ , McKenzieJE, BossuytPMet al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ372, n71 (2021).
   PubMed Web of Science ®Google Scholar
• Yan M , DurmGA, MamdaniHet al. Consolidation nivolumab/ipilimumab versus nivolumab following concurrent chemoradiation in patients with unresectable stage III NSCLC: a planned interim safety analysis from the BTCRC LUN 16-081 trial. J. Clin. Oncol.38(15), 9010–9010 (2020).
   Web of Science ®Google Scholar
• Herbst RS , MajemM, BarlesiFet al. COAST: an open-label, phase II, multidrug platform study of durvalumab alone or in combination with oleclumab or monalizumab in patients with unresectable, stage III non-small-cell lung cancer. J. Clin. Oncol.40(29), 3383–3393 (2022).
   PubMed Web of Science ®Google Scholar
• Liveringhouse C , LamNB, RosenbergSAet al. Prospective phase I/II study of radiation and chemotherapy with ipilimumab followed by nivolumab for patients with stage III unresectable NSCLC. Int. J. Radiat. Oncol. Biol. Phys.111(3), S3–S4 (2021).
   Web of Science ®Google Scholar
• Garassino MC , MazieresJ, ReckMet al. Durvalumab after sequential chemoradiotherapy in stage III, unresectable NSCLC: the phase 2 PACIFIC-6 trial. J. Thorac. Oncol.17(12), 1415–1427 (2022).
   PubMed Web of Science ®Google Scholar
• Christoph DC , GirardN, SmitHJMet al. Pacific-R real-world study: treatment duration and interim analysis of progression-free survival in unresectable stage III NSCLC patients treated with durvalumab after chemoradiotherapy. Oncol. Res. Treat.44(Suppl. 2), 53 (2021).
   Google Scholar
• Bruni A , ScottiV, BorghettiPet al. A real-world, multicenter, observational retrospective study of durvalumab after concomitant or sequential chemoradiation for unresectable stage III non-small cell lung cancer. Front. Oncol.11, 744956 (2021).
   PubMed Web of Science ®Google Scholar
• Wass R , HochmairM, KaiserBet al. Durvalumab after sequential high dose chemoradiotherapy versus standard of care (SoC) for stage III NSCLC: a bi-centric trospective comparison focusing on pulmonary toxicity. Cancers (Basel)14(13), 3226 (2022).
   PubMed Web of Science ®Google Scholar
• Zhou Q , ChenM, JiangOet al. Sugemalimab versus placebo after concurrent or sequential chemoradiotherapy in patients with locally advanced, unresectable, stage III non-small-cell lung cancer in China (GEMSTONE-301): interim results of a randomised, double-blind, multicentre, phase 3 trial. Lancet Oncol.23(2), 209–219 (2022).
   PubMed Web of Science ®Google Scholar
• Hwang WL , PikeLRG, RoyceTJ, MahalBA, LoefflerJS. Safety of combining radiotherapy with immune-checkpoint inhibition. Nat. Rev. Clin. Oncol.15(8), 477–494 (2018).
   PubMed Web of Science ®Google Scholar
• Deng L , LiangH, BurnetteBet al. Irradiation and anti-PD-L1 treatment synergistically promote antitumor immunity in mice. J. Clin. Invest.124(2), 687–695 (2014).
   PubMed Web of Science ®Google Scholar
• Sanmamed MF , ChenL. A paradigm shift in cancer immunotherapy: from enhancement to normalization. Cell175(2), 313–326 (2018).
   PubMed Web of Science ®Google Scholar
• Kuang Y , PierceCM, ChangHCet al. Chemoradiation-induced pneumonitis in patients with unresectable stage III non-small cell lung cancer: a systematic literature review and meta-analysis. Lung Cancer174, 174–185 (2022).
   PubMed Web of Science ®Google Scholar
• Park K , VansteenkisteJ, LeeKHet al. Pan-Asian adapted ESMO Clinical Practice Guidelines for the management of patients with locally-advanced unresectable non-small-cell lung cancer: a KSMO-ESMO initiative endorsed by CSCO, ISMPO, JSMO, MOS, SSO and TOS. Ann. Oncol.31(2), 191–201 (2020).
   PubMed Web of Science ®Google Scholar
• Daly ME , SinghN, IsmailaNet al. Management of stage III non-small-cell lung cancer: ASCO Guideline. J. Clin. Oncol.40(12), 1356–1384 (2022).
   PubMed Web of Science ®Google Scholar
• Walraven I , DamhuisRA, TenBerge MGet al. Treatment variation of sequential versus concurrent chemoradiotherapy in stage III non-small cell lung cancer patients in The Netherlands and Belgium. Clin. Oncol.29(11), e177–e185 (2017).
   PubMed Web of Science ®Google Scholar
• Hung A , LeeKM, LynchJAet al. Chemoradiation treatment patterns among United States Veteran Health Administration patients with unresectable stage III non-small cell lung cancer. BMC Cancer21(1), 824 (2021).
   PubMed Web of Science ®Google Scholar
• Spencer A , WilliamsJ, SamuelR, BoonIS, ClarkeK, JainP. Concurrent versus sequential chemoradiotherapy for unresectable locally advanced stage III non-small cell lung cancer: retrospective analysis in a single United Kingdom cancer centre. Cancer Treat. Res. Commun.29, 100460 (2021).
   PubMedGoogle Scholar
• Conibear J . Rationale for concurrent chemoradiotherapy for patients with stage III non-small-cell lung cancer. Br. J. Cancer123(Suppl. 1), 10–17 (2020).
   PubMed Web of Science ®Google Scholar
• Weinmann SC , PisetskyDS. Mechanisms of immune-related adverse events during the treatment of cancer with immune checkpoint inhibitors. Rheumatology58(Suppl. 7), vii59–vii67 (2019).
   PubMedGoogle Scholar
• Durm GA , MamdaniH, AlthouseSKet al. Consolidation nivolumab plus ipilimumab or nivolumab alone following concurrent chemoradiation for patients with unresectable stage III non-small cell lung cancer: BTCRC LUN 16-081. Journal of Clinical Oncology.40(Suppl. 16), 8509 (2022).
   Web of Science ®Google Scholar
• Xiao Y , YuS, ZhuBet al. RGMb is a novel binding partner for PD-L2 and its engagement with PD-L2 promotes respiratory tolerance. J. Exp. Med.211(5), 943–959 (2014).
   PubMed Web of Science ®Google Scholar
• Muraro E , RomanòR, FanettiGet al. Tissue and circulating PD-L2: moving from health and immune-mediated diseases to head and neck oncology. Crit. Rev. Oncol. Hematol.175, 103707 (2022).
   PubMed Web of Science ®Google Scholar
• Mayoux M , RollerA, PulkoVet al. Dendritic cells dictate responses to PD-L1 blockade cancer immunotherapy. Sci. Transl. Med.12(534), eaav7431 (2020).
   PubMed Web of Science ®Google Scholar
• Takeuchi M , DoiT, ObayashiKet al. Soluble PD-L1 with PD-1-binding capacity exists in the plasma of patients with non-small cell lung cancer. Immunol. Lett.196, 155–160 (2018).
   PubMed Web of Science ®Google Scholar
• Jalali S , Price-TroskaT, PaludoJet al. Soluble PD-1 ligands regulate T-cell function in Waldenstrom macroglobulinemia. Blood Adv.2(15), 1985–1997 (2018).
   PubMed Web of Science ®Google Scholar
• Senan S , BradeA, WangLHet al. PROCLAIM: Randomized Phase III Trial of Pemetrexed-Cisplatin or Etoposide-Cisplatin Plus Thoracic Radiation Therapy Followed by Consolidation Chemotherapy in Locally Advanced Nonsquamous Non-Small-Cell Lung Cancer. Journal of clinical oncology34(9), 953–62 (2016).
   PubMed Web of Science ®Google Scholar
• Eichkorn T , BozorgmehrF, RegnerySet al. Consolidation Immunotherapy After Platinum-Based Chemoradiotherapy in Patients With Unresectable Stage III Non-Small Cell Lung Cancer-Cross-Sectional Study of Eligibility and Administration Rates. Frontiers in oncology10, 586449 (2020).
   PubMed Web of Science ®Google Scholar
• Jabbour SK , LeeKH, FrostNet al. Pembrolizumab Plus Concurrent Chemoradiation Therapy in Patients With Unresectable, Locally Advanced, Stage III Non-Small Cell Lung Cancer: The Phase 2 KEYNOTE-799 Nonrandomized Trial. JAMA Oncol.7(9), 1–9 (2021).
   PubMed Web of Science ®Google Scholar
• Ryckman JM , BaineM, CarmichealJet al. Correlation of dosimetric factors with the development of symptomatic radiation pneumonitis in stereotactic body radiotherapy. Radiation oncology. 15(1), 33 ( 2020).
   PubMed Web of Science ®Google Scholar
• Pan WY , BianC, ZouGLet al. Combing NLR, V20 and mean lung dose to predict radiation induced lung injury in patients with lung cancer treated with intensity modulated radiation therapy and chemotherapy. Oncotarget.8(46), 81387–93 (2017).
   PubMedGoogle Scholar
• Chun SG , HuC, ChoyHet al. Impact of intensity-modulated radiation therapy technique for locally advanced non-small-cell lung cancer: a secondary analysis of the NRG Oncology RTOG 0617 randomized clinical trial. J. Clin. Oncol.35(1), 56–62 (2017).
   PubMed Web of Science ®Google Scholar
• Wurstbauer K , KazilM, MeinschadMet al. Locally advanced NSCLC: a plea for sparing the ipsilateral normal lung-prospective, clinical trial with DART-bid (dose-differentiated accelerated radiation therapy, 1.8 Gy twice daily) by VMAT. Radiat. Oncol.17(1), 120 (2022).
   PubMed Web of Science ®Google Scholar
• Baumann BC , MitraN, HartonJGet al. Comparative effectiveness of proton vs photon therapy as part of concurrent chemoradiotherapy for locally advanced cancer. JAMA Oncol.6(2), 237–246 (2020).
   PubMed Web of Science ®Google Scholar
• Bradley J , BaeK, ChoiNet al. A phase II comparative study of gross tumor volume definition with or without PET/CT fusion in dosimetric planning for non-small-cell lung cancer (NSCLC): primary analysis of Radiation Therapy Oncology Group (RTOG) 0515. International journal of radiation oncology, biology, physics82(1), 435–41.e1 (2012).
   PubMed Web of Science ®Google Scholar
• Zou L , ChuL, XiaFet al. Is clinical target volume necessary? – a failure pattern analysis in patients with locally advanced non-small cell lung cancer treated with concurrent chemoradiotherapy using intensity-modulated radiotherapy technique. Transl. Lung Cancer Res.9(5), 1986–1995 (2020).
   PubMed Web of Science ®Google Scholar
• Xia F , ZhouL, YangXet al. Is a clinical target volume (CTV) necessary for locally advanced non-small cell lung cancer treated with intensity-modulated radiotherapy? – a dosimetric evaluation of three different treatment plans. J. Thorac. Dis.9(12), 5194–5202 (2017).
   PubMed Web of Science ®Google Scholar
• Xue J , DuS, LuY, DickerA, LuB. Abstract 3671: anti-PD-1 treatment may potentiate the radiation-induced lung injury. Cancer Res.77(Suppl. 13), 3671 (2017).
   Google Scholar
• van der Woude LL , GorrisMAJ, WortelIMNet al. Tumor microenvironment shows an immunological abscopal effect in patients with NSCLC treated with pembrolizumab-radiotherapy combination. J. Immunother. Cancer10(10), e005248 (2022).
   PubMed Web of Science ®Google Scholar
• Xue J , LiX, LuYet al. Gene-modified mesenchymal stem cells protect against radiation-induced lung injury. Mol. Ther.21(2), 456–465 (2013).
   PubMed Web of Science ®Google Scholar
• Kim KH , PyoH, LeeHet al. Association of T cell senescence with radiation pneumonitis in patients with non-small cell lung cancer. Int. J. Radiat. Oncol. Biol. Phys.115(2), 464–475 (2022).
   PubMed Web of Science ®Google Scholar
• Kim KH , PyoH, LeeHet al. Dynamics of circulating immune cells during chemoradiotherapy in patients with non-small cell lung cancer support earlier administration of anti-PD-1/PD-L1 therapy. Int. J. Radiat. Oncol. Biol. Phys.113(2), 415–425 (2022).
   PubMed Web of Science ®Google Scholar
• Sierra-Rodero B , Cruz-BermúdezA, NadalEet al. Clinical and molecular parameters associated to pneumonitis development in non-small-cell lung cancer patients receiving chemoimmunotherapy from NADIM trial. J. Immunother. Cancer9(8), e002804 (2021).
   PubMed Web of Science ®Google Scholar
• Hawkins PG , BoonstraPS, HobsonSTet al. Radiation-induced lung toxicity in non-small-cell lung cancer: understanding the interactions of clinical factors and cytokines with the dose-toxicity relationship. Radiother. Oncol.125(1), 66–72 (2017).
   PubMed Web of Science ®Google Scholar
• Kainthola A , HaritwalT, TiwariMet al. Immunological aspect of radiation-induced pneumonitis, current treatment strategies, and future prospects. Front. Immunol.8, 506 (2017).
   PubMed Web of Science ®Google Scholar
• Brahmer JR , LacchettiC, SchneiderBJet al. Management of Immune-Related Adverse Events in Patients Treated With Immune Checkpoint Inhibitor Therapy: American Society of Clinical Oncology Clinical Practice Guideline. Journal of clinical oncology36(17), 1714–68 (2018).
   PubMed Web of Science ®Google Scholar