Cited by 256Cancer Immunotherapy and BiomarkersImmunotherapy and Immune ResponsesRadiomics and Machine Learning in Medical Imaging

The DOI matches its Crossref record; 212 of the 216 references it cites were found in a registry or an index.

Assessing the interactions between radiotherapy and antitumour immunity

Open access

Grassberger, Clemens, Ellsworth, Susannah G., Wilks, Moses Q., Keane, Florence K., Loeffler, Jay S.·2019·Nature Reviews Clinical Oncology

DOI 10.1038/s41571-019-0238-9PMC PMC13492067

Open this paper in CoChat — free account

Abstract

Immunotherapy, specifically the introduction of immune checkpoint inhibitors, has transformed the treatment of cancer, enabling long-term tumour control even in individuals with advanced-stage disease. Unfortunately, only a small subset of patients show a response to currently available immunotherapies. Despite a growing consensus that combining immune checkpoint inhibitors with radiotherapy can increase response rates, this approach might be limited by the development of persistent radiation-induced immunosuppression. The ultimate goal of combining immunotherapy with radiotherapy is to induce a shift from an ineffective, pre-existing immune response to a long-lasting, therapy-induced immune response at all sites of disease. To achieve this goal and enable the adaptation and monitoring of individualized treatment approaches, assessment of the dynamic changes in the immune system at the patient level is essential. In this Review, we summarize the available clinical data, including forthcoming methods to assess the immune response to radiotherapy at the patient level, ranging from serum biomarkers to imaging techniques that enable investigation of immune cell dynamics in patients. Furthermore, we discuss modelling approaches that have been developed to predict the interaction of immunotherapy with radiotherapy, and highlight how they could be combined with biomarkers of antitumour immunity to optimize radiotherapy regimens and maximize their synergy with immunotherapy.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1038/s41571-019-0238-9

Cites

212 of 212 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

PD-1 and PD-L1 Immune Checkpoint Blockade to Treat Breast Cancer
Hartkopf, A. D., Taran, F., Wallwiener, M., Walter, C. B., Krämer, B., Grischke, E., & Brucker, S. Y. (2016) · Breast Care · doi:10.1159/000453569 · Cited by 30,989
Intratumor Heterogeneity and Branched Evolution Revealed by Multiregion Sequencing
Gerlinger, M., Rowan, A. J., Horswell, S., Larkin, J., Endesfelder, D., Gronroos, E., Martinez, P., Matthews, N., Stewart, A., Tarpey, P., et al. (2012) · New England Journal of Medicine · doi:10.1056/nejmoa1113205 · Cited by 7,774
Cancer Immunoediting: Integrating Immunity’s Roles in Cancer Suppression and Promotion
Schreiber, R. D., Old, L. J., & Smyth, M. J. (2011) · Science · doi:10.1126/science.1203486 · Cited by 6,474
Nivolumab versus Everolimus in Advanced Renal-Cell Carcinoma
Motzer, R. J., Escudier, B., McDermott, D. F., George, S., Hammers, H. J., Srinivas, S., Tykodi, S. S., Sosman, J. A., Procopio, G., Plimack, E. R., et al. (2015) · New England Journal of Medicine · doi:10.1056/nejmoa1510665 · Cited by 5,807
Tumor-associated B7-H1 promotes T-cell apoptosis: A potential mechanism of immune evasion
Dong, H., Strome, S. E., Salomao, D. R., Tamura, H., Hirano, F., Flies, D. B., Roche, P. C., Lu, J., Zhu, G., Tamada, K., et al. (2002) · Nature Medicine · doi:10.1038/nm730 · Cited by 5,025
Atezolizumab versus docetaxel in patients with previously treated non-small-cell lung cancer (OAK): a phase 3, open-label, multicentre randomised controlled trial
Rittmeyer, A., Barlési, F., Waterkamp, D., Park, K., Ciardiello, F., von Pawel, J., Gadgeel, S. M., Hida, T., Kowalski, D. M., Cobo, M., et al. (2016) · The Lancet · doi:10.1016/s0140-6736(16)32517-x · Cited by 4,718
Innate and adaptive immune cells in the tumor microenvironment
Gajewski, T. F., Schreiber, H., & Fu, Y.-X. (2013) · Nature Immunology · doi:10.1038/ni.2703 · Cited by 4,148
Overall Survival with Durvalumab after Chemoradiotherapy in Stage III NSCLC
Antonia, S. J., Villegas, A., Daniel, D., Vicente, D., Murakami, S., Hui, R., Kurata, T., Chiappori, A., Lee, K. H., de Wit, M., et al. (2018) · New England Journal of Medicine · doi:10.1056/nejmoa1809697 · Cited by 2,798
Mechanism-driven biomarkers to guide immune checkpoint blockade in cancer therapy
Topalian, S. L., Taube, J. M., Anders, R. A., & Pardoll, D. M. (2016) · Nature Reviews Cancer · doi:10.1038/nrc.2016.36 · Cited by 2,733
Radiation and dual checkpoint blockade activate non-redundant immune mechanisms in cancer
Twyman-Saint Victor, C., Rech, A. J., Maity, A., Rengan, R., Pauken, K. E., Stelekati, E., Benci, J. L., Xu, B., Dada, H., Odorizzi, P. M., et al. (2015) · Nature · doi:10.1038/nature14292 · Cited by 2,434

Show all 216 references

Sorted by citations

Cold and hot tumors: from molecular mechanisms to targeted therapy
Wu, B., Zhang, B., Li, B., Wu, H., & Jiang, M. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01979-x · Cited by 776
Molecular Mechanisms of Radiation-Induced Cancer Cell Death: A Primer
Sia, J., Szmyd, R., Hau, E., & Gee, H. E. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00041 · Cited by 378
Towards clinical translation of FLASH radiotherapy
Vozenin, M., Bourhis, J., & Durante, M. (2022) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-022-00697-z · Cited by 370
Electromagnetic Nanomedicines for Combinational Cancer Immunotherapy
Li, J., Luo, Y., & Pu, K. (2020) · Angewandte Chemie International Edition · doi:10.1002/anie.202008386 · Cited by 223
Caffeic acid and its derivatives as potential modulators of oncogenic molecular pathways: New hope in the fight against cancer
Mirzaei, S., Gholami, M. H., Zabolian, A., Saleki, H., Farahani, M. V., Hamzehlou, S., Far, F. B., Sharifzadeh, S. O., Samarghandian, S., Khan, H. Z., et al. (2021) · Pharmacological Research · doi:10.1016/j.phrs.2021.105759 · Cited by 189
Interfering with Tumor Hypoxia for Radiotherapy Optimization
Telarović, I., Wenger, R. H., & Pruschy, M. N. (2021) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-021-02000-x · Cited by 203
Physics and biomedical challenges of cancer therapy with accelerated heavy ions
Durante, M., Debus, J., & Loeffler, J. S. (2021) · Nature Reviews Physics · doi:10.1038/s42254-021-00368-5 · Cited by 171
Self-citation
Gut microbiome diversity is an independent predictor of survival in cervical cancer patients receiving chemoradiation
Sims, T. T., El Alam, M. B., Karpinets, T. V., Dorta-Estremera, S., Hegde, V. L., Nookala, S., Yoshida-Court, K., Wu, X., Biegert, G. W. G., Delgado Medrano, A. Y., et al. (2021) · Communications Biology · doi:10.1038/s42003-021-01741-x · Cited by 135
Toll-like receptor 9 agonists and combination therapies: strategies to modulate the tumour immune microenvironment for systemic anti-tumour immunity
Dongye, Z., Li, J., & Wu, Y. (2022) · British Journal of Cancer · doi:10.1038/s41416-022-01876-6 · Cited by 138
Analyzing the mechanisms of iron oxide nanoparticles interactions with cells: A road from failure to success in clinical applications
Frtús, A., Smolková, B., Uzhytchak, M., Lunová, M., Jirsa, M., Kubinová, Š., Dejneka, A., & Lunov, O. (2020) · Journal of Controlled Release · doi:10.1016/j.jconrel.2020.08.036 · Cited by 119
Tumor Microenvironment as a Regulator of Radiation Therapy: New Insights into Stromal-Mediated Radioresistance
Krisnawan, V. E., Stanley, J. A., Schwarz, J. K., & DeNardo, D. G. (2020) · Cancers · doi:10.3390/cancers12102916 · Cited by 114
Checkpoint Inhibitors in Combination With Stereotactic Body Radiotherapy in Patients With Advanced Solid Tumors
Spaas, M., Sundahl, N., Krüse, V., Rottey, S., Maeseneer, D. J. D., Duprez, F., Lievens, Y. N., Surmont, V. F. M., Brochez, L., Reynders, D., et al. (2023) · JAMA Oncology · doi:10.1001/jamaoncol.2023.2132 · Cited by 107
X‐ray‐Induced Release of Nitric Oxide from Hafnium‐Based Nanoradiosensitizers for Enhanced Radio‐Immunotherapy
Liu, N., Zhu, J., Zhu, W., Chen, L., Li, M., Shen, J., Chen, M., Wu, Y., Pan, F., Deng, Z., et al. (2023) · Advanced Materials · doi:10.1002/adma.202302220 · Cited by 103
Effect of neoadjuvant chemoradiotherapy with or without PD-1 antibody sintilimab in pMMR locally advanced rectal cancer: A randomized clinical trial
Xiao, W., Chen, G., Gao, Y., Lin, J., Wu, X., Luo, H.-L., Lu, Z., Wang, Q., Sun, R., Cai, P., et al. (2024) · Cancer Cell · doi:10.1016/j.ccell.2024.07.004 · Cited by 104
Harnessing progress in radiotherapy for global cancer control
Jaffray, D. A., Knaul, F. M., Baumann, M. A., & Gospodarowicz, M. K. (2023) · Nature Cancer · doi:10.1038/s43018-023-00619-7 · Cited by 99
Oxygen-Independent Radiodynamic Therapy: Radiation-Boosted Chemodynamics for Reprogramming the Tumor Immune Environment and Enhancing Antitumor Immune Response
Chen, Y., Deng, Y., Li, Y., Qin, Y., Zhou, Z., Yang, H., & Sun, Y. (2024) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.4c00793 · Cited by 93
Myeloid-Derived Suppressor Cells and Radiotherapy
Jiménez‐Cortegana, C., Galassi, C., Klapp, V., Gabrilovich, D. I., & Galluzzi, L. (2022) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-21-1105 · Cited by 88
Nanomedicine embraces cancer radio-immunotherapy: mechanism, design, recent advances, and clinical translation
Li, H., Luo, Q., Zhang, H., Ma, X., Gu, Z., Gong, Q., & Luo, K. (2022) · Chemical Society Reviews · doi:10.1039/d2cs00437b · Cited by 91
Emerging Technologies for Local Cancer Treatment
Chua, C. Y. X., Ho, J., Demaria, S., Mauro Ferrari, B., & Grattoni, A. (2020) · Advanced Therapeutics · doi:10.1002/adtp.202000027 · Cited by 86
Immune-based combination therapy to convert immunologically cold tumors into hot tumors: an update and new insights
Ni, J., Zhang, Z., Ge, M.-J., Chen, J., & Zhuo, W. (2022) · Acta Pharmacologica Sinica · doi:10.1038/s41401-022-00953-z · Cited by 85
News on immune checkpoint inhibitors as immunotherapy strategies in adult and pediatric solid tumors
Melaiu, O., Lucarini, V., Giovannoni, R., Fruci, D., & Gemignani, F. (2020) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2020.07.001 · Cited by 76
Meningeal lymphatics regulate radiotherapy efficacy through modulating anti-tumor immunity
Zhou, C., Ma, L., Xu, H., Huo, Y., & Luo, J. (2022) · Cell Research · doi:10.1038/s41422-022-00639-5 · Cited by 77
Impacts of combining anti-PD-L1 immunotherapy and radiotherapy on the tumour immune microenvironment in a murine prostate cancer model
Philippou, Y., Sjoberg, H. T., Murphy, E. A., Alyacoubi, S., Jones, K. I., Gordon-Weeks, A. N., Phyu, S. M., Parkes, E. E., McKenna, W. G., Lamb, A. D. G., et al. (2020) · British Journal of Cancer · doi:10.1038/s41416-020-0956-x · Cited by 77
Changes in T Lymphocyte Subsets in Different Tumors Before and After Radiotherapy: A Meta-analysis
Wang, Q. L., Li, S., Qiao, S., Zheng, Z., Duan, X., & Zhu, X. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.648652 · Cited by 77
Ionizing Radiation Triggers the Antitumor Immunity by Inducing Gasdermin E-Mediated Pyroptosis in Tumor Cells
Cao, W., Chen, G., Wu, L., Yu, K. N., Sun, M., Yang, M., Jiang, Y., Jiang, Y., Yuan, X., Peng, S., et al. (2022) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2022.07.1841 · Cited by 74
Harnessing immune response using reactive oxygen Species-Generating/Eliminating inorganic biomaterials for disease treatment
Zhao, C., Deng, H., & Chen, X. S. (2022) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2022.114456 · Cited by 71
Monocyte programming by cancer therapy
Patysheva, M. R., Frolova, A. A., Larionova, I., Afanas’ev, S. G., Тарасова, А. С., Чердынцева, Н. В., & Kzhyshkowska, J. G. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.994319 · Cited by 65
Advances in radiotherapy and immunity in hepatocellular carcinoma
Yang, Y., Xiong, L., Li, M., Jiang, P., Wang, J., & Li, C. (2023) · Journal of Translational Medicine · doi:10.1186/s12967-023-04386-y · Cited by 68
Shielding Ferritin with a Biomineralized Shell Enables Efficient Modulation of Tumor Microenvironment and Targeted Delivery of Diverse Therapeutic Agents
Wang, C., Wang, X., Zhang, W., Ma, D., Li, F., Jia, R., Shi, M., Wang, Y., Ma, G., & Wei, W. (2021) · Advanced Materials · doi:10.1002/adma.202107150 · Cited by 62
An Immunocompetent Hafnium Oxide-Based STING Nanoagonist for Cancer Radio-immunotherapy
Cao, Y., Ding, S., Hu, Y., Zeng, L., Zhou, J., Lin, L., Zhang, X., Ma, Q., Cai, R., Zhang, Y., et al. (2024) · ACS Nano · doi:10.1021/acsnano.3c09293 · Cited by 63
Opportunities and challenges of targeting cGAS–STING in cancer
Lu, C., Wang, W., & Fu, Y. (2026) · Nature reviews. Cancer · doi:10.1038/s41568-025-00894-9 · Cited by 71
4D blood flow model for dose calculation to circulating blood and lymphocytes
Hammi, A., Paganetti, H., & Grassberger, C. (2020) · Physics in Medicine and Biology · doi:10.1088/1361-6560/ab6c41 · Cited by 60
Self-citation
Combined radiotherapy and immunotherapy in urothelial bladder cancer: harnessing the full potential of the anti-tumor immune response
Faye, M. D., Kassouf, W., Souhami, L., Marcq, G., Cury, F., Niazi, T. M., & Sargos, P. (2020) · World Journal of Urology · doi:10.1007/s00345-020-03440-4 · Cited by 60
Photothermal‐Triggered Sulfur Oxide Gas Therapy Augments Type I Photodynamic Therapy for Potentiating Cancer Stem Cell Ablation and Inhibiting Radioresistant Tumor Recurrence
Zhang, T., You, P., Suo, M., Lyu, M., Lam, J. W. Y., Jin, Z., Ning, S., & Tang, B. Z. (2023) · Advanced Science · doi:10.1002/advs.202304042 · Cited by 59
Molecular determinants of immunogenic cell death elicited by radiation therapy
Galassi, C., Klapp, V., Yamazaki, T., & Galluzzi, L. (2023) · Immunological Reviews · doi:10.1111/imr.13271 · Cited by 64
Advanced strategies for combinational immunotherapy of cancer based on polymeric nanomedicines
You, K., Wang, Q., Osman, M. S., Kim, D., Li, Q., Feng, C., Wang, L., & Yang, K. (2024) · BMEMat · doi:10.1002/bmm2.12067 · Cited by 58
HEDOS—a computational tool to assess radiation dose to circulating blood cells during external beam radiotherapy based on whole-body blood flow simulations
Shin, J., Xing, S., McCullum, L. B., Hammi, A., Pursley, J., Correa-Alfonso, C. M., Withrow, J. D., Domal, S. J., Bolch, W. E., Paganetti, H., et al. (2021) · Physics in Medicine and Biology · doi:10.1088/1361-6560/ac16ea · Cited by 61
Self-citation
A PD‐L1 siRNA‐Loaded Boron Nanoparticle for Targeted Cancer Radiotherapy and Immunotherapy
Deng, S., Hu, L., Chen, G., Ye, J., Xiao, Z., Guan, T., Guo, S., Xia, W., Cheng, D., Wan, X., et al. (2025) · Advanced Materials · doi:10.1002/adma.202419418 · Cited by 57
DNA Damage Baseline Predicts Resilience to Space Radiation and Radiotherapy
Pariset, E., Bertucci, A., Petay, M., Malkani, S., Lopez Macha, A., Paulino Lima, I. G., Gomez Gonzalez, V., Tin, A. S., Tang, J., Plante, I., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108434 · Cited by 56
Nanozyme‐Coated Bacteria Hitchhike on CD11b + Immune Cells to Boost Tumor Radioimmunotherapy
Li, H., Pei, P., He, Q., Dong, X., Zhang, C., Shen, W., Chen, H., Hu, L. T., Tao, Y., & Yang, K. (2023) · Advanced Materials · doi:10.1002/adma.202309332 · Cited by 56
Immunotherapy in cervix cancer
Attademo, L., Tuninetti, V., Pisano, C., Cecere, S. C., Napoli, M. D., Tambaro, R., Valabrega, G., Musacchio, L., Setola, S. V., Piccirillo, P., et al. (2020) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2020.102088 · Cited by 52
Hematological toxicity in patients with solid malignant tumors treated with radiation – Temporal analysis, dose response and impact on survival
Terrones‐Campos, C., Ledergerber, B., Vogelius, I. R., Helleberg, M., Specht, L., & Lundgren, J. D. (2021) · Radiotherapy and Oncology · doi:10.1016/j.radonc.2021.02.029 · Cited by 51
Grand challenges for medical physics in radiation oncology
Fiorino, C., Jeraj, R., Clark, C. H., Garibaldi, C., Georg, D., Muren, L. P., van Elmpt, W., Bortfeld, T. R., & Jornet, N. (2020) · Radiotherapy and Oncology · doi:10.1016/j.radonc.2020.10.001 · Cited by 51
Radiation-Associated Lymphopenia and Outcomes of Patients with Unresectable Hepatocellular Carcinoma Treated with Radiotherapy
De, B. S., Ng, S. P., Liu, A. Y., Avila, S., Tao, R., Holliday, E. B., Brownlee, Z., Kaseb, A. O., Lee, S., Raghav, K. P. S., et al. (2021) · Journal of Hepatocellular Carcinoma · doi:10.2147/jhc.s282062 · Cited by 50
Self-citation
Human Leukocyte Antigen Class I Antigen-Processing Machinery Upregulation by Anticancer Therapies in the Era of Checkpoint Inhibitors
Sadagopan, A., Michelakos, T. P., Boyiadzis, G., Ferrone, C. R., & Ferrone, S. (2021) · JAMA Oncology · doi:10.1001/jamaoncol.2021.5970 · Cited by 49
Preclinical study and phase II trial of adapting low-dose radiotherapy to immunotherapy in small cell lung cancer
Wang, H., Yao, Z., Kang, K., Zhou, L., Xiu, W., Sun, J., Xie, C., Yu, M., Li, Y., Zhang, Y., et al. (2024) · Med · doi:10.1016/j.medj.2024.06.002 · Cited by 50
Enhanced radiotherapy efficacy and induced anti-tumor immunity in HCC by improving hypoxia microenvironment using oxygen microcapsules
Dai, X., Ruan, J., Guo, Y., Sun, Z., Liu, J., Bao, X., Zhang, H., Li, Q., Ye, C., Wang, X., et al. (2021) · Chemical Engineering Journal · doi:10.1016/j.cej.2021.130109 · Cited by 49
Radiation therapy for extensive-stage small-cell lung cancer in the era of immunotherapy
Tian, Y., Ma, J., Jing, X., Zhai, X., Li, Y., Guo, Z., Yu, J., & Zhu, H. (2022) · Cancer Letters · doi:10.1016/j.canlet.2022.215719 · Cited by 48
A tumor-immune interaction model for hepatocellular carcinoma based on measured lymphocyte counts in patients undergoing radiotherapy
Sung, W., Grassberger, C., McNamara, A. L., Basler, L., Ehrbar, S., Tanadini‐Lang, S., Hong, T. S., & Paganetti, H. (2020) · Radiotherapy and Oncology · doi:10.1016/j.radonc.2020.07.025 · Cited by 53
Self-citation
Radiotherapy–Immunotherapy Combination: How Will We Bridge the Gap Between Pre-Clinical Promise and Effective Clinical Delivery?
Romano, E., Honeychurch, J., & Illidge, T. (2021) · Cancers · doi:10.3390/cancers13030457 · Cited by 48
Severe Radiation-Induced Lymphopenia Attenuates the Benefit of Durvalumab After Concurrent Chemoradiotherapy for NSCLC
Wang, J., Xu, T., Wu, L., Lopez, P. B., Grassberger, C., Ellsworth, S. G., Mohan, R., Hobbs, B. P., Blumenschein, G. R., Tu, J. C., et al. (2022) · JTO Clinical and Research Reports · doi:10.1016/j.jtocrr.2022.100391 · Cited by 47
Self-citation
Recent advances in the metal/organic hybrid nanomaterials for cancer theranostics
Ye, Z., Bao, Y., Chen, Z., Ye, H., Feng, Z., Li, Y., Zeng, Y., Pan, Z., Ouyang, D., Zhang, K., et al. (2024) · Coordination Chemistry Reviews · doi:10.1016/j.ccr.2023.215654 · Cited by 46
Mathematical Modeling to Simulate the Effect of Adding Radiation Therapy to Immunotherapy and Application to Hepatocellular Carcinoma
Sung, W., Hong, T. S., Poznansky, M. C., Paganetti, H., & Grassberger, C. (2021) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2021.11.008 · Cited by 46
Self-citation
Opportunities for improving brain cancer treatment outcomes through imaging-based mathematical modeling of the delivery of radiotherapy and immunotherapy
Hormuth, D. A., Farhat, M., Christenson, C., Curl, B. J., Quarles, C. C., Chung, C. D., & Yankeelov, T. E. (2022) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2022.114367 · Cited by 45
Reeducating Tumor-Associated Macrophages Using CpG@Au Nanocomposites to Modulate Immunosuppressive Microenvironment for Improved Radio-Immunotherapy
Cao, Y., Ding, S., Zeng, L., Miao, J., Wang, K., Chen, G., Li, C., Zhou, J., Bian, X., & Tian, G. (2021) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.1c07626 · Cited by 45
Is the Combination of Immunotherapy and Radiotherapy in Non-small Cell Lung Cancer a Feasible and Effective Approach?
Spaas, M., & Lievens, Y. N. (2019) · Frontiers in Medicine · doi:10.3389/fmed.2019.00244 · Cited by 45
Optimizing Radiation Therapy to Boost Systemic Immune Responses in Breast Cancer: A Critical Review for Breast Radiation Oncologists
Ho, A. Y., Wright, J. L., Blitzblau, R. C., Mutter, R. W., Duda, D. G., Norton, L., Bardia, A., Spring, L. M., Isakoff, S. J., Chen, J. H., et al. (2020) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2020.05.011 · Cited by 45
Self-citation
Proceedings of the National Cancer Institute Workshop on combining immunotherapy with radiotherapy: challenges and opportunities for clinical translation
Morris, Z. S., Demaria, S., Monjazeb, A. M., Formenti, S. C., Weichselbaum, R. R., Welsh, J. D., Enderling, H., Schoenfeld, J. D., Brody, J., McGee, H. M., et al. (2025) · The Lancet Oncology · doi:10.1016/s1470-2045(24)00656-9 · Cited by 46
Self-citation
Tumor-Associated Neutrophil Extracellular Traps Regulating Nanocarrier-Enhanced Inhibition of Malignant Tumor Growth and Distant Metastasis
Yin, H., Lu, H., Xiong, Y., Ye, L., Teng, C., Cao, X., Li, S., Sun, S., Liu, W., Lv, W., et al. (2021) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.1c18660 · Cited by 44
Angiogenesis and immune checkpoint dual blockade in combination with radiotherapy for treatment of solid cancers: opportunities and challenges
Zhu, L., Yu, X., Wang, L., Liu, J., Qu, Z., Zhang, H., Li, L., Chen, J., & Zhou, Q. (2021) · Oncogenesis · doi:10.1038/s41389-021-00335-w · Cited by 45
Anti-TGF-β/PD-L1 bispecific antibody synergizes with radiotherapy to enhance antitumor immunity and mitigate radiation-induced pulmonary fibrosis
Wu, Y., Yan, Y., Guo, Y., Niu, M., Zhou, B., Zhang, J., Zhou, P., Chu, Q., Mei, Q., Yi, M., et al. (2025) · Journal of Hematology & Oncology · doi:10.1186/s13045-025-01678-2 · Cited by 43
The Next Chapter in Immunotherapy and Radiation Combination Therapy: Cancer-Specific Perspectives
Wisdom, A. J., Barker, C. A., Chang, J. Y., Demaria, S., Formenti, S. C., Grassberger, C., Gregucci, F., Hoppe, B. S., Kirsch, D. G., Marciscano, A. E. E., et al. (2024) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2023.12.046 · Cited by 39
Self-citation
Single-Fraction Stereotactic Body Radiation Therapy: A Paradigm During the Coronavirus Disease 2019 (COVID-19) Pandemic and Beyond?
Ng, S. S. W., Ning, M. S., Lee, P. P., McMahon, R. A., Siva, S., & Chuong, M. D. (2020) · Advances in Radiation Oncology · doi:10.1016/j.adro.2020.06.011 · Cited by 38
The Potentiation of Anti-Tumor Immunity by Tumor Abolition with Alpha Particles, Protons, or Carbon Ion Radiation and Its Enforcement by Combination with Immunoadjuvants or Inhibitors of Immune Suppressor Cells and Checkpoint Molecules
Keisari, Y., & Kelson, I. (2021) · Cells · doi:10.3390/cells10020228 · Cited by 37
Tackling the current dilemma of immunotherapy in extensive-stage small cell lung cancer: A promising strategy of combining with radiotherapy
Kang, K., Wu, Y., Yao, Z., & Lü, Y. (2023) · Cancer Letters · doi:10.1016/j.canlet.2023.216239 · Cited by 39
Artificial intelligence in cancer research: learning at different levels of data granularity
Cirillo, D., Núñez‐Carpintero, I., & Valencia, A. (2021) · Molecular Oncology · doi:10.1002/1878-0261.12920 · Cited by 44
Combining Immunotherapy with Radiation Therapy in Non–Small Cell Lung Cancer
Fitzgerald, K., & Simone, C. B. (2020) · Thoracic surgery clinics/Thorac. surg. clin. · doi:10.1016/j.thorsurg.2020.01.002 · Cited by 34
Tumor-Derived C-C Motif Ligand 2 Induces the Recruitment and Polarization of Tumor-Associated Macrophages and Increases the Metastatic Potential of Bladder Cancer Cells in the Postirradiated Microenvironment
Chiang, Y., Tsai, Y., Wang, C., Hsueh, F.-J., Huang, C., Chung, S., Chen, C., Pu, Y., & Cheng, J. C. (2022) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2022.06.054 · Cited by 33
Radio-induced lymphopenia in the era of anti-cancer immunotherapy
de Kermenguy, F., Meziani, L., Mondini, M., Clémenson, C., Morel, D., Deutsch, É., & Robert, C. (2023) · International review of cytology · doi:10.1016/bs.ircmb.2023.03.002 · Cited by 34
C-C chemokine receptor 4 (CCR4)-positive regulatory T cells interact with tumor-associated macrophages to facilitate metastatic potential after radiation
Chiang, Y., Lu, L.-F., Tsai, C.-L., Tsai, Y., Wang, C., Hsueh, F.-J., Huang, C., Chen, C., Pu, Y., & Cheng, J. C. (2023) · European Journal of Cancer · doi:10.1016/j.ejca.2023.113521 · Cited by 33
Novel strategies for tumor radiosensitization mediated by multifunctional gold-based nanomaterials
Wang, Z., Ren, X., Wang, D., Guan, L., Li, X., Zhao, Y., Liu, A., He, L., Wang, T., Zvyagin, A. V., et al. (2022) · Biomaterials Science · doi:10.1039/d2bm01496c · Cited by 33
Effect of Interleukin-7 on Radiation-Induced Lymphopenia and Its Antitumor Effects in a Mouse Model
Byun, H. K., Kim, K. J., Han, S. C., & Seong, J. (2020) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2020.12.004 · Cited by 32
ROS-Responsive Nanocomplex of aPD-L1 and Cabazitaxel Improves Intratumor Delivery and Potentiates Radiation-Mediated Antitumor Immunity
Wang, J., Li, J., Wu, Y., Xu, X., Qian, X., Lei, Y., Liu, H., Zhang, Z., & Li, Y. (2022) · Nano Letters · doi:10.1021/acs.nanolett.2c03227 · Cited by 31
Nanoparticles augment the therapeutic window of RT and immunotherapy for treating cancers: pivotal role of autophagy
Wu, Y.-H., Chen, R.-J., Chiu, H., Yang, L., Wang, Y., Chen, Y., Yeh, Y.-L., Liao, M., & Wang, Y. (2022) · Theranostics · doi:10.7150/thno.77233 · Cited by 32
Nanointegrative In Situ Reprogramming of Tumor-Intrinsic Lipid Droplet Biogenesis for Low-Dose Radiation-Activated Ferroptosis Immunotherapy
Zhang, Q., Wang, X., Zhao, Y., Cheng, Z., Fang, D., Liu, Y., Tian, G., Li, M., & Luo, Z. Y. (2023) · ACS Nano · doi:10.1021/acsnano.3c08907 · Cited by 30
Beyond success: unveiling the hidden potential of radiotherapy and immunotherapy in solid tumors
Wu, Y., Yi, M., Niu, M., Zhou, B., Mei, Q., & Wu, K. (2024) · 癌症：英文版 · doi:10.1002/cac2.12576 · Cited by 30
Primary lung tumour stereotactic body radiotherapy followed by concurrent mediastinal chemoradiotherapy and adjuvant immunotherapy for locally advanced non-small-cell lung cancer: a multicentre, single-arm, phase 2 trial
Heinzerling, J. H., Mileham, K. F., Robinson, M. M., Symanowski, J. T., Induru, R. R., Brouse, G., Corso, C. D., Prabhu, R. S., Haggstrom, D. E., Moeller, B. J., et al. (2024) · The Lancet Oncology · doi:10.1016/s1470-2045(24)00573-4 · Cited by 30
Progress of immune checkpoint inhibitors therapy for non-small cell lung cancer with liver metastases
Qu, F., Zhou, Y., & Wu, S. (2023) · British Journal of Cancer · doi:10.1038/s41416-023-02482-w · Cited by 30
Tumor-immune ecosystem dynamics define an individual Radiation Immune Score to predict pan-cancer radiocurability
Alfonso, J. C. L., Grass, G. D., Welsh, E. A., Ahmed, K. A., Teer, J. K., Pilon‐Thomas, S., Harrison, L. B., Cleveland, J. L., Mulé, J. J., Eschrich, S. A., et al. (2021) · Neoplasia · doi:10.1016/j.neo.2021.09.003 · Cited by 29
Radiation dose, schedule, and novel systemic targets for radio-immunotherapy combinations
Karapetyan, L., Iheagwara, U. K., Olson, A. C., Chmura, S. J., Skinner, H. K., & Luke, J. J. (2023) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djad118 · Cited by 28
Radiotherapy for non-small cell lung cancer in the immunotherapy era: the opportunity and challenge—a narrative review
Xia, W.-Y., Feng, W., Zhang, C., Shen, Y., Zhang, Q., Yu, W. J., Cai, X., & Fu, X. (2020) · Translational Lung Cancer Research · doi:10.21037/tlcr-20-827 · Cited by 30
Combination of bacterial-targeted delivery of gold-based AIEgen radiosensitizer for fluorescence-image-guided enhanced radio-immunotherapy against advanced cancer
Duo, Y., Chen, Z., Li, Z., Li, X., Yao, Y., Xu, T., Gao, G., & Luo, G. (2023) · Bioactive Materials · doi:10.1016/j.bioactmat.2023.05.010 · Cited by 28
Metformin: (future) best friend of the radiation oncologist?
Chevalier, B., Pasquier, D., Lartigau, E. F., Chargari, C., Schernberg, A., Jannin, A., Mirabel, X., Vantyghem, M., & Escande, A. (2020) · Radiotherapy and Oncology · doi:10.1016/j.radonc.2020.06.030 · Cited by 27
Biogenic platinum nanoparticles on bacterial fragments for enhanced radiotherapy to boost antitumor immunity
Deng, Z., Liu, J., Xi, M., Wang, C., Fang, H., Wu, X., Zhang, C., Sun, G., Zhang, Y., Shen, L., et al. (2022) · Nano Today · doi:10.1016/j.nantod.2022.101656 · Cited by 27
Efficacy and Safety of Pembrolizumab (MK-3475) in Combination with Chemoradiotherapy Versus Chemoradiotherapy Alone in Muscle-invasive Bladder Cancer: The MK-3475-992/KEYNOTE-992 Trial
Tissot, G., & Xylinas, E. N. (2023) · European Urology Focus · doi:10.1016/j.euf.2022.12.012 · Cited by 26
Prognostic value of interim CT-based peritumoral and intratumoral radiomics in laryngeal and hypopharyngeal cancer patients undergoing definitive radiotherapy
Lin, C.-H., Yan, J., Yap, W., Kang, C., Chang, Y., Tsai, T., Chang, K., Liao, C., Hsu, C., Chou, W., et al. (2023) · Radiotherapy and Oncology · doi:10.1016/j.radonc.2023.109938 · Cited by 25
Novel Radiation Therapy Paradigms and Immunomodulation: Heresies and Hope
Dutt, S., Ahmed, M. M., Loo, B. W., & Strober, S. (2020) · Seminars in Radiation Oncology · doi:10.1016/j.semradonc.2019.12.006 · Cited by 27
Microvesicle-inspired oxygen-delivering nanosystem potentiates radiotherapy-mediated modulation of tumor stroma and antitumor immunity
Gong, X., Li, J., Xu, X., Wu, Y., Lei, Y., Liu, H., Qian, X., Li, Y., & Zhang, Z. (2022) · Biomaterials · doi:10.1016/j.biomaterials.2022.121855 · Cited by 25
High proportion of circulating CD8 + CD28- senescent T cells is an independent predictor of distant metastasis in nasopharyngeal carcinoma after radiotherapy
Xu, X., Wei, F., Xiao, L., Wu, R., Wei, B., Huang, S., Yi, J., & Cui, W. (2023) · Journal of Translational Medicine · doi:10.1186/s12967-023-03912-2 · Cited by 27
An Italian Retrospective Survey on Bone Metastasis in Melanoma: Impact of Immunotherapy and Radiotherapy on Survival
Mannavola, F., Mandalà, M., Todisco, A., Chiarion‐Sileni, V., Palla, M., Minisini, A. M., Pala, L., Morgese, F., Guardo, L. D., Stucci, L. S., et al. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.01652 · Cited by 24
Sintilimab, stereotactic body radiotherapy and granulocyte–macrophage colony stimulating factor as second-line therapy for advanced non-small cell lung cancer: safety run-in results of a multicenter, single-arm, phase II trial
Ni, J., Zhou, Y., Wu, L., Ai, X., Dong, X., Chu, Q., Han, C., Wang, X., & Zhu, Z. (2021) · Radiation Oncology · doi:10.1186/s13014-021-01905-3 · Cited by 24
Transcriptional Dynamics of DNA Damage Responsive Genes in Circulating Leukocytes during Radiotherapy
Cruz-Garcia, L., Nasser, F., O’Brien, G., Grepl, J., Vinnikov, V. A., Starenkiy, V., Artiukh, S. V., Gramatiuk, S. M., & Badie, C. (2022) · Cancers · doi:10.3390/cancers14112649 · Cited by 27
BCG invokes superior STING ‐mediated innate immune response over radiotherapy in a carcinogen murine model of urothelial cancer
Lombardo, K. A., Obradović, A., Singh, A. K., Liu, J. L., Joice, G. A., Kates, M. R., Bishai, W. R., McConkey, D. J., Chaux, A., Eich, M., et al. (2021) · The Journal of Pathology · doi:10.1002/path.5830 · Cited by 22
Lymphocyte Depletion Rate as a Biomarker of Radiation Dose to Circulating Lymphocytes During Fractionated Partial-Body Radiation Therapy
Ellsworth, S. G., Yalamanchali, A., Lautenschlaeger, T., Grossman, S. A., Grassberger, C., Lin, S. H., & Mohan, R. (2022) · Advances in Radiation Oncology · doi:10.1016/j.adro.2022.100959 · Cited by 23
Self-citation
A T‐Cell Inspired Sonoporation System Enhances Low‐Dose X‐Ray‐Mediated Pyroptosis and Radioimmunotherapy Efficacy by Restoring Gasdermin‐E Expression
Yin, H., Hu, X., Xie, C., Li, Y., Gao, Y., Zeng, H., Zhu, W., Xie, D., & Wang, Q. (2024) · Advanced Materials · doi:10.1002/adma.202401384 · Cited by 22
Chemoradiotherapy Versus Chemotherapy Alone for Advanced Esophageal Squamous Cell Carcinoma: The Role of Definitive Radiotherapy for Primary Tumor in the Metastatic Setting
Li, L., Fu, Q., Zhao, W., Wang, Y., Meng, W.-W., & Su, T. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.824206 · Cited by 22
Betulinic acid triggers apoptosis and inhibits migration and invasion of gastric cancer cells by impairing EMT progress
Chen, Y., Wu, X., Liu, C., & Zhou, Y. (2020) · Cell Biochemistry and Function · doi:10.1002/cbf.3537 · Cited by 22
Enzyme-responsive micellar JQ1 induces enhanced BET protein inhibition and immunotherapy of malignant tumors
Zhang, Z., Zhang, Q., Xie, J., Zhong, Z., & Deng, C. (2021) · Biomaterials Science · doi:10.1039/d1bm00724f · Cited by 22
Catalytic nanotechnology of X-ray photodynamics for cancer treatments
Zhang, G., Guo, M., Ma, H., Wang, J., & Zhang, X. (2022) · Biomaterials Science · doi:10.1039/d2bm01698b · Cited by 21
The Change of Soluble Programmed Cell Death-Ligand 1 in Glioma Patients Receiving Radiotherapy and Its Impact on Clinical Outcomes
Ding, X., Wang, L., Zhu, Y., Li, Y., Nie, S.-L., Yang, J., Liang, H. L., Weichselbaum, R. R., Yu, J., & Hu, M. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.580335 · Cited by 20

Authors: Grassberger, C., Ellsworth, S. G., Wilks, M. Q., Keane, F. K., & Loeffler, J. S.
Affiliations: Harvard University (US)
Indiana University School of Medicine (US)
Gordon Center for Medical Imaging (US)
Corresponding author: Grassberger, Clemens
ORCID: Grassberger, Clemens
Ellsworth, Susannah G.
Keane, Florence K.
Venue: Nature Reviews Clinical Oncology
Publisher: Springer Science and Business Media LLC
Published: 2019-06-26
Volume: 16
Issue: 12
Pages: 729-745
ISSN: 1759-4774 (ISSN-L)
1759-4782
DOI: 10.1038/s41571-019-0238-9
PMC: PMC13492067
OpenAlex: W2954542121
Cited by: 244
References: 216
Citations by year: 2026: 14 · 2025: 26 · 2024: 25 · 2023: 45 · 2022: 53 · 2021: 36 · 2020: 40 · 2019: 5
FWCI: 3.19
Type: journal article
Language: en
Open access: green
pmc.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature Reviews Clinical Oncology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (submittedVersion)
Funders: Massachusetts General Hospital
National Cancer Institute (R21CA241918, P01CA021239)
Topics: Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Radiomics and Machine Learning in Medical Imaging
Keywords: radiotherapy, antitumor immunity, immune checkpoint inhibitors, radiation-induced immunosuppression, immune response assessment, serum biomarkers, immune cell imaging, personalized radiotherapy, predictive biomarkers
MeSH terms: Combined Modality Therapy, Humans, Immune System, Immunotherapy, Neoplasms, Radiotherapy, Precision Medicine

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Assessing the interactions between radiotherapy and antitumour immunity

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks