Impact of (chemo)radiotherapy on immune cell composition and function in cervical cancer patients
Open accessAbstract
New treatments based on combinations of standard therapeutic modalities and immunotherapy are of potential use, but require a profound understanding of immune modulatory properties of standard therapies. Here, the impact of standard (chemo)radiotherapy on the immune system of cervical cancer patients was evaluated. Thirty patients with cervical cancer were treated with external beam radiation therapy (EBRT), using conventional three-dimensional or intensity modulated radiation therapy without constraints for bone marrow sparing. Serial blood sampling for immunomonitoring was performed before, midway and at 3, 6 and 9 weeks after EBRT to analyze the composition of lymphocyte and myeloid-cell populations, the expression of co-stimulatory molecules, T-cell reactivity and antigen presenting cell (APC) function. Therapy significantly decreased the absolute numbers of circulating leukocytes and lymphocytes. Furthermore, the capacity of the remaining T cells to respond to antigenic or mitogenic stimulation was impaired. During treatment the frequency of both CD4+ and CD8+ T cells dropped and CD4+ T cells displayed an increased expression of programmed cell death-1 (PD-1). In vitro blocking of PD-1 successfully increased T-cell reactivity in all five samples isolated before radiotherapy but was less successful in restoring reactivity in samples isolated at later time points. Moreover, (chemo)radiotherapy was associated with an increase in both circulating monocytes and myeloid-derived suppressor cells (MDSCs) and an impaired capacity of APCs to stimulate allogeneic T cells. T-cell reactivity was slowly restored at 6–9 weeks after cessation of therapy. We conclude that conventional (chemo)radiotherapy profoundly suppresses the immune system in cervical cancer patients, and may restrict its combination 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
Cites
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?
Chemoradiotherapy for cervical cancer induces unfavorable immune changes reflected by decreased circulating lymphocytes, both CD4+ and CD8+ T cells, and increased myeloid-cell populations including myeloid-derived suppressor cells and monocytes.
“Recent studies have already reported that chemoradiotherapy for CC induces unfavorable immune changes reflected by a decreased number of circulating lymphocytes, both CD4+ and CD8+ T cells, and an increased percentage in myeloid-cell populations, including myeloid-derived suppressor cells and monocytes23.”
From Gut microbiome diversity is an independent predictor of survival in cervical cancer patients receiving chemoradiation (2021) · cites this paper as [23]
The number and functional orientation of tumor-infiltrating CD4+ and CD8+ T cells and the presence of M1 type macrophages strongly correlate with survival in patients with cervical cancer after CRT.
“Previous studies have reported that the number and functional orientation of tumor-infiltrating CD4+ and CD8+ T cells and the presence of M1 type macrophages strongly correlates with survival in patients with CC after CRT23,24.”
From Gut microbiome diversity is an independent predictor of survival in cervical cancer patients receiving chemoradiation (2021) · cites this paper as [23]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Normalization of Tumor Vasculature: An Emerging Concept in Antiangiogenic Therapy
Jain, R. K. (2005) · Science · doi:10.1126/science.1104819 · Cited by 5,527 · see citing works
Natural History of Cervicovaginal Papillomavirus Infection in Young Women
Ho, G. Y. F., Bierman, R., Beardsley, L., Chang, C. J., & Burk, R. D. (1998) · New England Journal of Medicine · doi:10.1056/nejm199802123380703 · Cited by 2,329 · see citing works
The Tumour Microenvironment after Radiotherapy: Mechanisms of Resistance and Recurrence
Barker, H. E., Paget, J. T. E., Khan, A. A., & Harrington, K. J. (2015) · Nature Reviews Cancer · doi:10.1038/nrc3958 · Cited by 2,144 · cited 1× · see citing works
“to treatment success or failure, particularly in so-called immunogenic tumors.(8) Interestingly, it was shown that a pretreatment peripheral blood lymphocyte count at or above the median value was associated with higher clinical responses and survival rates.”
BackgroundNATURAL HISTORY OF CERVICOVAGINAL PAPILLOMAVIRUS INFECTION IN YOUNG WOMEN
Loria, G. R., Ierman, R. O. B., Eardsley, L. E. B., & Hang, H. J. C. (1998) · Cited by 1,887 · see citing works
Lee, Y., Auh, S. L., Wang, Y., Burnette, B., Wang, Y., Meng, Y., Beckett, M., Sharma, R., Chin, R., Tu, T., et al. (2009) · Blood · doi:10.1182/blood-2009-02-206870 · Cited by 1,324 · see citing works
Klug, F., Prakash, H., Huber, P. E., Seibel, T., Bender, N., Halama, N., Pfirschke, C., Voss, R. H., Timke, C., Umansky, L., et al. (2013) · Cancer Cell · doi:10.1016/j.ccr.2013.09.014 · Cited by 1,097 · see citing works
Combining Radiotherapy and Cancer Immunotherapy: A Paradigm Shift
Formenti, S. C., & Demaria, S. (2013) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djs629 · Cited by 1,058 · see citing works
Sturdza, A. E., Pötter, R., Fokdal, L. U., Haie-Méder, C., Tan, L. T., Mazeron, R., Petrič, P., Šegedin, B., Jurgenliemk-Schulz, I. M., Nomden, C., et al. (2016) · Radiotherapy and Oncology · doi:10.1016/j.radonc.2016.03.011 · Cited by 718 · see citing works
QUINN, M., BENEDET, J., Odicino, F. E., Maisonneuve, P., Beller, U., CREASMAN, W., Heintz, A. P. M., Ngan, H., & Pecorelli, S. L. (2006) · International Journal of Gynecology & Obstetrics · doi:10.1016/s0020-7292(06)60030-1 · Cited by 572 · see citing works
Hematopoietic stem cell compartment: acute and late effects of radiation therapy and chemotherapy.
Mauch, P., Constine, L., Greenberger, J., Knospe, W., Sullivan, J., Liesveld, J. L., & Deeg, H. J. (1995) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/0360-3016(94)00430-s · Cited by 507 · see citing works
Dimopoulos, J. C. A., Petrow, P. K., Tanderup, K., Petrič, P., Berger, D., Kirisits, C., Pedersen, E. M., Limbergen, E. V., Haie-Méder, C., & Pötter, R. (2012) · Radiotherapy and Oncology · doi:10.1016/j.radonc.2011.12.024 · Cited by 441 · see citing works
Chakraborty, M., Abrams, S. I., Coleman, C. N., Camphausen, K. A., Schlom, J., & Hodge, J. W. (2004) · Cancer Research · doi:10.1158/0008-5472.can-04-0073 · Cited by 435 · see citing works
Piersma, S. J., Jordanova, E. S., van Poelgeest, M. I. E., Kwappenberg, K. M. C., van der Hulst, J. M., Drijfhout, J. W., Melief, C. J. M., Kenter, G. G., Fleuren, G. J., Offringa, R., et al. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-3388 · Cited by 414 · see citing works
Self-citationThe Distribution of Active Bone Marrow in the Adult
Ellis, R. E. (1961) · Physics in Medicine and Biology · doi:10.1088/0031-9155/5/3/302 · Cited by 322 · see citing works
Tartour, É., Péré, H., Maillère, B., Terme, M., Merillon, N., Taı̈eb, J., Sandoval, F., Quintin‐Colonna, F., Lacerda, K., Karadimou, A., et al. (2011) · Cancer and Metastasis Reviews · doi:10.1007/s10555-011-9281-4 · Cited by 316 · see citing works
Workshop R: Tumor Immunology, Abstract R1 bis R30
Ganß, R., Ryschich, E., Klar, E., Arnold, B., & Hämmerling, G. J. (2001) · Immunobiology · doi:10.1078/0171-2985-00078 · Cited by 312 · see citing works
Jie, H.-B., Gildener‐Leapman, N., Li, J., Srivastava, R. M., Gibson, S. P., Whiteside, T. L., & Ferris, R. (2013) · British Journal of Cancer · doi:10.1038/bjc.2013.645 · Cited by 285 · see citing works
Karim, R., Jordanova, E. S., Piersma, S. J., Kenter, G. G., Chen, L., Boer, J. M., Melief, C. J. M., & van der Burg, S. H. (2009) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-09-1652 · Cited by 250 · see citing works
Self-citationHematologic Toxicity in RTOG 0418: A Phase 2 Study of Postoperative IMRT for Gynecologic Cancer
Klopp, A. H., Moughan, J., Portelance, L., Miller, B. E., Salehpour, M., Hildebrandt, E., Nuanjing, J., D'Souza, D. P., Souhami, L., Small, W. C., et al. (2013) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2013.01.017 · Cited by 240 · see citing works
Rijkmans, E. C., Nout, R. A., Rutten, I. H. H. M., Ketelaars, M., Neelis, K. J., Laman, M. S., Coen, V. L. M. A., Gaarenstroom, K. N., Kroep, J. R., & Creutzberg, C. L. (2014) · Gynecologic Oncology · doi:10.1016/j.ygyno.2014.08.027 · Cited by 240 · see citing works
Self-citationWelters, M. J. P., Kenter, G. G., van Steenwijk, P. J. D. V., Löwik, M. J. G., der Meer, D. M. A. B.-V., Essahsah, F., Stynenbosch, L. F. M., Vloon, A. P. G., Ramwadhdoebé, T. H., Piersma, S. J., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1006500107 · Cited by 239 · see citing works
Self-citationJordanova, E. S., Gorter, A., Ayachi, O., Prins, F., Durrant, L. G., Kenter, G. G., van der Burg, S. H., & Fleuren, G. J. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-4554 · Cited by 233 · see citing works
Self-citationCell intrinsic mechanisms of T‐cell inhibition and application to cancer therapy
Peggs, K. S., Quezada, S. A., & Allison, J. P. (2008) · Immunological Reviews · doi:10.1111/j.1600-065x.2008.00649.x · Cited by 228 · see citing works
Vaccination during myeloid cell depletion by cancer chemotherapy fosters robust T cell responses
Welters, M. J. P., van der Sluis, T. C., van Meir, H., Loof, N. M., van Ham, V. J., van Duikeren, S., Santegoets, S. J. A. M., Arens, R., de Kam, M. L., Cohen, A. F., et al. (2016) · Science Translational Medicine · doi:10.1126/scitranslmed.aad8307 · Cited by 216 · see citing works
Self-citationSantegoets, S. J. A. M., Dijkgraaf, E. M., Battaglia, A., Beckhove, P., Britten, C. M., Gallimore, A., Godkin, A. J., Gouttefangeas, C., de Gruijl, T. D., Koenen, H. J. P. M., et al. (2015) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-015-1729-x · Cited by 213 · see citing works
Self-citationAlbuquerque, K., Giangreco, D., Morrison, C. K., Siddiqui, M., Sinacore, J., Potkul, R. K., & Roeske, J. C. (2010) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2009.12.025 · Cited by 160 · see citing works
Soisson, A. P., Soper, J. T., Clarke‐Pearson, D. L., Berchuck, A., Montana, G. S., & Creasman, W. T. (1990) · Gynecologic Oncology · doi:10.1016/0090-8258(90)90374-t · Cited by 150 · see citing works
Harnessing the immune system to treat cancer
Bhardwaj, N. (2007) · Journal of Clinical Investigation · doi:10.1172/jci32136 · Cited by 131 · see citing works
van Steenwijk, P. J. D. V., Ramwadhdoebé, T. H., Goedemans, R., Doorduijn, E. M., van Ham, J. J., Gorter, A., van Hall, T., Kuijjer, M. L., van Poelgeest, M. I. E., van der Burg, S. H., et al. (2013) · International Journal of Cancer · doi:10.1002/ijc.28309 · Cited by 129 · see citing works
Nedergaard, B. S., Ladekarl, M. B., Nyengaard, J. R., & Nielsen, K. (2007) · Gynecologic Oncology · doi:10.1016/j.ygyno.2007.08.089 · Cited by 111 · see citing works
Parikh, F. S., Duluc, D., Imai, N., Clark, A., Misiukiewicz, K., Bonomi, M., Gupta, V., Patsias, A., Parides, M. K., Demicco, E. G., et al. (2014) · Cancer Research · doi:10.1158/0008-5472.can-14-1913 · Cited by 102 · see citing works
Santin, A. D., Hermonat, P. L., Ravaggi, A., Bellone, S., Roman, J. J., Pecorelli, S. L., Cannon, M. J., & Parham, G. P. (2000) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/s0360-3016(00)00769-0 · Cited by 94 · see citing works
Vacchelli, E., Vitale, I., Tartour, É., Eggermont, A. M. M., Sautès‐Fridman, C., Galon, J., Zitvogel, L., Kroemer, G., & Galluzzi, L. (2013) · OncoImmunology · doi:10.4161/onci.25595 · Cited by 91 · see citing works
Mizunuma, M., Yokoyama, Y., Futagami, M., Aoki, M., Takai, Y., & Mizunuma, H. (2015) · International Journal of Clinical Oncology · doi:10.1007/s10147-015-0807-6 · Cited by 84 · see citing works
Low-dose radiation enhances therapeutic HPV DNA vaccination in tumor-bearing hosts
Tseng, C.-W., Trimble, C. L., Zeng, Q., Monie, A., Alvarez, R. D., Huh, W. K., Hoory, T., Wang, M., Hung, C., & Wu, T. ‐. (2008) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-008-0596-0 · Cited by 62 · see citing works
Keisari, Y., Hochman, I., Confino, H., Korenstein, R., & Kelson, I. (2013) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-013-1462-2 · Cited by 54 · see citing works
Battaglia, A., Buzzonetti, A., Martinelli, E., Fanelli, M., Petrillo, M., Ferrandina, G., Scambia, G., & Fattorossi, A. (2010) · International Journal of Radiation Oncology, Biology, Physics · doi:10.1016/j.ijrobp.2009.10.014 · Cited by 50 · see citing works
McGuire, S., Bhatia, S. K., Sun, W., Jacobson, G. M., Menda, Y., Ponto, L. L. B., Smith, B. J., Gross, B., Bayouth, J. E., Sunderland, J. J., et al. (2016) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2016.04.009 · Cited by 49 · see citing works
Hellebrekers, Zwinderman, Kenter, Peters, Snijders-Keilholz, Graziosi, Fleuren, & Trimbos (1999) · International Journal of Gynecological Cancer · doi:10.1046/j.1525-1438.1999.99023.x · Cited by 42 · see citing works
Ovarian cancer screening. The role of ultrasound in early detection
Karlan, B. Y., & PLATT, L. D. (1995) · Cancer · doi:10.1002/1097-0142(19951115)76:10+ · Cited by 39 · see citing works
Choi, C. H., Kang, H., Kim, W. Y., Kim, T., Lee, J., Huh, S. J., Lee, J., Kim, B., & Bae, D. (2007) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2007.09.024 · Cited by 34 · see citing works
Pieterse, Q. D., Trimbos, J. B., Dijkman, A., Creutzberg, C. L., Gaarenstroom, K. N., Peters, A. A. W., & Kenter, G. G. (2006) · International Journal of Gynecological Cancer · doi:10.1111/j.1525-1438.2006.00600.x · Cited by 32 · see citing works
Self-citationHoskin, P., Rojas, A. M., Peiris, S. N., Mullassery, V. M., & Chong, I. Y.-S. (2014) · Clinical Oncology · doi:10.1016/j.clon.2013.11.023 · Cited by 30 · see citing works
The tumor area occupied by Tbet+ cells in deeply invading cervical cancer predicts clinical outcome
Gorter, A., Prins, F. A., van Diepen, M., Punt, S., & van der Burg, S. H. (2015) · Journal of Translational Medicine · doi:10.1186/s12967-015-0664-0 · Cited by 21 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- [2]Ganss R, Ryschich E, Klar E, Arnold B, Hammerling GJ Combination of T-cell therapy and trigger of inflammation induces remodeling of the vasculature and tumor eradication. Cancer Res 2002; 62(5): 1462- 70; PMID:11888921 11888921
Cited by
Sorted by citations
Hiam-Galvez, K. J., Allen, B. M., & Spitzer, M. H. (2021) · Nature Reviews Cancer · doi:10.1038/s41568-021-00347-z · Cited by 1,400 · see citing works
Cervical Cancer Immunotherapy: Facts and Hopes
Ferrall, L., Lin, K. Y., Roden, R. B. S., Hung, C., & Wu, T. ‐. (2021) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-20-2833 · Cited by 407 · see citing works
Challenges in developing personalized neoantigen cancer vaccines
Katsikis, P. D., Ishii, K. J., & Schliehe, C. (2023) · Nature reviews. Immunology · doi:10.1038/s41577-023-00937-y · Cited by 266 · see citing works
YTHDF2 inhibition potentiates radiotherapy antitumor efficacy
Wang, L., Dou, X., Chen, S., Yu, X., Huang, X., Zhang, L., Chen, Y., Wang, J., Yang, K., Bugno, J., et al. (2023) · Cancer Cell · doi:10.1016/j.ccell.2023.04.019 · Cited by 251 · see citing works
Ellsworth, S. G. (2018) · Advances in Radiation Oncology · doi:10.1016/j.adro.2018.08.014 · Cited by 189 · see citing works
Zhang, M., Zhang, Y., Zhang, L., & Tian, Q. (2019) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2019.02.013 · Cited by 177 · see citing works
Zhang, Y., Zhang, M., Jiang, Y., Li, X., He, Y., Zeng, P., Guo, Z., Chang, Y., Luo, H., Liu, Y., et al. (2018) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-018-2718-1 · Cited by 138 · see citing works
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 · see citing works
Immune modulatory effects of radiotherapy as basis for well-reasoned radioimmunotherapies
Rückert, M., Deloch, L., Fietkau, R., Frey, B., Hecht, M., & Gaipl, U. S. (2018) · Strahlentherapie und Onkologie · doi:10.1007/s00066-018-1287-1 · Cited by 113 · see citing works
Tumor microenvironment modulation enhances immunologic benefit of chemoradiotherapy
Hanoteau, A., Newton, J. M., Krupar, R., Huang, C. L., Liu, H., Gaspero, A., Gartrell, R. D., Saenger, Y. M., Hart, T. D., Santegoets, S. J. A. M., et al. (2019) · Journal for ImmunoTherapy of Cancer · doi:10.1186/s40425-018-0485-9 · Cited by 91 · see citing works
Self-citationMyeloid-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 · see citing works
Fujimoto, D., Uehara, K., Sato, Y., Sakanoue, I., Ito, M., Teraoka, S., Nagata, K., Nakagawa, A., Kosaka, Y., Otsuka, K., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-11949-9 · Cited by 86 · see citing works
Radiotherapy and cGAS/STING signaling: Impact on MDSCs in the tumor microenvironment
Kho, V. M., Mekers, V. E., Span, P. N., Bussink, J., & Adema, G. J. (2021) · Cellular Immunology · doi:10.1016/j.cellimm.2021.104298 · Cited by 80 · see citing works
The interactions and communications in tumor resistance to radiotherapy: Therapy perspectives
Ashrafizadeh, M., Farhood, B., Musa, A. E., Taeb, S., & Najafi, M. (2020) · International Immunopharmacology · doi:10.1016/j.intimp.2020.106807 · Cited by 78 · see citing works
Newton, J. M., Hanoteau, A., Liu, H., Gaspero, A., Parikh, F., Gartrell, R. D., Hart, T. D., Laoui, D., Ginderachter, J. A. V., Dharmaraj, N., et al. (2019) · Journal for ImmunoTherapy of Cancer · doi:10.1186/s40425-019-0698-6 · Cited by 79 · see citing works
Corbeau, A., Kuipers, S. C., de Boer, S. M., Horeweg, N., Hoogeman, M. S., Godart, J., & Nout, R. A. (2021) · Radiotherapy and Oncology · doi:10.1016/j.radonc.2021.09.009 · Cited by 76 · see citing works
Self-citationOstrand‐Rosenberg, S., Horn, L. A., & Ciavattone, N. G. (2019) · Frontiers in Oncology · doi:10.3389/fonc.2019.00215 · Cited by 72 · see citing works
Hou, Y., Yang, K., Wang, L., Wang, J., Huang, X., Piffkó, A., Luo, S. Z., Yu, X., Rao, E., Martinez, C. N., et al. (2024) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-23-3206 · Cited by 71 · see citing works
Enhancing the efficacy of immunotherapy using radiotherapy
Keam, S., Gill, S., Ebert, M. A., Nowak, A. K., & Cook, A. (2020) · Clinical & Translational Immunology · doi:10.1002/cti2.1169 · Cited by 67 · see citing works
Heeren, A. M., van Luijk, I. F., Lakeman, J., Pocorni, N., Kole, J., de Menezes, R. X., Kenter, G. G., Bosse, T., de Kroon, C. D., & Jordanova, E. S. (2019) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-019-02412-x · Cited by 65 · see citing works
Self-citationBhatt, K. H., Neller, M. A., Srihari, S., Crooks, P., Lekieffre, L., Aftab, B. T., Liu, H. Y.-H., Smith, C., Kenny, L., Porceddu, S. V., et al. (2020) · The Journal of Experimental Medicine · doi:10.1084/jem.20200389 · Cited by 64 · see citing works
Dammeijer, F. F., Lau, S. P., van Eijck, C. H. J., van der Burg, S. H., & Aerts, J. G. J. V. (2017) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2017.06.011 · Cited by 62 · see citing works
Eckert, F., Zwirner, K., Boeke, S., Thorwarth, D., Zips, D., & Huber, S. M. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00407 · Cited by 60 · see citing works
Wang, X., Wang, P., Zhao, Z., Mao, Q., Yu, J., & Li, M. (2020) · Therapeutic Advances in Medical Oncology · doi:10.1177/1758835920926822 · Cited by 59 · see citing works
Liu, C., Cheng, H., Luo, G., Yu, L., Jin, K., Guo, M., Ni, Q., & Yu, X. (2017) · International Journal of Oncology · doi:10.3892/ijo.2017.4032 · Cited by 56 · see citing works
Zhang, T., Yu, H., Ni, C., Zhang, T., Liu, L., Lv, Q., Zhang, Z., Wang, Z., Wu, D., Wu, P., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-04978-x · Cited by 56 · see citing works
Balázs, K., Kis, E., Badie, C., Bogdándi, E. N., Candéias, S. M., Garcia, L. C., Domińczyk, I., Frey, B., Gaipl, U. S., Jurányi, Z., et al. (2019) · Cancers · doi:10.3390/cancers11091324 · Cited by 56 · see citing works
Radiation Therapy and Myeloid-Derived Suppressor Cells: Breaking Down Their Cancerous Partnership
Bergerud, K. B., Berkseth, M., Pardoll, D. M., Ganguly, S., Kleinberg, L. R., Lawrence, J., Odde, D. J., Largaespada, D. A., Terezakis, S. A., & Sloan, L. (2023) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2023.11.050 · Cited by 53 · see citing works
Hasan, Y., Furtado, L. V., Tergas, A. I., Lee, N. K., Brooks, R. A., McCall, A. R., Golden, D. W., Jolly, S., Fleming, G. F., Morrow, M. P., et al. (2020) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2020.02.031 · Cited by 53 · see citing works
Impact of curative radiotherapy on the immune status of patients with localized prostate cancer
Eckert, F., Schaedle, P., Zips, D., Schmid-Horch, B. D., Rammensee, H., Gani, C., & Gouttefangeas, C. (2018) · OncoImmunology · doi:10.1080/2162402x.2018.1496881 · Cited by 51 · see citing works
Myeloid-Derived Suppressor Cells: A Multifaceted Accomplice in Tumor Progression
Cheng, J., Yuan, Y., Zhu, B., & Jia, Q. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.740827 · Cited by 49 · see citing works
Radiation-Induced Transformation of Immunoregulatory Networks in the Tumor Stroma
Martínez-Zubiaurre, I., Chalmers, A. J., & Hellevik, T. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01679 · Cited by 52 · see citing works
Kinetics of Intratumoral Immune Cell Activation During Chemoradiation for Cervical Cancer
Dorta-Estremera, S., Colbert, L. E., Nookala, S. S., Yanamandra, A. V., Yang, G., Delgado, A., Mikkelson, M., Eifel, P., Jhingran, A., Lilie, L. L., et al. (2018) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2018.06.404 · Cited by 48 · see citing works
Victorelli, F. D., Cardoso, V. M. D. O., Ferreira, N. N., Calixto, G. M. F., Fontana, C. R., Baltazar, F., Gremião, M. P. D., & Chorilli, M. (2020) · European Journal of Pharmaceutics and Biopharmaceutics · doi:10.1016/j.ejpb.2020.06.010 · Cited by 48 · see citing works
Dai, D., Tian, Q., Yu, G., Shui, Y., Jiang, H., & Wei, Q. (2022) · Cancers · doi:10.3390/cancers14123024 · Cited by 45 · see citing works
Radiotherapy as a Backbone for Novel Concepts in Cancer Immunotherapy
Kabiljo, J., Harpain, F., Carotta, S., & Bergmann, M. M. (2019) · Cancers · doi:10.3390/cancers12010079 · Cited by 45 · see citing works
Rückert, M., Deloch, L., Frey, B., Schlücker, E., Fietkau, R., & Gaipl, U. S. (2021) · Cancers · doi:10.3390/cancers13040714 · Cited by 44 · see citing works
Butner, J. D., Wang, Z., Elganainy, D., Feghali, K. A. A., Plodinec, M., Călin, G. A., Dogra, P., Nizzero, S., Ruiz-Ramírez, J., Martin, G. V., et al. (2021) · Nature Biomedical Engineering · doi:10.1038/s41551-020-00662-0 · Cited by 43 · see citing works
Li, R., Liu, Y., Yin, R., Yin, L., Li, K., Sun, C., Zhou, Z., Li, P., Tong, R., Xue, J., et al. (2021) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2021.03.003 · Cited by 45 · see citing works
The evolving landscape of PCSK9 inhibition in cancer
Oza, P. P., & Kashfi, K. (2023) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2023.175721 · Cited by 42 · see citing works
The Goldilocks Window of Personalized Chemotherapy: Getting the Immune Response Just Right
Park, D. S., Robertson‐Tessi, M., Luddy, K. A., Maini, P. K., Bonsall, M. B., Gatenby, R. A., & Anderson, A. R. A. (2019) · Cancer Research · doi:10.1158/0008-5472.can-18-3712 · Cited by 41 · see citing works
Victorelli, F. D., Calixto, G. M. F., dos Santos, K. C., Buzzá, H. H., & Chorilli, M. (2020) · Journal of Molecular Liquids · doi:10.1016/j.molliq.2020.115080 · Cited by 34 · see citing works
Wagener‐Ryczek, S., Schoemmel, M., Kraemer, M., Bruns, C. J., Schroeder, W., Zander, T., Gebauer, F., Alakus, H., Merkelbach‐Bruse, S., Buettner, R., et al. (2020) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-019-02475-w · Cited by 33 · see citing works
Lee, Y. J., Lee, S. B., Beak, S. K., Han, Y. D., Cho, M. S., Hur, H., Lee, K. Y., Kim, N. K., & Min, B. S. (2018) · Scientific Reports · doi:10.1038/s41598-018-25970-z · Cited by 32 · see citing works
Chitsike, L., & Duerksen-Hughes, P. J. (2020) · Current Treatment Options in Oncology · doi:10.1007/s11864-020-00790-4 · Cited by 29 · see citing works
Larsson, A.-M., Roxå, A., Leandersson, K., & Bergenfelz, C. (2019) · Scientific Reports · doi:10.1038/s41598-019-49943-y · Cited by 28 · see citing works
Skaličková, M., Vanova, K. H., Uher, O., Fialová, J. L., Petrláková, K., Masařík, M., Kejík, Z., Pavel Martasek, E., Pacák, K., & Jakubek, M. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1479483 · Cited by 27 · see citing works
Chi, W.-Y., Hu, Y., Huang, H., Kuo, H., Lin, S., Kuo, C.-T. J., Tao, J., Fan, D., Huang, Y.-M., Wu, A. A., et al. (2024) · Journal of Biomedical Science · doi:10.1186/s12929-024-01082-x · Cited by 26 · see citing works
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 25 · see citing works
Konnerth, D., Gaasch, A., Zinn, A., Rogowski, P., Rottler, M., Walter, F., Knoth, J., Sturdza, A. E., Oelmann, J., Grawe, F., et al. (2024) · Cancers · doi:10.3390/cancers16101842 · Cited by 24 · see citing works
Theobald, L., Stroeder, R., Melchior, P., Iordache, I.-I., Tänzer, T., Port, M., Glombitza, B., Marx, S., Schub, D., Herr, C., et al. (2021) · Molecular Oncology · doi:10.1002/1878-0261.13095 · Cited by 24 · see citing works
Lee, K. K., Go, K., Lee, E., Kim, H., Kim, S., Kim, J., Chae, M. S., & Jeong, J.-O. (2025) · Gels · doi:10.3390/gels11060426 · Cited by 23 · see citing works
Myeloid-Derived Suppressor Cells as Therapeutic Targets in Uterine Cervical and Endometrial Cancers
Mabuchi, S., & Sasano, T. (2021) · Cells · doi:10.3390/cells10051073 · Cited by 25 · see citing works
Influence of chemoradiation on the immune microenvironment of cervical cancer patients
Herter, J. M., Kiljan, M., Kunze, S., Reinscheid, M., Ibruli, O., Cai, J., Niu, L., Heßelmann, I., Trommer, M., Herter-Sprie, G. S., et al. (2022) · Strahlentherapie und Onkologie · doi:10.1007/s00066-022-02007-z · Cited by 23 · see citing works
Tuong, Z. K., Nöske, K., Kuo, P., Bashaw, A. A., Teoh, S. M., & Frazer, I. H. (2017) · Papillomavirus Research · doi:10.1016/j.pvr.2017.10.001 · Cited by 23 · see citing works
Modulation of PD-1/PD-L1 axis in myeloid-derived suppressor cells by anti-cancer treatments
Jachetti, E., Sangaletti, S., Chiodoni, C., Ferrara, R., & Colombo, M. P. (2021) · Cellular Immunology · doi:10.1016/j.cellimm.2021.104301 · Cited by 22 · see citing works
Odiase, O., Noah-Vermillion, L., Simone, B. A., & Aridgides, P. D. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.663749 · Cited by 22 · see citing works
Corbeau, A., Nout, R. A., Mens, J. W., Horeweg, N., Godart, J., Kerkhof, E. M., Kuipers, S. C., van Poelgeest, M. I. E., Kroep, J. R., Boere, I. A., et al. (2021) · Cancers · doi:10.3390/cancers13205179 · Cited by 22 · see citing works
Self-citationvan Luijk, I. F., Smith, S. M., Ojeda, M. C. M., Oei, A. L., Kenter, G. G., & Jordanova, E. S. (2022) · Journal of Clinical Medicine · doi:10.3390/jcm11092277 · Cited by 22 · see citing works
Self-citationMawardika, T., Afiyanti, Y., & Rahmah, H. (2019) · BMC Nursing · doi:10.1186/s12912-019-0355-x · Cited by 21 · see citing works
Kim, K. H., Pyo, H., Lee, H., Oh, D., Noh, J. M., Ahn, Y. C., Yoon, H. I., Moon, H., Lee, J., Park, S., et al. (2022) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2022.02.003 · Cited by 21 · see citing works
Frey, B., Mika, J., Jelonek, K., Cruz-Garcia, L., Roelants, C., Testard, I., Cherradi, N., Lumniczky, K., Polozov, S., Napieralska, A., et al. (2020) · Strahlentherapie und Onkologie · doi:10.1007/s00066-020-01637-5 · Cited by 20 · see citing works
Harnessing immunity for therapy in human papillomavirus driven cancers
Stern, P. L. (2021) · Tumour Virus Research · doi:10.1016/j.tvr.2021.200212 · Cited by 18 · see citing works
Prognostic features of the tumour microenvironment in oesophageal adenocarcinoma
McShane, R., Arya, S., Stewart, A. J., Caie, P. D., & Bates, M. (2021) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2021.188598 · Cited by 16 · see citing works
Oropharyngeal Squamous Cell Carcinoma Treatment in the Era of Immune Checkpoint Inhibitors
Stern, P. L., & Dalianis, T. (2021) · Viruses · doi:10.3390/v13071234 · Cited by 16 · see citing works
T cell subsets in cervical cancer tumor microenvironment: advances and therapeutic opportunities
Guo, W.-X., Dai, L., & Qiu, L. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1612032 · Cited by 16 · see citing works
Ocolotobiche, E. E., Banegas, Y. C., & Güerci, A. M. (2019) · International Journal of Radiation Biology · doi:10.1080/09553002.2019.1625489 · Cited by 15 · see citing works
Lentinan regulates the immune efficacy of macrophage for lung metastasis in triple negative breast
Guan, Z., Liu, Y., Liu, P., Yin, L., Chen, L., & Duan, W. (2023) · Journal of Functional Foods · doi:10.1016/j.jff.2023.105560 · Cited by 14 · see citing works
Hoffmann, E., Paulsen, F., Schaedle, P., Zips, D., Gani, C., Rammensee, H., Gouttefangeas, C., & Eckert, F. (2021) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-021-03002-6 · Cited by 13 · see citing works
Impact of hematologic toxicities during concurrent chemoradiation for cervical cancer
Shi, F., Yoder, A. K., Mach, C. M., Dalwadi, S. M., Anderson, M. L., Hall, T. R., & Ludwig, M. S. (2022) · Obstetrics & Gynecology Science · doi:10.5468/ogs.21308 · Cited by 13 · see citing works
Optimized radiotherapy to improve clinical outcomes for locally advanced lung cancer
Jaksic, N., Chajon, É., Bellec, J., Corre, R., Ricordel, C., Latour, B. R. D., Léna, H., Schick, U., de Crevoisier, R., & Castelli, J. (2018) · Radiation Oncology · doi:10.1186/s13014-018-1094-y · Cited by 13 · see citing works
Elbers, J. B. W., Gunsch, P. A., van Vulpen, M., Debets, R., Keereweer, S., van Meerten, E., Zindler, J. D., van Norden, Y., Hoogeman, M. S., Verduijn, G. M., et al. (2023) · BMC Cancer · doi:10.1186/s12885-023-11031-w · Cited by 12 · see citing works
Self-citationChang, C., Chen, C.-J., Yu, C., Tsai, H., Chen, G. T. Y., & Chiang, C. (2023) · Frontiers in Oncology · doi:10.3389/fonc.2023.1263873 · Cited by 12 · see citing works
Wark, A., Gupta, A. K., Meixner, E., König, L., Hörner‐Rieber, J., Förster, T., Lang, K., Ellerbrock, M., Herfarth, K. K., Debus, J., et al. (2024) · Technology in Cancer Research & Treatment · doi:10.1177/15330338241252622 · Cited by 12 · see citing works
Yang, Z., Zhang, S., Ying, L., Zhang, W., Chen, X., Liang, Y., Chen, R., Yao, K., Li, C., Yu, C., et al. (2024) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2024.2372880 · Cited by 13 · see citing works
RNA m6A methylation and MDSCs: Roles and therapeutic implications for radiotherapy
Wang, L., Katipally, R. R., Liang, H. L., Yang, K., Pitroda, S. P., He, C., & Weichselbaum, R. R. (2023) · Med · doi:10.1016/j.medj.2023.09.001 · Cited by 11 · see citing works
Lymphocyte-sparing pelvic radiotherapy for prostate cancer: An in-silico study
Baré, M., Poeta, S., Fernandes, P., Jourani, Y., Otte, F.-X., Brussel, S. V., Gestel, D. V., & den Begin, R. V. (2022) · Physics and Imaging in Radiation Oncology · doi:10.1016/j.phro.2022.07.006 · Cited by 10 · see citing works
TIME Is Ticking for Cervical Cancer
Kumar, V., Bauer, C., & Stewart, J. H. (2023) · Biology · doi:10.3390/biology12070941 · Cited by 11 · see citing works
Qin, X., Wang, C., Gong, G., Wang, L., Su, Y., & Yin, Y. (2022) · BMC Cancer · doi:10.1186/s12885-022-10254-7 · Cited by 10 · see citing works
Shadbar, S., Balu-Iyer, S. V., Auclair, J. R., & Dadon, D. B. (2025) · Journal of Pharmaceutical Sciences · doi:10.1016/j.xphs.2025.103870 · Cited by 9 · see citing works
Chauhan, D. S., Shao, K., Nanjundappa, R. H., Yu, D., Stanford, M. M., Gao, H., & Umeshappa, C. S. (2025) · Advanced Science · doi:10.1002/advs.202417657 · Cited by 9 · see citing works
Guo, Y., Feng, Y., Fan, P., Yao, X., Peng, Y., Wang, R., & Kuerban, G. (2021) · Immunological Investigations · doi:10.1080/08820139.2020.1867567 · Cited by 9 · see citing works
Wang, H., Mendez, L. C., Morton, G., Loblaw, A., Mesci, A., Chung, H. T.-K., Chan, S., Huang, X., Downes, M. R., Vesprini, D., et al. (2020) · Radiotherapy and Oncology · doi:10.1016/j.radonc.2020.10.029 · Cited by 9 · see citing works
Boustani, J., Joseph, E. L. M., Martin, E., Benhmida, S., Lecoester, B., Tochet, F., Mirjolet, C., Chevalier, C., Thibouw, D., Vulquin, N., et al. (2021) · BMC Immunology · doi:10.1186/s12865-021-00429-5 · Cited by 8 · see citing works
Brachytherapy for targeting the immune system in cervical cancer patients
Linares, I., Francés, M. Á. B., Cañas, R., Najjari-Jamal, D., Gutiérrez, C., Marı́n, S., Comas, S., Guedea, F., & Pujol-Canadell, M. (2023) · BMC Immunology · doi:10.1186/s12865-023-00559-y · Cited by 8 · see citing works
Changes of proportions of circulating lymphocyte subsets in cancer patients after chemotherapy
Wang, W., Wang, Y., & Cao, Z. (2021) · Translational Cancer Research · doi:10.21037/tcr-21-1688 · Cited by 8 · see citing works
Radiotherapy Combination: Insight from Tumor Immune Microenvironment (TIME)
Alimohammadi, M., Nazari, H. G., Alimohammadi, R., Bakhshandeh, M., Jalali, S. A., & Rezaei, N. (2023) · Avicenna Journal of Medical Biotechnology · doi:10.18502/ajmb.v15i4.13490 · Cited by 8 · see citing works
Lim, D., Kim, H. K., Jeong, J., Jung, Y. S., Lee, S. E., Jang, H., Jung, S., Choi, H.-S., Rhee, J. H., Lee, S., et al. (2020) · Microorganisms · doi:10.3390/microorganisms8050646 · Cited by 8 · see citing works
Gies, S., Melchior, P., Stroeder, R., Tänzer, T., Theobald, L., Pohlers, M., Glombitza, B., Sester, M., Solomayer, E., & Walch‐Rückheim, B. (2023) · International Journal of Cancer · doi:10.1002/ijc.34745 · Cited by 7 · see citing works
Zong, Y., Chang, Y., Huang, K., Liu, J., & Zhao, Y. (2023) · International Immunopharmacology · doi:10.1016/j.intimp.2023.111199 · Cited by 7 · see citing works
Hoi, E. T. V., Santegoets, S. J. A. M., Mooijaart, S. P., van Heemst, D., Özkan, A., Verdegaal, E. M. E., Slingerland, M., Kapiteijn, E., van der Burg, S. H., Portielje, J. E. A., et al. (2024) · Immunity & Ageing · doi:10.1186/s12979-024-00463-y · Cited by 7 · see citing works
Self-citationQin, X., Gong, G., Wang, L., Su, Y., & Yin, Y. (2022) · Radiation Oncology · doi:10.1186/s13014-022-02175-3 · Cited by 7 · see citing works
Gao, X. Y., Zhang, Y., Li, X., Jansen, L., Alwers, E., Bewerunge‐Hudler, M., Schick, M., Chang-Claude, J. C., Hoffmeister, M., & Brenner, H. (2021) · Cancers · doi:10.3390/cancers13122948 · Cited by 6 · see citing works
Ko, M.-W., Kaur, K., Chen, P.-C., Breznik, B., Senjor, E., Chovatiya, N., Wong, P., Turnšek, T. L., Kos, J., & Jewett, A. (2023) · Elsevier eBooks · doi:10.1016/b978-0-12-822620-9.00013-6 · Cited by 6 · see citing works
Yıldırım, B. A., Güler, O. C., Köse, F., & Önal, C. (2019) · Journal of Obstetrics and Gynaecology · doi:10.1080/01443615.2019.1586852 · Cited by 6 · see citing works
Combination of radiotherapy and immunotherapy in duality with the protumoral action of radiation
Paquette, B., & Oweida, A. J. (2024) · Cancer/Radiothérapie · doi:10.1016/j.canrad.2024.07.002 · Cited by 5 · see citing works
Wang, S., Zhao, M., Gao, Z., Yang, X., Yuan, L., & Fu, J. (2025) · International Journal of Medical Sciences · doi:10.7150/ijms.107392 · Cited by 5 · see citing works
Yu-cheng, L., Qiu, L., Shao, K., Yongshi, J., Zhan, W., Ding, J., & Chen, W. (2025) · Scientific Reports · doi:10.1038/s41598-025-91362-9 · Cited by 5 · see citing works
Chemotherapy to potentiate the radiation-induced immune response
Lecoester, B., Wespiser, M., Marguier, A., Mirjolet, C., Boustani, J., & Adotévi, O. (2023) · International review of cytology · doi:10.1016/bs.ircmb.2023.01.004 · Cited by 5 · see citing works
Circulating Leukocyte Subsets Before and After a Breast Cancer Diagnosis and Therapy
Kresovich, J. K., O’Brien, K. M., Xu, Z., Weinberg, C. R., Sandler, D. P., & Taylor, J. A. (2024) · JAMA Network Open · doi:10.1001/jamanetworkopen.2023.56113 · Cited by 5 · see citing works
- Authors
- van Meir, H., Nout, R. A., Welters, M. J. P., Loof, N. M., de Kam, M. L., van Ham, J. J., Samuels, S., Kenter, G. G., Cohen, A. F., Melief, C. J. M., Burggraaf, J., van Poelgeest, M. I. E., & van der Burg, S. H.
- Affiliations
- Department of Gynecology, Leiden University Medical Center, Leiden, the Netherlands
- Leiden University Medical Center (NL)
- Centre for Human Drug Research, Leiden, the Netherlands
- Department of Medical Oncology, Leiden University Medical Center, Leiden, the Netherlands
- The Netherlands Cancer Institute (NL)
- Centre for Human Drug Research (NL)
- ISA Pharmaceuticals (Netherlands) (NL)
- Venue
- OncoImmunology
- Publisher
- Informa UK Limited
- Published
- 2017-02
- Volume
- 6
- Issue
- 2
- Pages
- e1267095
- ISSN
- 2162-4011 (ISSN-L)
- 2162-402X
- PMC
- PMC5353924
- OpenAlex
- W2567712538
- Cited by
- 143
- References
- 44
- Citations by year
- 2026: 12 · 2025: 12 · 2024: 12 · 2023: 21 · 2022: 14 · 2021: 28 · 2020: 15 · 2019: 14 · 2018: 10 · 2017: 5
- FWCI
- 5.21
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- OncoImmunology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
- Leiden Repository (Leiden University) (submittedVersion)
- Pure Amsterdam UMC (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- Leids Universitair Medisch Centrum
- Topics
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Health Sciences › Medicine › Obstetrics and Gynecology › Endometrial and Cervical Cancer Treatments
- Keywords
- cervical cancer, chemoradiotherapy, external beam radiotherapy, immunosuppression, T cell response, PD-1, myeloid-derived suppressor cells, antigen-presenting cells, CD4+ T cells, CD8+ T cells, monocytes, combination immunotherapy, immune monitoring
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
