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Published in: Strahlentherapie und Onkologie 5/2022

01-05-2022 | Glioblastoma | Original Article

Association between treatment-related lymphopenia and survival in glioblastoma patients following postoperative chemoradiotherapy

Authors: Roberto Mapelli, Chiara Julita, Sofia Paola Bianchi, Nicolò Gallina, MD, Raffaella Lucchini, MD, Martina Midulla, MD, Flavia Puci, MD, Jessica Saddi, MD, Sara Trivellato, PhD, Denis Panizza, PhD, Elena De Ponti, PhD, Stefano Arcangeli, MD

Published in: Strahlentherapie und Onkologie | Issue 5/2022

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Abstract

Purpose

Our study investigated the association between treatment-related lymphopenia and overall survival (OS) in a series of glioblastoma (GBM) patients. We also explored clinical and dosimetric predictors of lymphocytes depletion.

Methods

Between 2015 and 2019, 64 patients were treated at the same institution with postoperative chemoradiotherapy. Peripheral lymphocyte count (PLC) data and dose–volume histogram parameters were collected. Radiotherapy (RT) schedule consisted in standard total dose of 60 Gy in 30 daily fractions, with concomitant and adjuvant temozolomide (TMZ). Posttreatment acute absolute lymphopenia (nadir AAL) was calculated as a PLC lower than 1.0 × 103/mm3. Acute relative lymphopenia (ARL) was expressed by the nadir-PLC/baseline-PLC ratio < 0.5. Nadir-PLC was the lowest PLC registered between the end of RT and the first month of follow-up. Survival rates were estimated with Kaplan–Meier curves. Clinical and dosimetric variables related to AAL/ARL and OS were identified by univariate and multivariate analyses.

Results

A total of 57 patients were eligible and included in the analyses. The median PLC was significantly decreased following chemoradiotherapy (2180/mm3 vs 900/mm3). Median OS was 16 months (range 5–55 months), with no significant difference between patients who developed nadir AAL and those who did not (16 months vs 16.5 months; p = 0.304). When considering ARL vs non-ARL, median OS was 14 months vs 26 months (p = 0.013), respectively. In multivariate Cox regression only age, sex, extent of surgery, access to adjuvant chemotherapy and brain D98% were independently associated with OS.

Conclusion

Although iatrogenic immunosuppression could be associated with inferior clinical outcomes, our data show that treatment-related lymphopenia does not adversely affect GBM survival. Prospective studies are required to confirm these findings.
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Literature
1.
go back to reference Shiraishi Y, Fang P, Xu C, Song J, Krishnan S, Koay EJ, Mehran RJ, Hofstetter WL, Blum-Murphy M, Ajani JA, Komaki R, Minsky B, Mohan R, Hsu CC, Hobbs BP, Lin SH (2018) Severe lymphopenia during neoadjuvant chemoradiation for esophageal cancer: a propensity matched analysis of the relative risk of proton versus photon-based radiation therapy. Radiother Oncol 128(1):154–160CrossRefPubMed Shiraishi Y, Fang P, Xu C, Song J, Krishnan S, Koay EJ, Mehran RJ, Hofstetter WL, Blum-Murphy M, Ajani JA, Komaki R, Minsky B, Mohan R, Hsu CC, Hobbs BP, Lin SH (2018) Severe lymphopenia during neoadjuvant chemoradiation for esophageal cancer: a propensity matched analysis of the relative risk of proton versus photon-based radiation therapy. Radiother Oncol 128(1):154–160CrossRefPubMed
2.
go back to reference Campian JL, Ye X, Brock M, Grossman SA (2013) Treatment-related lymphopenia in patients with stage III non-small-cell lung cancer. Cancer Invest 31(3):183–188CrossRefPubMedPubMedCentral Campian JL, Ye X, Brock M, Grossman SA (2013) Treatment-related lymphopenia in patients with stage III non-small-cell lung cancer. Cancer Invest 31(3):183–188CrossRefPubMedPubMedCentral
3.
go back to reference Tang C, Liao Z, Gomez D, Levy L, Zhuang Y, Gebremichael RA, Hong DS, Komaki R, Welsh JW (2014) Lymphopenia association with gross tumor volume and lung V5 and its effects on non-small cell lung cancer patient outcomes. Int J Radiat Oncol Biol Phys 89(5):1084–1091CrossRefPubMed Tang C, Liao Z, Gomez D, Levy L, Zhuang Y, Gebremichael RA, Hong DS, Komaki R, Welsh JW (2014) Lymphopenia association with gross tumor volume and lung V5 and its effects on non-small cell lung cancer patient outcomes. Int J Radiat Oncol Biol Phys 89(5):1084–1091CrossRefPubMed
4.
go back to reference Cho O, Oh YT, Chun M, Noh OK, Lee HW (2016) Radiation-related lymphopenia as a new prognostic factor in limited-stage small cell lung cancer. Tumour Biol 37(1):971–978CrossRefPubMed Cho O, Oh YT, Chun M, Noh OK, Lee HW (2016) Radiation-related lymphopenia as a new prognostic factor in limited-stage small cell lung cancer. Tumour Biol 37(1):971–978CrossRefPubMed
5.
go back to reference Wild AT, Ye X, Ellsworth SG, Smith JA, Narang AK, Garg T, Campian J, Laheru DA, Zheng L, Wolfgang CL, Tran PT, Grossman SA, Herman JM (2015) The association between chemoradiation-related lymphopenia and clinical outcomes in patients with locally advanced pancreatic adenocarcinoma. Am J Clin Oncol 38(3):259–265CrossRefPubMedPubMedCentral Wild AT, Ye X, Ellsworth SG, Smith JA, Narang AK, Garg T, Campian J, Laheru DA, Zheng L, Wolfgang CL, Tran PT, Grossman SA, Herman JM (2015) The association between chemoradiation-related lymphopenia and clinical outcomes in patients with locally advanced pancreatic adenocarcinoma. Am J Clin Oncol 38(3):259–265CrossRefPubMedPubMedCentral
6.
go back to reference Wu ES, Oduyebo T, Cobb LP, Cholakian D, Kong X, Fader AN, Levinson KL, Tanner EJ 3rd, Stone RL, Piotrowski A, Grossman S, Roche KL (2016) Lymphopenia and its association with survival in patients with locally advanced cervical cancer. Gynecol Oncol 140(1):76–82CrossRefPubMed Wu ES, Oduyebo T, Cobb LP, Cholakian D, Kong X, Fader AN, Levinson KL, Tanner EJ 3rd, Stone RL, Piotrowski A, Grossman S, Roche KL (2016) Lymphopenia and its association with survival in patients with locally advanced cervical cancer. Gynecol Oncol 140(1):76–82CrossRefPubMed
7.
go back to reference Cho O, Chun M, Chang SJ, Oh YT, Noh OK (2016) Prognostic value of severe lymphopenia during pelvic concurrent chemoradiotherapy in cervical cancer. Anticancer Res 36(7):3541–3547PubMed Cho O, Chun M, Chang SJ, Oh YT, Noh OK (2016) Prognostic value of severe lymphopenia during pelvic concurrent chemoradiotherapy in cervical cancer. Anticancer Res 36(7):3541–3547PubMed
8.
go back to reference Trowell OA (1952) The sensitivity of lymphocytes to ionising radiation. J Pathol Bacteriol 64(4):687–704CrossRefPubMed Trowell OA (1952) The sensitivity of lymphocytes to ionising radiation. J Pathol Bacteriol 64(4):687–704CrossRefPubMed
9.
go back to reference Nakamura N, Kusunoki Y, Akiyama M (1990) Radiosensitivity of CD4 or CD8 positive human T‑lymphocytes by an in vitro colony formation assay. Radiat Res 123(2):224–227CrossRefPubMed Nakamura N, Kusunoki Y, Akiyama M (1990) Radiosensitivity of CD4 or CD8 positive human T‑lymphocytes by an in vitro colony formation assay. Radiat Res 123(2):224–227CrossRefPubMed
10.
go back to reference Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B et al (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352(10):987–996CrossRefPubMed Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B et al (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352(10):987–996CrossRefPubMed
11.
go back to reference Grossman SA, Ye X, Lesser G, Sloan A, Carraway H, Desideri S, Piantadosi S (2011) Immunosuppression in patients with high-grade gliomas treated with radiation and temozolomide. Clin Cancer Res 17(16):5473–5480CrossRefPubMedPubMedCentral Grossman SA, Ye X, Lesser G, Sloan A, Carraway H, Desideri S, Piantadosi S (2011) Immunosuppression in patients with high-grade gliomas treated with radiation and temozolomide. Clin Cancer Res 17(16):5473–5480CrossRefPubMedPubMedCentral
12.
go back to reference Yu SK, Chalmers AJ (2007) Patients receiving standard-dose temozolomide therapy are at risk of Pneumocystis carinii pneumonia. Clin Oncol (R Coll Radiol) 19:631–632CrossRef Yu SK, Chalmers AJ (2007) Patients receiving standard-dose temozolomide therapy are at risk of Pneumocystis carinii pneumonia. Clin Oncol (R Coll Radiol) 19:631–632CrossRef
13.
go back to reference Schwarzberg AB, Stover EH, Sengupta T et al (2007) Selective lymphopenia and opportunistic infections in neuroendocrine tumor patients receiving temozolomide. Cancer Invest 25:249–255CrossRefPubMed Schwarzberg AB, Stover EH, Sengupta T et al (2007) Selective lymphopenia and opportunistic infections in neuroendocrine tumor patients receiving temozolomide. Cancer Invest 25:249–255CrossRefPubMed
14.
go back to reference Yaman E, Coskun U, Ozturk B et al (2009) Opportunistic cytomegalovirus infection in a patient receiving temozolomide for treatment of malignant glioma. J Clin Neurosci 16:591–592CrossRefPubMed Yaman E, Coskun U, Ozturk B et al (2009) Opportunistic cytomegalovirus infection in a patient receiving temozolomide for treatment of malignant glioma. J Clin Neurosci 16:591–592CrossRefPubMed
15.
go back to reference De Jesus A, Grossman SA, Paun O (2009) Cytomegalovirus associated colonic pseudotumor: a consequence of iatrogenic immunosuppression in a patient with primary brain tumor receiving radiation and temozolomide. J Neurooncol 94:445–448CrossRefPubMedPubMedCentral De Jesus A, Grossman SA, Paun O (2009) Cytomegalovirus associated colonic pseudotumor: a consequence of iatrogenic immunosuppression in a patient with primary brain tumor receiving radiation and temozolomide. J Neurooncol 94:445–448CrossRefPubMedPubMedCentral
16.
go back to reference Yovino S, Kleinberg L, Grossman SA, Narayanan M, Ford E (2013) The etiology of treatment-related lymphopenia in patients with malignant gliomas: modeling radiation dose to circulating lymphocytes explains clinical observations and suggests methods of modifying the impact of radiation on immune cells. Cancer Invest 31(2):140–144CrossRefPubMedPubMedCentral Yovino S, Kleinberg L, Grossman SA, Narayanan M, Ford E (2013) The etiology of treatment-related lymphopenia in patients with malignant gliomas: modeling radiation dose to circulating lymphocytes explains clinical observations and suggests methods of modifying the impact of radiation on immune cells. Cancer Invest 31(2):140–144CrossRefPubMedPubMedCentral
18.
go back to reference Reardon DA, Freeman G, Wu C, Chiocca EA, Wucherpfennig KW, Wen PY, Fritsch EF, Curry WT Jr, Sampson JH, Dranoff G (2014) Immunotherapy advances for glioblastoma. Neuro Oncol 16(11):1441–1458CrossRefPubMedPubMedCentral Reardon DA, Freeman G, Wu C, Chiocca EA, Wucherpfennig KW, Wen PY, Fritsch EF, Curry WT Jr, Sampson JH, Dranoff G (2014) Immunotherapy advances for glioblastoma. Neuro Oncol 16(11):1441–1458CrossRefPubMedPubMedCentral
19.
go back to reference Gupta T, Mohanty S, Moiyadi A, Jalali R (2013) Factors predicting temozolomide induced clinically significant acute hematologic toxicity in patients with high-grade gliomas: a clinical audit. Clin Neurol Neurosurg 115(9):1814–1819CrossRefPubMed Gupta T, Mohanty S, Moiyadi A, Jalali R (2013) Factors predicting temozolomide induced clinically significant acute hematologic toxicity in patients with high-grade gliomas: a clinical audit. Clin Neurol Neurosurg 115(9):1814–1819CrossRefPubMed
20.
go back to reference Hughes MA, Parisi M, Grossman S, Kleinberg L (2005) Primary brain tumors treated with steroids and radiotherapy: low CD4 counts and risk of infection. Int J Radiat Oncol Biol Phys 62(5):1423–1426CrossRefPubMed Hughes MA, Parisi M, Grossman S, Kleinberg L (2005) Primary brain tumors treated with steroids and radiotherapy: low CD4 counts and risk of infection. Int J Radiat Oncol Biol Phys 62(5):1423–1426CrossRefPubMed
21.
go back to reference Ishikawa E, Yamamoto T, Sakamoto N, Nakai K, Akutsu H, Tsuboi K, Takano S, Matsumura A (2010) Low peripheral lymphocyte count before focal radiotherapy plus concomitant temozolomide predicts severe lymphopenia during malignant glioma treatment. Neurol Med Chir (Tokyo) 50(8):638–644CrossRef Ishikawa E, Yamamoto T, Sakamoto N, Nakai K, Akutsu H, Tsuboi K, Takano S, Matsumura A (2010) Low peripheral lymphocyte count before focal radiotherapy plus concomitant temozolomide predicts severe lymphopenia during malignant glioma treatment. Neurol Med Chir (Tokyo) 50(8):638–644CrossRef
22.
go back to reference Cabrera AR, Kirkpatrick JP, Fiveash JB et al (2016) Radiation therapy for glioblastoma: executive summary of an American Society for Radiation Oncology evidence-based clinical practice guideline. Pract Radiat Oncol 6(4):217–225CrossRefPubMed Cabrera AR, Kirkpatrick JP, Fiveash JB et al (2016) Radiation therapy for glioblastoma: executive summary of an American Society for Radiation Oncology evidence-based clinical practice guideline. Pract Radiat Oncol 6(4):217–225CrossRefPubMed
23.
go back to reference Demaria S, Ng B, Devitt ML, Babb JS, Kawashima N, Liebes L, Formenti SC (2004) Ionizing radiation inhibition of distant untreated tumors (abscopal effect) is immune mediated. Int J Radiat Oncol Biol Phys 58(3):862–870CrossRefPubMed Demaria S, Ng B, Devitt ML, Babb JS, Kawashima N, Liebes L, Formenti SC (2004) Ionizing radiation inhibition of distant untreated tumors (abscopal effect) is immune mediated. Int J Radiat Oncol Biol Phys 58(3):862–870CrossRefPubMed
24.
go back to reference Golden EB, Chachoua A, Fenton-Kerimian MB et al (2015) Abscopal responses in metastatic non-small cell lung cancer (NSCLC) patients treated on a phase 2 study of combined radiation therapy and ipilimumab: evidence for the in situ vaccination hypothesis of radiation. Int J Radiat Oncol Biol Phys 93:S66–S67CrossRef Golden EB, Chachoua A, Fenton-Kerimian MB et al (2015) Abscopal responses in metastatic non-small cell lung cancer (NSCLC) patients treated on a phase 2 study of combined radiation therapy and ipilimumab: evidence for the in situ vaccination hypothesis of radiation. Int J Radiat Oncol Biol Phys 93:S66–S67CrossRef
25.
go back to reference Koshy M, Villano JL, Dolecek TA, Howard A, Mahmood U, Chmura SJ, Weichselbaum RR, McCarthy BJ (2012) Improved survival time trends of glioblastoma using the SEER 17 population-based registries. J Neurooncol 107(1):207–212CrossRefPubMed Koshy M, Villano JL, Dolecek TA, Howard A, Mahmood U, Chmura SJ, Weichselbaum RR, McCarthy BJ (2012) Improved survival time trends of glioblastoma using the SEER 17 population-based registries. J Neurooncol 107(1):207–212CrossRefPubMed
26.
go back to reference Ye LL, Fan XW, Hu CS, He XY, Wang XS, Shen CY, Xu TT, Ying HM (2019) Dosimetry of the brain and hypothalamus predicting acute lymphopenia and the survival of glioma patients with postoperative radiotherapy. Cancer Med 8(6):2759–2768CrossRefPubMedPubMedCentral Ye LL, Fan XW, Hu CS, He XY, Wang XS, Shen CY, Xu TT, Ying HM (2019) Dosimetry of the brain and hypothalamus predicting acute lymphopenia and the survival of glioma patients with postoperative radiotherapy. Cancer Med 8(6):2759–2768CrossRefPubMedPubMedCentral
27.
go back to reference Mendez JS, Govindan A, Leong J, Gao F, Huang J, Campian JL (2016) Association between treatment-related lymphopenia and overall survival in elderly patients with newly diagnosed glioblastoma. J Neurooncol 127(2):329–335CrossRefPubMedPubMedCentral Mendez JS, Govindan A, Leong J, Gao F, Huang J, Campian JL (2016) Association between treatment-related lymphopenia and overall survival in elderly patients with newly diagnosed glioblastoma. J Neurooncol 127(2):329–335CrossRefPubMedPubMedCentral
28.
go back to reference Sun GY, Wang SL, Song YW, Jin J, Wang WH, Liu YP, Ren H, Fang H, Tang Y, Zhao XR, Song YC, Yu ZH, Liu XF, Li YX (2020) Radiation-induced lymphopenia predicts poorer prognosis in patients with breast cancer: a post hoc analysis of a randomized controlled trial of postmastectomy hypofractionated radiation therapy. Int J Radiat Oncol Biol Phys 108(1):277–285CrossRefPubMed Sun GY, Wang SL, Song YW, Jin J, Wang WH, Liu YP, Ren H, Fang H, Tang Y, Zhao XR, Song YC, Yu ZH, Liu XF, Li YX (2020) Radiation-induced lymphopenia predicts poorer prognosis in patients with breast cancer: a post hoc analysis of a randomized controlled trial of postmastectomy hypofractionated radiation therapy. Int J Radiat Oncol Biol Phys 108(1):277–285CrossRefPubMed
29.
go back to reference Baciu I, Hriscu M, Saulea G (2003) Hypothalamic mechanisms of immunity. Int J Neurosci 113(2):259–277CrossRefPubMed Baciu I, Hriscu M, Saulea G (2003) Hypothalamic mechanisms of immunity. Int J Neurosci 113(2):259–277CrossRefPubMed
30.
go back to reference Pavlov VA, Tracey KJ (2017) Neural regulation of immunity: molecular mechanisms and clinical translation. Nat Neurosci 20(2):156–166CrossRefPubMed Pavlov VA, Tracey KJ (2017) Neural regulation of immunity: molecular mechanisms and clinical translation. Nat Neurosci 20(2):156–166CrossRefPubMed
31.
go back to reference Huang J, DeWees T, Badiyan SN, Speirs CK, Mullen DF, Fergus S, Tran DD, Linette G, Campian JL, Chicoine MR, Kim AH, Dunn G, Simpson JR, Robinson CG (2015) Clinical and dosimetric predictors of acute severe lymphopenia during radiation therapy and concurrent temozolomide for high-grade glioma. Int J Radiat Oncol Biol Phys 92(5):1000–1007CrossRefPubMed Huang J, DeWees T, Badiyan SN, Speirs CK, Mullen DF, Fergus S, Tran DD, Linette G, Campian JL, Chicoine MR, Kim AH, Dunn G, Simpson JR, Robinson CG (2015) Clinical and dosimetric predictors of acute severe lymphopenia during radiation therapy and concurrent temozolomide for high-grade glioma. Int J Radiat Oncol Biol Phys 92(5):1000–1007CrossRefPubMed
32.
go back to reference Zarrinkoob L, Ambarki K, Wåhlin A, Birgander R, Eklund A, Malm J (2015) Blood flow distribution in cerebral arteries. J Cereb Blood Flow Metab 35(4):648–654CrossRefPubMedPubMedCentral Zarrinkoob L, Ambarki K, Wåhlin A, Birgander R, Eklund A, Malm J (2015) Blood flow distribution in cerebral arteries. J Cereb Blood Flow Metab 35(4):648–654CrossRefPubMedPubMedCentral
33.
go back to reference Howell RM, Scarboro SB, Kry SF, Yaldo DZ (2010) Accuracy of out-of-field dose calculations by a commercial treatment planning system. Phys Med Biol 55(23):6999–7008CrossRefPubMedPubMedCentral Howell RM, Scarboro SB, Kry SF, Yaldo DZ (2010) Accuracy of out-of-field dose calculations by a commercial treatment planning system. Phys Med Biol 55(23):6999–7008CrossRefPubMedPubMedCentral
34.
go back to reference Howell RM, Scarboro SB, Taddei PJ, Krishnan S, Kry SF, Newhauser WD (2010) Methodology for determining doses to in-field, out-of-field and partially in-field organs for late effects studies in photon radiotherapy. Phys Med Biol 55(23):7009–7023CrossRefPubMedPubMedCentral Howell RM, Scarboro SB, Taddei PJ, Krishnan S, Kry SF, Newhauser WD (2010) Methodology for determining doses to in-field, out-of-field and partially in-field organs for late effects studies in photon radiotherapy. Phys Med Biol 55(23):7009–7023CrossRefPubMedPubMedCentral
35.
go back to reference Kaderka R, Schardt D, Durante M, Berger T, Ramm U, Licher J, La Tessa C (2012) Out-of-field dose measurements in a water phantom using different radiotherapy modalities. Phys Med Biol 57:5059–5074CrossRefPubMed Kaderka R, Schardt D, Durante M, Berger T, Ramm U, Licher J, La Tessa C (2012) Out-of-field dose measurements in a water phantom using different radiotherapy modalities. Phys Med Biol 57:5059–5074CrossRefPubMed
36.
go back to reference Huang JY, Followill DS, Wang XA, Kry SF (2013) Accuracy and sources of error of out-of field dose calculations by a commercial treatment planning system for intensity-modulated radiation therapy treatments. J Appl Clin Med Phys 14(2):4139CrossRefPubMed Huang JY, Followill DS, Wang XA, Kry SF (2013) Accuracy and sources of error of out-of field dose calculations by a commercial treatment planning system for intensity-modulated radiation therapy treatments. J Appl Clin Med Phys 14(2):4139CrossRefPubMed
37.
go back to reference Ojala JJ, Kapanen MK, Hyödynmaa SJ, Wigren TK, Pitkänen MA (2014) Performance of dose calculation algorithms from three generations in lung SBRT: comparison with full Monte Carlo-based dose distributions. J Appl Clin Med Phys 15(2):4662CrossRefPubMed Ojala JJ, Kapanen MK, Hyödynmaa SJ, Wigren TK, Pitkänen MA (2014) Performance of dose calculation algorithms from three generations in lung SBRT: comparison with full Monte Carlo-based dose distributions. J Appl Clin Med Phys 15(2):4662CrossRefPubMed
38.
go back to reference Covington EL, Ritter TA, Moran JM, Owrangi AM, Prisciandaro JI (2016) Technical Report: Evaluation of peripheral dose for flattening filter free photon beams. Med Phys 43(8):4789CrossRefPubMedPubMedCentral Covington EL, Ritter TA, Moran JM, Owrangi AM, Prisciandaro JI (2016) Technical Report: Evaluation of peripheral dose for flattening filter free photon beams. Med Phys 43(8):4789CrossRefPubMedPubMedCentral
39.
go back to reference Ślosarek K, Osewski W, Grządziel A et al (2015) Integral dose: comparison between four techniques for prostate radiotherapy. Rep Pract Oncol Radiother 20(2):99–103CrossRefPubMed Ślosarek K, Osewski W, Grządziel A et al (2015) Integral dose: comparison between four techniques for prostate radiotherapy. Rep Pract Oncol Radiother 20(2):99–103CrossRefPubMed
40.
go back to reference Kondrack RM, Harbertson J, Tan JT, McBreen ME, Surh CD, Bradley LM (2003) Interleukin 7 regulates the survival and generation of memory CD4 cells. J Exp Med 198(12):1797–1806CrossRefPubMedPubMedCentral Kondrack RM, Harbertson J, Tan JT, McBreen ME, Surh CD, Bradley LM (2003) Interleukin 7 regulates the survival and generation of memory CD4 cells. J Exp Med 198(12):1797–1806CrossRefPubMedPubMedCentral
41.
go back to reference Lee Y, Auh SL, Wang Y, Burnette B, Wang Y, Meng Y, Beckett M, Sharma R, Chin R, Tu T, Weichselbaum RR, Fu YX (2009) Therapeutic effects of ablative radiation on local tumor require CD8+ T cells: changing strategies for cancer treatment. Blood 114(3):589–595CrossRefPubMedPubMedCentral Lee Y, Auh SL, Wang Y, Burnette B, Wang Y, Meng Y, Beckett M, Sharma R, Chin R, Tu T, Weichselbaum RR, Fu YX (2009) Therapeutic effects of ablative radiation on local tumor require CD8+ T cells: changing strategies for cancer treatment. Blood 114(3):589–595CrossRefPubMedPubMedCentral
Metadata
Title
Association between treatment-related lymphopenia and survival in glioblastoma patients following postoperative chemoradiotherapy
Authors
Roberto Mapelli
Chiara Julita
Sofia Paola Bianchi
Nicolò Gallina, MD
Raffaella Lucchini, MD
Martina Midulla, MD
Flavia Puci, MD
Jessica Saddi, MD
Sara Trivellato, PhD
Denis Panizza, PhD
Elena De Ponti, PhD
Stefano Arcangeli, MD
Publication date
01-05-2022
Publisher
Springer Berlin Heidelberg
Published in
Strahlentherapie und Onkologie / Issue 5/2022
Print ISSN: 0179-7158
Electronic ISSN: 1439-099X
DOI
https://doi.org/10.1007/s00066-021-01855-5

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