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May 17, 2022; 98 (20) Research Article

Sex-Dependent Analysis of Temozolomide-Induced Myelosuppression and Effects on Survival in a Large Real-life Cohort of Patients With Glioma

View ORCID ProfilePia S. Zeiner, View ORCID ProfileKatharina Filipski, Natalie Filmann, Marie-Thérèse Forster, Martin Voss, Emmanouil Fokas, Ulrich Herrlinger, View ORCID ProfilePatrick N. Harter, Joachim P. Steinbach, View ORCID ProfileMichael W. Ronellenfitsch
First published March 29, 2022, DOI: https://doi.org/10.1212/WNL.0000000000200254
Pia S. Zeiner
From the Dr. Senckenberg Institute of Neurooncology (P.S.Z., M.V., J.P.S., M.W.R.), University Cancer Center (UCT) Frankfurt (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Frankfurt Cancer Institute (FCI) (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Institute of Neurology (Edinger-Institute) (K.F., P.N.H.), Institute of Biostatistics and Mathematical Modeling (N.F.), Department of Neurosurgery (M.-T.F.), and Department of Radiotherapy and Oncology (E.F.), University Hospital Frankfurt, Goethe University; German Cancer Consortium (DKTK) (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Frankfurt am Main; and Division of Clinical Neurooncology, Department of Neurology and Centre of Integrated Oncology (U.H.), University Hospital Bonn, Germany.
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Katharina Filipski
From the Dr. Senckenberg Institute of Neurooncology (P.S.Z., M.V., J.P.S., M.W.R.), University Cancer Center (UCT) Frankfurt (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Frankfurt Cancer Institute (FCI) (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Institute of Neurology (Edinger-Institute) (K.F., P.N.H.), Institute of Biostatistics and Mathematical Modeling (N.F.), Department of Neurosurgery (M.-T.F.), and Department of Radiotherapy and Oncology (E.F.), University Hospital Frankfurt, Goethe University; German Cancer Consortium (DKTK) (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Frankfurt am Main; and Division of Clinical Neurooncology, Department of Neurology and Centre of Integrated Oncology (U.H.), University Hospital Bonn, Germany.
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Natalie Filmann
From the Dr. Senckenberg Institute of Neurooncology (P.S.Z., M.V., J.P.S., M.W.R.), University Cancer Center (UCT) Frankfurt (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Frankfurt Cancer Institute (FCI) (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Institute of Neurology (Edinger-Institute) (K.F., P.N.H.), Institute of Biostatistics and Mathematical Modeling (N.F.), Department of Neurosurgery (M.-T.F.), and Department of Radiotherapy and Oncology (E.F.), University Hospital Frankfurt, Goethe University; German Cancer Consortium (DKTK) (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Frankfurt am Main; and Division of Clinical Neurooncology, Department of Neurology and Centre of Integrated Oncology (U.H.), University Hospital Bonn, Germany.
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Marie-Thérèse Forster
From the Dr. Senckenberg Institute of Neurooncology (P.S.Z., M.V., J.P.S., M.W.R.), University Cancer Center (UCT) Frankfurt (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Frankfurt Cancer Institute (FCI) (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Institute of Neurology (Edinger-Institute) (K.F., P.N.H.), Institute of Biostatistics and Mathematical Modeling (N.F.), Department of Neurosurgery (M.-T.F.), and Department of Radiotherapy and Oncology (E.F.), University Hospital Frankfurt, Goethe University; German Cancer Consortium (DKTK) (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Frankfurt am Main; and Division of Clinical Neurooncology, Department of Neurology and Centre of Integrated Oncology (U.H.), University Hospital Bonn, Germany.
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Martin Voss
From the Dr. Senckenberg Institute of Neurooncology (P.S.Z., M.V., J.P.S., M.W.R.), University Cancer Center (UCT) Frankfurt (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Frankfurt Cancer Institute (FCI) (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Institute of Neurology (Edinger-Institute) (K.F., P.N.H.), Institute of Biostatistics and Mathematical Modeling (N.F.), Department of Neurosurgery (M.-T.F.), and Department of Radiotherapy and Oncology (E.F.), University Hospital Frankfurt, Goethe University; German Cancer Consortium (DKTK) (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Frankfurt am Main; and Division of Clinical Neurooncology, Department of Neurology and Centre of Integrated Oncology (U.H.), University Hospital Bonn, Germany.
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Emmanouil Fokas
From the Dr. Senckenberg Institute of Neurooncology (P.S.Z., M.V., J.P.S., M.W.R.), University Cancer Center (UCT) Frankfurt (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Frankfurt Cancer Institute (FCI) (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Institute of Neurology (Edinger-Institute) (K.F., P.N.H.), Institute of Biostatistics and Mathematical Modeling (N.F.), Department of Neurosurgery (M.-T.F.), and Department of Radiotherapy and Oncology (E.F.), University Hospital Frankfurt, Goethe University; German Cancer Consortium (DKTK) (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Frankfurt am Main; and Division of Clinical Neurooncology, Department of Neurology and Centre of Integrated Oncology (U.H.), University Hospital Bonn, Germany.
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Ulrich Herrlinger
From the Dr. Senckenberg Institute of Neurooncology (P.S.Z., M.V., J.P.S., M.W.R.), University Cancer Center (UCT) Frankfurt (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Frankfurt Cancer Institute (FCI) (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Institute of Neurology (Edinger-Institute) (K.F., P.N.H.), Institute of Biostatistics and Mathematical Modeling (N.F.), Department of Neurosurgery (M.-T.F.), and Department of Radiotherapy and Oncology (E.F.), University Hospital Frankfurt, Goethe University; German Cancer Consortium (DKTK) (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Frankfurt am Main; and Division of Clinical Neurooncology, Department of Neurology and Centre of Integrated Oncology (U.H.), University Hospital Bonn, Germany.
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Patrick N. Harter
From the Dr. Senckenberg Institute of Neurooncology (P.S.Z., M.V., J.P.S., M.W.R.), University Cancer Center (UCT) Frankfurt (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Frankfurt Cancer Institute (FCI) (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Institute of Neurology (Edinger-Institute) (K.F., P.N.H.), Institute of Biostatistics and Mathematical Modeling (N.F.), Department of Neurosurgery (M.-T.F.), and Department of Radiotherapy and Oncology (E.F.), University Hospital Frankfurt, Goethe University; German Cancer Consortium (DKTK) (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Frankfurt am Main; and Division of Clinical Neurooncology, Department of Neurology and Centre of Integrated Oncology (U.H.), University Hospital Bonn, Germany.
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Joachim P. Steinbach
From the Dr. Senckenberg Institute of Neurooncology (P.S.Z., M.V., J.P.S., M.W.R.), University Cancer Center (UCT) Frankfurt (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Frankfurt Cancer Institute (FCI) (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Institute of Neurology (Edinger-Institute) (K.F., P.N.H.), Institute of Biostatistics and Mathematical Modeling (N.F.), Department of Neurosurgery (M.-T.F.), and Department of Radiotherapy and Oncology (E.F.), University Hospital Frankfurt, Goethe University; German Cancer Consortium (DKTK) (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Frankfurt am Main; and Division of Clinical Neurooncology, Department of Neurology and Centre of Integrated Oncology (U.H.), University Hospital Bonn, Germany.
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Michael W. Ronellenfitsch
From the Dr. Senckenberg Institute of Neurooncology (P.S.Z., M.V., J.P.S., M.W.R.), University Cancer Center (UCT) Frankfurt (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Frankfurt Cancer Institute (FCI) (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Institute of Neurology (Edinger-Institute) (K.F., P.N.H.), Institute of Biostatistics and Mathematical Modeling (N.F.), Department of Neurosurgery (M.-T.F.), and Department of Radiotherapy and Oncology (E.F.), University Hospital Frankfurt, Goethe University; German Cancer Consortium (DKTK) (P.S.Z., K.F., M.V., E.F., P.N.H., J.P.S., M.W.R.), Frankfurt am Main; and Division of Clinical Neurooncology, Department of Neurology and Centre of Integrated Oncology (U.H.), University Hospital Bonn, Germany.
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Sex-Dependent Analysis of Temozolomide-Induced Myelosuppression and Effects on Survival in a Large Real-life Cohort of Patients With Glioma
Pia S. Zeiner, Katharina Filipski, Natalie Filmann, Marie-Thérèse Forster, Martin Voss, Emmanouil Fokas, Ulrich Herrlinger, Patrick N. Harter, Joachim P. Steinbach, Michael W. Ronellenfitsch
Neurology May 2022, 98 (20) e2073-e2083; DOI: 10.1212/WNL.0000000000200254

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Abstract

Background and Objective To investigate the association of radiochemotherapy-induced cytopenia with sex and its potential effect on survival in patients with glioma.

Methods We retrospectively analyzed cytopenia during temozolomide-based concomitant radiochemotherapy in 492 patients with glioma. Histologic grading, molecular pathology, surgical procedures, adjuvant chemotherapy subsequent to the radiochemotherapy phase, and overall survival (OS) were recorded. The extent of cytopenia was correlated with sex and outcome.

Results Treatment-induced severe cytopenia (leukocytopenia, lymphocytopenia, neutropenia, and thrombocytopenia) was more frequent in women than men (44 vs 18%; p = 0.0002). In women with IDH-wt high-grade astrocytomas, there was a negative correlation of severe cytopenia in general and thrombocytopenia in particular during temozolomide radiochemotherapy with OS independent from other predictors (92 [77–111] vs 73 [21–127] weeks; p < 0.05). In men, there was also a trend for this unfavorable effect. In addition, severe cytopenia in all blood cell lineages correlated with reduced temozolomide dose exposure during radiochemotherapy (all p < 0.05 in the total cohort) and reduced dose exposure was independently associated with worse OS (hazard ratios for OS in complete vs reduced temozolomide dose in the total and female cohort 0.66 [0.47–0.92] and 0.4 [0.24–0.69], p < 0.05).

Discussion Our analysis of treatment-induced cytopenia in a large cohort of patients with glioma confirms that women are at higher risk and demonstrates an association of cytopenia with shortened survival in women.

Classification of Evidence This study provides Class II evidence that women with glioma treated with temozolomide-based concomitant radiochemotherapy have more frequent treatment-induced severe cytopenia than men and that severe myelosuppression correlates with worse OS in women.

Glossary

BMI=
body mass index;
CTCAE=
Common Terminology Criteria for Adverse Events;
IDH=
isocitrate dehydrogenase;
LBM=
lean body mass;
MGMT=
O6-methylguanine methyltransferase;
OS=
overall survival;
TMZ-RCT=
temozolomide radiochemotherapy

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Class of Evidence: NPub.org/coe

  • Received August 11, 2021.
  • Accepted in final form February 4, 2022.
  • © 2022 American Academy of Neurology
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