Advertisement

Digital biomarkers: Importance of patient stratification for re-irradiation of glioma patients – Review of latest developments regarding scoring assessment

  • Kerstin A. Kessel
    Correspondence
    Corresponding author at: Department of Radiation Oncology, Klinikum rechts der Isar, Technical University Munich (TUM), Ismaninger Straße 22, 81675 Munich, Germany.
    Affiliations
    Department of Radiation Oncology, Technical University of Munich (TUM), Ismaninger Straße 22, Munich, Germany

    Institute for Radiation Medicine (IRM), Helmholtz Zentrum München, Ingolstädter Landstraße 1, Neuherberg, Germany

    Deutsches Konsortium für Translationale Krebsforschung (DKTK), DKTK Partner Site Munich, Germany
    Search for articles by this author
  • Stephanie E. Combs
    Affiliations
    Department of Radiation Oncology, Technical University of Munich (TUM), Ismaninger Straße 22, Munich, Germany

    Institute for Radiation Medicine (IRM), Helmholtz Zentrum München, Ingolstädter Landstraße 1, Neuherberg, Germany

    Deutsches Konsortium für Translationale Krebsforschung (DKTK), DKTK Partner Site Munich, Germany
    Search for articles by this author
Published:October 14, 2019DOI:https://doi.org/10.1016/j.ejmp.2019.10.021

      Highlights

      • Several scores have been developed to predict outcome in recurrent HGG.
      • Reirradiation gains more relevance, due to precise techniques and experience.
      • Due to heterogeneity of data at re-irradiation, patient stratification is important.

      Abstract

      Purpose

      To review scoring assessments in re-irradiation of high-grade glioma (HGG) patients and how to use scoring for patient stratification. The next aim was to investigate the different approaches employed by the scoring systems and the way they can be applied to build homogeneous patient groups for a reliable prognosis.

      Methods

      We searched the Medline/Pubmed and Web of science databases for relevant articles regarding scores for re-irradiation of recurrent HGG. All references were divided into the following groups: novel score establishment (n = 5), score validation (n = 6), not relevant to this evaluation (n = 26).

      Results

      We identified five scoring systems. Two are modifications of an already existing score. Calculations differ immensely from easy point addition to a more complex formula with including three up to 10 individual parameters. Six validation articles were found for three of the scores; one was validated four times. Two scores were never validated.

      Conclusion

      For recurrent HGG, the clinical situation remains demanding. Due to the heterogeneity of data at re-irradiation, patient stratification is important. Several scoring systems have been developed to predict prognosis. As a digital biomarker, scores are of high value regarding quick patient assessment and therapy decision making. For the next generation of digital biomarkers, easy calculation, and inclusion of easily available parameters are crucial.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Physica Medica: European Journal of Medical Physics
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Sperduto P.W.
        • Chao S.T.
        • Sneed P.K.
        • Luo X.
        • Suh J.
        • Roberge D.
        • et al.
        Diagnosis-specific prognostic factors, indexes, and treatment outcomes for patients with newly diagnosed brain metastases: a multi-institutional analysis of 4,259 patients.
        Int J Radiat Oncol Biol Phys. 2010; 77: 655-661
        • Nieder C.
        • Mehta M.P.
        Prognostic indices for brain metastases-usefulness and challenges.
        Radiat Oncol. 2009; 4: 10
        • Brockman J.A.
        • Alanee S.
        • Vickers A.J.
        • Scardino P.T.
        • Wood D.P.
        • Kibel A.S.
        • et al.
        Nomogram predicting prostate cancer-specific mortality for men with biochemical recurrence after radical prostatectomy.
        Eur Urol. 2015; 67: 1160-1167
        • Combs S.E.
        • Edler L.
        • Rausch R.
        • Welzel T.
        • Wick W.
        • Debus J.
        Generation and validation of a prognostic score to predict outcome after re-irradiation of recurrent glioma.
        Acta Oncol. 2013; 52: 147-152
        • Muller K.
        • Henke G.
        • Pietschmann S.
        • van Gool S.
        • De Vleeschouwer S.
        • von Bueren A.O.
        • et al.
        Re-irradiation or re-operation followed by dendritic cell vaccination? Comparison of two different salvage strategies for relapsed high-grade gliomas by means of a new prognostic model.
        J Neurooncol. 2015; 124: 325-332
        • Krauze A.V.
        • Peters C.
        • Cheng J.
        • Ning H.
        • Mackey M.
        • Rowe L.
        • et al.
        Re-irradiation for recurrent glioma- the NCI experience in tumor control, OAR toxicity and proposal of a novel prognostic scoring system.
        Radiat Oncol. 2017; 12: 191
        • Kessel K.A.
        • Hesse J.
        • Straube C.
        • Zimmer C.
        • Schmidt-Graf F.
        • Schlegel J.
        • et al.
        Modification and optimization of an established prognostic score after re-irradiation of recurrent glioma.
        PLoS ONE. 2017; 12e0180457
        • Niyazi M.
        • Adeberg S.
        • Kaul D.
        • Boulesteix A.L.
        • Bougatf N.
        • Fleischmann D.F.
        • et al.
        Independent validation of a new reirradiation risk score (RRRS) for glioma patients predicting post-recurrence survival: a multicenter DKTK/ROG analysis.
        Radiother Oncol. 2018; 127: 121-127
        • Park J.K.
        • Hodges T.
        • Arko L.
        • Shen M.
        • Dello Iacono D.
        • McNabb A.
        • et al.
        Scale to predict survival after surgery for recurrent glioblastoma multiforme.
        J Clin Oncol. 2010; 28: 3838-3843
        • Peeken J.C.
        • Goldberg T.
        • Pyka T.
        • Bernhofer M.
        • Wiestler B.
        • Kessel K.A.
        • et al.
        Combining multimodal imaging and treatment features improves machine learning-based prognostic assessment in patients with glioblastoma multiforme.
        Cancer Med. 2019; 8: 128-136
        • Peeken J.C.
        • Molina-Romero M.
        • Diehl C.
        • Menze B.H.
        • Straube C.
        • Meyer B.
        • et al.
        Deep learning derived tumor infiltration maps for personalized target definition in Glioblastoma radiotherapy.
        Radiother Oncol. 2019; 138: 166-172
        • Peeken J.C.
        • Nusslin F.
        • Combs S.E.
        “Radio-oncomics”: the potential of radiomics in radiation oncology.
        Strahlenther Onkol. 2017; 193: 767-779
        • Straube C.
        • Kessel K.A.
        • Zimmer C.
        • Schmidt-Graf F.
        • Schlegel J.
        • Gempt J.
        • et al.
        A second course of radiotherapy in patients with recurrent malignant gliomas: clinical data on re-irradiation, prognostic factors, and usefulness of digital biomarkers.
        Curr Treat Options Oncol. 2019; 20: 71
        • Kazmi F.
        • Soon Y.Y.
        • Leong Y.H.
        • Koh W.Y.
        • Vellayappan B.
        Re-irradiation for recurrent glioblastoma (GBM): a systematic review and meta-analysis.
        J Neurooncol. 2019; 142: 79-90
        • Weller M.
        • Cloughesy T.
        • Perry J.R.
        • Wick W.
        Standards of care for treatment of recurrent glioblastoma-are we there yet?.
        Neuro Oncol. 2013; 15: 4-27
        • Combs S.E.
        • Thilmann C.
        • Edler L.
        • Debus J.
        • Schulz-Ertner D.
        Efficacy of fractionated stereotactic reirradiation in recurrent gliomas: long-term results in 172 patients treated in a single institution.
        J Clin Oncol. 2005; 23: 8863-8869
        • Combs S.E.
        • Niyazi M.
        • Adeberg S.
        • Bougatf N.
        • Kaul D.
        • Fleischmann D.F.
        • et al.
        Re-irradiation of recurrent gliomas: pooled analysis and validation of an established prognostic score-report of the Radiation Oncology Group (ROG) of the German Cancer Consortium (DKTK).
        Cancer Med. 2018; 7: 1742-1749
        • Ringel F.
        • Pape H.
        • Sabel M.
        • Krex D.
        • Bock H.C.
        • Misch M.
        • et al.
        Clinical benefit from resection of recurrent glioblastomas: results of a multicenter study including 503 patients with recurrent glioblastomas undergoing surgical resection.
        Neuro Oncol. 2016; 18: 96-104
        • Straube C.
        • Schmidt-Graf F.
        • Wiestler B.
        • Zimmer C.
        • Meyer B.
        • Combs S.E.
        The algorithms of adjuvant therapy in gliomas and their effect on survival.
        J Neurosurg Sci. 2019; 63: 179-186
        • Combs S.E.
        • Kessel K.A.
        • Hesse J.
        • Straube C.
        • Zimmer C.
        • Schmidt-Graf F.
        • et al.
        Moving second courses of radiotherapy forward: early re-irradiation after surgical resection for recurrent gliomas improves efficacy with excellent tolerability.
        Neurosurgery. 2018; 83: 1241-1248
        • Straube C.
        • Scherb H.
        • Gempt J.
        • Kirschke J.
        • Zimmer C.
        • Schmidt-Graf F.
        • et al.
        Adjuvant stereotactic fractionated radiotherapy to the resection cavity in recurrent glioblastoma – the GlioCave study (NOA 17 – ARO 2016/3 – DKTK ROG trial).
        BMC Cancer. 2018; 18: 15
        • Wick W.
        • Fricke H.
        • Junge K.
        • Kobyakov G.
        • Martens T.
        • Heese O.
        • et al.
        A phase II, randomized, study of weekly APG101+reirradiation versus reirradiation in progressive glioblastoma.
        Clin Cancer Res. 2014; 20: 6304-6313
        • Minniti G.
        • Scaringi C.
        • De Sanctis V.
        • Lanzetta G.
        • Falco T.
        • Di Stefano D.
        • et al.
        Hypofractionated stereotactic radiotherapy and continuous low-dose temozolomide in patients with recurrent or progressive malignant gliomas.
        J Neurooncol. 2013; 111: 187-194
        • Lacroix M.
        • Abi-Said D.
        • Fourney D.R.
        • Gokaslan Z.L.
        • Shi W.
        • DeMonte F.
        • et al.
        A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival.
        J Neurosurg. 2001; 95: 190-198
        • Fogh S.E.
        • Andrews D.W.
        • Glass J.
        • Curran W.
        • Glass C.
        • Champ C.
        • et al.
        Hypofractionated stereotactic radiation therapy: an effective therapy for recurrent high-grade gliomas.
        J Clin Oncol. 2010; 28: 3048-3053
        • Lee J.
        • Cho J.
        • Chang J.H.
        • Suh C.O.
        Re-irradiation for recurrent gliomas: treatment outcomes and prognostic factors.
        Yonsei Med J. 2016; 57: 824-830
        • Navarria P.
        • Minniti G.
        • Clerici E.
        • Tomatis S.
        • Pinzi V.
        • Ciammella P.
        • Galaverni M.
        • Amelio D.
        • Scartoni D.
        • Scoccianti S.
        • et al.
        Re-irradiation for recurrent glioma: outcome evaluation, toxicity and prognostic factors assessment. A multicenter study of the Radiation Oncology Italian Association (AIRO).
        J Neurooncol. 2019; 142: 59-67
        • Arvold N.D.
        • Shi D.D.
        • Aizer A.A.
        • Norden A.D.
        • Reardon D.A.
        • Lee E.Q.
        • et al.
        Salvage re-irradiation for recurrent high-grade glioma and comparison to bevacizumab alone.
        J Neurooncol. 2017; 135: 581-591
        • Azoulay M.
        • Santos F.
        • Shenouda G.
        • Petrecca K.
        • Oweida A.
        • Guiot M.C.
        • et al.
        Benefit of re-operation and salvage therapies for recurrent glioblastoma multiforme: results from a single institution.
        J Neurooncol. 2017; 132: 419-426
        • Bir S.C.
        • Connor Jr., D.E.
        • Ambekar S.
        • Wilden J.A.
        • Nanda A.
        Factors predictive of improved overall survival following stereotactic radiosurgery for recurrent glioblastoma.
        Neurosurg Rev. 2015; 38: 705-713
        • Palmer J.D.
        • Siglin J.
        • Yamoah K.
        • Dan T.
        • Champ C.E.
        • Bar-Ad V.
        • et al.
        Re-resection for recurrent high-grade glioma in the setting of re-irradiation: more is not always better.
        J Neurooncol. 2015; 124: 215-221
        • Scholtyssek F.
        • Zwiener I.
        • Schlamann A.
        • Seidel C.
        • Meixensberger J.
        • Bauer M.
        • et al.
        Reirradiation in progressive high-grade gliomas: outcome, role of concurrent chemotherapy, prognostic factors and validation of a new prognostic score with an independent patient cohort.
        Radiat Oncol. 2013; 8: 161
        • Shi W.
        • Blomain E.S.
        • Siglin J.
        • Palmer J.D.
        • Dan T.
        • Wang Y.
        • et al.
        Salvage fractionated stereotactic re-irradiation (FSRT) for patients with recurrent high grade gliomas progressed after bevacizumab treatment.
        J Neurooncol. 2018; 137: 171-177
        • van Linde M.E.
        • Brahm C.G.
        • de Witt Hamer P.C.
        • Reijneveld J.C.
        • Bruynzeel A.M.E.
        • Vandertop W.P.
        • et al.
        Treatment outcome of patients with recurrent glioblastoma multiforme: a retrospective multicenter analysis.
        J Neurooncol. 2017; 135: 183-192
        • De Vleeschouwer S.
        • Ardon H.
        • Van Calenbergh F.
        • Sciot R.
        • Wilms G.
        • van Loon J.
        • et al.
        Stratification according to HGG-IMMUNO RPA model predicts outcome in a large group of patients with relapsed malignant glioma treated by adjuvant postoperative dendritic cell vaccination.
        Cancer Immunol Immunother. 2012; 61: 2105-2112
        • Post C.C.B.
        • Kramer M.C.A.
        • Smid E.J.
        • van der Weide H.L.
        • Kleynen C.E.
        • Heesters M.
        • et al.
        Patterns of re-irradiation for recurrent gliomas and validation of a prognostic score.
        Radiother Oncol. 2019; 130: 156-163
        • Kessel K.A.
        • Hesse J.
        • Straube C.
        • Zimmer C.
        • Schmidt-Graf F.
        • Schlegel J.
        • et al.
        Validation of an established prognostic score after re-irradiation of recurrent glioma.
        Acta Oncol. 2017; 56: 422-426
        • Muller K.
        • Henke G.
        • Compter I.
        • von Bueren A.O.
        • Friedrich C.
        • Janssens G.
        • et al.
        External validation of a prognostic model estimating the survival of patients with recurrent high-grade gliomas after reirradiation.
        Pract Radiat Oncol. 2015; 5: e143-e150
        • Niyazi M.
        • Flieger M.
        • Ganswindt U.
        • Combs S.E.
        • Belka C.
        Validation of the prognostic Heidelberg re-irradiation score in an independent mono-institutional patient cohort.
        Radiat Oncol. 2014; 9: 128
        • Emami B.
        • Lyman J.
        • Brown A.
        • Coia L.
        • Goitein M.
        • Munzenrider J.E.
        • et al.
        Tolerance of normal tissue to therapeutic irradiation.
        Int J Radiat Oncol Biol Phys. 1991; 21: 109-122
        • Bauman G.S.
        • Sneed P.K.
        • Wara W.M.
        • Stalpers L.J.
        • Chang S.M.
        • McDermott M.W.
        • et al.
        Reirradiation of primary CNS tumors.
        Int J Radiat Oncol Biol Phys. 1996; 36: 433-441
        • Combs S.E.
        • Widmer V.
        • Thilmann C.
        • Hof H.
        • Debus J.
        • Schulz-Ertner D.
        Stereotactic radiosurgery (SRS): treatment option for recurrent glioblastoma multiforme (GBM).
        Cancer. 2005; 104: 2168-2173
        • Combs S.E.
        • Debus J.
        • Schulz-Ertner D.
        Radiotherapeutic alternatives for previously irradiated recurrent gliomas.
        BMC Cancer. 2007; 7: 167
        • Moller S.
        • Law I.
        • Munck A.F.
        • Rosenschold P.
        • Costa J.
        • Poulsen H.S.
        • et al.
        Prognostic value of (18)F-FET PET imaging in re-irradiation of high-grade glioma: Results of a phase I clinical trial.
        Radiother Oncol. 2016; 121: 132-137