Abstract
Purpose
To identify the preoperative nonmedical predictors of functional impairment after brain tumor surgery.
Methods
Patients were evaluated before brain tumor surgery and after 3 months. The cognitive evaluation included MOCA for the general cognitive status, TMT for attention and executive functions, ROWL-IR and ROWL-DR for memory, and the F-A-S for verbal fluency. Anxiety, depression, social support, resilience, personality, disability, and quality of life were evaluated with the following patient-reported outcome measures (PROMs): HADS, OSS-3, RS-14, TIPI, WHODAS-12, and EORTC-QLQ C30. Functional status was measured with KPS. Regression analyses were performed to identify preoperative nonmedical predictors of functional impairment; PROMs and cognitive tests were compared with the normative values.
Results
A total of 149 patients were enrolled (64 glioma; 85 meningioma). Increasing age, lower education, higher disability, and lower ROWL-DR scores were predictors of functional impairment in glioma patients while higher TMT scores and disability were predictors in meningioma patients. In multiple regression, only a worse performance in TMT remains a predictor in meningioma patients. Cognitive tests were not significantly worse than normative values, while psychosocial functioning was impaired.
Conclusion
TMT could be used in the preoperative evaluation and as a potential predictor in the research field on outcome predictors. Psychosocial functioning should be studied further and considered in a clinical context to identify who need major support and to plan tailored interventions.
Similar content being viewed by others
Data availability
The data that support the findings of this study are available from the corresponding author, SS, upon reasonable request.
References
Marcus HJ, Williams S, Hughes-Hallett A, Camp SJ, Nandi D, Thorne L (2017) Predicting surgical outcome in patients with glioblastoma multiforme using pre-operative magnetic resonance imaging: development and preliminary validation of a grading system. Neurosurg Rev 40(4):621–631. https://doi.org/10.1007/s10143-017-0817-0
Cinotti R, Bruder N, Srairi M et al (2018) Prediction score for postoperative neurologic complications after brain tumor craniotomy: a multicenter observational study. Anesthesiology 129(6):1111–1120. https://doi.org/10.1097/ALN.0000000000002426
Aman RA, Wisyesa K, Nugroho AW et al (2020) Pre-and post-surgical health-related quality of life evaluation of spheno-orbital meningioma patients based on eortc qlq-c30 questionnaire at Dr. Cipto mangunkusumo general hospital. Acta Neurol Taiwan 29(4):99–103
Kim CW, Joo JD, Kim YH, Han JH, Kim CY (2016) Health-related quality of life in brain tumor patients treated with surgery: preliminary result of a single institution. Brain Tumor Res Treat 4(2):87–93. https://doi.org/10.14791/btrt.2016.4.2.87
Teng KX, Price B, Joshi S et al (2021) Life after surgical resection of a low-grade glioma: a prospective cross-sectional study evaluating health-related quality of life. J Clin Neurosci 88:259–267. https://doi.org/10.1016/j.jocn.2021.03.038
Davis FG, McCarthy BJ, Freels S, Kupelian V, Bondy ML (1999) The conditional probability of survival of patients with primary malignant brain tumors: surveillance, epidemiology, and end results (SEER) data. Cancer 85(2):485–491. https://doi.org/10.1002/(SICI)1097-0142(19990115)85:2%3c485::AID-CNCR29%3e3.0.CO;2-L
Senders JT, Staples PC, Karhade AV et al (2018) Machine learning and neurosurgical outcome prediction: a systematic review. World Neurosurg 109:476-486.e1. https://doi.org/10.1016/j.wneu.2017.09.149
Ferroli P, Broggi M, Schiavolin S et al (2015) Predicting functional impairment in brain tumor surgery: The Big Five and the Milan Complexity Scale. Neurosurg Focus 39(6):E14. https://doi.org/10.3171/2015.9.FOCUS15339
Staartjes VE, Broggi M, Zattra CM et al (2021) Development and external validation of a clinical prediction model for functional impairment after intracranial tumor surgery. J Neurosurg 134(6):1743–1750. https://doi.org/10.3171/2020.4.JNS20643
Schiavolin S, Raggi A, Scaratti C et al (2021) Outcome prediction in brain tumor surgery: a literature review on the influence of nonmedical factors. Neurosurg Rev 44(2):807–819. https://doi.org/10.1007/s10143-020-01289-0
Tsay S-L, Chang J-Y, Yates P, Lin K-C, Liang S-Y (2012) Factors influencing quality of life in patients with benign primary brain tumors: prior to and following surgery. Support Care Cancer 20(1):57–64. https://doi.org/10.1007/s00520-010-1053-0
Bunevicius A, Tamasauskas S, Deltuva V, Tamasauskas A, Radziunas A, Bunevicius R (2014) Predictors of health-related quality of life in neurosurgical brain tumor patients: focus on patient-centered perspective. Acta Neurochir (Wien) 156(2):367–374. https://doi.org/10.1007/s00701-013-1930-7
Budrukkar A, Jalali R, Dutta D et al (2009) Prospective assessment of quality of life in adult patients with primary brain tumors in routine neurooncology practice. J Neurooncol 95(3):413–419. https://doi.org/10.1007/s11060-009-9939-8
Recinos PF, Dunphy CJ, Thompson N, Schuschu J, Urchek JL, Katzan IL (2017) Patient satisfaction with collection of patient-reported outcome measures in routine care. Adv Ther 34(2):452–465. https://doi.org/10.1007/s12325-016-0463-x
Papagno C, Casarotti A, Comi A, Gallucci M, Riva M, Bello L (2012) Measuring clinical outcomes in neuro-oncology. A battery to evaluate low-grade gliomas (LGG). J. Neurooncol 108(2):269–275. https://doi.org/10.1007/s11060-012-0824-5
Lageman SK, Cerhan JH, Locke DEC, Anderson SK, Wu W, Brown PD (2010) Comparing neuropsychological tasks to optimize brief cognitive batteries for brain tumor clinical trials. J Neurooncol 96(2):271–276. https://doi.org/10.1007/s11060-009-9960-y
Rofes A, Mandonnet E, Godden J et al (2017) Survey on current cognitive practices within the European Low-Grade Glioma Network: towards a European assessment protocol. Acta Neurochir (Wien) 159(7):1167–1178. https://doi.org/10.1007/s00701-017-3192-2
Costantini M, Musso M, Viterbori P et al (1999) Detecting psychological distress in cancer patients: validity of the Italian version of the Hospital Anxiety and Depression Scale. Support Care Cancer 7(3):121–127. https://doi.org/10.1007/s005200050241
Iani L, Lauriola M, Costantini M (2014) A confirmatory bifactor analysis of the hospital anxiety and depression scale in an Italian community sample. Health Qual Life Outcomes 12(1):1–8. https://doi.org/10.1186/1477-7525-12-84
Meltzer H (2003) Development of a common instrument for mental health. In A. Nosikov C. Gudex (Eds) EUROHIS: Developing Common Instruments for Health Surveys. IOS press, Amsterdam, pp 35–60
Callegari C, Bertù L, Lucano M, Ielmini M, Braggio E, Vender S (2016) Reliability and validity of the Italian version of the 14-item resilience scale. Psychol Res Behav Manag 9:277–284. https://doi.org/10.2147/PRBM.S115657
Chiorri C, Bracco F, Piccinno T, Modafferi C, Battini V (2015) Psychometric properties of a revised version of the ten item personality inventory. Eur J Psychol Assess 31(2):109–119. https://doi.org/10.1027/1015-5759/a000215
http://who.int/whodas. Accessed 26 Aug 2021
Andrews G, Kemp A, Sunderland M, von Korff M, Ustun TB (2009) Normative data for the 12 item WHO disability assessment schedule 2.0. PLoS One 4(12):1–6. https://doi.org/10.1371/journal.pone.0008343
Aaronson NK, Ahmedzai S, Bergman B et al (1993) The European organization for research and treatment of cancer QLQ-C30: a quality-of-life instrument for use in international clinical trials in oncology. J Natl Cancer Inst 85(5):365–376. https://doi.org/10.1093/jnci/85.5.365
Scott NW, Fayers PM, Aaronson NK, Bottomley A, de Graeff A, Groenvold M, Gundy C, Koller M, Petersen MA, Sprangers MAG, EORTC Quality of Life Group (2008) EORTC QLQ-C30 Reference Values Manual. EORTC Quality of Life Group, Belgium
Taphoorn MJB, Claassens L, Aaronson NK et al (2010) An international validation study of the EORTC brain cancer module (EORTC QLQ-BN20) for assessing health-related quality of life and symptoms in brain cancer patients. Eur J Cancer 46(6):1033–1040. https://doi.org/10.1016/j.ejca.2010.01.012
Santangelo G, Siciliano M, Pedone R et al (2015) Normative data for the Montreal Cognitive Assessment in an Italian population sample. Neurol Sci 36(4):585–591. https://doi.org/10.1007/s10072-014-1995-y
Giovagnoli AR, Del Pesce M, Mascheroni S, Simoncelli M, Laiacona M, Capitani E (1996) Trail Making Test: normative values from 287 normal adult controls. Ital J Neurol Sci 17(4):305–309. https://doi.org/10.1007/BF01997792
Carlesimo GA, Caltagirone C, Gainotti G et al (1996) The mental deterioration battery: normative data, diagnostic reliability and qualitative analyses of cognitive impairment. Eur Neurol 36(6):378–384. https://doi.org/10.1159/000117297
Novelli G, Papagno C, Capitani E, Laiacona M, Vallar G, Cappa SF (1986) Tre test clinici di ricerca e produzione lessicale. Taratura su soggetti normali. Arch. di Psicol. Neurol. e Psichiatr 4(47):477–506
Karnofsky DA, Burchenal JH (1949) The clinical evaluation of chemotherapeutic agents in cancer. In: MacLe CM (ed) Evaluation of Chemotherapeutic Agents. University Press, Columbia, p 196
Pirracchio R, Resche-Rigon M, Bresson D et al (2010) One-year outcome after neurosurgery for intracranial tumor in elderly patients. J Neurosurg Anesthesiol 22(4):342–346. https://doi.org/10.1097/ANA.0b013e3181e6daa2
Bunevicius A, Deltuva VP, Tamasauskas A (2017) Association of pre-operative depressive and anxiety symptoms with five-year survival of glioma and meningioma patients: a prospective cohort study. Oncotarget 8(34):57543–57551. https://doi.org/10.18632/oncotarget.15743
Chaichana K, Parker S, Olivi A, Quiñones-Hinojosa A (2010) A proposed classification system that projects outcomes based on preoperative variables for adult patients with glioblastoma multiforme. J Neurosurg 112(5):997–1004. https://doi.org/10.3171/2009.9.JNS09805
Bunevicius A (2018) Personality traits, patient-centered health status and prognosis of brain tumor patients. J Neurooncol 137(3):593–600. https://doi.org/10.1007/s11060-018-2751-6
Chang SM, Guha A, Newton HBVM (2010) Principles and practice of neuro-oncology: a multidisciplinary approach. Demos Medical Publishing, New York
Lee ST, Park CK, Kim JW et al (2015) Early cognitive function tests predict early progression in glioblastoma. Neuro-Oncology Pract 2(3):137–143. https://doi.org/10.1093/nop/npv007
Schiavolin S, Mariniello A, Broggi M et al (2021) Characteristics of patients returning to work after brain tumor surgery. Front Hum Neurosci 14:609080. https://doi.org/10.3389/fnhum.2020.609080
Johnson DR, Sawyer AM, Meyers CA, O’Neill BP, Wefel JS (2012) Early measures of cognitive function predict survival in patients with newly diagnosed glioblastoma. Neuro Oncol 14(6):808–816. https://doi.org/10.1093/neuonc/nos082
Vazzana R, Bandinelli S, Lauretani F et al (2010) Trail making test predicts physical impairment and mortality in older persons. J Am Geriatr Soc 58(4):719–723. https://doi.org/10.1111/j.1532-5415.2010.02780.x
Stark AM, Van De Bergh J, Hedderich J, Mehdorn HM, Nabavi A (2012) Glioblastoma: clinical characteristics, prognostic factors and survival in 492 patients. Clin Neurol Neurosurg 114(7):840–845. https://doi.org/10.1016/j.clineuro.2012.01.026
Ilmberger J, Ruge M, Kreth F-W, Briegel J, Reulen H-J, Tonn JC (2008) Intraoperative mapping of language functions: a longitudinal neurolinguistic analysis - Clinical article. J Neurosurg 109(4):583–592. https://doi.org/10.3171/JNS/2008/109/10/0583
Benz LS, Wrensch MR, Schildkraut JM et al (2018) Quality of life after surgery for intracranial meningioma. Cancer 124(1):161–166. https://doi.org/10.1002/cncr.30975
Funding
Silvia Schiavolin is supported by a grant from the Italian Ministry of Health (Ricerca Corrente, Fondazione Istituto Neurologico C. Besta, Linea 4—Outcome Research: dagli Indicatori alle Raccomandazioni Cliniche).
Author information
Authors and Affiliations
Contributions
Silvia Schiavolin contributed to the acquisition, analysis and interpretation of data, and drafting of the manuscript, and she will act as the overall guarantor. Arianna Mariniello, Morgan Broggi, Francesco DiMeco, and Paolo Ferroli participated in the data acquisition and interpretation; Paolo Ferroli, Matilde Leonardi, and Morgan Broggi contributed to the concept and design of the project. All authors contributed to the revision of the manuscript and approved the final version for submission.
Corresponding author
Ethics declarations
Ethics approval
Approval was obtained from the Institutional Ethical Committee of Fondazione IRCCS Istituto Neurologico Carlo Besta.
Consent to participate
Informed consent was obtained from all individual participants included in the study.
Consent for publication
Patients signed informed consent regarding publishing their data.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
520_2021_6732_MOESM1_ESM.docx
Supplementary file1 Results of the univariate linear regression on preoperative predictors of KPS change after 3 months from surgery in patients with glioma. ROWL, IR, 15 Rey-Osterrieth Word List immediate recall; ROWL, DR, 15 Rey-Osterrieth Word List delayed recall; TMT, Trail Making Test; MOCA, Montreal Cognitive Assessment; WHODAS-12, 12 item World Health Organization Disability Assessment Schedule; HADS, Hospital Anxiety and Depression Scale; OSS-3, Oslo-3 Social Support Scale; TIPI, Ten Item Personality Inventory; RS-14, 14-item Resilience Scale; EORTC QLQ-C30, European Organization for Research and Treatment of Cancer Quality of Life Questionnaire. (DOCX 16 KB)
520_2021_6732_MOESM2_ESM.docx
Supplementary file2 Results of the univariate linear regression on preoperative predictors of KPS change after 3 months from surgery in patients with meningioma. ROWL, IR, 15 Rey-Osterrieth Word List immediate recall; ROWL, DR, 15 Rey-Osterrieth Word List delayed recall; TMT, Trail Making Test; MOCA, Montreal Cognitive Assessment; WHODAS-12, 12 item World Health Organization Disability Assessment Schedule; HADS, Hospital Anxiety and Depression Scale; OSS-3, Oslo-3 Social Support Scale; TIPI, Ten Item Personality Inventory; RS-14, 14-item Resilience Scale; EORTC QLQ-C30, European Organization for Research and Treatment of Cancer Quality of Life Questionnaire. (DOCX 16 KB)
Rights and permissions
About this article
Cite this article
Schiavolin, S., Mariniello, A., Broggi, M. et al. Preoperative nonmedical predictors of functional impairment after brain tumor surgery. Support Care Cancer 30, 3441–3450 (2022). https://doi.org/10.1007/s00520-021-06732-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00520-021-06732-6