Cognitive functioning early after surgery of gliomas in eloquent areas

Clinical article

Djaina Satoer M.A. 1 , Judith Vork M.Sc. 1 , Evy Visch-Brink Ph.D. 1 , Marion Smits M.D., Ph.D. 2 , Clemens Dirven M.D., Ph.D. 1 and Arnaud Vincent M.D., Ph.D. 1
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  • 1 Departments of Neurosurgery and
  • 2 Radiology, Erasmus MC, University Medical Center, Rotterdam, The Netherlands
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Object

Patients with gliomas frequently have cognitive deficits, and surgery can exacerbate these deficits. Preoperative assessment is therefore crucial in patients undergoing surgery for glioma in eloquent areas, because the proximity of functional areas increases the risk of permanent postoperative cognitive disturbances. Although pre- and postoperative language and motor function in patients with glioma have been investigated frequently, data on good cognition studies are scarce. Most studies have focused on clinical neurological functioning or have only used brief neurological instruments. The authors investigated whether surgery for glioma in eloquent areas influences cognition early after surgery, by using an elaborate test protocol.

Methods

Twenty-eight patients with gliomas of the left hemisphere in language and nonlanguage areas were assessed before and 3 months after surgery with a comprehensive neuropsychological test protocol. The authors performed a correlation analysis between change in cognitive performance and tumor characteristics (that is, location, volume, pathological features, and histological grade) and between cognitive change and treatment-related factors (the extent of the resection and postoperative treatment with chemo- and radiotherapy).

Results

Both pre- and postoperatively, the mean performance of the patients was worse than the performance of the normal population in the language domain, the memory domain, and the executive functions (p < 0.05). Postoperatively, a decline was found in the language domain (t = 2.34, p = 0.027) and in the executive functions (t = 2.45, p = 0.022). However, cognitive change postsurgery was influenced by the location of the tumor; the decrease of cognitive score in the language domain was only observed in patients with tumors in or close to language areas (t = 2.33, p = 0.029). No effect on cognitive change was found for the other tumor characteristics and treatment-related factors.

Conclusions

This study underlines the importance of the use of a neuropsychological test protocol before and after surgery in patients with glioma, because several tasks in the domains of language, memory, and executive functions appeared to deteriorate after surgery. Tumor resection in language areas increases the risk of cognitive deficits in the language domain postoperatively.

Abbreviations used in this paper:AAT = Aachener Aphasia Test; ASRS = Aphasia Severity Rating Scale; BNT = Boston Naming Test; HGG = high-grade glioma; LGG = low-grade glioma; TMT = Trail-Making Test; TMTA, TMTB, TMTBA = TMT Parts A, B, BA; 15WT = 15 Words Test.

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Contributor Notes

Address correspondence to: Djaina Satoer, M.A., Department of Neurosurgery, Erasmus MC, University Medical Center, Dr. Molewaterplein 50-60, PO Box 2040, 3015 GE, Rotterdam, The Netherlands. email: d.satoer@erasmusmc.nl.

* Ms. Satoer and Ms. Vork contributed equally to this work.

Please include this information when citing this paper: published online August 31, 2012; DOI: 10.3171/2012.7.JNS12263.

  • 1

    Bosma I, , Reijneveld JC, , Klein M, , Douw L, , van Dijk BW, & Heimans JJ, : Disturbed functional brain networks and neurocognitive function in low-grade glioma patients: a graph theoretical analysis of resting-state MEG. Nonlinear Biomed Phys 3:9, 2009

    • Search Google Scholar
    • Export Citation
  • 2

    Brodaty H, & Moore CM: The Clock Drawing Test for dementia of the Alzheimer's type: a comparison of three scoring methods in a memory disorders clinic. Int J Geriatr Psychiatry 12:619627, 1997

    • Search Google Scholar
    • Export Citation
  • 3

    Correa DD, , DeAngelis LM, , Shi W, , Thaler HT, , Lin M, & Abrey LE: Cognitive functions in low-grade gliomas: disease and treatment effects. J Neurooncol 81:175184, 2007

    • Search Google Scholar
    • Export Citation
  • 4

    De Benedictis A, , Moritz-Gasser S, & Duffau H: Awake mapping optimizes the extent of resection for low-grade gliomas in eloquent areas. Neurosurgery 66:10741084, 2010

    • Search Google Scholar
    • Export Citation
  • 5

    Douw L, , Klein M, , Fagel SS, , van den Heuvel J, , Taphoorn MJ, & Aaronson NK, : Cognitive and radiological effects of radiotherapy in patients with low-grade glioma: long-term follow-up. Lancet Neurol 8:810818, 2009

    • Search Google Scholar
    • Export Citation
  • 6

    Drane DL, & Meador KJ: Cognitive and behavioral effects of antiepileptic drugs. Epilepsy Behav 3:5S 4953, 2002

  • 7

    du Boisgueheneuc F, , Levy R, , Volle E, , Seassau M, , Duffau H, & Kinkingnehun S, : Functions of the left superior frontal gyrus in humans: a lesion study. Brain 129:33153328, 2006

    • Search Google Scholar
    • Export Citation
  • 8

    Duffau H: Awake surgery for nonlanguage mapping. Neurosurgery 66:523529, 2010

  • 9

    Duffau H: A personal consecutive series of surgically treated 51 cases of insular WHO Grade II glioma: advances and limitations. Clinical article. J Neurosurg 110:696708, 2009

    • Search Google Scholar
    • Export Citation
  • 10

    Duffau H, , Capelle L, , Denvil D, , Sichez N, , Gatignol P, & Taillandier L, : Usefulness of intraoperative electrical subcortical mapping during surgery for low-grade gliomas located within eloquent brain regions: functional results in a consecutive series of 103 patients. J Neurosurg 98:764778, 2003

    • Search Google Scholar
    • Export Citation
  • 11

    Folstein MF, , Folstein SE, & McHugh PR: “Mini-mental state:” a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189198, 1975

    • Search Google Scholar
    • Export Citation
  • 12

    Gehring K, , Sitskoorn MM, , Gundy CM, , Sikkes SA, , Klein M, & Postma TJ, : Cognitive rehabilitation in patients with gliomas: a randomized, controlled trial. J Clin Oncol 27:37123722, 2009

    • Search Google Scholar
    • Export Citation
  • 13

    Goldstein B, , Obrzut JE, , John C, , Ledakis G, & Armstrong CL: The impact of frontal and non-frontal brain tumor lesions on Wisconsin Card Sorting Test performance. Brain Cogn 54:110116, 2004

    • Search Google Scholar
    • Export Citation
  • 14

    Goodglass H, & Kaplan E: The Assessment of Aphasia and Related Disorders ed 2 Philadelphia, Lea & Febiger, 1983

  • 15

    Graetz S, , De Blesser P, & Willmes K: Akense Afasie Test Lisse, The Netherlands, Swets & Zeitlinger, 1992

  • 16

    Hubbard EJ, , Santini V, , Blankevoort CG, , Volkers KM, , Barrup MS, & Byerly L, : Clock drawing performance in cognitively normal elderly. Arch Clin Neuropsychol 23:295327, 2008

    • Search Google Scholar
    • Export Citation
  • 17

    Ilmberger J, , Ruge M, , Kreth FW, , Briegel J, , Reulen HJ, & Tonn JC: Intraoperative mapping of language functions: a longitudinal neurolinguistic analysis. Clinical article. J Neurosurg 109:583592, 2008

    • Search Google Scholar
    • Export Citation
  • 18

    Kaplan E, , Goodglass H, & Weintraub S: Boston Naming Test ed 2 Philadelphia, Lippincott, Williams & Wilkins, 2001

  • 19

    Keime-Guibert F, , Napolitano M, & Delattre JY: Neurological complications of radiotherapy and chemotherapy. J Neurol 245:695708, 1998

  • 20

    Kiebert GM, , Curran D, , Aaronson NK, , Bolla M, , Menten J, & Rutten EH, : Quality of life after radiation therapy of cerebral low-grade gliomas of the adult: results of a randomised phase III trial on dose response (EORTC trial 22844). Eur J Cancer 34:19021909, 1998

    • Search Google Scholar
    • Export Citation
  • 21

    Kleihues P, , Louis DN, , Scheithauer BW, , Rorke LB, , Reifenberger G, & Burger PC, : The WHO classification of tumors of the nervous system. J Neuropathol Exp Neurol 61:215229, 2002

    • Search Google Scholar
    • Export Citation
  • 22

    Klein M, , Heimans JJ, , Aaronson NK, , van der Ploeg HM, , Grit J, & Muller M, : Effect of radiotherapy and other treatmentrelated factors on mid-term to long-term cognitive sequelae in low-grade gliomas: a comparative study. Lancet 360:13611368, 2002

    • Search Google Scholar
    • Export Citation
  • 23

    Lageman SK, , Cerhan JH, , Locke DE, , Anderson SK, , Wu W, & Brown PD: Comparing neuropsychological tasks to optimize brief cognitive batteries for brain tumor clinical trials. J Neurooncol 96:271276, 2010

    • Search Google Scholar
    • Export Citation
  • 24

    Le Rhun E, , Delbeuck X, , Devos P, , Pasquier F, & Dubois F: [Cognitive disorders and adult grade II and III gliomas: analysis of a series of 15 patients.]. Neurochirurgie 55:303308, 2009. (Fr)

    • Search Google Scholar
    • Export Citation
  • 25

    Lezak MD: Neuropsychological Assessment ed 4 New York, Oxford University Press, 2004

  • 26

    Luteijn F, & Barelds DPF: Groninger Intelligentie Test II (GIT II) Amsterdam, Pearson, 2004

  • 27

    Mendez MF, , Ala T, & Underwood KL: Development of scoring criteria for the clock drawing task in Alzheimer's disease. J Am Geriatr Soc 40:10951099, 1992

    • Search Google Scholar
    • Export Citation
  • 28

    Naidich TP, , Hof PR, , Gannon PJ, , Yousry TA, & Yousry I: Anatomic substrates of language: emphasizing speech. Neuroimaging Clin N Am 11:305341, ix, 2001

    • Search Google Scholar
    • Export Citation
  • 29

    Price CJ: The anatomy of language: a review of 100 fMRI studies published in 2009. Ann N Y Acad Sci 1191:6288, 2010

  • 30

    Sanai N, , Mirzadeh Z, & Berger MS: Functional outcome after language mapping for glioma resection. N Engl J Med 358:1827, 2008

  • 31

    Schäffler L, , Lüders HO, & Beck GJ: Quantitative comparison of language deficits produced by extraoperative electrical stimulation of Broca's, Wernicke's, and basal temporal language areas. Epilepsia 37:463475, 1996

    • Search Google Scholar
    • Export Citation
  • 32

    Scheibel RS, , Meyers CA, & Levin VA: Cognitive dysfunction following surgery for intracerebral glioma: influence of histopathology, lesion location, and treatment. J Neurooncol 30:6169, 1996

    • Search Google Scholar
    • Export Citation
  • 33

    Schmand B, , Groenink SC, & van den Dungen M: Letterfluency: psychometrische eigenschappen en Nederlandse normen. Tijdschr Gerontol Geriatr 39:6577, 2008

    • Search Google Scholar
    • Export Citation
  • 34

    Talacchi A, , Santini B, , Savazzi S, & Gerosa M: Cognitive effects of tumour and surgical treatment in glioma patients. J Neurooncol 103:541549, 2011

    • Search Google Scholar
    • Export Citation
  • 35

    Taphoorn MJ, & Klein M: Cognitive deficits in adult patients with brain tumours. Lancet Neurol 3:159168, 2004

  • 36

    Taphoorn MJ, , Schiphorst AK, , Snoek FJ, , Lindeboom J, , Wolbers JG, & Karim AB, : Cognitive functions and quality of life in patients with low-grade gliomas: the impact of radiotherapy. Ann Neurol 36:4854, 1994

    • Search Google Scholar
    • Export Citation
  • 37

    Taphoorn MJ, , Sizoo EM, & Bottomley A: Review on quality of life issues in patients with primary brain tumors. Oncologist 15:618626, 2010

    • Search Google Scholar
    • Export Citation
  • 38

    Teixidor P, , Gatignol P, , Leroy M, , Masuet-Aumatell C, , Capelle L, & Duffau H: Assessment of verbal working memory before and after surgery for low-grade glioma. J Neurooncol 81:305313, 2007

    • Search Google Scholar
    • Export Citation
  • 39

    Tucha O, , Smely C, , Preier M, , Becker G, , Paul GM, & Lange KW: Preoperative and postoperative cognitive functioning in patients with frontal meningiomas. J Neurosurg 98:2131, 2003

    • Search Google Scholar
    • Export Citation
  • 40

    Tucha O, , Smely C, , Preier M, & Lange KW: Cognitive deficits before treatment among patients with brain tumors. Neurosurgery 47:324334, 2000

    • Search Google Scholar
    • Export Citation
  • 41

    Van der Elst W, , van Boxtel MP, , van Breukelen GJ, & Jolles J: Rey's verbal learning test: normative data for 1855 healthy participants aged 24–81 years and the influence of age, sex, education, and mode of presentation. J Int Neuropsychol Soc 11:290302, 2005

    • Search Google Scholar
    • Export Citation

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