Cognitive status and quality of life in
patients with suspected versus
proven low-grade gliomas
J.C. Reijneveld, MD; M.M. Sitskoorn, PhD; M. Klein, PhD; J. Nuyen; and M.J.B. Taphoorn, MD, PhD
Article abstract—Background: The preferred management of patients with suspected low-grade gliomas (S-LGG) re-
mains controversial. The benefits of resection or radiotherapy early in the course of the disease have not been proven in
terms of survival. Little is known about the effects of early therapy on quality of life (QOL) and cognitive status. The
authors compared functional status, QOL, and cognitive status of patients suspected of having a LGG, in whom treatment
was deferred, and patients with proven LGG (P-LGG), who underwent early surgery. Methods: The authors recruited 24
patients suspected of having an LGG. These patients were matched with 24 patients with a histologically proven LGG and
healthy control subjects for educational level, handedness, age, and gender. The two patient groups were also matched for
tumor laterality, use of anticonvulsants, and interval between diagnosis and testing. Functional status was determined in
both patient groups. QOL and cognitive status were compared between the three groups. Results: Matching criteria and
functional status did not differ significantly between groups. Both patient groups scored worse on QOL scales than
healthy control subjects. Unoperated patients with S-LGG scored better on most items than patients with P-LGG.
Cognitive status was worse in both groups than in healthy control subjects, but, again, patients with S-LGG performed
better than patients with P-LGG. Conclusion: These data suggest that a wait-and-see policy in patients with S-LGG has
no negative effect on cognitive performance and QOL.
A recurring dilemma arises when a patient presents
with late-onset epilepsy and brain imaging shows a
lesion suggestive of a low-grade glioma (LGG).1-3Al-
though several retrospective analyses have sug-
gested a survival benefit in patients with early
radiotherapy, these studies are confounded by pa-
tient selection.4,5Preliminary results of a large ran-
domized trial indicate that early radiotherapy fails
to prolong survival in LGG patients.6Also, in the
dose range evaluated, a randomized clinical trial
failed to demonstrate a dose–response relationship
for radiation in LGG patients.7The benefits of surgical
resection have not been proven either, as retrospective
studies show conflicting results.5,8Therefore, deferring
intervention and even biopsy may be justified in these
Health-related quality of life (QOL) has become an
increasingly important measure in studies of brain
tumor patients.10Assessment of QOL in glioma pa-
tients is particularly relevant, as these patients can-
not be cured and nearly all will eventually die of
their disease. The effects on QOL of all treatment
modalities in patients with glioma have to be bal-
anced against their possible survival benefits.10,11
QOL of patients with glioma is often impaired by a
decreased general and neurologic performance status
and decreased cognitive functioning.12Patients with
LGG do not have a significantly affected perfor-
mance status, but they do show serious cognitive
impairment.13Modern radiotherapy to moderate
doses does not lead to significant cognitive impair-
ment within a median of 3 years of treatment, but
the results of longer-term studies are yet to be re-
ported.14Therefore, cognitive disturbances should
probably be attributed to damage by the tumor itself
or surgical procedures or to psychological effects.14,15
To our knowledge, no studies have assessed QOL
and cognitive performance status (CPS) in patients
with suspected but unconfirmed LGG (S-LGG). Un-
certainty about the diagnosis may negatively influ-
ence CPS and QOL, as has been shown in other
patient groups.16If this also applies to S-LGG pa-
tients, it would be a reason to aim at a definite
diagnosis at an early stage. On the other hand, sur-
gical procedures (stereotactic biopsy or resection)
necessary to reach this goal may also have a nega-
tive impact on CPS and QOL.
The present study was undertaken to determine
the CPS and QOL of patients with S-LGG and inves-
tigate whether there is a difference in CPS and QOL
between S-LGG patients and patients with a proven
LGG (P-LGG). We therefore assessed CPS and QOL
in 24 S-LGG patients in whom all intervention for
the tumor was deferred. These results were com-
From the Departments of Neurology (Drs. Reijneveld and Taphoorn) and Psychiatry (Dr. Sitskoorn and J. Nuyen), University Medical Center Utrecht; and
Department of Medical Psychology (Dr. Klein), “Vrije Universiteit” Medical Center, Amsterdam, the Netherlands.
Received July 27, 2000. Accepted in final form November 8, 2000.
Address correspondence and reprint requests to Dr. J.C. Reijneveld, Department of Neurology, G03.228, University Medical Center Utrecht, P.O. Box 85500,
3508 GA Utrecht, the Netherlands; e-mail: J.Reijneveld@neuro.azu.nl
Copyright © 2001 by AAN Enterprises, Inc.
pared with data of carefully matched healthy control
subjects and with data of patients with P-LGG who
underwent subtotal resection or biopsy.
S-LGG were recruited from 16 hospitals in the western
and central part of the Netherlands. Recruitment of this
group took approximately 1 year. The subjects were stud-
ied between June 1998 and July 1999. All patients were at
least 18 years old and had presented with epileptic sei-
zures without neurologic deficits. All patients showed non-
enhancing supratentorial lesions on MRI or CT, without
edema or mass effect. Furthermore, none of the patients
had radiologic or clinical signs of progression for at least 6
months from the moment of the presumed diagnosis. None
of the patients used corticosteroids. All patients gave writ-
ten informed consent before assessment, and the ethical
committee of the University Medical Center Utrecht ap-
proved all aspects of the study.
Patients with P-LGG were recruited from a database of
200 patients with histologically proven supratentorial
LGG from the “Vrije Universiteit” Medical Center (Amster-
dam, the Netherlands). All patients had also presented
with epileptic seizures, and none of them had neurologic
deficits. They had undergone biopsy or resection at least 6
months previously and had been without progression since
then. None of them had been treated with radiotherapy.
They were selected to match S-LGG patients on tumor
laterality, handedness, educational level, number of years
of full-time education, interval between diagnosis and test-
ing, gender, and age. Healthy control patients were re-
cruited from a database of the University of Maastricht
(the Netherlands; MAAS study; CPS data)17and the Neth-
erlands Organization for Applied Scientific Research
(TNO; Medical Outcomes Study [MOS] SF-36 Short Form
Health Survey QOL data). They were matched with the
patients for handedness (CPS data only), educational level,
gender, and age.
Functional impairment was as-
sessed with the Karnofsky Performance Status (KPS)18
and the Barthel Index.19Neurologic functioning of patients
was rated by means of the Neurologic Functional Status
Quality of life.
The QOL was assessed with the MOS
SF-36 Short-Form Health Survey, which has been trans-
lated into the Dutch language.21,22It is a self-report ques-
tionnaire, composed of 36 items, organized into eight
multi-item scales assessing physical functioning, physical
role functioning, emotional role functioning, pain, vitality,
social functioning, mental health, and general health per-
ceptions. A supplementary questionnaire module, the
Brain Cancer Module 20 (BCM20), was employed to assess
brain tumor-specific QOL issues. The BCM20 contains four
multi-item scales assessing visual disorder, communica-
tion deficit, motor dysfunction, and uncertainty about the
future and seven single items about headache, seizures,
drowsiness, hair loss, itching, weakness of the legs, and
difficulty in bladder control.23To assess the self-perceived
level of cognitive functioning, we used the Cognitive Func-
tioning Scale (CFS), a six-item scale reflecting problem
solving, concentration, confusion, forgetfulness, sustained
attention, and slowness.21The summary “cognitive com-
Patients and control subjects.
plaints” score of this scale was used for statistical analysis.
Filling in of all questionnaires took ?45 minutes.
Cognitive performance status.
test battery was administered to each patient by trained
psychometricians, who were supervised by a neuropsychol-
ogist. This test battery consisted of the following tests:
Visual Verbal Learning Test,24Working Memory Task,25
Letter–Digit Substitution Test,26Categoric Word Fluen-
cy,27Concept Shifting Test,28Stroop Color Word Test,29and
Working Memory Task.25Summary measures were calcu-
lated to detect possible deficits in the domains of attention
and concentration, visual–verbal memory, executive func-
tion, and psychomotor function. Administration of these
tests, which were administered in a fixed order for each
patient, took an average of 90 minutes. Because of missing
data, 21 subjects of the S-LGG group and 23 subjects of the
healthy control group were used in the final analysis of the
All statistical analyses were car-
ried out with the Statistical Package for the Social Sci-
ences (SPSS version 9.0 for Windows). All tests were two
sided, and significance was accepted at the 5% level. Sta-
tistical analysis of the matching criteria was done with ?2
tests (sex, handedness), Fisher’s exact test (tumor location,
anticonvulsants), analysis of variance (ANOVA; age, years
of full-time education, interval between diagnosis and test-
ing), and Kruskal–Wallis H test (educational level). Statis-
tical analysis of tumor diameter, KPS, Barthel Index, and
NFSS was done with Mann–Whitney U tests.
Considerable obliquity of distribution was present in all
groups for most of the QOL variables. This obliquity also
seemed to account for the inequality of variances among
the groups for several QOL variables. Transformations
were not helpful to overcome this problem. Therefore, the
QOL scales were treated independently and analyzed by
means of nonparametric tests. In case of the MOS SF-36,
Kruskal–Wallis H tests were performed to assess whether
there were overall differences between patients and control
subjects. We used post hoc Mann–Whitney U tests with
Bonferroni adjustment to determine which of the three
groups differed from each other. In case of the BCM, we
used Mann–Whitney U tests to demonstrate possible dif-
ferences between both patient groups. Performances of the
patient groups on the CFS (i.e., summary “cognitive com-
plaints” scores) were compared with a one-way univariate
For analysis of the CPS data, all test scores were
rescaled to obtain z scores (standard equivalents) by using
the means and the standard deviations of a matched con-
trol group as norm scores. The advantage of the use of
means and standard deviations of control subjects to ob-
tain z scores, instead of ratings of the general population,
is that the control subjects in our study were matched for
demographic characteristics of the patient groups (i.e., sex
distribution, handedness, age at test, and educational lev-
el). The four summary functional domain scores for each
subject were calculated by averaging the z scores for a
similar domain. A multivariate ANOVA was performed,
with the four functional domain scores serving as depen-
dent variables and group (i.e., S-LGG patients, P-LGG pa-
tients, and healthy control subjects) as independent
variables. In case of a significant multivariate effect, uni-
variate analyses were performed to examine overall group
March (1 of 2) 2001
differences for a specific functional domain. These were
followed by t-tests with Bonferroni adjustment to deter-
mine differences between the three groups.
To investigate possible relationships between cognitive
impairment and tumor size, Spearman correlation coeffi-
cients were used to correlate individual CPS and QOL data
and tumor diameter. Bonferroni corrections were applied
to adjust for multiple testing.
Matching criteria did not differ significantly between the
two patient groups. Moreover, we found no significant dif-
ferences in performance on the KPS, Barthel Index, and
NFSS between the two patient groups. High scores for the
KPS, Barthel Index, and NFSS were found in both groups,
indicating that patients were functionally independent,
were able to carry on normal activity, and showed only
minor signs or symptoms of disease. Seventeen patients
with P-LGG had undergone (sub-)total resection (71%) and
six patients stereotactic biopsy (25%); data on the type of
operation were not available in one patient. The histologic
diagnosis was low-grade astrocytoma (WHO classification)
in all patients. Tumor diameter on the latest MR or CT
scan before surgery (P-LGG patients) or before testing (S-
LGG patients) did not differ significantly between the two
groups. Data on tumor diameter were not available in
three S-LGG and two P-LGG patients. Eight patients with
P-LGG noticed a change in the pattern or frequency of
seizures after biopsy or resection. In four of them, seizure
frequency decreased; in two of them, there was an in-
crease; and in the other two, the type of seizures changed.
At the time of testing, 19 of 24 S-LGG patients (79%) and
15 of 24 P-LGG patients (63%) were using anticonvulsants.
The interval between diagnosis and testing did not differ
significantly between the two groups (S-LGG patients, 4.4 ?
4.5 years; P-LGG patients, 5.5 ? 3.7 years). Since the end
of the study, two patients with S-LGG have been operated
on because of clinical deterioration in combination with an
enhancing and mass-occupying lesion on MRI; the histo-
logic diagnosis was anaplastic astrocytoma in both. The
table shows the demographic, clinical, and radiographic
characteristics of the two patient groups. The two healthy
control groups did not differ significantly from the two
patient groups on the matching criteria (QOL healthy con-
trol subjects: 13 male, mean age 42.8 ? 12.0 years [range
19 to 71 years], mean educational level 4.0; CPS healthy
control subjects, 13 male, mean age 42.8 ? 11.6 years
[range 25 to 71 years], mean educational level 4.5, 22
Quality of life.
Kruskal–Wallis U tests showed overall
group differences for the domains of general health percep-
tions (p ? 0.05), vitality (p ? 0.005), social functioning
(p ? 0.05), and mental health (p ? 0.05) of the MOS-SF 36.
Post hoc Mann–Whitney U tests with Bonferroni adjust-
ment indicated that patients with P-LGG scored worse
than normal control subjects on all four scales (i.e., general
Table Characteristics of patients with suspected (S-LGG) and proven (P-LGG) low-grade glioma
CharacteristicS-LGG patients P-LGG patientsSignificance
No. of persons 2424—
Sex, M/F10/14 15/9NS*
Age at test, y; mean ? SD (range)42.8 ? 12.1 (18–71)38.2 ? 10.6 (20–55) NS‡
Handedness, R/L 21/322/2NS*†
Tumor location, R/L11/13 11/13NS†
Tumor diameter, cm 4.24 ? 2.32 (n ? 21)3.59 ? 1.59 (n ? 22)NS?
Treatment, stereotactic biopsy/surgery/unknown—6/17/1—
Educational level¶ 5.03.5NS§
Education, y12.5 ? 3.612.9 ? 4.0NS‡
Anticonvulsants, N/Y5/19 9/15NS†
Diagnosis to test interval, y; mean ? SD4.4 ? 4.55.5 ? 3.7 NS‡
Barthel Index, mean ? SD20.0 ? 0.219.9 ? 0.4NS?
Neurologic Functional Status Scale, mean ? SD1.0 ? 0.0 1.0 ? 0.0 NS?
Karnofsky Performance Scale, mean ? SD92.5 ? 9.088.7 ? 9.7 NS?
† Fisher’s exact test.
‡ Analysis of variance.
§ Kruskal–Wallis H test.
? Mann–Whitney U test.
¶ Educational level was measured by a Dutch scoring system ranging from unfinished primary education (level 1) to university educa-
tion (level 8).
March (1 of 2) 2001
health perceptions, p ? 0.05; vitality, p ? 0.01; social func-
tioning, p ? 0.05; mental health, p ? 0.05). Patients with
S-LGG scored worse on the general health perceptions do-
main than normal control subjects (p ? 0.05). With the
exception of the physical functioning domain, we found a
consistent tendency for patients with P-LGG to score lower
on all domains than S-LGG patients, as illustrated in fig-
ure 1A. The difference was significant only for the vitality
domain. BCM20 data show the same tendency of better
scores for patients with S-LGG (figure 1B). Mann–Whitney
U tests showed worse scores for patients with P-LGG
than for those with S-LGG on the scale motor dysfunc-
tion (p ? 0.001) and the single item measuring difficulty
in bladder control (p ? 0.05). We found no significant
difference in the score for the dimension future uncer-
tainty between both groups. The CFS data are shown in
figure 1C. ANOVA revealed no significant differences
between the total sum scores of both patient groups
(S-LGG, 18.87 ? 12.61; P-LGG, 22.11 ? 5.57). We found
no correlation between tumor diameter and the scores
on the different QOL subscales.
ANOVA showed an overall difference between the groups
(F [2.65] ? 2.51, p ? 0.05). Univariate analysis indicated
group differences for psychomotor functioning (F [2.65] ?
7.47, p ? 0.005). No significant group differences were
found for the other three functional domains. Post hoc t
tests with Bonferroni adjustment showed that patients
Figure 1. Quality of life of patients
with proven (P-LGG) and suspected (S-
LGG) low-grade glioma. (A) Scores of
patients with P-LGG (filled columns)
and S-LGG (hatched columns) on the
eight domains of the Medical Outcomes
Study SF-36 Short Form Health Survey
compared with those of healthy control
subjects (open columns) (mean and
SEM; higher score means fewer com-
plaints). *Lower score for P-LGG pa-
tients compared with control subjects;
**lower score for S-LGG patients com-
pared with control subjects; ***lower
score for P-LGG compared with S-LGG.
(B) Scores of patients with P-LGG
(filled columns) and S-LGG (hatched
columns) on the subscales of the Brain
Cancer Module 20 (mean and SEM;
higher score means more complaints).
*Worse scores for P-LGG compared
with S-LGG patients. (C) Scores of pa-
tients with P-LGG (filled columns) and
S-LGG (hatched columns) on the items
of the self-rating Cognitive Functioning
Scale (mean and SEM; higher score
means fewer complaints).
March (1 of 2) 2001
with P-LGG performed worse on the psychomotor function-
ing than S-LGG patients (p ? 0.005) and than healthy
control subjects (p ? 0.01) (figure 2). We found no correla-
tion between tumor diameter and the scores on the four
tients with P- or S-LGG have a worse QOL and cog-
nitive status than healthy control subjects and that
patients with LGG who underwent resection or bi-
opsy are worse on these measures than patients with
S-LGG who were managed conservatively. Patients
with S-LGG show significantly better scores for the
QOL domains vitality, motor dysfunction, and diffi-
culty in bladder control than patients with P-LGG.
Psychomotor functioning was significantly worse for
patients with P-LGG.
QOL has become an increasingly important mea-
sure in glioma studies.10,30The measurement of QOL
in recent studies, however, was more or less re-
stricted to the patient’s functional status18or cogni-
tive functioning.31Nowadays, it is generally accepted
that a more comprehensive set of measures reflect-
ing health status, CPS, and QOL is needed for a
more complete assessment.10,13,14,32This is again illus-
trated by our study: Despite an excellent perfor-
mance status and the absence of neurologic deficits,
both groups demonstrate deficits in CPS as well as a
reduction in perceived QOL, when measured with an
extensive battery of validated tools.
Neuropsychological assessment showed a signifi-
cantly worse performance on the domain of psy-
chomotor functioning for P-LGG patients, although
they had fewer cognitive symptoms on the self-rating
CFS. This discrepancy between subjective com-
plaints and objective test results has been described
before14and indicates that P-LGG patients may not
be aware of their cognitive deficits.
This study demonstrates that pa-
The results of our study may have been biased by
the selection of patients. Initial treatment of patients
with LGG depends on the local neurologist’s and
neurosurgeon’s view about the benefit of early, ag-
gressive treatment, the clinical status of the patient,
the site and extent of the lesion, and the patient’s
preferences. Presumably, patients with more exten-
sive neurologic deficits or nondominant lesions will
more frequently undergo early treatment. All our
patients presented with epileptic seizures but were
otherwise clinically normal. We found no significant
difference in the number of patients taking anticon-
vulsants between both groups. The patients in our
study were matched on tumor laterality, but the
groups were too small to use tumor location as a
supplementary matching criterion. Tumor size, how-
ever, did not differ significantly between the two
groups and was not correlated to performance on the
QOL or CPS subscales. Furthermore, patients who
cannot deal with uncertainty about their diagnosis
may insist on early treatment. Premorbid patient
characteristics determine, among other factors, the
capability of patients to deal with this uncertainty.
Therefore, age and educational level, which are a
relatively accurate indication of premorbid function-
ing level, were used as matching criteria.
We do not know whether the decreased QOL and
cognitive dysfunctioning of patients with P-LGG
should be attributed to the surgical procedures. Pre-
vious reports at least have not shown clear benefits
of the surgical approach in terms of survival time
or progression-free interval.4,7,8,33Hope of improv-
ing epilepsy may be another reason to operate on
patients with LGG. In our group of P-LGG pa-
tients, however, epilepsy improved in 4 of 24 pa-
tients (17%) after the operation but got worse in at
least 2 other patients (8%).
Another reason for operation could be that know-
ing the definite diagnosis would diminish feelings of
uncertainty about the future. Patients with glioma
are faced with uncertainty about several issues such
as length of survival and anxiety about neurologic
impairment with disability.15Uncertainty about the
future, however, did not differ between the two pa-
tient groups in our study. Therefore, we conclude
that a definite diagnosis does not lead to a large
reduction of these feelings.
The authors thank Dr. J.E.C. Bromberg (Department of Neurol-
ogy) and D.R. van Rij, S.P.W.M. Bouts, and M. van der Linden
(Department of Psychiatry, University Medical Center Utrecht,
the Netherlands) for assistance in different parts of this study.
They also thank Prof. Dr. J. van Gijn (Department of Neurology,
University Medical Center Utrecht), Prof. Dr. N. Aaronson (De-
partment of Psychosocial Research and Epidemiology, Nether-
(Department of Neurology, “Vrije Universiteit” Medical Center,
Amsterdam), and Prof. H.M. van der Ploeg (Department of Medi-
cal Psychology, “Vrije Universiteit” Medical Center, Amsterdam,
the Netherlands) for valuable comments on previous versions of
Figure 2. Mean z scores for patients with proven (P-LGG;
filled columns) and suspected (S-LGG; hatched columns)
low-grade glioma on the four cognitive domains compared
with the scores of a matched group of healthy control sub-
jects. The mean z scores of the healthy control subjects
(open columns) were rescaled to zero for all four domains
to visualize the relative performance of the two patient
groups (mean and SEM; higher score means better perfor-
mance). *Lower score for P-LGG patients compared with
healthy control subjects and S-LGG patients.
March (1 of 2) 2001
References Download full-text
1. Cairncross JG, Laperriere NJ. Low-grade glioma: to treat or
not to treat? Arch Neurol 1989;46:1238–1239.
2. Levin VA. Controversies in the treatment of low-grade astro-
cytomas and oligodendrogliomas. Curr Opin Neurol 1996;8:
3. Cairncross JG. Understanding low-grade glioma: a decade of
progress. Neurology 2000;54:1402–1403.
4. Medbery CA, Straus KL, Steinberg SM, et al. Low-grade as-
trocytomas: treatment results and prognostic variables. Int J
Radiat Oncol Biol Phys 1988;15:837–841.
5. Shaw EG, Daumas-Duport C, Scheithauer BW, et al. Radia-
tion therapy in the management of low-grade supratentorial
astrocytomas. J Neurosurg 1989;70:853–861.
6. Karim ABMF, Cornu P, Bleehen N. Immediate postoperative
radiotherapy in low-grade glioma improves progression free
survival but not overall survival: preliminary results of an
EORTC/MRC randomized phase III study. J Clin Oncol 1998;
7. Karim ABMF, Maat B, Hatlevoll R, et al. A randomized trial
on dose–response in radiation therapy of low-grade cerebral
glioma: European Organization for Research and Treatment
of Cancer (EORTC) study 22844. Int J Radiat Oncol Biol Phys
8. Piepmeier JM. Observations on the current treatment of low-
grade astrocytic tumors of the cerebral hemispheres. J Neuro-
9. Recht LD, Lew R, Smith TW. Suspected low-grade glioma: is
deferring treatment safe? Ann Neurol 1992;31:431–436.
10. Kiebert GM, Curran D, Aaronson NK, et al. 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 1998;34:1902–1909.
11. Choucair AK, Scott C, Urtasun R, et al. Quality of life and
neuropsychological evaluation for patients with malignant as-
trocytomas: RTOG 91–14. Radiation Therapy Oncology Group.
Int J Radiat Oncol Biol Phys 1997;38:9–20.
12. Osoba D, Aaronson NK, Muller M, et al. Effect of neurological
dysfunction on health-related quality of life in patients with
high-grade glioma. J Neurooncol 1997;34:263–278.
13. Taphoorn MJB, Heimans JJ, Snoek FJ, et al. Assessment of
quality of life in patients treated for low-grade glioma; a pre-
liminary report. J Neurol Neurosurg Psychiatry 1992;55:372–
14. Taphoorn MJB, Klein Schiphorst A, Snoek FJ, et al. Cognitive
functions and quality of life in patients with low-grade glio-
mas: the impact of radiotherapy. Ann Neurol 1994;36:48–54.
15. Newton C, Mateo MA. Uncertainty: strategies for patients
with brain tumor and their family. Cancer Nurs 1994;17:137–
16. Kash KM, Holland JC, Osborne MP, et al. Psychological coun-
seling strategies for women at risk of breast cancer. JNCI
17. Jolles J, van Boxtel MP, Ponds RW, Metsemakers JF, Houx
PJ. The Maastricht Aging Study (MAAS). The longitudinal
perspective of cognitive aging. Tijdschr Gerontol Geriatr 1998;
18. Sachsenheimer W, Piotrowski W, Bimmler T. Quality of life in
patients with intracranial tumors on the basis of Karnofsky’s
performance status. J Neurooncol 1992;13:177–181.
19. Brazil L, Thomas R, Laing R, et al. Verbally administered
Barthel Index as functional assessment in brain tumour pa-
tients. J Neurooncol 1997;34:187–192.
20. North CA, North RB, Epstein JA, et al. Low-grade cerebral
astrocytomas: survival and quality of life after radiation ther-
apy. Cancer 1990;66:6–14.
21. Stewart AL, Ware JE. Measuring functioning and well-being:
the medical outcomes study approach. Durham: Duke Univer-
sity Press, 1992.
22. Aaronson NK, Muller M, Cohen PD, et al. Translation, valida-
tion, and norming of the Dutch language version of the SF-36
Health Survey in community and chronic disease populations.
J Clin Epidemiol 1998;51:1055–1068.
23. Osoba D, Aaronson NK, Muller M, et al. The development and
psychometric validation of a brain cancer quality-of-life ques-
tionnaire for use in combination with general cancer-specific
questionnaires. Qual Life Res 1996;5:139–150.
24. Brand N, Jolles J. Learning and retrieval rate of words pre-
sented auditorily and visually. J Gen Psychol 1985;112:201–210.
25. Brand N, Jolles J. Information processing in depression and
anxiety. Psychol Med 1987;17:145–153.
26. Watson CG, Gasser B, Schaefer A, et al. Separation of brain-
damaged from psychiatric patients with ability and personal-
ity measures. J Clin Psychol 1981;37:347–353.
27. Butters N, Granholm E, Salmon DP, et al. Episodic and se-
mantic memory: a comparison of amnesic and demented pa-
tients. J Clin Exp Neuropsychol 1987;9:479–497.
28. Eson ME, Yen JK, Bourke RS. Assessment of recovery from
serious head injury. J Neurol Neurosurg Psychiatry 1978;41:
29. Houx PJ, Jolles J, Vreeling FW. Stroop interference: aging
effects assessed with the Stroop Color-Word Test. Exp Aging
30. Weitzner MA, Meyers CA. Cognitive functioning and quality
of life in malignant glioma patients: a review of the literature.
31. Trojanowski T, Peszynski J, Turowski K, et al. Quality of sur-
vival of patients with brain gliomas treated with postoperative
CCNU and radiation therapy. J Neurosurg 1989;70:18–23.
32. Mackworth N, Fobair P, Prados MD. Quality of life self-reports
from 200 brain tumor patients: comparisons with Karnofsky per-
formance scores. J Neurooncol 1992;14:243–253.
33. Medbery CA, Straus KL, Steinberg SM, et al. Low-grade as-
trocytomas: treatment results and prognostic variables. Int J
Radiat Oncol Biol Phys 1988;15:837–841.
March (1 of 2) 2001