ArticlePDF Available

Language processing in glioma patients: speed or accuracy as a sensitive measure?

Taylor & Francis
Aphasiology
Authors:

Abstract and Figures

Background Glioma (brain tumour) patients can suffer from mild linguistic and non-linguistic cognitive problems when the glioma is localised in an eloquent brain area. Word-finding problems are among the most frequently reported complaints. However, mild problems are difficult to measure with standard language tests because they are generally designed for more severe aphasic patients. Aims The aim of the present study was to investigate whether word-finding problems reported by patients with a glioma can be objectified with a standard object naming test, and a linguistic processing speed test. In addition, we examined whether word-finding problems and linguistic processing speed are related to non-verbal cognitive abilities. Methods & Procedures We tested glioma patients (N=36) as part of their standard pre-treatment clinical work-up. Word-finding problems were identified by a clinical linguist during the anamnesis. Linguistic processing speed was assessed with a newly designed sentence judgment test (SJT) as part of the Diagnostic Instrument for Mild Aphasia (DIMA), lexical retrieval with the Boston Naming Test (BNT), presence of aphasia with a Token Test (TT), and non-verbal processing with the Trail Making Test A and B (TMT). Test performances of glioma patients were compared to those of healthy control participants (N=35). Outcomes & Results The results show that many glioma patients (58%) report word-finding problems; these complaints were in only half of the cases supported by deviant scores on the BNT. Moreover, the presence of reported word-finding problems did not correlate with the BNT scores. However, word-finding problems were significantly correlated with reaction times on the SJT and the TMT. Although there were no significant differences between the patient and control group on the SJT, a subgroup of patients with a glioma in the frontal lobe of the language-dominant hemisphere was slower on the SJT. Finally, performance on the SJT and TMT were significantly correlated in the patient group but not in the control group. Conclusions Linguistic processing speed appears to be an important factor in explaining reported word-finding problems. Moreover, the overlap between speed of language processing and non-verbal processing indicates that patients may rely on more domain-general cognitive abilities as compared to healthy participants. The variability observed between patients emphasises the need for tailored neuro-linguistic assessments including an extensive anamnesis regarding language problems in clinical work-up.
Content may be subject to copyright.
Full Terms & Conditions of access and use can be found at
https://www.tandfonline.com/action/journalInformation?journalCode=paph20
Aphasiology
ISSN: (Print) (Online) Journal homepage: https://www.tandfonline.com/loi/paph20
Language processing in glioma patients: speed or
accuracy as a sensitive measure?
Saskia Mooijman, Laura S. Bos, Elke De Witte, Arnaud Vincent, Evy Visch-
Brink & Djaina Satoer
To cite this article: Saskia Mooijman, Laura S. Bos, Elke De Witte, Arnaud Vincent, Evy Visch-
Brink & Djaina Satoer (2021): Language processing in glioma patients: speed or accuracy as a
sensitive measure?, Aphasiology, DOI: 10.1080/02687038.2021.1970099
To link to this article: https://doi.org/10.1080/02687038.2021.1970099
© 2021 The Author(s). Published by Informa
UK Limited, trading as Taylor & Francis
Group.
Published online: 21 Sep 2021.
Submit your article to this journal
View related articles
View Crossmark data
Language processing in glioma patients: speed or accuracy as
a sensitive measure?
Saskia Mooijman
a,b,c
, Laura S. Bos
a,b
, Elke De Witte
a,d
, Arnaud Vincent
a
, Evy Visch-
Brink
a
and Djaina Satoer
a
a
Department of Neurosurgery, Erasmus Mc University Medical Centre Rotterdam, The Netherlands;
b
Amsterdam Centre for Language and Communication, University of Amsterdam, The Netherlands;
c
Centre
for Language Studies, Radboud University, Nijmegen, The Netherlands;
d
Centre for Linguistics, Clinical and
Experimental Neurolinguistics, Free University, Brussels, Belgium
ABSTRACT
Background: Glioma (brain tumour) patients can suer from mild
linguistic and non-linguistic cognitive problems when the glioma is
localised in an eloquent brain area. Word-nding problems are
among the most frequently reported complaints. However, mild
problems are dicult to measure with standard language tests
because they are generally designed for more severe aphasic
patients.
Aims: The aim of the present study was to investigate whether
word-nding problems reported by patients with a glioma can be
objectied with a standard object naming test, and a linguistic
processing speed test. In addition, we examined whether word-
nding problems and linguistic processing speed are related to
non-verbal cognitive abilities.
Methods & Procedures: We tested glioma patients (N=36) as part
of their standard pre-treatment clinical work-up. Word-nding pro-
blems were identied by a clinical linguist during the anamnesis.
Linguistic processing speed was assessed with a newly designed
sentence judgment test (SJT) as part of the Diagnostic Instrument
for Mild Aphasia (DIMA), lexical retrieval with the Boston Naming
Test (BNT), presence of aphasia with a Token Test (TT), and non-
verbal processing with the Trail Making Test A and B (TMT). Test
performances of glioma patients were compared to those of
healthy control participants (N=35).
Outcomes & Results: The results show that many glioma patients
(58%) report word-nding problems; these complaints were in only
half of the cases supported by deviant scores on the BNT. Moreover,
the presence of reported word-nding problems did not correlate
with the BNT scores. However, word-nding problems were signi-
cantly correlated with reaction times on the SJT and the TMT.
Although there were no signicant dierences between the patient
and control group on the SJT, a subgroup of patients with a glioma
in the frontal lobe of the language-dominant hemisphere was
ARTICLE HISTORY
Received 23 February 2021
Accepted 16 August 2021
KEYWORDS
Glioma; processing speed;
word-finding problems;
cognition
CONTACT Saskia Mooijman s.mooijman@erasmusmc.nl Department of Neurosurgery, Erasmus MC - University
Medical Center 3000 CA Rotterdam, The Netherlands.
APHASIOLOGY
https://doi.org/10.1080/02687038.2021.1970099
© 2021 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/
licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly
cited.
slower on the SJT. Finally, performance on the SJT and TMT were
signicantly correlated in the patient group but not in the control
group.
Conclusions: Linguistic processing speed appears to be an impor-
tant factor in explaining reported word-nding problems.
Moreover, the overlap between speed of language processing
and non-verbal processing indicates that patients may rely on
more domain-general cognitive abilities as compared to healthy
participants. The variability observed between patients emphasises
the need for tailored neuro-linguistic assessments including an
extensive anamnesis regarding language problems in clinical work-
up.
Introduction
Gliomas
Gliomas are the most common type of primary brain tumour. The World Health
Organization categorises gliomas into four grades. High-grade gliomas (HGG, grades III–
IV) are more aggressive and more common than low-grade gliomas (LGG, grades I–II;
Sanai & Berger, 2012). Gliomas are often located in eloquent areas of the brain (Duau &
Capelle, 2004; Gerritsen et al., 2019). In these cases, surgery is aimed at resecting the
tumour whilst preserving cognitive functions (Ilmberger et al., 2008; Sanai & Berger, 2008;
De Witte & Mariën, 2013). Due to the preferential localisation of gliomas in eloquent areas
of the brain, patients may experience neurological and cognitive impairments that can
have serious consequences on their quality of life.
Sensitivity of assessments
It is of central importance for quality of life to investigate how patients subjectively
experience (loss of) abilities, such as language (Cruice, Worrall, & Hickson, 2006). Word
retrieval diculties are among the most common complaints of people with a glioma
(Racine et al., 2015). Importantly, performance on objective cognitive tests may not
necessarily reect the patients’ complaints (Gehring et al., 2015; Racine et al., 2015;
Taphoorn & Klein, 2004; Van der Linden et al., 2020). More specically, patients appear
to report language complaints that are not supported by lower scores on standard
language measures, demonstrating insucient sensitivity of those tests (Brownsett
et al., 2019; Satoer et al., 2012).
For instance, Satoer et al. (2012) compared scores on the Aphasia Severity Rating Scale
(ASRS; Goodglass et al., 2001) to the self-reported problems and found that more patients
reported issues in daily communication than were shown to have impairments based on
the ASRS (57% vs. 39%, respectively). This shows the value of combining standardised
tests with an evaluation of self-reported complaints in the assessment of cognitive
abilities of glioma patients (Taphoorn & Klein, 2004).
A potential reason for the discrepancy between subjectively experienced language
diculties and objective test performance, is that aphasia assessments are generally
designed for patients who suered a stroke. Glioma patients, with comparable lesion
2S. MOOIJMAN ET AL.
size and location, typically have milder language and/or cognitive decits (Anderson et al.,
1990). These mild impairments can be the result of neural reorganisation (i.e., compensa-
tion for loss of function) due to the slow growth rate of gliomas as compared to the
sudden onset of neurological damage caused by stroke (Duau, 2008, 2014). The subtlety
of cognitive-linguistic impairments in glioma patients poses a problem for the assessment
of their cognitive functions.
Processing speed
Including a measure of response speed in the assessment of glioma patients may increase
sensitivity of standard measures and provide a way to objectively measure self-reported
word-nding problems. Language processing in patients with a glioma was investigated
by Moritz-Gasser et al. (2012), who studied the correlation between naming capacities and
the ability to return to work after surgery. They found that naming speed, rather than
accuracy, signicantly predicted return to work, an important marker for quality of life.
Importantly, none of the patients in their study was classied as “aphasic” according to
the Boston Diagnostic Aphasia Examination (BDAE; Goodglass & Kaplan, 1972), a test
battery originally designed for stroke patients. Another recent study has shown that
patients with gliomas are signicantly slower on a speeded naming test compared to
healthy participants (Ras et al., 2020). This dierence could not be explained by naming
ability measured with the Boston Naming Test (BNT; Kaplan et al., 2001).
As for non-verbal processing speed, previous studies have shown that glioma patients
performed signicantly worse than a healthy control group (Habets et al., 2014; Wefel
et al., 2016). Interestingly, it even appeared to be the most-often impaired cognitive ability
in this patient group (Ek et al., 2010). These studies typically operationalise non-verbal
processing speed with a Symbol Digit Modalities Test (Smith, 1973) or the Trail Making
Test Part A (TMT-A; Army Individual Test Battery, 1944).
Including an assessment of processing speed may not only increase the sensitivity of
measures, but may also bear a direct relationship with communicative diculties experi-
enced by patients in everyday conversations. Everyday communication requires the
conversational partners to process information quickly and respond to it in an appropriate
manner, and speedy processing of linguistic information is crucial (e.g., Carragher et al.,
2012). Subjectively experienced word-nding problems may therefore be the result of not
only a lexical retrieval problem, but may also be due to slowed processing.
Domain generality of processing speed
The nding that patients with a glioma are slower on both linguistic (Moritz-Gasser et al.,
2012; Ras et al., 2020) and non-linguistic tasks (Ek et al., 2010; Habets et al., 2014; Wefel
et al., 2016), raises the question whether slowed performance of a language test is specic
to language processing, or whether it has a more domain-general origin. This topic has
been investigated in people with aphasia due to stroke. For example, individuals with
aphasia (and individuals with left-hemispheric lesions without aphasia) were found to have
lower processing speed both within and outside the language domain (Yoo et al., 2021).
APHASIOLOGY 3
Moritz-Gasser et al. (2012) and Ras et al. (2020), on the other hand, found that naming
speed of patients with a glioma could not be explained by non-verbal processing speed
measured with the TMT-A. Their ndings suggest that there is a discrepancy between naming
accuracy, naming speed, and general processing speed. However, these two studies investi-
gated processing speed in the production of language, leaving receptive linguistic processing
speed of patients with a glioma open for investigation. It is not self-evident that the inuence
of processing speed is the same in both language modalities, as a discrepancy between
decits in language production and reception has been described (De Witte et al., 2015b).
From this discussion of the literature it has become clear that the subjectively experi-
enced communication diculties are not always supported by impaired performance on
standard language measures. Measuring processing speed may be useful in objectively
assessing subjectively experienced word-nding problems, not only because information
processing speed has often been found to be impaired in patients with a glioma, but also
because everyday communication relies on speeded integration of linguistic information.
Problems in everyday communication may therefore be the result of slower linguistic or
non-linguistic processing abilities.
Present study
We aim to investigate whether including a measure of response speed in a receptive
language test is a sensitive measure for self-reported word-nding problems in patients
with a glioma. The presence of self-reported word-nding problems was correlated with
lexical retrieval, receptive linguistic processing speed, and non-verbal cognitive abilities.
We compared a group of patients with a glioma to a group of age- and education-
matched healthy control participants. Individual patients were also described and com-
pared to norm groups. The following research questions were investigated:
RQ1: To what extent can self-reported word-nding problems of patients with gliomas be
explained by:
i. Lexical retrieval as measured with the Boston Naming Test or performance on a Token
Test?
ii. Linguistic processing speed as measured with a time-pressured sentence judgment test?
iii. Non-verbal cognitive abilities as measured with the Trail Making Test A and B?
RQ2: Is linguistic processing speed of patients with gliomas related to non-linguistic cognitive
abilities?
Based on previous ndings in the literature, we hypothesised a discrepancy between the
subjectively experienced word-nding problems and the objectively measured abilities of
patients (Brownsett et al., 2019; Satoer et al., 2012). The addition of reaction time measures to
a sentence judgment test is expected to lead to a sensitive measure that can explain
anamnestic complaints (Moritz-Gasser et al., 2012; Ras et al., 2020). Finally, if the word-
4S. MOOIJMAN ET AL.
nding problems and slower language processing are the result of a more global cognitive
impairment, we expect that patients will also exhibit longer reaction times on a non-linguistic
task.
Methods
Participants
The study group consists of glioma patients (N = 50) who have undergone awake
surgery (between March 2015 and November 2017) at the Erasmus MC University
Medical Centre. All patients diagnosed with a glioma, regardless of the hemispheric
localisation, were included in the study, as previous research has shown that patients
with a glioma in the right hemisphere may also experience language diculties
(Vilasboas et al., 2017; De Witte et al., 2015c). Fourteen patients were excluded due to
a recurrent tumour with second or third surgery (N = 10)
1
; too many missing data
(N = 2); or co-occurring developmental dyslexia (N = 1) or Noonan Syndrome (N = 1).
This resulted in 36 participants in the patient group. All patients were native speakers of
Dutch.
Healthy native speakers of Dutch (N = 35) constituted the control group of the study.
They were matched to the patient group on age and education but not on gender, as
gender has generally not been shown to inuence performance on standard language
tests (e.g., Snitz et al., 2009; De Witte et al., 2015b). They were included if they had no
(history of) cardiovascular, neurological, psychiatric, or developmental language disor-
ders; no toxic substance abuse; normal vision and hearing; no sleep medication, psycho-
tropic, or neuroleptic drugs. The demographic information of the patients and control
participants is given in Table 1. None of the participants was nancially compensated for
his/her participation. The Ethical Committee of the Erasmus MC approved of the study
and all participants gave their informed consent.
Materials
Word-finding problems
Information on word-nding problems in patients was based on complaints reported
during the preoperative anamnesis. The information in the anamnesis is gathered in an
interview with the patient by a clinical linguist, using a standard set of questions about
encountered problems with language, memory, attention, and executive functioning. The
word-nding complaints were labelled as follows: 0: no complaints; 1: mild complaints, if
the patients only reported diculties after more targeted questions, if they indicate that
they “sometimes” experience problems, or if their partner reported word-nding dicul-
ties; 2: clear complaints, if the patient presented their word-nding complaints centrally in
the anamnesis, or with modiers such as “often”, or “severe”. The same coder re-coded the
data at a later timepoint and the intra-coder reliability was assessed using an intra-class
correlation analysis. The intra-class correlation estimate was based on a single-rating,
absolute-agreement, two-way mixed-eects model. The results show that agreement
between these two timepoints was good-excellent (intraclass correlation coecient = .89,
p < .001).
APHASIOLOGY 5
An example of a mild complaint
“Patient does not report cognitive problems. After additional questions, he reports subtle
word-nding diculties. Handwriting is also a bit messier.”
An example of a clear complaint
“Patient reports word-nding diculties that result in avoiding talking to people. Word is in
mind but cannot be pronounced. Patient also fails in writing and typing. In addition, there are
sound changes, and articles and function words that are forgotten.”
Standard language tests
The Boston Naming Test (BNT; Kaplan et al., 2001), a standard test to assess anomia in
individuals with aphasia was administered. Patients also completed the shortened Token
Test (TT; De Renzi & Faglioni, 1978), a standard test to measure aphasia severity.
Linguistic processing speed
The Sentence judgment Test (SJT), a subtest of the Diagnostic Instrument for Mild Aphasia
(DIMA; Satoer et al., 2021), was used to test comprehension and language processing on
the semantic, syntactic, and phonological level. The SJT was administered in E-Prime
Table 1. Demographic and tumour characteristics. Education level based on Verhage (1964): Dutch
classification system including 7 categories. 1: did not finish primary school, 2: finished primary school, 3:
did not finish secondary school, 4: finished secondary school, low level, 5: finished secondary school,
medium level, 6: finished secondary school, highest level, and/or college degree, 7: university degree).
Demographic characteristics for patients and control participants
Group Patients Control participants
Gender Female 12 20
Male 24 15
Mean age (range) 45.37 (18–73) 42.75 (19–61)
Mean education (range) 5.36 (3–7) 5.53 (3–7)
Handedness Right 28 N/A
Left 8 N/A
Tumour characteristics for 36 patients
Variable Count (%)
Hemispheric lateralisation Left hemisphere 24 (67)
Right hemisphere 12 (33)
Tumour localisation: lobe Frontal 19 (53)
Temporal 7 (19)
Insular 1 (3)
Parietal 3 (8)
Frontoparietal 2 (6)
Parietotemporal 1 (3)
Temporoparietal 1 (3)
Frontotemporal 2 (6)
Tumour histological type Astrocytoma 13 (36)
Oligodendroglioma 12 (33)
Glioblastoma 10 (28)
Xanthoastrocytoma 1 (3)
Tumour grade (WHO classification) Grade I 1 (3)
Grade II 20 (56)
Grade II 5 (14)
Grade IV 10 (26)
6S. MOOIJMAN ET AL.
software (Psychology Software Tools, 2012) or in Praat (Boersma & Weenink, 2018). The
SJT consists of 30 sentences, half of which contain errors in three dierent linguistic
domains. The phonological items aim to assess phonological awareness by including
pseudo-words (Example 1). The syntactic items contain errors in verb inection (tense and
agreement), word order, or pronouns (Example 2), and the semantic items include
sentences with semantic anomalies (Example 3).
Example 1 De zanper koopt een blando.
The zanper buy-AGR a blando
“The zanper buys a blando”.
Example 2 Linda zingt gisteren een lied.
Linda sing-AGR.PRES yesterday a song
“Linda sings a song yesterday”.
Example 3 De loodgieter repareert de regenboog.
The plumber repair-AGR the rainbow
“The plumber repairs the rainbow”.
The participants read the sentences on a computer screen and rated their correct-
ness by pressing the keys “F” for fout “wrong” and “J” for juist “right” on the
keyboard. Reaction times (RTs) in milliseconds and accuracy were measured. RTs
were operationalised as the time between the start of the stimulus presentation
and the manual response of the participant. Items were presented in randomised
order, and the test contained four practice items to familiarise participants with the
procedure.
Non-language tests
Nonverbal cognitive abilities of the participants were assessed using the Trail Making
Test A and B (TMT-A and -B; Army Individual Test Battery, 1944). In the TMT-A, the
participant connects numbers (1–25) in an ascending order on a paper sheet. The
TMT-B requires the participant to connect alternating numbers and letters (i.e.,
1-A-2-B-3 etc.). The score on both tasks consists of the time in seconds it takes to
nish. Visuoperceptual speed underlies performance on the TMT-A, while TMT-B
relies more heavily on updating and concept-shifting abilities (Sánchez-Cubillo
et al., 2009). The dierence score TMT-BA, operationalised as the ratio score B:A,
provides a relatively pure measure of cognitive exibility.
Procedure
The clinical sta at the Erasmus MC University Medical Centre collected the data of
the patients. An elaborate neuro-linguistic test protocol was administered as part of
the standard clinical work-up, and the tests we report on in the present study are
part of this protocol. The results of the preoperative assessment were compared to
APHASIOLOGY 7
the performance of healthy control participants, who were tested in a private setting.
The BNT, SJT, and TMT were administered in a random order. The entire procedure
lasted approximately 15 minutes.
Data analysis
All statistical analyses were carried out in R (R Core Team, 2019) and the graphics were
created using R-package ggplot2 (Wickham, 2016). The results on the SJT, TMT, TT, and BNT
constitute the dependent variables. The data were analysed using regression models in the
R package lme4 (Bates et al., 2015) and lmerTest (Kuznetsova et al., 2017) to retrieve p-values.
The accuracy scores and RTs of the SJT were analysed with a (generalised) linear mixed-
eects regression model with random slopes for participants and items. The outcomes of
the TMT, TT, and BNT were analysed using a linear regression model. The scores on the TMT
were log-transformed to meet the model criteria. We adhered to an α-level of 0.05.
The main predictor in each model was group (patients vs. control participants), and
covariates age and education level were included in all models. Within the patient group,
the eects of tumour grade (LGG vs. HGG) and hemisphere (left vs. right) and the interac-
tion eect between these factors were estimated. The output of the statistical models is
included in the Appendix.
The analysis of the SJT results was carried out with the anomalous sentences.
2
Linguistic levels (semantics, syntax, phonology) and trial-by-trial sequence (i.e., the position
of each item in the test) were included as additional within-participant predictors. We
removed outliers before the group analysis of the RTs of the SJT. Items with an RT below
500 milliseconds were removed as it is assumed that participants need at least 500
milliseconds to properly assess an item, so shorter RTs are likely due to slips of attention.
In addition, items with an RT above 10 seconds were removed, as the E-Prime experiment
included a time limit and any responses longer than 10 seconds were classied as null
responses. This led to the exclusion of 13 trials (0.7%). Thereafter, outliers per participant
were calculated and removed from the dataset using the trimr package (Grange, 2015). An
outlier was dened as an RT value of 2 SD above or below the mean for each participant.
This led to the exclusion of 87 trials (5%). The remainder of the RTs were log transformed
to normalise the data and meet the model criteria. The log-transformed RTs provided
a good t for the raw data = .96, p < .001).
To estimate the relationship between the anamnestic complaints and the scores on the
objective measures, the correlation between these measures was calculated using
Pearson’s correlation coecient.
Results
Lexical retrieval
The results at the individual patient level are presented in Table 2. Preoperatively, 15 out
of 36 patients (42%) did not report any word-nding diculties. Twenty-one patients
(58%) reported word-nding problems of which twelve patients (33%) reported mild
word-nding problems, and nine patients (25%) reported serious word-nding problems.
Tumour grade did not signicantly inuence the experienced word-nding problems
8S. MOOIJMAN ET AL.
Table 2. Individual patient scores. Table legend: PP; participant number, Age; age in years at time of assessment, Edu; education level based on Verhage (1964),
Sex; male (M) or female (F), Hand; handedness left (L) or right (R), Grade; tumour grade from I–IV based on WHO classification, Location; location of the tumour: left
(L) or right (R) hemisphere followed by lobe, WFP; word-finding problems, BNT; score on Boston Naming Test, TT; score on shortened Token Test, TMT-A; score
(sec) on Trail Making Test-A, TMT-B; score (sec) on Trial Making Test-B, TMT-BA; ratio of difference score TMT part A and B, SJT; reaction times (ms) and accuracy
scores on the Sentence Judgment Test. Deviant scores marked in bold.
PP Age Edu Sex Hand Grade Location WFP BNT TT TMT-A TMT-B TMT-BA SJT
Semantics Syntax Phonology Accuracy
118 6 M L I L Frontal No 58 36 21 38 1.8 1759 2459 1824 15
221 5 M R III L Fronto-parietal Mild 45 34 41 100 2.4 3313 4473 2842 12
323 5 F R II L Frontal Clear 56 36 28 64 2.3
423 6 M R IV L Frontal No 48 36 17 33 1.9 1723 2088 1333 15
532 5 F L III L Fronto-temporal Clear 49 31 55 174 3.2
632 5 M R III R Parietal No 51 28 29 80 2.8
733 4 M R II R Frontal Mild 44 34 37 108 2.9 2696 4035 2827 14
834 5 M L II L Frontal No 48 33 29 58 2.0
936 7 M R II R Frontal Mild 58 34 24 34 1.4 1479 1576 1327 15
10 36 5 M R II L Frontal Clear 54 33 34 84 2.5 6695 5977 4228 11
11 36 6 M R IV L Temporo-parietal Clear 54 35 19 46 2.4 3647 3012 1491 15
12 42 5 F L IV L Temporal Clear 34 25 46 127 2.8 3163 4300 2991 15
13 42 5 F R IV L Frontal No 38 34 23 84 3.7 3648 2660 2707 13
14 42 7 M R III R Parieto-temporal Mild 57 35 22 48 2.2 2404 2421 1441 11
15 43 5 F R II R Frontal No 52 34 17 56 3.3 1578 2180 1142 15
16 45 5 M R II R Fronto-parietal Clear 56 36 24 87 3.6
17 46 6 M L III L Frontal Mild 50 36 18 40 2.2 2468 4789 2271 14
18 47 3 F R II L Frontal No 48 35 30 103 3.4
19 47 5 M R II R Temporal Mild 2898 2597 2211 12
20 48 5 M R II R Frontal No 49 33 41 52 1.3 2309 3157 1405 14
21 49 6 F L IV L Frontal No 56 30 27 62 2.3
22 49 5 F R II R Temporal No 54 35 31 60 1.9 2506 3582 1599 14
23 50 7 M R II R Frontal No 59 35 14 38 2.7 1596 2408 1404 15
24 51 5 F R II L Parietal Mild 35 35 21 34 1.6
25 51 6 M R II L Insular Clear 48 35 33 52 1.6
26 51 7 M R II L Frontal No 58 36 19 34 1.8
27 52 5 M R II L Temporal Mild 54 29 80 2.8
28 53 4 M L II L Parietal No 34 33 35 79 2.3
29 54 5 F R IV L Temporal Mild 44
30 57 5 M R II R Frontal Mild 36 36 42 56 1.3 2210 2683 1853 13
31 59 6 M R II R Fronto-temporal No 53 36 15 49 3.3 2586 2152 2774 13
(Continued)
APHASIOLOGY 9
Table 2. (Continued).
PP Age Edu Sex Hand Grade Location WFP BNT TT TMT-A TMT-B TMT-BA SJT
Semantics Syntax Phonology Accuracy
32 62 5 F R II L Temporal Mild 55 17 37 2.2 1414 2097 1103 12
33 63 5 M R IV L Frontal Mild 53 35 3329 3614 3225 13
34 66 5 M R IV L Frontal No 32 53 106 2.0
35 69 6 F L IV L Temporal Clear 20 32.5 38 199 5.2
36 73 6 M R IV L Frontal Clear 54 35 48 318 6.6 5595 6030 4928 14
10 S. MOOIJMAN ET AL.
(ß = −0.26, SE = 0.34, p = .45), neither did the hemispheric localisation (ß = 0.58, SE = 0.62,
p = .36). There was no signicant interaction between grade and hemispheric localisation
(ß = 0.36, SE = 0.72, p = .62).
At the group level, patients (M = 48.9, 82%) deviated from the control participants
(M = 52.9, 88%) on the BNT (ß = 3.54, SE = 1.62, p = .03). The patients’ BNT scores were not
signicantly inuenced by tumour grade = 4.41, SE = 3.71, p = .24), hemispheric
localisation = 8.57, SE = 6.78, p = .22), or an interaction between these factors
= −7.23, SE = 7.87, p = .37). The experienced word-nding problems were not always
accompanied by deviant scores on the BNT and these outcomes were not correlated
= −.15, p = .40). Of the patients who reported word-nding diculties, one did not
perform the BNT. Ten out of the remaining twenty patients with reported word-nding
problems (50%) also showed deviant scores on the BNT.
The scores on the shortened Token Test did not correlate with the reported word-
nding diculties (ρ = −.07, p = .71). The mean score of the patient group was 33.8 out of
36 points. Adhering to the cut-o score of 29 (De Renzi & Faglioni, 1978), only one patient
showed a deviant score on the Token Test. The Token Test scores were not signicantly
inuenced by tumour grade = 1.79, SE = 1.08, p = .11), or hemispheric localisation
= −1.38, SE = 1.86, p = .47). And there was no signicant interaction eect between
these variables (ß = 1.43, SE = 2.19, p = .52).
Linguistic processing speed
At the group level, there were no signicant dierences for RTs between patients and
control participants (ß = −0.02, SE = 0.08, p = .84), but the dierence between the two
groups on accuracy scores in all linguistic domains combined was signicant = 1.16,
SE = 0.41, p = .01). The dierences between the groups are presented in Figure 1. Tumour
grade, hemispheric localisation, or the interaction between these factors, did not signi-
cantly aect RTs nor accuracy scores. The reported word-nding problems were strongly
correlated with the RTs on the SJT averaged over all linguistic domains (ρ = .64, p < .01),
and with each linguistic level separately (syntax: ρ = .61, p = .003; semantics: ρ = .64,
p = .002; phonology: ρ = .55, p = .01). However, the word-nding complaints did not
correlate signicantly with the accuracy scores on the SJT over all linguistic domains
(ρ = −.23, p = .31).
At the individual patient level, it appears that there is a subgroup of patients with
deviant RTs in the SJT compared to normative data (Satoer et al., 2021). Six out of twenty-
one (29%) patients had slightly deviant RTs (≥1.5 SD from population mean) in at least one
of the three linguistic domains (phonology, semantics, syntax). All six patients with
deviant RTs on the SJT had a glioma in the left hemisphere, and all but one (83%) in
the frontal lobe. One patient (17%) had a grade-II glioma, two patients (33%) a grade-III
glioma, and three patients (50%) had a grade-IV glioma. Eight out of twenty-one (38%)
patients showed deviant accuracy scores on the SJT. Nine out of 35 control participants
(26%) had deviant RTs on one of the language domains of the SJT, and two control
participants (6%) showed deviant accuracy scores.
APHASIOLOGY 11
Non-verbal cognitive measures
At the group level, there was no statistically signicant dierence between the patient
group and the control group on the TMT-A and B (ß = 0.08, SE = 0.08, p = .30 for TMT-A
and ß = 0.13, SE = 0.09, p = .16 for TMT-B). However, patients had a larger dierence score
on the TMT-BA compared to healthy participants = 0.56, SE = 0.19, p = .004). The
dierences between the groups are presented in Figure 2. Within the patient group,
patients with an HGG were slower to nish the TMT-B (ß = −0.51, SE = 0.22, p = .03) and
had a larger ratio score on TMT-BA (ß = −0.96, SE = 0.45, p = .04) compared to patients
with an LGG. This was not the case for the TMT-A (ß = −0.22, SE = 0.16, p = .17). There were
no signicant main eects of hemispheric localisation or interaction eects between
these factors on any of the TMTs.
Figure 1. Reaction times (in milliseconds) and accuracy (percentage correct) on the SJT for healthy
control participants (HC) and patients (PT) and per linguistic domain. Error bars represent the standard
error.
12 S. MOOIJMAN ET AL.
In the patient group, performance speed on the TMT-A and -B strongly correlated with
the RTs on the SJT (ρ = .61, p = .01 for TMT-A and ρ = .74, p < .001 for TMT-B), indicating
that longer RTs on the SJT were accompanied by longer completion time on the TMT-A
and -B. The ratio of the dierence score TMT-BA also correlated moderately with the RTs
on the SJT = .59, p = .01), indicating a shifting component in the SJT independent of
speed. Interestingly, in the control group signicant correlations between the RTs on the
SJT and the TMT-A and -B were absent (ρ = .20, p = .256 and ρ = .10, p = .58, respectively).
In the control participants, the ratio score of the dierence TMT-BA also did not correlate
signicantly with the RTs on the SJT (ρ = −.07, p = .682). These correlations are presented
in Figure 3.
There was a weak but signicant correlation between the reported word-nding pro-
blems and the TMT-B (ρ = .44, p = .01) and a marginally signicant correlation between the
word-nding problems and the TMT-A (ρ = .34, p = .052). The correlation between word-
Figure 2. Scores (in seconds) on the TMT-A and TMT-B and ratio scores on TMT-BA per participant
group. Error bars represent the standard error.
APHASIOLOGY 13
nding problems and the TMT-BA was not signicant (ρ = .32, p = .07). Model comparison
showed that the linear regression model with only the RTs in the SJT as a predictor (and no
TMT measure) yielded the best t for the word-nding problems (Figure 4).
Eleven out of 33 patients (33%) had an impaired score on at least one of the
subcomponents of the TMT (Tombaugh, 2004). Three patients (9%) scored >1.5 SD
from the normal score on both the TMT-A and B. Three patients (9%) had problems
with the TMT-B and a deviant dierence score TMT-BA (cut-o ratio score >3,
Arbuthnott and Frank, 2000). Five out of 33 patients (15%) had a selective problem
with concept shifting (cognitive exibility), exemplied by a deviant dierence score
TMT-BA.
Figure 3. Correlations between the reaction times (milliseconds) on the SJT and the TMT-A (A), TMT-B
(B), and TMT-BA (C).
14 S. MOOIJMAN ET AL.
Discussion
Linguistic processing speed and word-nding complaints
We aimed to examine whether assessment of processing speed in a receptive language
test would provide a sensitive measure to objectively determine reported language
problems, and whether it is related to non-verbal processing speed. First, we showed
that 58% of glioma patients experience word-nding diculties in daily life, but that their
reported problems were supported by deviant BNT scores in only 50% of the cases. The
reported word-nding problems also did not correlate with the accuracy scores on the
SJT. The Token Test proved to be insensitive to detect language problems in this patient
group; only one patient scored below the cut-o level and the scores were not correlated
with the reported word-nding problems. At the group level, however, glioma patients
scored signicantly worse on the BNT and had worse accuracy scores on the SJT com-
pared to the control group.
The discrepancy between reported language complaints and scores on objective
language measures has been described in previous research (Satoer et al., 2012). In
addition, there is evidence that impaired linguistic variables found in spontaneous speech
Figure 4. Visualisation of linear regression model of the reported severity of word-finding problems
predicted by the reaction times (milliseconds) on the SJT.
APHASIOLOGY 15
of glioma patients do not correlate with performance on standardised language tests
(Satoer et al., 2018, 2013). At the same time, Brownsett et al. (2019) found that after
surgery, 58% of glioma patients reported communication diculties, which did not
correspond with the Aphasia Quotient of the Western Aphasia Battery-Revised (Kertesz,
2006, 27% of patients scoring below normal cut-o), but could be explained with the
scores on the Comprehensive Aphasia Test (Swinburn et al., 2004, 77% of patients scoring
below normal cut-o). The inconsistency between the BNT scores and the language
complaints we found in the current study could indicate that the word-nding problems
originate from an issue other than a pure lexical retrieval decit.
We investigated the relationship between the reported complaints and linguistic
processing speed. Previously, productive language tasks with a time constraint have
been reported to be dicult for glioma patients, illustrated by longer response times
on naming tasks (Moritz-Gasser et al., 2012; Ras et al., 2020). In contrast to our expecta-
tions, the results of the current study did not show deviant group-level performance on
the RT measure of the SJT, which assesses speed of receptive language processing.
However, glioma patients had signicantly lower accuracy scores compared to the control
group. This could be due to a deviant speed/accuracy trade-o, in which higher response
speed is favoured over accurate responding.
In a subsequent analysis, we looked at the individual RT scores in the SJT and found
that all patients with long RTs had a glioma in the language-dominant hemisphere, mostly
in the frontal lobe. This seems to suggest that assessing speed of language processing in
patients with left frontal damage may be particularly useful, although data from more
patients is necessary to further investigate this observation.
In contrast to the absence of a signicant correlation between the word-nding
problems and BNT and accuracy scores, more severe word-nding complaints were
accompanied by longer RTs on the SJT. We found that the presence of word-nding
problems was signicantly correlated with the overall RTs in the SJT, but also with each
linguistic level separately. The commonalities between the dierent linguistic levels may
point to a shared underlying attentional component required to perform this task. This is
in accordance with the nding that the reported complaints also correlated with perfor-
mance of the TMT. Although the TMT is not a perfectly matched non-verbal equivalent of
the linguistic processing speed task, it provides a measure of visuoperceptual speed and
relies on attention. Therefore, our ndings could imply that domain-general attentional
mechanisms underlie experienced word-nding problems. This aligns with previous
research in which attentional decits were observed in persons with self-reported mild
anomia, who performed within normal limits on standard language assessments
(Hunting-Pompon et al., 2011).
At the same time, it must be noted that the observed correlations between reported
word-nding problems and the TMT were weaker than the correlations with the SJT.
A model with linguistic processing speed as a sole predictor best t the word-nding
complaints of the patients, compared to models also including scores on the TMT as
predictors. This indicates that, despite an important role for more domain-general proces-
sing abilities in lexical retrieval, there appears to be an indispensable linguistic factor to
word-retrieval diculties.
16 S. MOOIJMAN ET AL.
The word-nding problems may be the most salient issue that glioma patients experi-
ence in everyday communication. Dialogues require conversational partners to process
verbal information quickly and respond to it promptly in an appropriate manner. This
entails the integration of a range of dierent abilities, which may be challenging for
individuals with aphasia. For example, they have been shown to experience more di-
culties with language production on a story retelling task, when they have to perform
another task simultaneously (Harmon et al., 2019). Apart from linguistically meaningful
and grammatically correct output, other cognitive functions, attention and executive
functioning in particular, have been shown to play a crucial role in the successful everyday
communication of aphasic speakers (Fridriksson et al., 2006; Olsson et al., 2019). This may
be an explanation for the relationship between word-nding complaints and slower
processing of both linguistic and non-linguistic tasks. Given the characteristics of func-
tional communication, their experienced word-nding problems could be the result of
slowed processing rather than lost function.
Underlying mechanism of linguistic processing speed
The signicant correlation between performance of the TMT and the presence of reported
word-nding diculties could imply that there is a domain-general attentional basis for the
experienced language diculties. This is corroborated by the signicant correlation
between RTs on the language task (SJT) and performance on the non-verbal tasks (TMT-
A and B), indicating that longer completion time on the TMT co-occurred with longer
reaction times on the SJT. The cognitive abilities known to underlie performance speed on
the TMT are visuoperceptual speed (TMT-A and -B) and concept shifting (TMT-B and -BA).
Remarkably, a signicant correlation only existed in the patient group and was absent
in the control group. This suggests that linguistic and non-linguistic functions are more
heavily interconnected in glioma patients as compared to healthy participants. In addi-
tion, the contribution of domain-general abilities in performing language tasks could
explain why the outcomes on the BNT and SJT were not inuenced by hemispheric
tumour localisation. If patients recruit domain-general cognitive abilities to perform
language tasks, lesions in the left or right hemisphere may lead to impairments.
These results show that the receptive linguistic processing speed partially constitutes
a more general cognitive speed. This is in accordance with the literature on persons with
aphasia due to stroke. For example, Yoo et al. (2021) found that persons with aphasia
show domain-general cognitive slowing, as indicated by slower processing speed on
linguistic and non-linguistic tasks. However, our nding is in contrast with Ras et al.’s
(2020) and Moritz-Gasser et al.’s (2012) results for patients with a glioma, who did not nd
a signicant correlation between the RTs on a rapid naming test and overall processing
speed measured with the TMT-A.
One potential explanation for this discrepancy lies in the dierence between modalities of
the used language tests. In the present study, we measured receptive reading abilities,
whereas Ras et al. and Moritz-Gasser et al. administered a speeded naming test, assessing
language production in a more isolated manner. As Sánchez-Cubillo et al. (2009) noted, the
TMT-A mainly relies on visual search and perceptual speed. Therefore, a comparison between
a reading task such as the SJT (both perceptual and visual) and the TMT-A may result in
stronger relationships than with a naming task. Importantly, Moritz-Gasser et al. did nd
APHASIOLOGY 17
naming speed to be highly correlated with executive tasks that require lexical access (uency
and the Stroop test), and argue that the decreased naming speed, in absence of impaired
naming accuracy, is due to the cognitive functions involved in language processing.
We found that linguistic processing speed was correlated with the ratio score of the
TMT-BA, a measure of concept shifting. This could be because multiple linguistic levels are
combined in the SJT. The participants assessed correct sentences and sentences that
contain a semantic, syntactic, or phonological error. The correct and incorrect items are
presented in a randomised order. It could thus be argued that there is constant task
switching within the SJT, placing a higher demand on cognitive exibility (Rubinstein
et al., 2001) and explaining the signicant correlation with the ratio score of the TMT-BA.
Combining various tests and presenting them in a rapidly alternating way has previously
been shown to be a good way to assess brain tumour patients (De Witte et al., 2015b). The
SJT requires the participant to simultaneously integrate various processes, such as sen-
tence processing, sentence evaluation, and task switching.
Limitations of the present study
A rst limitation is that there was missing information on the language lateralisation via
fMRI for the left-handed patients (N = 8). All left-handed patients had a glioma in the left
hemisphere. Previous research has shown that while language lateralisation is more mixed,
the majority of non-right-handed people nevertheless show typical language lateralisation
in the left hemisphere (Szaarski et al., 2002). Secondly, we could not perform analysis on
the specic tumour location and its eects on linguistic and non-linguistic functions due to
small group sizes. This is an important direction for future work. Thirdly, although the
reported word-nding problems were coded twice at dierent timepoints, allowing for an
intra-coder reliability analysis, having multiple independent coders assess the complaints
would have further increased the reliability of the scoring. A fourth limitation is the task
choice of the present study. Considering that data collection took place in a clinical context,
we were bound by the tasks that are part of the standard clinical work-up. While the TMT
and SJT are good measures of visuoperceptual processing speed and linguistic processing
speed, respectively, and both tasks rely on attentional processes, the two tasks are not
perfectly matched verbal and non-verbal variants. A nal limitation of the study is that
a pure reading task was not part of the test protocol. Consequently, we could not verify
whether reading issues interfered with performance on the SJT. While this should be
addressed in future studies, previous research has shown that reading performance is
generally unaected in glioma patients (Satoer et al., 2014, 2012).
Clinical implications and future directions
In clinical practice, demands for brevity generally compete with needs for sensitivity (e.g.,
Ek et al., 2010). Therefore, critical evaluation of the sensitivity of tests can guide the
selection of materials for a patient group. The SJT is part of the DIMA (Satoer et al., 2021),
which is designed to be both short and sensitive enough to detect mild language
diculties in patients with neurological diseases. The nding that deviant RTs in the SJT
were most often observed in glioma patients with a lesion in the frontal lobes of the
dominant hemisphere suggests that the task may be particularly suitable for this patient
18 S. MOOIJMAN ET AL.
group. This is in accordance with De Witte et al. (2015b) who also suggest the adminis-
tration of sentence judgment tests in patients with gliomas in the frontal and temporal
(sub)cortical areas. Including measures of RTs, as was done for the SJT in the DIMA, could
further increase the value of such judgment tests.
The nding that, despite a signicant correlation between the TMT and the RTs on the
SJT, not all patients with deviant scores on the SJT show impaired performance on the TMT
(or vice versa) is an indication that both tests are necessary for a reliable interpretation of
cognitive functioning. Additionally, considering that at the group level, patients do not
show signicantly lower processing speed than healthy control participants, demonstrates
the need for elaborate anamnesis and assessment tailored to the individual patient.
Our results imply that administering the SJT could be benecial for patients who report
word-nding problems, but do not show deviant scores on Token tests or standard naming
tests. Assessing linguistic processing speed provides a way to objectively assess these
complaints. The nding that word-nding problems were signicantly, but weakly correlated
with the TMT-A and B, shows that lexical retrieval has a general processing speed
component but cannot be fully explained by this. This is an important observation that
deserves attention in the clinical setting. Clinicians could try to gain additional information
on the distinction between delayed and failed lexical access by administering a naming test
under time pressure. The anamnesis is another valuable source of information; clinicians
could ask patients more targeted questions about word retrieval. Patients dier in how they
present their complaints during the anamnesis, which emphasises the importance of asking
more thorough questions. Examples of such questions are whether dicult words surface
eventually or not at all, or whether there are specic circumstances (noisy environments,
time pressured conversations, etc.) under which word-nding problems are more prominent.
Finally, investigating the relationship between the performance of the SJT and non-
linguistic functions in populations with dierent neurological diseases, such as stroke or
traumatic brain injury, is a potential direction for future work. The result that response
speed of the SJT only correlates with visual search speed and concept shifting in the patient
group, and not in healthy participants, suggests that patients may recruit a wider network
to perform language tasks. It is interesting to see if similar relationships can be observed in
patients with other neurological impairments. Moreover, this nding can serve as a starting
point for therapy. Previous work on cognitive rehabilitation of glioma patients has found
that in-person training (Locke et al., 2008), and telerehabilitation (Van der Linden et al.,
2018) of cognitive functions is feasible and evaluated positively. Cognitive rehabilitation has
short-term positive eects on subjective cognitive functioning and longer-term objective
benets for attention and verbal memory (Gehring et al., 2009). However, detailed indivi-
dual assessment of the patient’s impairments should guide the choice of therapy.
Conclusions
This research studied the linguistic processing speed in glioma patients and investigated
whether these abilities could be a more sensitive measure to capture word-nding com-
plaints. We found that patients’ reported word-nding problems were not correlated with the
BNT, a well-known test to assess lexical retrieval diculties, nor with accuracy scores on the
SJT. However, the word-nding problems were correlated with linguistic processing speed,
operationalised as response speed in the SJT. At group-level, apart from patients with a glioma
APHASIOLOGY 19
in the frontal lobe of the dominant hemisphere, response speed of the SJT was not deviant in
glioma patients compared to the healthy control group. Furthermore, a relationship between
linguistic processing speed and non-verbal functioning was found in the glioma patients but
not in the healthy control group, suggesting that patients rely on more domain-general
abilities to perform the task. These results indicate that the SJT, a time-constrained task
assessing receptive language abilities, appears to be inuenced by non-verbal processing
speed, and that processing speed may contribute to subjectively experienced problems. This
demonstrates the importance of administering tasks that assess language as well as non-
verbal cognitive processing speed for the interpretation and dissociation of impairments.
Notes
1. Patients with a recurrent tumour are excluded because it is impossible to attribute their
preoperative impairments to the presence of the tumour alone, as their impairments may
also be the result of the previous surgery.
2. An analysis including both correct and incorrect target items showed that there was
a signicant main eect of correctness of the item on the reaction times across both groups
= 0.25, SE = 0.05, p < .001). Participants responded signicantly faster to anomalous
sentences than to correct target sentences.
Acknowledgments
We would like to thank two anonymous reviewers and Josje Verhagen for their invaluable input and
feedback on earlier versions of this manuscript. We are very grateful to all participants who took part in
this study.
Disclosure statement
No potential conict of interest was reported by the author(s).
ORCID
Saskia Mooijman http://orcid.org/0000-0001-5084-3362
Laura S. Bos http://orcid.org/0000-0002-5160-888X
Evy Visch-Brink http://orcid.org/0000-0001-7833-0112
Djaina Satoer http://orcid.org/0000-0002-5751-8113
References
Anderson, S. W., Damasio, H., & Tranel, D. (1990). Neuropsychological impairments associated with
lesions caused by tumor or stroke. Archives of Neurology, 47(4), 397–405. https://doi.org/10.1001/
archneur.1990.00530040039017
Arbuthnott, K., & Frank, J. (2000). Trail Making Test, Part B as a Measure of Executive Control:
Validation Using a Set-Switching Paradigm. Journal of Clinical and Experimental
Neuropsychology, 22(4), 518–528. https://doi.org/10.1076/1380-3395(200008)22:4;1-0;FT518
Army Individual Test Battery. (1944) . Trail Making Test. Manual of directions and scoring. War
Department, Adjutant General’s Oce.
Bates, D., Maechler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-eects models using lme4.
Journal of Statistical Software, 67(1), 1–48. https://doi.org/doi:10.18637/jss.v067.i01
20 S. MOOIJMAN ET AL.
Boersma, P., & Weenink, D. (2018). Praat: Doing phonetics by computer (Version 6.0.34) [Computer
software]. http://www.praat.org/
Brownsett, S. L. E., Ramajoo, K., Copland, D., McMahon, K. L., Robinson, G., Drummond, K.,
Jeree, R. L., Olson, S., Ong, B., & Zubicaray, G. D. (2019). Language decits following
dominant hemisphere tumour resection are signicantly underestimated by
syndrome-based aphasia assessments. Aphasiology, 33(10), 1163–1181. https://doi.org/10.
1080/02687038.2019.1614760
Carragher, M., Conroy, P., Sage, K., & Wilkinson, R. (2012). Can impairment-focused therapy change
the everyday conversations of people with aphasia? A review of the literature and future
directions. Aphasiology, 26(7), 895–916. https://doi.org/10.1080/02687038.2012.676164
Cruice, M., Worrall, L., & Hickson, L. (2006). Perspectives of quality of life by people with aphasia and
their family: Suggestions for successful living. Topics in Stroke Rehabilitation, 13(1), 14–24. https://
doi.org/10.1310/4JW5-7VG8-G6X3-1QVJ
De Renzi, E., & Faglioni, P. (1978). Normative data and screening power of a shortened version of the
Token Test. Cortex, 14(1), 41–49. https://doi.org/10.1016/S0010-9452(78)80006-9
De Witte, E., & Mariën, P. (2013). The neurolinguistic approach to awake surgery reviewed. Clinical
Neurology and Neurosurgery, 115(2), 127–145. https://doi.org/10.1016/j.clineuro.2012.09.015
De Witte, E., Satoer, D., Colle, H., Robert, E., Visch-Brink, E., & Mariën, P. (2015a). Subcortical language
and non-language mapping in awake brain surgery: The use of multimodal tests. Acta
Neurochirurgica, 157(4), 577–588. https://doi.org/10.1007/s00701-014-2317-0
De Witte, E., Satoer, D., Robert, E., Colle, H., Verheyen, S., Visch-Brink, E., & Mariën, P. (2015b). The
Dutch Linguistic Intraoperative Protocol: A valid linguistic approach to awake brain surgery. Brain
and Language, 140, 35–48. https://doi.org/10.1016/j.bandl.2014.10.011
De Witte, E., Satoer, D., Visch-Brink, E., & Mariën, P. (2015c). Cognitive outcome after awake surgery
for left and right hemisphere tumours [Conference presentation abstract]. Academy of Aphasia
53rd Annual Meeting, Tucson, AZ, United States. https://doi.org/10.3389/conf.
fpsyg.2015.65.00065
Duau, H. (2008). Brain plasticity and tumors. In J. D. Pickard, N. Akalan, C. Di Rocco, V. V. Dolenc, J. L.
Antunes, J. J. A. Mooij, J. Schramm, & M. Sindou (Eds.), Advances and Technical Standards in
Neurosurgery (pp. 3–33). Springer. https://doi.org/10.1007/978-3-211-72283-1_1
Duau, H. (2014). The huge plastic potential of adult brain and the role of connectomics: New
insights provided by serial mappings in glioma surgery. Cortex, 58, 325–337. https://doi.org/10.
1016/j.cortex.2013.08.005
Duau, H., & Capelle, L. (2004). Preferential brain locations of low-grade gliomas: Comparison with
glioblastomas and review of hypothesis. Cancer, 100(12), 2622–2626. https://doi.org/10.1002/
cncr.20297
Ek, L., Almkvist, O., Kristoersen Wiberg, M., Stragliotto, G., & Smits, A. (2010). Early cognitive
impairment in a subset of patients with presumed low-grade glioma. Neurocase, 16(6),
503–511. https://doi.org/10.1080/13554791003730634
Fridriksson, J., Nettles, C., Davis, M., Morrow, L., & Montgomery, A. (2006). Functional communication
and executive function in aphasia. Clinical Linguistics & Phonetics, 20(6), 401–410. https://doi.org/
10.1080/02699200500075781
Gehring, K., Sitskoorn, M. M., Gundy, C. M., Sikkes, S. A. M., Klein, M., Postma, T. J., van den Bent, M. J.,
Beute, G. N., Enting, R. H., Kappelle, A. C., Boogerd, W., Veninga, T., Twijnstra, A., Boerman, D. H.,
Taphoorn, M. J. B., & Aaronson, N. K. (2009). Cognitive rehabilitation in patients with gliomas:
A randomized, controlled trial. Journal of Clinical Oncology, 27(22), 3712–3722. https://doi.org/10.
1200/JCO.2008.20.5765
Gehring, K., Taphoorn, M. J. B., Sitskoorn, M. M., & Aaronson, N. K. (2015). Predictors of subjective
versus objective cognitive functioning in patients with stable grades II and III glioma. Neuro-
Oncology Practice, 2(1), 20–31. https://doi.org/10.1093/nop/npu035
Gerritsen, J. K. W., Arends, L., Klimek, M., Dirven, C. M. F., & Vincent, A. J. P. E. (2019). Impact of
intraoperative stimulation mapping on high-grade glioma surgery outcome: A meta-analysis.
Acta Neurochirurgica, 161(1), 99–107. https://doi.org/10.1007/s00701-018-3732-4
APHASIOLOGY 21
Goodglass, H., & Kaplan, E. (1972). Boston Diagnostic Aphasia Examination (BDAE) (2nd ed. ed.). Lea &
Febiger.
Goodglass, H., Kaplan, E., & Barresi, B. (2001). The assessment of aphasia and related disorders (2nd ed.
ed.). Lea & Febiger.
Grange, J. (2015). trimr: An implementation of common response time trimming methods (Version
1.0.1) [Computer software]. https://CRAN.R-project.org/package=trimr
Habets, E. J. J., Kloet, A., Walchenbach, R., Vecht, C. J., Klein, M., & Taphoorn, M. J. B. (2014). Tumour
and surgery eects on cognitive functioning in high-grade glioma patients. Acta Neurochirurgica,
156(8), 1451–1459. https://doi.org/10.1007/s00701-014-2115-8
Harmon, T. G., Jacks, A., Haley, K. L., & Bailliard, A. (2019). Dual-task eects on story retell for
participants with moderate, mild, or no aphasia: Quantitative and qualitative ndings. Journal
of Speech, Language, and Hearing Research, 62(6), 1890–1905. https://doi.org/10.1044/2019_
JSLHR-L-18-0399
Hunting-Pompon, R., Kendall, D., & Bacon Moore, A. (2011). Examining attention and cognitive
processing in participants with self-reported mild anomia. Aphasiology, 25(6–7), 800–812. https://
doi.org/10.1080/02687038.2010.542562
Ilmberger, J., Ruge, M., Kreth, F.-W., Briegel, J., Reulen, H.-J., & Tonn, J.-C. (2008). Intraoperative
mapping of language functions: A longitudinal neurolinguistic analysis. Journal of Neurosurgery,
109(4), 583–592. https://doi.org/10.3171/JNS/2008/109/10/0583
Kaplan, E., Goodglass, H., & Weintraub, S. (2001). Boston Naming Test (2nd ed. ed.). Pro-Ed.
Kertesz, A. (2006). Western Aphasia Battery. Pearson.
Kuznetsova, A., Brockho, F. B., & Christensen, R. H. B. (2017). lmerTest package: Tests in linear
mixed eects models. Journal of Statistical Software, 82(13), 1–26. https://doi.org/10.18637/jss.
v082.i13
Locke, D. E. C., Cerhan, J. H., Wu, W., Malec, J. F., Clark, M. M., Rummans, T. A., & Brown, P. D. (2008).
Cognitive rehabilitation and problem- solving to improve quality of life of patients with primary
brain tumors: A pilot study. The Journal of Supportive Oncology, 6(8), 383–391.
Moritz-Gasser, S., Herbet, G., Maldonado, I. L., & Duau, H. (2012). Lexical access speed is signicantly
correlated with the return to professional activities after awake surgery for low-grade gliomas.
Journal of Neuro-Oncology, 107(3), 633–641. https://doi.org/10.1007/s11060-011-0789-9
Olsson, C., Arvidsson, P., & Johansson, M. B. (2019). Relations between executive function, language,
and functional communication in severe aphasia. Aphasiology, 33(7), 821–845. https://doi.org/10.
1080/02687038.2019.1602813
Psychology Software Tools (2012). E-Prime 2.0. (Version 2.0.8.22) [Computer software].
R Core Team.(2019). R: A language and environment for statistical computing. R Foundation for
Statistical Computing. https://www.R-project.org/
Racine, C. A., Li, J., Molinaro, A. M., Butowski, N., & Berger, M. S. (2015). Neurocognitive function in
newly diagnosed low-grade glioma patients undergoing surgical resection with awake mapping
techniques. Neurosurgery, 77(3), 371–379. https://doi.org/10.1227/NEU.0000000000000779
Ras, P., Satoer, D., Rutten, G.-J. M., Vincent, A. J.-P. E., & Visch-Brink, E. (2020). Een sensitieve snelle
benoemtest voor woordvindproblemen bij patiënten met een laaggradig glioom. Stem-, Spraak-
En Taalpathologie, 25, 15–29. https://doi.org/10.21827/32.8310/2020-15
Rubinstein, J. S., Meyer, D. E., & Evans, J. E. (2001). Executive control of cognitive processes in task
switching. Journal of Experimental Psychology: Human Perception and Performance, 27(4),
763–797. https://doi.org/10.1037/0096-1523.27.4.763
Sanai, N., & Berger, M. S. (2008). Glioma extent of resection and its impact on patient outcome.
Neurosurgery, 62(4), 753–766. https://doi.org/10.1227/01.neu.0000318159.21731.cf
Sanai, N., & Berger, M. S. (2012). Recent surgical management of gliomas. In R.Yamanaka (Ed.),
Glioma (pp. 12–25). Springer.
Sánchez-Cubillo, I. 1., Periáñez, J. A., Adrover-Roig, D., Rodríguez-Sanchez, J. M., Ríos-Lago, M.,
Tirapu, J., & Barceló, F. (2009). Construct validity of the Trail Making Test: Role of task-switching,
working memory, inhibition/interference control, and visuomotor abilities. Journal of the
International Neuropsychological Society, 15(3), 438–450. https://doi.org/10.1017/
S1355617709090626
22 S. MOOIJMAN ET AL.
Satoer, D., De Witte, E., Bulte, B., Bastiaanse, R., Smits, M., Vincent, A., Mariën, P., & Visch-Brink, E.
(2021). Dutch Diagnostic Instrument for Mild Aphasia (DIMA-NL): Standardization and clinical
application. [Manuscript submitted for publication]. Department of Neurosurgery, Erasmus MC
University Medical Centre Rotterdam.
Satoer, D., Vincent, A., Ruhaak, L., Smits, M., Dirven, C., & Visch-Brink, E. (2018). Spontaneous speech
in patients with gliomas in eloquent areas: Evaluation until 1 year after surgery. Clinical Neurology
and Neurosurgery, 167, 112–116. https://doi.org/10.1016/j.clineuro.2018.02.018
Satoer, D., Vincent, A., Smits, M., Dirven, C., & Visch-Brink, E. (2013). Spontaneous speech of patients
with gliomas in eloquent areas before and early after surgery. Acta Neurochirurgica, 155(4),
685–692. https://doi.org/10.1007/s00701-013-1638-8
Satoer, D., Visch-Brink, E., Smits, M., Kloet, A., Looman, C., Dirven, C., & Vincent, A. (2014). Long-term
evaluation of cognition after glioma surgery in eloquent areas. Journal of Neuro-Oncology, 116(1),
153–160. https://doi.org/10.1007/s11060-013-1275-3
Satoer, D., Vork, J., Visch-Brink, E., Smits, M., Dirven, C., & Vincent, A. (2012). Cognitive functioning
early after surgery of gliomas in eloquent areas. Journal of Neurosurgery, 117(5), 831–838. https://
doi.org/10.3171/2012.7.JNS12263
Smith, A. (1973). Symbol digit modalities test. Western Psychological Services.
Snitz, B. E., Unverzagt, F. W., Chang, -C.-C. H., Vander Bilt, J., Gao, S., Saxton, J., Hall, K. S., & Ganguli, M.
(2009). Eects of age, gender, education and race on two tests of language ability in
community-based older adults. International Psychogeriatrics, 21(6), 1051–1062. https://dx.doi.
org/10.1017%2FS1041610209990214
Swinburn, K., Porter, G., & Howard, D. (2004). Comprehensive Aphasia Test. Taylor & Francis.
Szaarski, J. P., Binder, J. R., Possing, E. T., McKiernan, K. A., Ward, B. D., & Hammeke, T. A. (2002).
Language lateralization in left-handed and ambidextrous people: FMRI data. Neurology, 59(2),
238–244. https://doi.org/10.1212/WNL.59.2.238
Taphoorn, M. J. B., & Klein, M. (2004). Cognitive decits in adult patients with brain tumours. The
Lancet. Neurology, 3(3), 159–168. https://doi.org/10.1016/S1474-4422(04)00680-5
Tombaugh, T. N. (2004). Trail Making Test A and B: Normative data stratied by age and education.
Archives of Clinical Neuropsychology, 19(2), 203–214. https://doi.org/10.1016/S0887-6177(03)
00039-8
van der Linden, S. D., Gehring, K., De Baene, W., Emons, W. H. M., Rutten, G.-J. M., & Sitskoorn, M. M.
(2020). Assessment of executive functioning in patients with meningioma and low-grade glioma:
A comparison of self-report, proxy-report, and test performance. Journal of the International
Neuropsychological Society, 26(2), 187–196. https://doi.org/10.1017/S1355617719001164
van der Linden, S. D., Sitskoorn, M. M., Rutten, G.-J. M., & Gehring, K. (2018). Feasibility of the
evidence-based cognitive telerehabilitation program Remind for patients with primary brain
tumors. Journal of Neuro-Oncology, 137(3), 523–532. https://doi.org/10.1007/s11060-017-2738-
8
Verhage, F. (1964). Intelligentie en leeftijd: Onderzoek bij Nederlanders van twaalf tot zevenenzeventig
jaar. Van Gorcum.
Vilasboas, T., Herbet, G., & Duau, H. (2017). Challenging the myth of right nondominant
hemisphere: Lessons from corticosubcortical stimulation mapping in awake surgery and
surgical implications. World Neurosurgery, 103, 449–456. https://doi.org/10.1016/j.wneu.2017.
04.021
Wefel, J. S., Noll, K. R., Rao, G., & Cahill, D. P. (2016). Neurocognitive function varies by IDH1 genetic
mutation status in patients with malignant glioma prior to surgical resection. Neuro-Oncology, 18
(12), 1656–1663. https://doi.org/10.1093/neuonc/now165
Wickham, H. (2016). ggplot2: Elegant graphics for data analysis. Springer.
Yoo, H., McNeil, M. R., Dickey, M. W., & Terhorst, L. (2021). Linguistic and nonlinguistic processing
speed across age-matched normal healthy controls and individuals with left-hemisphere
damage, with and without aphasia. Aphasiology. 1–23. https://doi.org/10.1080/02687038.2020.
1853966.
APHASIOLOGY 23
Appendices
Outcomes of the statistical models.
Inuence of participant characteristics
The demographic factors age and education level were included in the statistical models as
covariates. These factors contributed signicantly to the outcomes of the BNT, TMT, and the RT
measures of the SJT. The eect of age and education level on these tests has been corroborated in
earlier studies (Snitz et al., 2009; Tombaugh, 2004; De Witte et al., 2015b). In addition, signicant
interaction eects between age, education, and group on the SJT RTs, TMT-B, and TMT-BA, seem to
suggest that older patients with lower education are more aected by their glioma than younger
patients with a higher education when it comes to linguistic processing speed, visuoperceptual
speed, and concept shifting.
Table A. BNT Score by group, age, and education level.
Estimate Std.Error t-value p-value
(Intercept) 51.082 0.812 62.908 0.000
Group 3.543 1.624 2.182 0.033*
Age −0.022 0.061 −0.352 0.726
Education level 3.422 0.945 3.621 0.001*
Group x Age 0.275 0.122 2.249 0.028*
Group x Education level −0.963 1.890 −0.510 0.612
Age x Education level −0.049 0.086 −0.574 0.568
Group x Age x Education level 0.093 0.172 0.542 0.590
Table B. Reaction times on the sentence judgment test.
Estimate Std.Error df t-value p-value
(Intercept) 7.612 0.054 40.535 141.781 0.000
Group 0.016 0.081 47.968 0.201 0.841
Education level −0.131 0.050 48.042 −2.623 0.012*
Age 0.000 0.003 47.937 0.157 0.876
Order −0.010 0.002 722.384 −5.320 0.000*
Semantics-Phonology 0.165 0.051 11.803 3.206 0.008*
Syntax-Phonology 0.357 0.052 11.957 6.920 0.000*
Group x Education level 0.008 0.100 48.023 0.081 0.936
Group x Age −0.003 0.006 47.951 −0.438 0.663
Education level x Age 0.015 0.005 47.996 3.222 0.002*
Order x Condition Sem-Phon 0.007 0.003 722.336 2.450 0.015*
Order x Condition Syn-Phon 0.009 0.003 724.654 3.109 0.002*
Group x Education x Age −0.018 0.009 48.001 −1.947 0.057
Table C. Summary accuracy scores Sentence Judgment Test.
Estimate Std.Error z-value p-value
(Intercept) 6.850 2.154 3.180 0.001
Group 1.156 0.414 2.790 0.005*
Education level 0.431 0.248 1.740 0.082
Age 0.010 0.014 0.706 0.480
Order 0.201 0.200 1.009 0.313
Semantics-Phonology −3.351 2.169 −1.545 0.122
Syntax-Phonology −4.485 2.155 −2.081 0.037*
Group x Education level −0.136 0.497 −0.273 0.785
Group x Age 0.023 0.029 0.810 0.418
Education level x Age −0.008 0.020 −0.413 0.680
Order x Condition Sem-Phon −0.233 0.204 −1.143 0.253
Order x Condition Syn-Phon −0.128 0.202 −0.637 0.524
Group x Education x Age −0.011 0.039 −0.285 0.775
24 S. MOOIJMAN ET AL.
Table D. TMT-A Score by group, age, and education level.
Estimate Std.Error t-value p-value
(Intercept) 3.351 0.039 86.054 0.000
Group 0.082 0.078 1.048 0.299
Age 0.002 0.003 0.541 0.591
Education level −0.131 0.045 −2.886 0.005*
Group x Age −0.006 0.006 −1.090 0.280
Group x Education level 0.132 0.091 1.454 0.151
Age x Education level 0.006 0.004 1.373 0.175
Group x Age x Education level −0.004 0.008 −0.479 0.633
Table E. TMT-B Score by group, age, and education level.
Estimate Std.Error t-value p-value
(Intercept) 4.100 0.044 93.613 0.000
Group −0.125 0.088 −1.431 0.158
Age 0.004 0.003 1.175 0.245
Education level −0.181 0.051 −3.562 0.001*
Group x Age −0.011 0.007 −1.683 0.098
Group x Education level 0.188 0.101 1.851 0.069
Age x Education level 0.018 0.005 3.831 0.000*
Group x Age x Education level −0.028 0.009 −2.988 0.004*
Table F. Ratio score TMT-BA score by group, age, and education level.
Estimate Std.Error t-value p-value
(Intercept) 2.249 0.094 23.900 0.000
Group −0.558 0.188 −2.966 0.004*
Age 0.013 0.007 1.790 0.079
Education level −0.101 0.109 −0.926 0.358
Group x Age −0.027 0.014 −1.891 0.063
Group x Education level 0.129 0.218 0.593 0.555
Age x Education level 0.033 0.010 3.307 0.002*
Group x Age x Education level −0.067 0.020 −3.345 0.001*
APHASIOLOGY 25
... In recent years, the language abilities of people with brain tumours have received much attention (Mooijman et al., 2021;Rofes, Mandonnet, et al., 2017;Satoer et al., 2013). Tasks and assessments at the sentence and at the word level have been employed. ...
... Satoer et al. (2013) reported that during preoperative spontaneous speech individuals with brain tumours produced more incomplete sentences and had shorter mean length of utterance than a matched control group. However, even though people with brain tumours report word finding problems, single-word object naming tasks are not always sensitive enough to detect any preoperative difficulties (Mooijman et al., 2021). More importantly, the numbers of patients that are classified as 'impaired' seem to differ according to the linguistic modality and the linguistic stimuli used in each neurosurgical centre. ...
Article
Full-text available
People with tumours in specific brain sites might face difficulties in tasks with different linguistic material. Previous lesion‐symptom mapping studies (VLSM) demonstrated that people with tumours in posterior temporal regions have more severe linguistic impairments. However, to the best of our knowledge, preoperative performance and lesion location on tasks with different linguistic stimuli have not been examined. In the present study, we performed VLSM on 52 people with left gliomas to examine whether tumour distribution differs depending on the tasks of the Aachen Aphasia Test. The VLSM analysis revealed that single‐word production (e.g. object naming) was associated with the inferior parietal lobe and that compound and sentence production were additionally associated with posterior temporal gyri. Word repetition was affected in people with tumours in inferior parietal areas, whereas sentence repetition was the only task to be associated with frontal regions. Subcortically, word and sentence production were found to be affected in people with tumours reaching the arcuate fasciculus, and compound production was primarily associated with tumours affecting the inferior longitudinal and inferior fronto‐occipital fasciculus. Our work shows that tasks with linguistic stimuli other than single‐word naming (e.g. compound and sentence production) relate to additional cortical and subcortical brain areas. At a clinical level, we show that tasks that target the same processes (e.g. repetition) can have different neural correlates depending on the linguistic stimuli used. Also, we highlight the importance of left temporoparietal areas.
... These tests are not always sensitive for mild language deficits (Brownsett et al., 2019;Davie et al., 2009;Satoer et al., 2012). In addition, despite the often absent objectified aphasia, LGG patients do report language complaints (Brownsett et al., 2019;Mooijman et al., 2022;Satoer et al., 2012) underlining the need for suitable tests. Standardized tests that are often described to be sensitive in LGG patients are verbal fluency (category and letter) and (rapid) naming (objects and actions) and are therefore recommended in a minimal test-battery to tap into the language domain ( (Papagno et al., 2012) (see also Rofes et al. (2017) for a European survey on cognitive assessment). ...
Chapter
Full-text available
Brain tumours, which are classified as rare diseases, primarily include glioblastoma, with an annual occurrence of 300,000 cases. Unfortunately, this condition leads to the loss of 241,000 lives each year, highlighting its devastating nature. However, recent advancements in diagnosis and treatment have significantly improved the management and care of brain tumours. In this chapter, we will first provide an overview of the common types of primary brain tumours (gliomas and meningiomas). We will then delve into techniques for identifying and mapping tumours that impact language processing, utilizing both non-invasive and invasive methods. Lastly, we will discuss the effects of surgery on language and cognitive functions. The focus of this chapter is on tumours affecting language processing in the brain and the application of diffusion-weighted tractography to map the white matter language system.
... However, the outcomes can assist selection of variables in future studies. Language domains that appear most promising in relation to FC networks are word retrieval (as assessed with object naming), grammar, and comprehension of visual input when using a sufficiently sensitive test (e.g., combination of accuracy and speed, Mooijman et al., 2021) and to a lesser extent semantics and writing. FC network characteristics that appear most promising in relation to language functioning are MST degree, eccentricity and diameter in the theta band, and weighted small-world index in the alpha band. ...
Article
Full-text available
Introduction: Preservation of language functioning in patients undergoing brain tumor surgery is essential because language impairments negatively impact the quality of life. Brain tumor patients have alterations in functional connectivity (FC), the extent to which brain areas functionally interact. We studied FC networks in relation to language functioning in glioma and meningioma patients. Method: Patients with a low-grade glioma (N = 15) or meningioma (N = 10) infiltrating into/pressing on the language-dominant hemisphere underwent extensive language testing before and 1 year after surgery. Resting-state EEG was registered preoperatively, postoperatively (glioma patients only), and once in healthy individuals. After analyzing FC in theta and alpha frequency bands, weighted networks and Minimum Spanning Trees were quantified by various network measures. Results: Pre-operative FC network characteristics did not differ between glioma patients and healthy individuals. However, hub presence and higher local and global FC are associated with poorer language functioning before surgery in glioma patients and predict worse language performance at 1 year after surgery. For meningioma patients, a greater small worldness was related to worse language performance and hub presence; better average clustering and global integration were predictive of worse outcome on language function 1 year after surgery. The average eccentricity, diameter and tree hierarchy seem to be the network metrics with the more pronounced relation to language performance. Discussion: In this exploratory study, we demonstrated that preoperative FC networks are informative for pre- and postoperative language functioning in glioma patients and to a lesser extent in meningioma patients.
Article
Background: Patients with glioma often report language complaints with devastating effect on daily life. Analysing spontaneous speech can help to understand underlying language problems. Spontaneous speech monitoring is also of importance during awake brain surgery: it can guide tumour resection and contributes to maintaining language function. We aimed to investigate the spontaneous speech of patients with glioma in the perioperative period and the additional value of spontaneous speech analyses compared to standardised language testing. Methods: We elicited and transcribed spontaneous speech of eight patients with glioma elected for awake brain surgery preoperatively, intraoperatively and 2.0-3.5 months postoperatively. Linguistic errors were coded. Type Token Ratio, Mean Length of Utterance of words, minimal utterances, and errors were extracted from the transcriptions. Patients were categorised based on total error patterns: stable, decrease or increase during surgery. Reliable Change Index scores were calculated for all spontaneous speech variables to objectify changes between time points. Language performance on language tests was compared to spontaneous speech variables. Results: Most errors occurred in lexico-syntax, followed by phonology/articulation, syntax, and semantics. The predominant errors were Repetitions, Self-corrections, and Incomplete sentences. Most patients remained stable over time in almost all spontaneous speech variables, except in Incomplete sentences, which deteriorated in most patients postoperatively compared to intraoperatively. Some spontaneous speech variables (total errors, MLUw, TTR) gave more information on language change than a standard language test. Conclusions: While the course of spontaneous speech over time remained relatively stable in most patients, Incomplete sentences seems to be a robust marker of language difficulties patients with glioma. These errors can be prioritised in spontaneous speech analysis to save time, especially to determine intra- to postoperative deterioration. Importantly, spontaneous speech analyses can give more information on language change than standardised language testing and should therefore be used in addition to standardised language tests.
Article
Purpose: To investigate the course of fatigue, subjective and objective language functions in patients with lower-grade gliomas during the first year of disease. Further, to examine if subjective and objective language variables predicted ratings of fatigue. Methods: Fatigue was assessed with the Fatigue Severity Scale, subjective language with self-reported word-finding, expression of thoughts, reading and writing from the Functional Assessment of Cancer Therapy - Brain, and objective language with standardized tests. Mixed models were used to investigate changes in variables over time and predictors of fatigue. Results: Twenty-three patients with gliomas (WHO 1-3) were included. Average ratings of fatigue did not change significantly, but altering patterns were observed. Subjective concerns about word-finding and expression of thoughts increased significantly during follow-up. The regression analyses showed that concerns about abilities to read and write significantly predicted fatigue. The results indicated that less concerns about reading and writing were associated with lower levels of fatigue. Conclusions: Patients with lower-grade gliomas report fatigue and language concerns throughout the first year. Concerns about reading and writing call for careful consideration as they seem to provoke fatigue. The findings underline the importance of the patients' perspective in treatment and follow-up.
Article
Impaired lexical retrieval is common in persons with low-grade glioma (LGG). Several studies have reported a discrepancy between subjective word-finding difficulties and results on formal tests. Analysis of spontaneous speech might be more sensitive to signs of word-finding difficulties, hence we aimed to explore disfluencies in a spontaneous-speech task performed by participants with presumed LGG before and after surgery. Further, we wanted to explore how the presence of disfluencies in spontaneous speech differed in the participants with and without objectively established lexical-retrieval impairment and with and without self-reported subjective experience of impaired language, speech and communication. Speech samples of 26 persons with presumed low-grade glioma were analysed with regard to disfluency features. The post-operative speech samples had a higher occurrence of fillers, implying more disfluent language production. The participants performed worse on two of the word fluency tests, and after surgery the number of participants who were assessed as having an impaired lexical retrieval had increased from 6 to 12. The number of participants who experienced a change in their language, speech or communication had increased from 9 to 12. Additional comparisons showed that those with impaired lexical retrieval had a higher proportion of false starts after surgery than those with normal lexical retrieval, and differences in articulation rate and speech rate, favouring those not having experienced any change in language, speech or communication. Taken together, the findings from this study strengthen the existing claim that temporal aspects of language and speech are important when assessing persons with gliomas.
Article
Full-text available
Low grade glioma patients report word finding difficulties during the anamnesis. However, these are often not objectified with naming tests used in clinical practice. The aim of the current study was to develop a sensitive speeded naming test for word finding difficulties in low grade glioma patients. Reaction times on a picture naming test were obtained for 18 glioma patients and 20 healthy participants. Results of a measure of cognitive speed (TrailMaking Test A) were taken into account to exclude the possibility of slower response rates in glioma patients due to overall cognitive slowing. Naming test results were compared with results of a naming test commonly used in clinical practice, the BostonNaming Test (BNT), in order to evaluate the additional value of the speeded naming test. Also, the effect of word frequency and age of acquisition (AoA) on naming latencies was investigated. Glioma patients were significantly slower than the healthy participants in object naming.The slower naming latencies were not explained by an overall lower speed of processing. BNT scores could not explain the slower naming latencies. A qualitative comparison between results of the speeded naming test and BNT pointed to a higher sensitivity of the naming test for word finding difficulties. Although an effect of word frequency and AoA emerged in the healthy participant group, there was no effect on the naming latencies in the patient group for these variables. The results showed a clear difference between naming latencies of low grade glioma patients and healthy controls, while patients rarely achieved clinical scores on the BNT. There is support for the use of a speeded naming test in daily clinical practice in which reaction times are included as a critical component for diagnosing word finding difficulties in glioma patients.
Article
Full-text available
Objective This study aimed to examine: (1) patient–proxy agreement on executive functioning (EF) of patients with primary brain tumors, (2) the relationships between patient- and proxy-report with performance-based measures of EF, and (3) the potential influence of performance-based measures on the level of agreement. Methods Meningioma and low-grade glioma patients and their informal caregivers completed the Behavior Rating Inventory of Executive Function (BRIEF-A) 3 months after surgery. The two index scores of the BRIEF-A, Behavioral Regulation and Metacognition, were evaluated. Mean scores of patients and proxies were compared with normative values and with each other. Patient–proxy agreement was evaluated with Lin’s concordance correlation coefficients (CCCs) and Bland–Altman plots. Pearson correlation coefficients between reported EF and performance-based measures of EF were calculated. Multiple regression analysis was used to evaluate the potential influence of test performance on differences in dyadic reports. Results A total of 47 dyads were included. Patients reported significantly more problems on the Metacognition Index compared to norms, and also in comparison with their proxies. Effect sizes indicated small differences. Moderate to substantial agreement was observed between patients and proxies, with CCCs of 0.57 and 0.61 for Metacognition and Behavioral Regulation, respectively. Correlations between reported EF and test performance ranged between −0.37 and 0.10. Dyadic agreement was not significantly influenced by test performance. Conclusions Patient–proxy agreement was found to be moderate. No clear associations were found between reported EF and test performance. Future studies should further explore the existing and new methods to assess everyday EF in brain tumor patients.
Article
Full-text available
Purpose The aims of the study were to determine dual-task effects on content accuracy, delivery speed, and perceived effort during narrative discourse in people with moderate, mild, or no aphasia and to explore subjective reactions to retelling a story with a concurrent task. Method Two studies (1 quantitative and 1 qualitative) were conducted. In Study 1, participants with mild or moderate aphasia and neurotypical controls retold short stories in isolation and while simultaneously distinguishing between high and low tones. Story retell accuracy (speech productivity and efficiency), speed (speech rate, repetitions, and pauses), and perceived effort were measured and compared. In Study 2, participants completed semistructured interviews about their story retell experience. These interviews were recorded, transcribed orthographically, and coded qualitatively using thematic analysis. Results The dual task interfered more with spoken language of people with aphasia than controls, but different speed–accuracy trade-off patterns were noted. Participants in the moderate aphasia group reduced accuracy with little alteration to speed, whereas participants in the mild aphasia group maintained accuracy and reduced their speed. Participants in both groups also reported more negative emotional and behavioral reactions to the dual-task condition than their neurotypical peers. Intentional strategies for coping with the cognitive demands of the dual-task condition were only reported by participants with mild aphasia. Conclusion The findings suggest that, although communicating with a competing task is more difficult for people with aphasia than neurotypical controls, participants with mild aphasia may be better able to cope with cognitively demanding communication situations than participants with moderate aphasia. Supplemental Material https://doi.org/10.23641/asha.8233391
Article
Full-text available
Background: Intervention in severe aphasia often means aiming for access to meaningful social interaction in spite of linguistic barriers that might not be treatable. This demands knowledge about the different factors that influence functional communication. Apart from linguistic ability, executive functions are thought to play an important role. Aims: To expand the understanding of the relations of executive functions and linguistic ability to functional communication in severe aphasia. Methods and Procedures: Executive functions, linguistic ability, and functional communication were assessed in 47 participants with severe aphasia. The results were analysed for the total sample and for a verbal and a nonverbal subgroup. Outcomes and Results: Impairment of executive function was found in 85% of the participants. There were moderate to strong correlations between all subtests of executive functions and linguistic ability. In the total sample, significant partial correlation was found between functional communication and verbal output. In the nonverbal subgroup, there was a significant partial correlation between executive function and functional communication, when controlling for linguistic ability. In the verbal subgroup, no relations were found between executive functions or language and functional communication. Conclusions: Impairments of executive functions are common in people with severe aphasia, and executive function and linguistic ability are closely related. The ability to produce verbal output is strongly related to functional communication, but in people with extreme limitation or total absence of verbal output, executive functions seem to be an important factor for functional communication. There is a large variation of executive functions and functional communication in people with severe aphasia, especially in the nonverbal subgroup. It is important that people with severe aphasia are given a complete and proper evaluation of their abilities, and that the possible importance of executive function to communication is considered in communication intervention.
Article
Full-text available
Background Intraoperative stimulation mapping (ISM) using electrocortical mapping (awake craniotomy, AC) or evoked potentials has become a solid option for the resection of supratentorial low-grade gliomas in eloquent areas, but not as much for high-grade gliomas. This meta-analysis aims to determine whether the surgeon, when using ISM and AC, is able to achieve improved overall survival and decreased neurological morbidity in patients with high-grade glioma as compared to resection under general anesthesia (GA). Methods A systematic search was performed to identify relevant studies. Adult patients were included who had undergone craniotomy for high-grade glioma (WHO grade III or IV) using ISM (among which AC) or GA. Primary outcomes were rate of postoperative complications, overall postoperative survival, and percentage of gross total resections (GTR). Secondary outcomes were extent of resection and percentage of eloquent areas. Results Review of 2049 articles led to the inclusion of 53 studies in the analysis, including 9102 patients. The overall postoperative median survival in the AC group was significantly longer (16.87 versus 12.04 months; p < 0.001) and the postoperative complication rate was significantly lower (0.13 versus 0.21; p < 0.001). Mean percentage of GTR was significantly higher in the ISM group (79.1% versus 47.7%, p < 0.0001). Extent of resection and preoperative patient KPS were indicated as prognostic factors, whereas patient KPS and involvement of eloquent areas were identified as predictive factors. Conclusions These findings suggest that surgeons using ISM and AC during their resections of high-grade glioma in eloquent areas experienced better surgical outcomes: a significantly longer overall postoperative survival, a lower rate of postoperative complications, and a higher percentage of GTR.
Article
Full-text available
Many patients with primary brain tumors experience cognitive deficits. Cognitive rehabilitation programs focus on alleviating these deficits, but availability of such programs is limited. Our large randomized controlled trial (RCT) demonstrated positive effects of the cognitive rehabilitation program developed by our group. We converted the program into the iPad-based cognitive rehabilitation program ReMind, to increase its accessibility. The app incorporates psychoeducation, strategy training and retraining. This pilot study in patients with primary brain tumors evaluates the feasibility of the use of the ReMind-app in a clinical (research) setting in terms of accrual, attrition, adherence and patient satisfaction. The intervention commenced 3 months after resective surgery and patients were advised to spend 3 h per week on the program for 10 weeks. Of 28 eligible patients, 15 patients with presumed low-grade glioma or meningioma provided informed consent. Most important reason for decline was that patients (7) experienced no cognitive complaints. Participants completed on average 71% of the strategy training and 76% of the retraining. Some patients evaluated the retraining as too easy. Overall, 85% of the patients evaluated the intervention as “good” or “excellent”. All patients indicated that they would recommend the program to other patients with brain tumors. The ReMind-app is the first evidence-based cognitive telerehabilitation program for adult patients with brain tumors and this pilot study suggests that postoperative cognitive rehabilitation via this app is feasible. Based on patients’ feedback, we have expanded the retraining with more difficult exercises. We will evaluate the efficacy of ReMind in an RCT.
Article
Background Slowed language production and comprehension in people with aphasia (PWA) is frequently cited as a characteristic of the disorder, even after full recovery. However, results supporting the existence of slowness are inconsistent and the mechanisms are unclear. Previous research has failed to determine the neurocognitive locus of the slowing and whether it is due to left hemisphere damage, general aging, or language-specific mechanisms. The goals of this study are: (1) to explore whether reduced processing speed is present and specific to the presence of aphasia or due to left-hemisphere damage more generally and (2) whether it is specific to the linguistic domain of cognition. Results The results of the mixed effects model revealed significant main effects for groups and domains, and no significant interactions among groups or between domains. The two brain-damaged groups exhibited significantly longer processing times across tasks compared to the NHC group. The processing speed of the PWA group was significantly longer than that of the LHD group across simple perceptual and more cognitively complex tasks. Groups were not significantly different on three nonlinguistic sensory-motor tasks. Conclusions Left-hemisphere damage-related slowing, as well as aphasia-additive slowing, was demonstrated as evidenced by significant differences between the two brain-damaged groups and between these two groups and the NHC group. Therefore, the observed slowing in the PWA group appears to be due to both brain-damage-related and aphasia-additive slowing. Domain-specificity was not observed as evidenced by significant slowing on both linguistic and nonlinguistic tasks in both brain-damaged groups compared to the performance of the NHCs.
Article
Background: In assessing post-operative language impairment, clinical teams typically rely on “aphasia subtype” classifications, based on post-stroke patterns of impairment. However, this approach may significantly underestimate the prevalence of post-surgical language impairments due to the different pathophysiological mechanisms involved. There is a paucity of research in chronic post-surgical patients. Aims: We investigated post-surgical language performance in the chronic phase. Methods & Procedures: Using both the Western Aphasia battery Revised (WAB-R) and the Comprehensive Aphasia test (CAT), we assessed a range of language skills in 26 right-handed patients approximately 6–12 months after they underwent surgery to remove a primary tumour in their left cerebral hemisphere. Participants’ self-reports of their speech and language skills post-surgery were also collected. Outcomes and Results: Following surgery, 77% of patients scored below normal cut-off on one or more language subtests of the CAT battery. This contrasted with only 27% on the WAB AQ. The CAT findings were supported by subjective data, with 58% of patients self-reporting post-surgical communication difficulty. Conclusions: Our results show that current “aphasia subtype” testing is inadequate, and is likely to significantly underestimate chronic language deficits in this population. Alternative approaches to formal language assessment need to be used in this group of patients whose pattern of impairments is very different from that observed in post-stroke aphasia.
Article
Objective: Glioma patients often complain about problems in daily conversation with a negative impact on quality of life. Disorders in standardized language tests (e.g. naming and fluency), are frequently observed. Most studies claim recovery of language functions within 3 months. However, long-term effects of surgery on spontaneous speech remain unknown. Patients and Methods: Eighteen glioma patients were compared to healthy controls in spontaneous speech variables: Type Token Ratio (TTR), Mean Length of Utterance words (MLUw), Incomplete Sentences, Self-corrections and Repetitions. Boston Naming Test (BNT) and Category Fluency (CF) were also assessed. We compared: pre- and 3 months postoperatively (T1-T2), 3 months and 1 year postoperatively (T2-T3), pre- and 1 year postoperatively (T1-T3). Correlations were computed between deviating variables and BNT/CF, tumor localization, and tumor grade. Results: Patients had deficits in Incomplete sentences (T1, T2, T3), TTR (T2,T3), MLUw (T3) and Self-corrections (T2). Between T1-T2 no decline was present. Between T2-T3 and T1-T3, there was a decrease of MLUw, Self-corrections and Repetitions and an increase of Incomplete Sentences, BNT and CF were impaired (T1, T2, T3) without differences between test-moments. Most spontaneous speech variables did not correlate with standardized tests. Tumor localization and grade had no influence on spontaneous speech . Conclusion: Glioma patients showed impaired spontaneous speech combined with naming and fluency deficits. Surgery appeared to have deteriorated the quality of spontaneous speech until long-term but not the performance at test-level. Hence, spontaneous speech has an added value to standardized tests for diagnosis of language impairments.