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AJSLP

Research Article

Effects of Epilepsy on Language


Functions: Scoping Review
and Data Mining Findings
Manaswita Dutta,a Laura Murray,b Wendy Miller,c and Doyle Grovesc

Purpose: This study involved a scoping review to identify underrepresented. Most studies utilized aphasia tests and
possible gaps in the empirical description of language primarily assessed single-word productions; few studies
functioning in epilepsy in adults. With access to social included healthy control groups. Data mining revealed
network data, data mining was used to determine if several posts regarding epilepsy-related language problems,
individuals with epilepsy are expressing language-related including word retrieval, reading, writing, verbal memory
concerns. difficulties, and negative effects of epilepsy treatment on
Method: For the scoping review, scientific databases were language.
explored to identify pertinent articles. Findings regarding Conclusion: Our findings underscore the need for future
the nature of epilepsy etiologies, patient characteristics, specification of the integrity of language in epilepsy,
tested language modalities, and language measures particularly with respect to discourse and high-level
were compiled. Data mining focused on social network language abilities. Increased awareness of epilepsy-
databases to obtain a set of relevant language-related related language issues and understanding the patients’
posts. perspectives about their language concerns will allow
Results: The search yielded 66 articles. Epilepsy etiologies researchers and speech-language pathologists to utilize
except temporal lobe epilepsy and older adults were appropriate assessments and improve quality of care.

E
pilepsy is a recurring neurological condition affect- Elger, 2003; MacAllister & Schaffer, 2007; Rai et al., 2015).
ing approximately 2 million Americans with Of interest to speech-language pathology clinicians and
150,000 new cases each year (Epilepsy Statistics, researchers is that language deficits have also been frequently
2014). Nearly 2% of adults aged 18 years or older and 1% reported, which may fluctuate due to the nature and extent
of children under 17 years of age have a history of epi- of epilepsy or in response to corrective surgeries or medica-
lepsy, with highest epilepsy incidence among children and tions (e.g., Abou-Khalil & Abou-Khalil, 2015; Caplan et al.,
older adults. Extensive research has established that epi- 2009; Sherman et al., 2011).
lepsy alters cognition in children and adults, documenting Within the epilepsy research base, greater empirical
prevalent and persistent attention, memory, and executive attention has been thus far dedicated to describing lan-
function problems (e.g., Griffith, Martin, Bambara, Marson, guage functioning in children and adolescents as opposed
& Faught, 2006; Helmstaedter, Kurthen, Lux, Reuber, & to language functioning in adults, perhaps as a disturbance
to this domain can significantly impair learning, with long-
term effects on children’s academic performance and social-
a
Department of Speech and Hearing Sciences, Indiana University, emotional functioning (Caplan et al., 2009; Fastenau et al.,
Bloomington 2004; Hermann et al., 2008; Staden, Isaacs, Boyd, Brandl,
b
School of Communication Sciences and Disorders, Western & Neville, 1998). Language disturbances are, however, fre-
University, London, Ontario, Canada quently observed in adults with epilepsy (e.g., Hamberger
c
School of Nursing, Indiana University, Bloomington & Seidel, 2003; Helmstaedter, Gleissner, Zentner, & Elger,
Correspondence to Manaswita Dutta: mdutta@indiana.edu 1998; Miller et al., 2016), but research for this age group
Editor: Krista Wilkinson remains incomplete, warranting a thorough investigation
Associate Editor: Daniel Kempler (Doering & Trinka, 2014). Therefore, the current study’s fo-
Received October 31, 2016 cus was limited to examining the language profiles of adults
Revision received June 9, 2017 with epilepsy.
Accepted August 29, 2017
https://doi.org/10.1044/2017_AJSLP-16-0195
Publisher Note: This article is part of the Special Issue: Select Papers Disclosure: The authors have declared that no competing interests existed at the time
From the 46th Clinical Aphasiology Conference. of publication.

350 American Journal of Speech-Language Pathology • Vol. 27 • 350–378 • March 2018 • Copyright © 2018 American Speech-Language-Hearing Association

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With respect to epilepsy-related language impair- Study design issues include infrequent inclusion of age- and
ments, the term “postictal aphasia” has sometimes been education-matched healthy controls (e.g., Field et al., 2000;
used, particularly by medical professionals (Abou-Khalil Toledano et al., 2013) and inadequate sample sizes when
& Abou-Khalil, 2015; Gabr, Luders, Dinner, Morris, & evaluating language skills other than word retrieval (e.g.,
Wylie, 1989), as a label for difficulties frequently observed Bartha et al., 2004; Sadiq, Hussain, & Norton, 2012). Hence,
in word finding, spontaneous speech, reading, and writing it is important to determine if such procedural concerns
(Privitera, Morris, & Gilliam, 1991). Generally, the lin- (e.g., tests used, interpretation of test results) are contribut-
guistic deficits associated with both generalized and fo- ing to the heterogeneous language outcomes in the epilepsy
cal epilepsies overlap (Giovagnoli, Canafoglia, Reati, literature. It is additionally important to have a complete
Raviglione, & Franceschetti, 2009). For example, naming description of possible language profiles and the identifica-
and auditory comprehension deficits have been reported tion of appropriate language measures to guide clinicians
in temporal lobe epilepsy (TLE), frontal lobe epilepsy and researchers in their assessment and management of
(FLE), and idiopathic generalized epilepsy. Patients with adults with epilepsy.
idiopathic generalized epilepsy may additionally show Indeed, a descriptive systematic review was con-
repetition and semantic processing errors. Across epilepsy ducted by Doering and Trinka (2014), who described
types, however, left TLE patients appear to be at greatest 31 published studies on language functions in adults with
risk for language disturbances (Bell, Lin, Seidenberg, & epilepsy and commented on the general paucity of litera-
Hermann, 2011). TLE-related language impairments are ture on the topic. Whereas the authors summarized findings
often described as mild, with word retrieval difficulties from the included studies, they did not use any objective
being the most frequent symptom (Condret-Santi et al., 2014; means of assessing the studies’ methodological quality or
Rai et al., 2015). There is concern, however, that such clarify the research-related shortcomings in the existing
deficits are significant enough to confound TLE patients’ literature. As this was a systematic review, the authors
performance of verbal cognitive measures, including verbal followed a fairly strict inclusionary/exclusionary criterion.
learning, memory, and intelligence (Busch et al., 2013). For instance, they excluded studies that included less than
Despite frequent reports of epilepsy-based language 10 participants or that reported findings following adminis-
symptoms, the breadth and severity of such impairments tration of antiepileptic drugs or epilepsy surgery; reviews,
have yet to be solidified for the adult patient population. case reports, and studies involving behavioral treatment of
For example, researchers have primarily focused on assess- epilepsy-related language functions were also not included.
ing spoken language production, with word-level measures Hence, due to the focused nature of their review and the ex-
(i.e., confrontation naming, verbal fluency) predominating clusion of several potentially relevant studies, the extent and
(Bartha, Benke, Bauer, & Trinka, 2005). In contrast, there nature of research conducted regarding language deficits in
are limited descriptions of other linguistic domains and adults with epilepsy has yet to be conclusively established.
modalities including auditory comprehension, repetition, Another research and clinical gap pertains to deter-
discourse, reading, and writing. Moreover, the majority of mining if individuals living with epilepsy have concerns
prior studies have assessed individuals with TLE, leaving regarding their language abilities. One relatively new ap-
nominal empirical description of language profiles in other proach to identify these possible concerns is data mining,
epilepsy types (Doering & Trinka, 2014). An additional the analytical process of exploring large volumes of data
limitation is that there are some contradictory language for meaningful information and correlations via statistical
findings. For instance, whereas Fargo et al. (2003) found and mathematical methods (Kantardzic, 2011; Larose &
significant deficits in left TLE patients’ visual naming, Larose, 2014). This technique allows not only characterizing
Hamberger and Tamny (1999) reported no such deficits. problems from patients’ perspectives but also determining
Similarly, among TLE patients, Bell, Seidenberg, Hermann, their impressions about healthcare practices for those prob-
and Douville (2003) found mild narrative discourse deficits, lems (Reardon, 2015). With respect to the World Health
but Field, Saling, and Berkovic (2000) did not. Organization’s International Classification of Functioning,
Relatedly, there are some concerns regarding the Disability and Health (2016), such information fosters ex-
procedures that have been used to characterize the lan- tending a description of epilepsy symptoms beyond the
guage abilities of adults with epilepsy. In particular, there impairment level (which the extant literature has thus far
has been an inordinate use of standardized assessment solely focused) and determining the activity and participa-
tools designed for individuals with aphasia, even though tion challenges for which patients are seeking assistance.
such measures may be inadequate not only to identify the Data mining techniques have been utilized previ-
mild or subtle language deficits previously reported in this ously to answer health-related queries of individuals with
population (Gauffin et al., 2013; Turkstra, Ylvisaker, et al., chronic medical conditions (e.g., epilepsy, depression) that
2005) but also to determine challenges in daily communica- are not always possible using traditional research methods
tion activities and interactions (Threats, 2012; Worrall & (Miller, Groves, Knopf, Otte, & Silverman, 2017). For
Holland, 2003). Furthermore, the extent to which these example, social media data have been mined to examine
measures have evaluated specific linguistic processes (e.g., the topics of conversation among individuals with autism
lexical–semantic, syntactic, and orthographic processing spectrum disorders and their caregivers and family mem-
skills) in epilepsy is questionable (Murray & Clark, 2015). bers (Beykikhoshk, Arandjelović, Phung, Venkatesh, &

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Caelli, 2014) and to explore differences in the typing pat- and language deficits to poor test performance, leading to
terns of individuals with autism spectrum disorder and confounding findings (Doering & Trinka, 2014; Howieson
neurotypical Twitter users (Newton, Kramer, & McIntosh, & Lezak, 2010). Unpublished dissertations and conference
2009). Likewise, Robillard, Johnson, Hennessey, Beattie, presentations were also excluded. These inclusionary and
and Illes (2013) data mined Twitter to collect messages exclusionary criteria were developed post hoc, after in-
posted by individuals with dementia and to investigate the creasing familiarity with the available literature on the
general themes of their tweets. key research question of language disorders in epilepsy
Accordingly, the overall purpose of this study was (Arksey & O’Malley, 2005).
to extend the limited literature regarding language abilities All articles were screened by reviewing the title, key-
in adults with epilepsy. The specific aims were as follows: words, and abstract to determine if they met the eligibility
(a) via a scoping review, expand on the results of Doering criteria (see Figure 1). Based on the titles, articles were
and Trinka (2014) and determine the types of language removed that did not address communication deficits in
functions and assessment procedures that have been evalu- epilepsy. The abstracts of the remaining articles were
ated and used, respectively, in the existing epilepsy research reviewed next, and the ones that were not relevant to the
base to identify possible gaps in our understanding of research question were rejected. An in-depth review of the
vulnerable language functions and patient profiles and remaining full-text articles was undertaken to determine
(b) use data mining as a complimentary approach to the language modalities evaluated and the assessment
search online social media databases to determine if individ- methods used and to ensure that the selected articles de-
uals dealing with epilepsy are expressing language-related scribed language functions in epilepsy. Two authors se-
concerns. lected and screened the articles to ensure a consensus was
reached.

Method Quality Appraisal


Scoping Review Procedures The methodological quality of all articles included in
the scoping review was evaluated using a rating framework
The following scoping review procedures were
adapted from Spencer, Ritchie, Lewis, and Dillon (2003)
adapted from the framework of Arksey and O’Malley
and an assessment scale designed for pre–post studies de-
(2005).
veloped by the National Heart, Lung and Blood Institute,
National Institute of Health, U.S. Department of Health
Identification, Screening, and Selection of Relevant Studies and Human Services (2014). The adapted rating scale eval-
PubMed, Google Scholar, ASHAWire, and PsycInfo uated the quality of research design, participant recruit-
electronic databases were searched via the keywords “epi- ment and demographics, data collection, data analysis,
lepsy,” “seizure disorder,” “language disorders,” “commu- and research findings; ratings of 0 or 1 were assigned if
nication disorders,” and “adults.” These search terms were the article met or did not meet, respectively, each category
combined using the operators “AND” and “OR.” The (see Table 1). Two independent raters completed the study
scoping review was limited to data-generating studies in quality ratings. Intra- and interrater reliability for all in-
peer-reviewed journals between 1988 and 2017. cluded articles were as follows: 92.8% interrater agree-
Only full-text English-language articles were included, ment (k = 0.928, p = .000) and 90% intrarater agreement
and abstracts were excluded, as they may not always be (k = 0.905, p = .000) across all rating scale subsections,
representative of the content in the full article. Duplicate indicating acceptable agreement (Cohen, 1960). Scoring
references were filtered out from each database searched. disagreements were resolved through discussion.
In addition to the electronic databases search, the reference
lists of identified articles were also searched. The timescale Study Content Extraction
of all search strategies was from September 2015 to May The “descriptive–analytical” method of Arksey and
2017. O’Malley (2005) was utilized to collect standard infor-
To be included in the review, a study had to (a) in- mation from each study included in the scoping review.
clude participants who were adults (18 years or older) with Information regarding the authors, year of publication,
congenital or acquired epilepsy (with no restriction applied number of participants, nature of epilepsy etiologies, par-
to epilepsy etiology) and (b) use some sort of language ticipant characteristics, language modalities assessed, lan-
assessment tool, formal or informal. Studies assessing cere- guage measures used, and relevant findings was compiled.
bral dominance and cortical organization for language in
epilepsy were excluded as most did not employ or specify
detailed language testing procedures. In addition, articles Data Mining Procedures
solely involving neuropsychological tests of verbal memory Data mining focused on the ChaCha (a free social
and/or intelligence to describe language abilities were not platform that allows anyone to ask questions about a wide
included in the scoping review, as they are not considered range of topics), Epilepsy Foundation (a public Q&A forum,
true tests of language function; that is, such tests do not on which individuals post epilepsy-related questions), and
allow differentiating between the contributions of cognitive Twitter databases (a popular social networking platform

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Figure 1. Flowchart for scoping review procedure.

that allows users to post 140-character long messages); more specific phrases (e.g., “hard to remember words,”
these databases were used as they were the only ones the “difficulty during conversation,” “trouble thinking of
authors had permission to access. words,” “difficulty following a conversation”) helped in
The Word Adjacency Graph modeling, which is a better matching against the questions and comments avail-
social network analysis method, was implemented to ob- able in the data sets. Analysis also included identifying
tain a set of relevant questions from the three data sets, clusters of frequently discussed topics related to epilepsy-
recorded between 2009–2012, 2004–2015, and June 2014 related language problems from the text in the available
to March 2016, respectively. An initial list of keywords/ databases. Information regarding the geographic location,
phrases was generated based on the terminology and age, and gender of users was also obtained from all data
expressions that have been commonly used to describe sets, when users indicated such details.
epilepsy-related language problems in research studies and
online forums for individuals with epilepsy. The list was
revised to filter the retrieved results and obtain a set of Results
posts that specifically pertained to epilepsy-related lan-
guage problems. The final list of words and phrases was Scoping Review Findings
then used against a preselected set of known epilepsy- Out of a total of 4,424 potentially relevant online re-
related questions only (see Figure 2). Using longer and cords, the titles and abstracts of 116 articles were screened

Dutta et al.: Effects of Epilepsy on Language Functions 353


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Table 1. Rating scale used to assess the methodological quality of articles in the scoping review.

Section Quality of methodology criteria Scores (yes = 1, no = 0)

A Research design
The study objective was clearly stated.
The type of research was documented (i.e., case study, quasiexperimental, review, etc.).
Aims and design of the study set in the context of existing knowledge/understanding were
described clearly.
The rationale for the study, including how the design was related to the overall aims/objectives
of the study, was clearly outlined.
The test / intervention was clearly described and delivered consistently across the study population.
The outcome measures were prespecified, clearly defined, valid, reliable, and assessed consistently
across all study participants.
B Participant recruitment and demographics
The process of participant recruitment and the selection criteria for the study were clearly stated.
Information regarding the nature and severity of epilepsy, age of onset, age at testing, and education
was provided to describe the participants included in the study.
The sample size was sufficiently large to provide confidence in findings (i.e., the total number of
participants included at least 20 individuals), and justification of sample size was provided.
C Data collection
The techniques and testing procedures used to collect the data were adequately documented to
the extent that replication would be possible.
The majority of the variables were assessed using standardized measures for which normative
data exist.
The outcome measures of interest were taken both before and after the intervention, and statistical
analysis was conducted to compare pre-to-post changes.
D Data analysis
The specific techniques used to analyze the date were outlined.
Presentation of observations and discussion of explanations were provided.
E Research findings
Findings/conclusions are supported by data/study evidence and are clearly linked to the purposes
of the study.
The findings help in identifying new areas for investigation.
Limitations of evidence and what remains unknown/unclear or the need for further information/research
were discussed
TOTAL SCORE /17

Note. Adapted from Spencer et al. (2003; Copyright © 2003 Crown) and the National Heart, Lung and Blood Institute, National Institute of
Health, U.S. Department of Health and Human Services (2014).

for eligibility based on the a priori inclusionary/exclusionary studies received low scores in terms of research design
criteria (see Figure 1). Common reasons for exclusion in- and data collection (e.g., Davies, Hermann, & Wyler,
cluded the following: (a) focus on language lateralization 1997; Howell, Saling, Bradley, & Berkovic, 1994; Perrone-
versus description of the integrity of language abilities; Bertolotti, Zoubrinetzky, Yvert, Le Bas, & Baciu, 2012).
(b) failure to include assessments that specifically tested The processes of participant recruitment and selection
language functions and instead use only a basic evaluation were not clearly stated (e.g., Hermann, Wyler, Steenman,
of cognitive function, such as the Mini-Mental State Exam- & Richey, 1988; Langfitt & Rausch, 1996), particularly in
ination (Folstein, Folstein, McHugh, & Fanjiang, 2001) studies that also failed to document research design (e.g.,
or the Dementia Rating Scale (Mattis, 1988); and (c) the case study, quasiexperimental, review). The sample size
participant sample did not include adults. A final 49 studies of some studies was small (n < 20), limiting confidence in
passed the screening process. With the additional 17 articles findings (e.g., Bartha et al., 2004; Hermann & Wyler, 1988;
included from hand searching references of retrieved arti- Minkina et al., 2013). In terms of data collection, a few
cles, a total of 66 articles regarding language disorders in studies did not incorporate standardized language mea-
the context of adult epilepsy were included in the scoping sures (e.g., Bell, Seidenberg, et al., 2003; Hamberger &
review (see Table 2). Seidel, 2003; Hamberger & Tamny, 1999), and some scored
a “0” as they did not assess language outcomes before
Methodological Quality Assessment and after the intervention, instead only completing a
The 66 reviewed articles represented a range of study posttreatment evaluation (e.g., Glosser & Donofrio, 2001;
designs (e.g., case studies, cross-sectional, prospective). The Helmstaedter et al., 1998; Schwarz & Pauli, 2009). A num-
average quality rating score was 15.8/17 (range = 11–17): ber of studies failed to summarize their study limitations
23 received a full score, 24 received 16/17, and the remain- and highlight areas in need of further investigation (e.g.,
ing 19 received a score of 15 or less (see Table 3). Many Loddenkemper et al., 2004; Sadiq et al., 2012).

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Figure 2. List of keywords used for data mining procedure. the articles were likely affected by the inclusionary criterion
of being published in English; thus, some pertinent articles
may have been overlooked.
In terms of patient characteristics (see Table 2), the
mean age ranged from 20 to 67 years, with most studies
involving younger adults with epilepsy (i.e., age of 35 years
or younger). Whereas comparisons between different epi-
lepsy groups were common, only 14 articles compared the
language performances of participants with epilepsy to
those of age- and education-matched healthy control par-
ticipants (e.g., Giovagnoli et al., 2009; Kho et al., 2008;
Miller et al., 2016). Most frequently, participants had TLE,
with left-hemisphere TLE (LTLE) more frequent than
right-hemisphere TLE (RTLE). Some studies also tested
other participant groups including generalized epilepsy,
FLE, and hippocampal sclerosis (e.g., Davies et al., 1998;
Helmstaedter et al., 1998).
Most studies included a variety of language mea-
sures, with tests developed for the aphasic population most
popular. The Boston Naming Test (Kaplan, Goodglass, &
Weintraub, 2001) and Multilingual Aphasia Examination
(Benton, Hamsher, & Sivan, 1994) were most frequently
used, followed by the Boston Diagnostic Aphasia Exami-
nation (Goodglass & Kaplan, 1972), Western Aphasia Bat-
tery (Kertesz, 1982), Philadelphia Naming Test (Roach,
Schwartz, Martin, Grewal, & Brecher, 1996), and Token
Test (De Renzi & Vignolo, 1962). Six studies included lan-
guage tests developed by the study authors. Other studies
used more general, academic assessments to evaluate lan-
guage abilities (e.g., Wide Range Achievement Test–Revised;
Jastak & Wilkinson, 1984).
In terms of the language modalities tested, verbal flu-
ency (i.e., phonemic and semantic) and naming measures
were most popular. Auditory comprehension, repetition,
and reading and writing were occasionally tested in some
studies. Few studies assessed language functioning beyond
the word or sentence level, and many studies failed to pro-
vide information regarding the severity of the observed
language deficits. A more detailed summary of each lan-
guage modality is provided below.
Naming. Naming was the most frequently tested and
Study Content Summary the most affected language function, with 54 of the 66 stud-
The purpose of a large number of the studies was ies reporting naming difficulty in adults with epilepsy. LTLE
to compare and describe language functioning in adults was associated with the most significant naming difficul-
undergoing surgery to alleviate epilepsy symptoms (see ties characterized by significantly lower accuracy scores
Table 2). Language skills were most frequently assessed (e.g., Giovagnoli et al., 2009; Toledano et al., 2013) and lon-
along with other cognitive functions as a part of a routine ger response latencies (e.g., Bell, Seidenberg, et al., 2003;
neuropsychological examination at different time points Hamberger & Tamny, 1999) compared to the naming per-
across studies. Authors of the articles represented various formances of age- and education-matched healthy controls.
medical disciplines, including speech-language pathology, There were, however, some inconsistent findings across stud-
neurosurgery, neurology, epileptology, physical medicine, ies. For example, in contrast to the reports of differences in vi-
psychology, and cognitive neuroscience. Most studies were sual naming ability across epilepsy types (e.g., Fargo, Schefft,
published by researchers in the United States (48%, n = 32), Dulay, Privitera, & Yeh, 2005; Ramirez et al., 2010), four
followed by Germany (8%, n = 5), with one to two publi- studies identified no such differences (Hamberger & Seidel,
cations emanating from each of the following: the United 2003; Hamberger, Seidel, McKhann, & Goodman, 2010;
Kingdom, France, Sweden, Austria, the Netherlands, Italy, Hamberger & Tamny, 1999; Lomlomdjian, Solis, Medel, &
Australia, China, Japan, India, Brazil, Argentina, and Kochen, 2011). Similarly, three studies reported poor auditory
Spain. These findings pertaining to the country of origin of naming (i.e., naming objects based on oral descriptions)

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356
American Journal of Speech-Language Pathology • Vol. 27 • 350–378 • March 2018

Table 2. Summary of findings from studies included in the scoping review.

Study Number of participants Tests Language modalities Results

Hermann & ATL of dominant ATL of nondominant MAE-COWAT, Visual naming, Pre-op: dominant temporal
Wyler (1988) lobe (n = 15) lobe (n = 14) Token Test sentence lobe foci associated
Mean age of onset 13.5 18.4 repetition, with poorer language
Mean age 31.3 36.5 oral spelling, function
Education 12.4 11.9 auditory Post-op: dominant ATL
Gender (M/F) 7/8 5/9 comprehension group performed poorly
(words/phrases), on all language tests
reading
comprehension
(words and
phrases)
Hermann TLE (n = 25) MAE, Token Visual naming, Visual naming, verbal
et al. (1988) Test sentence fluency and auditory
repetition, comprehension scores—
oral spelling, most powerful predictors
auditory of verbal memory and
comprehension learning performance
(words/phrases),
reading
comprehension
(words and
phrases),
verbal fluency
Stafiniak LT-ER LT-NER RT-ER RT-NER BNT Visual naming 6 out of 10 patients declined
et al. (1990) (n = 12) (n = 10) (n = 17) (n = 6) post left ATL in naming;
Mean age of onset 1 14.4 1.5 19.3 no decline in right ATL
Mean age 26.2 30.7 32.7 33.2 patients
Education 13.0 13.2 13.6 13.0
Gender (M/F) 6/6 6/4 9/8 3/3
Hermann ATL of dominant MAE, Token Visual naming, No significant language loss
et al. (1991) lobe (n = 29) Test sentence noted post-op; significant
ATL of nondominant repetition, improvement in receptive
lobe (n = 35) oral spelling, language
auditory
comprehension,
reading
comprehension
(table continues)

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Table 2. (Continued).

Study Number of participants Tests Language modalities Results


Howell et al. LTLE RTLE PGE BNT, MAE- Visual naming, LTLE: significantly lower
(1994) (n = 10) (n = 10) (n = 10) COWAT, narrative naming and lexical
Mean onset age 16.6 22.3 12.3 Cartoon discourse retrieval difficulties
Mean age 34.7 35.2 25.2 description
Gender (M/F) 6/4 4/6 4/6
Loring et al. LT (n = 12) RT (n = 11) MCG aphasia Visual naming, Post-op: TLE patients
(1994) One-year f/u One-year f/u screening auditory showed subtle language
(n = 18) (n = 16) test, MAE- comprehension, deficits; poor visual
Age 29 25.9 COWAT, repetition, naming
28.1 25.7 Token Test verbal fluency
(1 year) (1 year) 1-year follow-up: improved
Education 11.3 13 COWAT scores,
12.8 12.5 generalized verbal
(1 year) (1 year) fluency decline
Saykin et al. LT-ER RT-ER LT-NER RT-NER MAE-COWAT, Semantic verbal Pre-op: LT groups showed
(1995) (n = 45) (n = 49) (n = 27) (n = 33) BDAE, fluency, visual selective visual naming
Mean onset age 8.6 10.7 18.4 20.9 WRAT-R naming, sentence deficits
Mean age 29.2 32 31.4 34.7 repetition, auditory Post-op: LT-NER showed
Education 13 12.9 13.1 13.8 comprehension, overall language decline
Gender (M/F) 44/56 43/57 63/37 45/55 oral reading
Langfitt & Patients with epilepsy (n = 59) BNT Visual naming Increased word-finding
Rausch difficulty post left ATL
Dutta et al.: Effects of Epilepsy on Language Functions

(1996) (1 year f/u)


O’Shea et al. Medically refractory left (n = 23) MAE Visual naming, Increased word retrieval
(1996) Medically refractory right (n = 16) repetition, deficits in TLE vs.
Idiopathic primary GE-controls (n = 38) auditory other groups
comprehension
Davies et al. MLTLE Lat/R TLE MAE, Token Visual naming, Impaired language function
(1997) (n = 39) (n = 13) Test sentence in LTLE vs. RTLE
Mean onset age 11.9 7.6 repetition,
Mean age 30.4 28.5 oral spelling,
Education 13.2 12.6 auditory
comprehension
(words and
phrases), reading
comprehension
(words and
phrases)
(table continues)
357

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Table 2. (Continued).

Study Number of participants Tests Language modalities Results


Hermann R-ATL R-ATL L-ATL L-ATL MAE, Token Visual naming, L-MTLE+ performed
et al. (1997) MTLE− MTLE+ MTLE− MTLE+ Test sentence significantly worse
(n = 62) (n = 45) (n = 66) (n = 41) repetition, than L-MTLE− on
Mean onset age 20.2 6.1 20.6 6.9 verbal fluency, naming, auditory
Mean age 32 31.8 33.4 29.8 oral spelling, and reading
Education 3.6 11.8 13.6 12.5 auditory comprehension;
and reading R-MTLE+ performed
comprehension significantly worse
of words and than R-MTLE− on
phrases naming
Helmstaedter FLE (n = 33) German Phonemic fluency FLE patients showed
et al. (1998) RTLE (n = 21) Intelligence mild deterioration
LTLE (n = 24) Test (Word (3-month f/u)
Healthy controls (n = 22) Fluency
subtest)
Davies et al. HS− (n = 34) HS+ (n = 61) MAE, BNT Visual naming, Left hemisphere
(1998) Mean onset age 19.9 7.2 verbal fluency dominant patients
Mean age 32.4 30.9 at risk for naming
Gender (M/F) 16/18 29/32 deficits after ATL
(may be associated
with no or minimal HS)
Seidenberg Nonsurgical Left MTLE ATL non- Right ATL non- MAE Visual naming, The left non-MTLE
et al. (1998) epilepsy (n = 30) MTLE MTLE MTLE auditory group showed
(n = 40) (n = 23) (n = 21) (n = 13) comprehension significant decline
Mean age 15.5 6.7 20.5 5.6 17.9 in naming compared
of onset to MTLE
Mean age 32.2 30.2 32.6 33.8 31.3
Education 13.5 12.2 13.4 11.6 13.8
Giovagnoli Temporal lobe epilepsy (n = 26) Standardized Visual naming, Left TLE-significant
(1999) Extratemporal lobe epilepsy (n = 21) stimuli auditory verbal semantic
Healthy controls (n = 23) developed comprehension, memory deficits
by Snodgrass semantic
& Vanderwart judgment,
(1980) and spontaneous
Novelli et al. speech
(1986), Semantic
questionnaire,
Token Test
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Table 2. (Continued).

Study Number of participants Tests Language modalities Results


Hamberger LTLE RTLE Healthy Stimuli developed Auditory and LTLE: poorer scores on
& Tamny (n = 10) (n = 10) controls by authors visual naming auditory naming.
(1999) (n = 62) No group differences on
Mean age 34.5 33.9 27.1 visual naming
Education 14.7 15.1 16.3
Hermann Individuals with epilepsy (n = 217) BNT Visual naming Significant decline in
et al. (1999) Mean age of onset: 14.1 naming scores post ATL
Mean age: 31.9 resection regardless of
Education: 13.1 surgical technique used
Gender: 58.9% (F), 41.1% (M)
Field et al. TLE Healthy BNT, MAE- Visual naming, Poorer visual naming
(2000) (n = 16) controls COWAT, narrative in LTLE; no group
(n = 17) Cartoon discourse difference on COWAT;
Age range 16–61 16–61 description (speaking Discourse: increased
Education 11.8 12.9 time, word speaking time for TLE;
Gender (M/F) 9/7 9/8 count, and no group difference on
fluency) fluency measures
Strauss et al. L-ATL (n = 79) BNT Visual naming Impaired naming ability
(2000) Mean age of onset: 13.6 for living things
Mean age: 31.2
Gender: 36 (M); 43 (F)
Glosser & R-ATL L-ATL BNT, ANT Object and L-ATL group showed
Donofrio (n = 26) (n = 30) action naming, selective deficits with
Dutta et al.: Effects of Epilepsy on Language Functions

(2001) Mean onset age 11.2 14.1 synonym nouns compared to


Mean age 31.2 34.6 generation, verbs in naming and
Education 12.8 13.3 semantic comprehension
Gender 38% (M)/ 43% (M)/57% (F) judgment
62% (F)
Paradiso et al. Patients with Patients with no MAE, Token Verbal Lower scores among
(2001) depression depression Test, WRAT-R performance, depressed participants
(n = 24) (n = 46) reading and on all tests
Mean onset age 11.3 10 visual naming
Mean age 31.6 29
Education 12.4 13.1
Gender 66.6% (F)/ 33.3% (F)/
33.4% (M) 66.7% (M)
Moore & B/L TLE (n = 80) Graded Naming Verbal fluency, Mild expressive language
Baker (2002) LTLE (n = 109) Test, Benton visual naming deficits; affected visual
RTLE (n = 84) Verbal Fluency naming
Task
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360
American Journal of Speech-Language Pathology • Vol. 27 • 350–378 • March 2018

Table 2. (Continued).

Study Number of participants Tests Language modalities Results


Bell, Seidenberg, TLE (n = 16) Healthy Stimuli developed Auditory and TLE group performed
et al. (2003) controls by authors visual naming worse on auditory
(n = 11) naming vs. controls;
Mean onset age 20.1 — severity of word-finding
Mean age 33.4 31 difficulty correlated
Education 12.6 13.6 better with auditory
Gender (M/F) 19%/81% 45%/55% naming scores
Bell, Dow, TLE (n = 27) Healthy Discourse (from Narrative and Procedural discourse:
et al. (2003) controls a battery of procedural no significant group
(n = 28) neuropsychological discourse differences; narrative
Mean onset age 7.1 — tests) discourse: TLE group
Mean age 35.4 33 worse than controls.
Education 12.9 12.2 Reduced speech rate,
inadequate descriptive
detail, excessive word
fragment and repetition
errors
Hamberger & Healthy Retested LTLE RTLE Nonsurgical Stimuli developed Visual and Visual naming: no
Seidel (2003) controls healthy (n = 34) (n = 22) epilepsy by authors auditory significant group
(n = 100) controls (n = 20) naming differences. Auditory
(n = 60) naming: significantly
Mean age 34.3 36.5 39.9 39.2 38.8 lower scores for LTLE
Education 15.6 15.5 14.7 14.8 14.1 vs. RTLE; significantly
correlated with
perceived word
finding difficulties
Oddo et al. TLE group (n = 71) BNT, Barcelona Visual naming, Impaired language in
(2003) Healthy controls (n = 25) Reading Test, reading 33% of patients;
Token Test naming and word
finding difficulty
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Table 2. (Continued).

Study Number of participants Tests Language modalities Results


Schefft et al. LTLE RTLE BNT, VNT subtest Visual naming LTLE worse than RTLE
(2003) (n = 40) (n = 40) of the MAE on naming; phonemic
Mean onset age 18.4 17.5 paraphasias noted
Mean age 34.7 36.2
Education 12.4 13.1
Bartha et al. TLE (n = 10) AAT, IBT, Word Communicative Pre-op: some showed
(2004) Mean age of onset: 14.3 years Fluency Test behavior, word finding and
Mean age: 43.1 years (German) articulation, comprehension deficits.
Gender: 6(M); 4(F) prosody, Affected word fluency
semantic, in all patients
syntactic Post-op: no significant
structure of pre vs. post language
spontaneous differences in some,
speech profound word finding
impairment (n = 4);
circumlocutions and
semantic paraphasias
noted. Affected
comprehension of
words/sentences.
Reading and
writing-intact
Loddenkemper Patient with epilepsy (n = 1) Standard Spontaneous Expressive aphasia; word
Dutta et al.: Effects of Epilepsy on Language Functions

et al. (2004) Age: 55 neurological speech, finding difficulties in


examination auditory conversation, reduced
comprehension, word fluency and
word and sentence repetition;
sentence decline in auditory
repetition, comprehension and
visual naming, sentence repetition
and reading (8 months post)
Bartha et al. TLE (n = 23) AAT, IBT, Word Language Fluent, well-articulated
(2005) Mean age of onset: 13.9 Fluency Test comprehension, spontaneous speech;
Mean age: 43.2 (German) word fluency, 2 out of 23 patients
production had word finding
of single and deficits, mild sentence
compound repetition and word
words and composition errors;
sentences all showed word
fluency impairment
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362
American Journal of Speech-Language Pathology • Vol. 27 • 350–378 • March 2018

Table 2. (Continued).

Study Number of participants Tests Language modalities Results


Fargo et al. DTLE NDTLE PNES BNT Visual naming LTLE worst on naming;
(2005) (n = 52) (n = 47) (n = 54) semantic paraphasias
Mean onset age 19.4 17.3 29.4 noted in all patients
Mean age 36.0 36.1 35.0 (>TLE)
Education 12.2 13.3 12.7
Fritz et al. TGB (n = 15) TPM (n = 15) BNT, Leistungs- Phonemic TGB group: significant
(2005) Mean onset age 14.6 11.2 Pruf System fluency, decrease in verbal
Mean age 39.2 33.8 Test (Word semantic fluency and language
Gender (M/F) 9/6 9/6 Fluency subtest), fluency, comprehension. TPM
Education 15 15 AAT (Token auditory group: worse than
Test subtest) comprehension, TGB group on
and visual language tests
naming
Schwarz et al. TLE (n = 45) BNT Visual naming Seizure onset age of
(2005) Healthy controls (n = 40) 14 years or later
associated with
greater risk of naming
impairment post
epilepsy surgery
Alessio et al. Patients with MTLE with ipsilateral hippocampal atrophy (n = 39) BNT, Verbal Verbal fluency, Degree of hippocampal
(2006) Mean age: 35 Fluency Test visual naming atrophy positively
correlated with
extent of verbal
fluency impairment
Griffith et al. Older Amnestic Healthy CFL Word Verbal fluency Older adults with epilepsy
(2006) adults MCI controls Fluency Test had worst fluency
with (n = 26) (n = 27)
epilepsy
(n = 26)
Mean age 64.7 65.2 65.4
Gender (M/F) 14/12 13/13 11/15
Education 13 13.9 13.9
Piazzini et al. Epilepsy Healthy Verbal Fluency Letter fluency Older adults with epilepsy
(2006) (n = 40) controls Test (Novelli showed significantly
(n = 40) et al., 1986) poorer verbal fluency
Mean age of onset 20 — skills
Mean age 67 67.5
Education 8.2 8.5
Hamberger Nonlesional Lesional BNT, ANT Auditory and Nonlesional group likely
et al. (2007) (n = 25) (n = 18) visual naming to have more naming
Mean onset age 16.8 27.8 difficulty vs. lesional
Mean age 35.6 30.9 group
Education 14.6 15
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Table 2. (Continued).

Study Number of participants Tests Language modalities Results


Drane et al. Dominant Nondominant Other MAE, BNT Visual naming Category-specific
(2008) TLE TLE (n = 6) seizure recognition and
(n = 10) onset naming deficits in
(n = 6) individuals with TLE
Mean onset age 29.2 17.1 19.4
Mean age 40.1 38.7 30
Education 13.3 13.8 11.8
Kho et al. Dominant Nondominant Healthy AAT, Token Single word and No significant differences
(2008) TLE TLE (n = 16) controls Test, prosody sentence between pre- and
(n = 16) (n = 47) comprehension understanding post-op scores except
Mean onset age 18.8 19.8 — tests (auditory and naming; more affective
Mean age 35.6 38.1 34.5 visual), repetition, prosody errors
Education (median) 5 5 5 visual naming,
writing,
spontaneous
speech
McDonald TLE (n = 17) BNT, Delis-Kaplan Letter fluency, Structural compromises
et al. (2008) Healthy controls (n = 17) Executive visual naming noted in relation to
Functioning memory and language
System (verbal in TLE
fluency subtest)
Ramirez et al. DOM NDOM BNT, BDAE Visual naming Quantitative differences
(2008) (n = 32) (n = 28) in naming between
Mean age 32.7 37.5 both groups
Dutta et al.: Effects of Epilepsy on Language Functions

Education 12.5 13.4


Giovagnoli ULD Cryptogenic Healthy BNT, Token test Language ULD: significant
et al. (2009) (n = 21) TLE controls comprehension, impairments in verbal
(n = 21) (n = 21) verbal initiative initiative, fluency,
Mean onset age 12.3 17.4 — and fluency, comprehension,
Mean age 39.2 39.7 41.8 lexical retrieval and naming; similar
Education 8.7 10.4 9.5 impairments in patient
groups except for
auditory comprehension
and naming
Schwarz & LTLE (n = 24) BNT, AVSC, ACW, Visual naming, Increased naming decline
Pauli (2009) RTLE (n = 34) WPR, MWT-B semantic in LTLE-associated
Mean onset age: 17 processing, with impaired semantic
Mean age: 34.8 phonological functions; difficulty
Gender: 20(M); 14(F) input and with categorization
processing, of objects
verbal
intelligence
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364

Table 2. (Continued).

Study Number of participants Tests Language modalities Results


American Journal of Speech-Language Pathology • Vol. 27 • 350–378 • March 2018

Trebuchon-Da LTLE RTLE Stimuli developed Word fluency, LTLE worse than RTLE;
Fonseca et al. (n = 28) (n = 15) by authors, word and lexical access difficulty
(2009) Mean onset age 18 16 Token test sentence
Mean age 42 34 repetition,
Gender (M/F) 9/18 10/11 visual naming
Education Level 1(14); Level 1(6);
Level 2(7); Level 2(5);
Level 3(6) Level 3(3)
Hamberger Left MTLE Right MTLE BNT, ANT, VNT Auditory and Left MTLE: decline in
et al. (2010) (n = 25) (n = 20) subtest of the visual naming visual but not auditory
Mean age 38.9 37 MAE naming; RTLE better
Education 14.7 15.2 than LTLE on auditory
Gender (M/F) 7/18 10/11 naming; RTLE = LTLE
on visual naming
Ramirez et al. FLE Left Right MTLE BNT, MAE-COWAT, Visual naming, Left MTLE = FLE (across
(2010) (n = 30) MTLE (n = 34) Token Test word fluency, all language measures);
(n = 43) auditory right MTLE-intact
Mean age 33.4 40.6 38.3 comprehension language
Education 13.6 12.9 13.8 Depression associated
with worse language
performance
Yogarajah LTLE RTLE (n = 20) McKenna Graded Visual naming, Structural reorganization
et al. (2010) (n = 26) Naming Test, letter fluency following ATL resection,
Mean age 37 37 Verbal Fluency which may damage
Gender 10 (M)/16 (F) 8 (M)/12 (F) Test dorsolateral language
pathway
Lomlomdjian LTLE RTLE (n = 13) BNT, ANT Visual and auditory Significantly lower BNT
et al. (2011) (n = 13) naming and ANT scores for
Mean onset age 10 12.5 LTLE vs. RTLE; 1/3
Mean age 40.7 34.6 showed difficulty
Education 10 12.1 with word finding
Gender (M/F) 5/8 7/6 in spontaneous speech,
no differences between
auditory and visual
naming
Maeda & TLE (n = 1) Aphasia test Reading, writing, Alexia with agraphia
Ogawa (Japanese) visual naming, (in Kanji) due to TLE
(2011) calculation
questions
Wang et al. TLE (n = 65) Modified MAE, Verbal fluency, 78% of TLE patients
(2011) Mean age of onset: 21.2 WAIS-III (Verbal visual naming, showed language
Mean age: 33.5 Comprehension auditory deficits
Education: 12.6 Index), Token comprehension
Test
Bonelli et al. LTLE (n = 24) RTLE (n = 20) McKenna Graded Visual naming, Greater naming decline in
(2012) Median onset age 6 12 Naming Test, verbal fluency LTLE post-op vs. RTLE
Gender 12(F)/12 (M) 13(F)/7 (M) Verbal Fluency
Test
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Table 2. (Continued).

Study Number of participants Tests Language modalities Results


Perrone- Left mesiotemporal DO80 (Test of Spontaneous speech, Phonemic and semantic
Bertolotti epilepsy (n = 1) Denomination- phonemic fluency, abilities unaltered;
et al. (2012) Healthy controls (n = 24) French); semantic fluency, no differences in
WAIS-III and visual naming spontaneous speech
noted
Sadiq et al. TLE (n = 1) Standard Spontaneous speech, Nonfluent spontaneous
(2012) Age: 67 neurological repetition, visual speech, unable to
examination naming, reading, read, write, or repeat
writing, and auditory simple words or
comprehension sentences, visual
naming difficulty;
pronounced paraphasic
errors. Comprehension
unaffected
Szaflarski & TLE on topimerate (n = 8) BNT Verbal fluency Epilepsy patients poorer
Allendorfer RTLE on topimerate (n = 8) vs. healthy controls;
(2012) TLE not on topimerate (n = 8) significant fMRI signal
Healthy controls (n = 32) differences between
those taking vs. not
taking medication
Gargaro Ipsi MTLE B/L MTLE Contra MTLE GCI Controls BNT Visual naming Ipsilateral and bilateral
et al. (n = 105) (n = 105) (n = 53) (n = 32) (n = 135) temporal epilepsy had
(2013) Despite HS lower naming scores
Dutta et al.: Effects of Epilepsy on Language Functions

Mean onset age 9.1 8.5 8.4 7.6 10.4 (post-op); Control
Mean age 36.8 36.6 36.5 35.3 37.2 group had significant
Gender 54% (F)/ 55% (F)/ 45% (F)/ 59% (F)/ 58% (F)/ declines in naming
46% (M) 45% (M) 55% (M) 41% (M) 42% (M) after surgery
Education 6.9 5.6 7.2 2.4 9.2
Gauffin et al. Patients with Healthy FAS, TLC Sentence repetition, GE: sentence repetition,
(2013) epilepsy controls (Swedish)- construction, construction, and
(n = 11) (n = 17) BeSS tasks comprehension, comprehension
Mean onset age 26.5 25.5 text comprehension problems
Mean age 24 ± 8 20 ± 7 GE = Healthy controls on
Education 13.2 13.2 text comprehension
Gender (M/F) 5/6 5/6
Janecek et al. Right ATL (n = 10) BNT Visual naming Left ATL patients with
(2013) Left ATL (n = 12) bilateral language at
greatest risk for naming
decline vs. right ATL
patients
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American Journal of Speech-Language Pathology • Vol. 27 • 350–378 • March 2018

Table 2. (Continued).

Study Number of participants Tests Language modalities Results


Minkina et al. TLE (n = 1) WAB, BNT, Low- Verbal and visual Mild naming deficits;
(2013) Age = 61 Frequency memory; visual AQ-within functional
Common naming limits; average to high
Noun Test scores on verbal and
visual memory; pre-
and posttreatment
language test
scores did not
significantly differ
Sarkis et al. FLE verbal FLE verbal MAE-COWAT Verbal fluency 25% of all participants had
(2013) fluency fluency verbal fluency decline
decliners nondecliners post FLE surgery
(n = 9) (n = 27)
Mean onset age 10.1 11.6
Mean age 33 30.6
Gender (M/F) 5/4 15/12
Education 12.9 12.6
Toledano TLE Healthy PNT, the Cambridge Visual naming, Patients with left-sided
et al. (2013) (n = 15) controls 64-Item Naming visual semantic lesions demonstrated
(n = 10) Task, Camel and associative aphasia during
Mean onset age 23.5 — Cactus Test, knowledge, their seizures with
Mean age 38.5 37 Cambridge categorical pronounced semantic
Gender 7(F), 8(M) NR Semantic Battery- fluency test impairment
Education 15.6 16 Category Fluency
Test
Witt et al. TPM Without Untreated Healthy Leistungs-Pruf- Phonemic verbal 77% of TPM patients,
(2013) (n = 421) TPM (n = 108) controls System (verbal fluency 22% of untreated
(n = 351) (n = 108) fluency subtest) patients, and 31% of
Mean onset age 15.7 17 29.9 — patients w/o TPM had
Mean age 35.5 34.5 36.3 35 impaired verbal fluency
Gender (M/F) 214/207 186/165 68/40 50/50
Education 203 (>10); 188 (>10); 50 (>10); 76 (>10);
218 (<10) 163 (<10) 50 (<10) 32 (<10)
Zhang et al. Epilepsy patients (n = 24) WAB (Chinese) Fluency, 20 patients showed drop
(2013) comprehension, in AQ; 1 patient had
repetition, visual surgery-induced
naming, reading, deficits; language
writing decline shortly after
surgery but improved
after 3 months for
15 patients
Drane et al. TL resections (n = 39) BNT Visual naming 21 of 22 LTLE patients
(2015) SLAH procedure (n = 19) showed performance
decline following TL
resections vs. SLAH
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Table 2. (Continued).

Study Number of participants Tests Language modalities Results


Ljunggren FLR (n = 30) Controls Chicago Word Verbal fluency Verbal fluency ability
et al. (2015) (n = 25) Fluency Test, remained stable at the
Mean onset age 16 — COWAT 2-year f/u postsurgery
Mean age 31.9 35
Education 12.1 11.6
Rai et al. TLE (n = 59) ETLE (n = 43) WAB Spontaneous 47% of refractory
(2015) Mean onset age 12(±8) 9.7(±8) speech, epilepsy patients
Education 13.2 13.2 comprehension, had language deficits;
Gender 38.2% (M)/ 29% (M)/ repetition, and anomic aphasia (41%);
61.8% (F) 71% (F) visual naming no group difference
on WAB subtests,
except repetition lower
for FLE vs. TLE (30%)
Miller et al. Patients with Healthy BNT, verbal Visual naming; ~16% of epilepsy group
(2016) epilepsy controls fluency test semantic verbal showed poorer verbal
(n = 35) (n = 29) fluency memory and language
Mean age 65.2 61 skills vs. healthy controls
Gender 52.6% (F)/ 89.7% (F)/
47.4% (M) 10.3% (M)
Education 14.7 15.4
Dutta et al.: Effects of Epilepsy on Language Functions

Note. AAT = Aachener Aphasia Test (Huber et al., 1983); ACW = Auditory Comprehension Test for Words (Blanken, 1999); ANT = Action Naming Test (Hamberger & Tamny, 1999;
Hamberger & Seidel, 2003); AQ = aphasia quotient; ATL = anterior temporal lobectomy; AVSC = Auditory and Visual Speech Comprehension Test for Word Meaning (Blanken, 1996);
B/L = bilateral; BDAE = Boston Diagnostic Aphasia Examination (Goodglass & Kaplan, 1972); BeSS = Bedomning av Subtila Sprakstorningar (Assessment of Subtle Language Deficits;
Laakso et al., 2000); BNT = Boston Naming Test; CFL = phonemic fluency test (Spreen & Strauss, 1991); COWAT = Controlled Oral Word Association Test from the MAE (Benton
et al., 1994); DOM = dominant lobe; DTLE = dominant temporal lobe epilepsy; ER = early risk for developing seizures; ETLE = extratemporal lobe epilepsy; F = female; FAS = Swedish version
of the COWAT (as in Gauffin et al., 2013); FLE = frontal lobe epilepsy; FLR = frontal lobe resection; fMRI = functional magnetic resonance imaging; f/u = follow-up; GCI = global cognitive
impairment; GE = generalized epilepsy; HS = hippocampal sclerosis; IBT = Innsbrucker Benenn Test (Bartha et al., 2001); L-ATL = left anterior temporal lobectomy; Lat/R = lateral/right;
LT = left; LTLE = lateral temporal lobe epilepsy; M = male; MAE = Multilingual Aphasia Examination (Benton et al., 1994); MCG = bedside aphasia screening test (Benson, 1985); MCI = mild
cognitive impairment; MLTLE = mesial lateral temporal lobe epilepsy; MTLE = mesial temporal lobe epilepsy; MWT-B = Mehrfachwahl-Wortschatz-Intelligenz Test (Lehrl, 2005); NDOM =
nondominant lobe; NDTLE = nondominant temporal lobe epilepsy; NER = not at early risk for developing seizures; NR = not reported; PGE = primary generalized epilepsy; PNES =
psychogenic nonepileptic seizures; PNT = Philadelphia Naming Test; R-ATL = right anterior temporal lobectomy; RT = right; RTLE = right hemisphere temporal lobe epilepsy;
SLAH = stereotactic laser amygdalohippocampotomy; TGB = tiagabine; TL = temporal lobe; TLC = Test of Language Competence (Wiig & Secord, 1989); TLE = temporal lobe
epilepsy; TPM = topiramate; ULD = Unverricht-Lundborg disease; VNT = Visual Naming Subtest of the MAE (Benton et al., 1994); WAB = Western Aphasia Battery; WAIS-III =
Wechsler Adult Intelligence Scale–Third Edition (Wechsler, 1997); WPR = Word Production Test (Blanken et al., 1999); WRAT-R = Wide Range Achievement Test–Revised (Jastak
& Wilkinson, 1984).
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Table 3. Proportion of studies receiving full scores in each subsection of the quality rating scale.

Total articles reviewed: 66


A B C D E
Research design Participant recruitment and demographics Data collection Data analysis Research findings

33 55 50 62 59
43% 81% 74% 93% 88%

among individuals with TLE, but Hamberger et al. (2010) 1991). Seven studies included oral reading measures, with
identified no such deficits. Naming was most frequently evalu- compromised word and sentence reading performance
ated in terms of noun retrieval, with only one study (Glosser noted in TLE (e.g., Maeda & Ogawa, 2011; Paradiso,
& Donofrio, 2001) testing verb retrieval. Only four studies Hermann, Blumer, Davies, & Robinson, 2001). Writing
conducted qualitative analyses of naming errors, with seman- skills were assessed in four studies: In two investigations,
tic and phonemic paraphasias most frequently reported impaired sentence-level writing was identified in only par-
(Bartha et al., 2004; Fargo et al., 2005; Sadiq et al., 2012; ticipants with TLE (Maeda & Ogawa, 2011; Sadiq et al.,
Schefft, Testa, Dulay, Privitera, & Yeh, 2003). 2012).
Verbal fluency. Verbal fluency measures (i.e., phone- Repetition. Of the 15 studies examining repetition
mic, semantic, or both) were common, being used in 28 ar- skills, most (n = 10) reported word- and sentence-level
ticles; no study included an action word/verb fluency task. repetition deficits in TLE participants (e.g., Bartha et al.,
Both epilepsy as well as antiepilepsy medications were 2005; Loddenkemper et al., 2004), albeit similar problems
shown to negatively affect verbal fluency performance were also identified in other epilepsy types (e.g., FLE by
in at least some individuals. That is, some individuals gen- Rai et al., 2015; generalized epilepsy by Gauffin et al.,
erated significantly fewer category exemplars compared 2013).
to the established test norms (e.g., Bartha et al., 2004; Spoken discourse. Spoken discourse production was
Loddenkemper et al., 2004). In studies investigating effects studied using a combination of measures reflecting speech
of antiepileptic medications, individuals prescribed topiramate production abilities as well as use of linguistic structure
tended to demonstrate significantly lower verbal fluency and complexity. Three studies evaluated discourse produc-
scores compared to those patients not taking this medica- tion via cartoon story descriptions: Howell et al. (1994)
tion (e.g., Fritz et al., 2005; Witt, Elger, & Helmstaedter, evaluated the phonation times and pause durations of the
2013). In addition, Bartha et al. (2004) noted frequent ver- participants’ speech, whereas Field et al. (2000) and Bell,
bal perseverations in some individuals with epilepsy during Dow, et al. (2003) conducted more in-depth analyses in-
this task. Across epilepsy types, TLE patients were most af- cluding documenting speaking rate and time, word counts,
fected (e.g., McDonald et al., 2008; Trebuchon-Da Fonseca fluency, a noncommunicative index, core story compo-
et al., 2009). Verbal fluency was also negatively affected nents, and a total words-to-clause index. Bell, Dow, et al.
in FLE (e.g., Helmstaedter et al., 1998, reported mild dete- (2003) also examined procedural discourse in individuals
rioration in phonemic fluency ability in FLE vs. TLE). with TLE. Howell et al. (1994) and Bell, Dow, et al. (2003)
Auditory comprehension. Less than half of the studies documented mild narrative discourse deficits in partici-
(n = 22) examined auditory comprehension skills. Difficul- pants with TLE, characterized by longer pause durations,
ties with auditory comprehension of words, grammatically slower speaking rate, and inadequate descriptive detail com-
simple sentences, and more complex verbal material (e.g., pared to individuals with generalized epilepsy or healthy
Aachener Aphasic Comprehension subtest; Huber, Poeck, controls, respectively. Field et al. (2000), however, observed
Weniger, & Williams, 1983; Token Test) were most com- no such changes in their participants with TLE.
mon in TLE (e.g., Bartha et al., 2004; Fritz et al., 2005; Nine studies analyzed discourse data from semi-
Loddenkemper et al., 2004) and FLE (e.g., Ramirez et al., structured interviews (e.g., subtests from standardized
2010). Impairments, however, were inconsistent across stud- aphasia tests, part of a routine neurological evaluation)
ies, with some researchers concluding that auditory com- and examined variables such as overall communicative
prehension is unaffected in epilepsy (e.g., Kho et al., 2008; effectiveness, articulation, prosody, speech automatisms,
Sadiq et al., 2012). syntactic structure, word retrieval difficulties, and infor-
Reading and written language skills. Across studies, mativeness. The findings were inconsistent across these
reading and writing were infrequently examined. Among the studies. For example, whereas two studies identified labored
three studies that evaluated reading comprehension of words and mildly nonfluent spoken output in TLE (Loddenkemper
and phrases, two identified mild difficulties among partic- et al., 2004; Sadiq et al., 2012), Perrone-Bertolotti et al.
ipants with TLE (Hermann, Seidenberg, Schoenfeld, & (2012) found no such problems before or after surgery for
Davies, 1997; Hermann & Wyler, 1988), whereas the third TLE. Uniquely, Lomlomdjian et al. (2011) designed a ques-
study found no such deficits (Hermann, Wyler, & Somes, tionnaire to evaluate the perception of spontaneous speech

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difficulties in individuals with RTLE or LTLE and found The identified content clusters appeared to represent
higher perceived difficulty among those with LTLE, who queries regarding epilepsy-related language and communi-
reported frequent word finding difficulties during conversa- cation difficulties and general cognitive side effects. The
tion. No study evaluated written discourse production. most frequently used words and phrases included aphasia,
speech, hard, trouble, disorder, trouble reading, and speech
therapist, with topics of the posts varying widely. Within
Data Mining Findings the context of their epilepsy-related questions and postings,
From the filtered set of queries, 10,000 epilepsy- users mentioned word finding difficulties, aphasia, reading
related and 9,200 language-related questions that matched and writing difficulties, verbal memory loss, and/or surgery
our a priori keywords/phrases were identified from the and medication effects on speech and language skills, fol-
ChaCha database. Just under half of the content categories lowing onset of epilepsy (see Figure 4).
(i.e., 6/16) were found to be relevant (see Figure 3). The Demographic information could only be obtained from
Epilepsy Foundation data yielded 111 posts relevant to the the ChaCha data. In terms of gender, 66.2% of the users
search topic, whereas the Twitter data yielded no relevant asking questions relevant to language difficulties in epilepsy
posts. were female. Questions were posted by users between ages

Figure 3. Discussion topics identified through Word Adjacency Graph Modeling clustering analysis.

Dutta et al.: Effects of Epilepsy on Language Functions 369


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Figure 4. A selection of questions and posts from ChaCha and Epilepsy Foundation data.

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of 13 and 65 years, with younger adults posting more with epilepsy, and the connectivity between these neural
frequently. The majority of the posts were retrieved from regions and mesial temporal lobe structures may explain
users in the Pacific and Northeastern regions of the the overlap in the language profile frequently observed in
United States. FLE and TLE (Ramirez et al., 2010; Sarkis et al., 2013).
Accordingly, the presence and description of language
problems associated with ETLE must be investigated in
Discussion greater detail.
The overall purpose of this study was to investigate With respect to participant age, very little is known
language abilities in adults with epilepsy. In addition to about the effect of epilepsy on language functions in older
compiling findings regarding epilepsy-related language dif- adults (Griffith et al., 2006). Only five studies in our
ficulties from existing studies, the main focus of the scop- scoping review, all of which identified language deficits,
ing review was to identify and evaluate issues relating to included adults who were 60 years or older (Field et al.,
methodology of and data interpretation within these studies. 2000; Griffith et al., 2006; Miller et al., 2016; Piazzini,
The current investigation also applied data mining applica- Canevini, Turner, Chifari, & Canger, 2006; Sadiq et al.,
tions to social network data to identify the language-related 2012). Furthermore, each of these studies had a relatively
concerns of persons currently living with epilepsy. Very small sample size; hence, generalization of these findings
broadly, the study results indicated that adults with epilepsy must be undertaken with caution. It is possible that there
may demonstrate and report language difficulties. A more has been limited examination of language abilities in the
detailed discussion follows, by first recapitulating the scop- older epilepsy population because their linguistic difficul-
ing review outcomes. ties are often mistaken for aspects of typical aging (Austin
& Abdulla, 2012). Interestingly, similar participant sam-
ple concerns have been raised in the pediatric epilepsy
Scoping Review literature (Hermann et al., 2008). Children with benign
Across the 66 studies that met our inclusionary cri- rolandic epilepsy have been most frequently studied (Riva
teria, a number of trends were identified in terms of partic- et al., 2007; Staden et al., 1998), leaving nominal de-
ipant characteristics, language measures used, and, most scription of linguistic abilities in other epilepsy etiologies
importantly, reported language outcomes. Furthermore, (Guimaraes et al., 2007; Henkin et al., 2003). Moreover,
the quality ratings of these studies revealed a number of these studies on children with epilepsy were also limited
concerns with the existing literature describing language in sample size and age representation, providing incom-
functioning in adults with epilepsy. plete information about the effects of epilepsy on the lan-
Participant characteristics. Individuals with epilepsy guage development across childhood and into adolescence
types other than TLE and older adults were underrepresented (Caplan et al., 2009; Stark, Bleile, Brandt, Freeman, &
across studies. TLE is the most common type of epilepsy Vining, 1995).
and is frequently associated with impaired cognitive–linguistic Additional participant-related issues included that
functions (Zhao et al., 2014), which may be why this syn- no study incorporated hearing or visual screenings, despite
drome has been studied extensively. Likewise, research may the possible confound of such sensory problems on lan-
focus on TLE given that temporal lobe damage, particu- guage test performance and the frequency of such sensory
larly within the language-dominant hemisphere, is known problems in the adult population (Murray & Clark, 2015;
to produce difficulties in semantic processing and lexical re- Wingfield, Tun, & McCoy, 2005). For instance, visual
trieval (De Haan, Mishkin, Baldeweg, & Vargha-Khadem, and hearing acuity have been shown to account for ap-
2006; Hamberger & Tamny, 1999; Hermann et al., 1988), proximately 50% of the variance in the cognitive–linguistic
as well as cognitive abilities such as verbal short-term mem- functions of the aging population (Schneider, Daneman,
ory deficits (Ojemann & Dodrill, 1985) intimately tied to Murphy, & See, 2000). Furthermore, as also noted by
language abilities (Giovagnoli et al., 2016). In their system- Hermann et al. (2008) in the pediatric literature, the major-
atic review, Doering and Trinka (2014) similarly identified ity of the adult studies compared performances among
a predominance of language studies focused on TLE, but different patient groups (e.g., different types of epilepsy;
very few involving extratemporal lobe epilepsies (ETLEs). epilepsy vs. other neurological diagnosis) versus a compari-
Albeit ETLE prevalence is lower than TLE, impaired lan- son group of age- and education-matched healthy peers.
guage functioning in other focal and general epilepsy etiolo- Therefore, whether or not all or only some of the epilepsy
gies has been noted (Dash & Tripathi, 2014). Furthermore, groups were performing outside of the normal range, espe-
a growing literature has documented the contributions cially on the nonstandardized language measures (e.g.,
of extratemporal neural regions to language processing as Bell, Seidenberg, et al., 2003; Hamberger & Tamny, 1999),
well as cognitive skills that support language processing requires verification.
(e.g., Gaillard et al., 2007); therefore, it is reasonable to sus- Language measures and outcomes. The scoping review
pect that adults with ETLE may be experiencing language revealed a heavy reliance upon aphasia tests in the epilepsy
difficulties. For instance, damage to the prefrontal cortex, literature. Thus, most studies only provided information
orbitofrontal, superior medial, and lateral regions of the fron- about basic spoken and written language skills (Murray &
tal lobe are associated with language dysfunction in adults Clark, 2015). Using standardized tests developed for persons

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with aphasia to evaluate language abilities in other neuro- errors (e.g., types of paraphasias, perseverations) was typi-
logical populations such as epilepsy may be inappropri- cally overlooked. A few studies did include qualitative
ate, as such tests are not sensitive to mild or higher-level error analyses, finding production of semantic and phone-
language deficits (e.g., discourse comprehension; abstract mic paraphasias and circumlocutions by adults with TLE
language use; Turkstra, Coelho, & Ylvisaker, 2005), thus (Bartha et al., 2004; Fargo et al., 2005; Schefft et al., 2003).
leading to an incomplete description of the breadth of epi- However, further research is needed to examine the integ-
lepsy effects on language. Moreover, several of the frequently rity of the underlying lexical representations and access
used standardized tests, such as the Boston Naming Test, in individuals with epilepsy who demonstrate word find-
have limited normative data based on educational level, de- ing difficulties, as such information is critical to guide ap-
spite many research studies demonstrating the influence of propriate intervention (Burke, MacKay, Worthley, &
education on vocabulary and naming ability (Patricacou, Wade, 1991).
Psallida, Pring, & Dipper, 2007; Welch, Doineau, Johnson, Across studies, language was typically evaluated as
& King, 1996). a part of a routine neuropsychological protocol for epi-
Among the language abilities evaluated, naming was lepsy treatment involving surgical resection or medical in-
found to be the most affected language function, possibly tervention. Certain types of epilepsy surgeries (e.g., anterior
because, however, naming was also the most frequently temporal lobectomies) and medications (e.g., topiramate,
tested language skill. Despite being commonly assessed across tiagabine) were found to cause language deterioration in
studies, the evaluation of naming rarely went beyond noun some patients. For example, individuals with TLE were
retrieval. Word fluency and vocabulary measures were also observed to demonstrate surgery-induced language impair-
popular. Although production at such a single word level ments, including declines in auditory comprehension, spo-
may be considered an index of microlinguistic function, it is ken naming, and spontaneous speech (Gargaro et al., 2013;
an insufficient indicator of complex or higher-level language Schwarz, Pauli, & Stefan, 2005; Zhang et al., 2013), and
functioning (Field et al., 2000; Glosser & Deser, 1991). In- Sarkis et al. (2013) reported a decline in verbal fluency post-
deed, Bartha et al. (2005) pointed out that researchers have surgery in individuals with FLE. Abou-Khalil and Abou-
often tried to characterize general language impairment Khalil (2015) reported that individuals prescribed with anti-
in individuals with epilepsy based on such focal measures. epileptic medications commonly experienced problems with
Moreover, the ecological validity of these word-level mea- language, especially word finding, that seemed to reduce
sures as indicators of daily language abilities has been ques- when the medication was withdrawn or the dosage was low-
tioned (Mayer & Murray, 2003). Only Gauffin et al. (2013) ered. Similar medication-related side effects on language
assessed and identified deficits in high-level language skills, were consistently reported in studies included in our review
such as sentence construction and understanding complex, (e.g., Fritz et al., 2005; Szaflarski & Allendorfer, 2012).
ambiguous sentences, and metaphors. Researchers have Moreover, compared to children, the surgery-related ver-
raised similar concerns about the pediatric epilepsy litera- bal language deficits in adults are more long term, eventu-
ture (Caplan et al., 2009; Strekas, Ratner, Berl, & Gaillard, ally affecting their vocational abilities and overall quality
2013): The majority of articles studying language functions of life (Sperling, Saykin, Roberts, French, & O’Connor,
have focused on single-word production using general 1995; Williams, Griebel, Sharp, & Boop, 1998). Therefore,
psychoeducational or neuropsychological measures (e.g., language difficulties cannot only occur as a direct result
Wechsler Intelligence Scale for Children–Fourth Edition of epilepsy but might also be a problem in those individuals
[Wechsler, 2003] or NEPSY [Korkman, Kirk, & Kemp, receiving epilepsy treatment. Hence, such changes in lin-
1998], respectively), which are ill-suited to measure functional guistic abilities must be identified and monitored by speech-
or high-level language abilities. Identification of such lan- language pathologists in clinical practice to effectively
guage disturbances in epilepsy is crucial, as they often provide treatment for these individuals.
reflect deficits in other cognitive abilities, such as seman- Quality rating findings. The shortcomings across the
tic memory, executive functioning, or working memory studies identified via our adapted rating framework related
(Antonsson et al., 2016; Van Ettinger-Veenstra, McAllister, mainly to the following quality indicators: research design,
Lundberg, Karlsson, & Engström, 2016), abilities that demographics, participant recruitment, and data collec-
have been found vulnerable in epilepsy (Jaimes-Bautista, tion procedures. More specifically, some studies failed to
Rodriguez-Camacho, Martinez-Juarez, & Rodriguez-Agudelo, explicitly document their study design, and demographic
2015; Kim, Lee, Yoo, Kang, & Lee, 2006). Testing of data were not consistently reported in all studies (e.g.,
such linguistic abilities must also be considered, as they Perrone-Bertolotti et al., 2012; Zhang et al., 2013). Stud-
have proven vulnerable in most neurological disorders, such ies varied greatly in terms of participant sample size (n range:
as traumatic brain injury (Moran & Gillon, 2004), right 1–988), with several having a relatively small sample size
hemisphere damage (van Ettinger-Veenstra et al., 2010), (e.g., Loddenkemper et al., 2004; Minkina et al., 2013).
Parkinson’s disease (Berg, Björnram, Hartelius, Laakso, & With regard to data collection procedures, the outcome
Johnels, 2003), and, importantly, pediatric epilepsy (Caplan language measures of interest were inconsistently col-
et al., 2002, 2006). lected before and after medical or surgical intervention
Although spoken word retrieval assessment was ubiq- in some earlier studies (e.g., Hermann et al., 1997; Howell
uitous across studies, characterization of word retrieval et al., 1994), making it difficult to draw qualitative and

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quantitative comparisons between the individuals’ pre- for additional research. For instance, the scoping review
and postintervention language levels. Moreover, only a identified that few prior epilepsy studies examined written
limited number of studies monitored long-term language language abilities, even though these abilities were fre-
outcomes past a year (Helmstaeder et al., 1998; Langfitt quent areas of concern in the social media postings. Like-
& Rausch, 1996; Loring, Meador, & Lee, 1994). The qual- wise, the data mining procedures identified a mismatch
ity assessment of these studies highlighted the lack of con- between apparent healthcare practice and findings in the
sistency in the evaluation and reporting of epilepsy-related literature and social media regarding epilepsy-based lan-
language functions by researchers, which poses a problem guage difficulties. Even though language deficits have
for clinicians during management planning for persons been frequently documented in the extant literature, the
with epilepsy and, more generally, in terms of evidence- queries retrieved from social media indicated a lack in
based practice. addressing such issues by healthcare providers, including
The aforementioned review of research evidence speech language pathologists (e.g., patient education
confirms the co-occurrence of language deficits with adults about language symptoms, referrals for speech-language
with epilepsy, with studies reporting considerable deficits pathology services; Miller et al., 2017).
in spoken word retrieval, verbal fluency, auditory com- To our knowledge, this is the first study that has eval-
prehension, and written language skills across epilepsy eti- uated concerns of individuals with a communication dis-
ologies. Collectively, however, the findings on this topic order by going beyond Twitter and exploring other social
remain incomplete given the inadequate representation of media platforms. Data used in this study are more repre-
various epilepsy types, use of assessment measures that sentative than those generated using traditional research
do not fully describe the language modalities, rare assess- methods; that is, they are more reflective of genuine con-
ment of high-level language and discourse abilities, and cerns, having been organically generated by individuals
some study quality concerns. Hence, it remains premature with epilepsy rather than via a researcher and his or her
to draw a comprehensive picture of epilepsy-related lin- questions (Priest et al., 2016). The information retrieved
guistic difficulties and relatedly identify an expected lan- from social media may offer rich information that could be
guage profile for types of epilepsy based on the current used by researchers and health providers (including speech-
research findings. language pathologists) to guide the development and
provision of management procedures for people with epi-
lepsy, because this technique not only highlights the dearth
Data Mining in knowledge and awareness among people with epilepsy
The Word Adjacency Graph modeling approach and their caregivers but also allows identifying the areas
allowed successful identification of important questions that need to be addressed by medical professionals and re-
that individuals are asking regarding language disorders in searchers to better support individuals with epilepsy. The
epilepsy. Of the three data sets explored, the most relevant findings from our study will hopefully motivate additional
questions were obtained from the Epilepsy Foundation data mining research on the language difficulties and needs
database, with no relevant comments/concerns retrieved of not only individuals with epilepsy but also those with
from Twitter. This might suggest that individuals with epi- other disorders.
lepsy are more comfortable sharing their language-related
concerns anonymously on platforms such as ChaCha ver-
sus an open social platform such as Twitter where their Study Limitations
identity might be revealed (Priest et al., 2016). Another The literature search that was performed as a part
reason for finding most enquiries concerning epilepsy-related of the scoping review had some limitations. Only articles
language difficulties in the Epilepsy Foundation database published in English were included; as a result, some im-
might be that we analyzed a wider date range from this data portant studies may have been excluded. Limitations in
set. The majority of questions and concerns were posted by scientific databases may have led to missing some relevant
individuals with epilepsy themselves or their family mem- studies that met the inclusion criteria. Due to our limited
bers. The most common concerns related to problems with access to as well as heterogeneity in the social network
verbal memory, word finding, reading, writing, and spell- data, the data mining findings from our study might not
ing. Most queries were about language problems that occurred be completely representative of the overall language prob-
in adults typically after epilepsy surgery or as side effect of lems or concerns reported by individuals with epilepsy
antiepileptic medications. or their caregivers living in the United States.
It is important to note that some of these queries
regarding the common language problems and epilepsy
treatment–related side effects confirm the scoping review Conclusions
findings discussed earlier in this article. That is, similar to The present study has highlighted that language func-
the language deficits identified in the empirical literature, tioning in adults with epilepsy has been understudied, par-
patients and their caregivers are expressing language-related ticularly in the field of speech-language pathology. Several
concerns, for which they are seeking assistance. These gaps and heterogeneity in language outcomes were identi-
queries retrieved from social media also highlight directions fied in the research literature, which in turn collectively

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confound characterizing language profiles associated with Arksey, H., & O’Malley, L. (2005). Scoping studies: Towards a
epilepsy. The discrepant results may in part relate to rare methodological framework. International Journal of Social
use of appropriate testing procedures that are sensitive and Research Methodology, 8(1), 19–32.
Austin, J., & Abdulla, A. (2012). Identifying and managing epi-
challenging enough to detect language deficits in the epi-
lepsy in older adults. Nursing Times, 109(3), 20–23.
lepsy population (e.g., nominal examination of both spoken Bartha, L., Benke, T., Bauer, G., & Trinka, E. (2005). Interictal
and written high-level language and discourse abilities). In language functions in temporal lobe epilepsy. Journal of Neu-
addition, the present study’s findings have underscored the rology, Neurosurgery & Psychiatry, 76(6), 808–814.
need to evaluate language functioning in individuals with Bartha, L., Delazer, M., & Benke, T. (2001). Die Entwicklung
epilepsy types involving extratemporal regions as well as des Innsbrucker Benenntest (IBT) [The development of the
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Bell, B., Lin, J. J., Seidenberg, M., & Hermann, B. (2011). The
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