BRIEF RESEARCH REPORT
published: 10 September 2020
doi: 10.3389/fneur.2020.01011
Frontiers in Neurology | www.frontiersin.org 1 September 2020 | Volume 11 | Article 1011
Edited by:
Nicola Smania,
University of Verona, Italy
Reviewed by:
Alessandro Giustini,
Istituto di Riabilitazione Santo
Stefano, Italy
Toshiyuki Fujiwara,
Juntendo University, Japan
*Correspondence:
Jan Stubberud
Specialty section:
This article was submitted to
Neurorehabilitation,
a section of the journal
Frontiers in Neurology
Received: 18 May 2020
Accepted: 31 July 2020
Published: 10 September 2020
Citation:
Stubberud J, Løvstad M, Solbakk A-K,
Schanke A-K and Tornås S (2020 )
Emotional Regulation Following
Acquired Brain Injury: Associations
With Executive Functioning in Daily
Life and Symptoms of Anxiety and
Depression. Front. Neurol. 11:1011.
doi: 10.3389/fneur.2020.01011
Emotional Regulation Following
Acquired Brain Injury: Associations
With Executive Functioning in Daily
Life and Symptoms of Anxiety and
Depression
Jan Stubberud
1,2,3
*
, Marianne Løvstad
1,3
, Anne-Kristin Solbakk
1,4,5,6
,
Anne-Kristine Schanke
1,3
and Sveinung Tornås
3
1
Department of Psychology, University of Oslo, Oslo, Norway,
2
Department of Research, Lovisenberg D iaconal Ho spital,
Oslo, Norway,
3
Department of Research, Sunnaas Rehabilitation H os pital, Nesodden, Norway,
4
RITMO Centre for
Interdisciplinary Studies in Rhythm, Time and Motion, University of Oslo, Oslo, Norway,
5
Department of Neurosurgery, Oslo
University Hospital, Olso, Norway,
6
Department of Neuropsychology, Helgeland H os pital, Mosjøen, Norway
Objective: To examine whether a questionnaire measuring emotional regulation
after acquired brain injury adds clinical information beyond what can be obtained
with a comprehensive executive function questionnaire and an anxiety and
depression measure.
Method: Seventy adult persons (age 19–66 years, M
age
= 43, SD
age
= 13) with
acquired brain injury in the chronic phase and executive function complaints. All were
recruited to participate in a randomized controlled trial (NCT02692352) evaluating the
effects of cognitive rehabilitat ion. Traumatic brain injury was the dominant cause of injury
(64%), and mean time since injury was 8 years. Emotional regulation was assessed with
the Brain Injury Trust Regulation of Emotions Questionnaire (BREQ). Executive function
was assessed with the Behavior Rating Inventory of Executive Function Adult Version
(BRIEF-A). The Hopkins Symptom Checklist 25 (HCSL-25) was employed to measure
anxiety and depression symptoms.
Results: Overall, significant correlations were found between reports of emotional
regulation (BREQ) and executive function in daily life (BRIEF-A). Furthermore, our analyses
revealed a significant relationship between self-reported scores of emotional regulation
(BREQ) and symptoms of anxiety and depression (HSCL-25).
Conclusion: The significant associations between the BREQ and most of the other
clinical mea sures indicate that, for patients with acquired brain injury, the BREQ does
not add substantial information beyond what can be assessed with the BRIEF-A and
the HSCL-25.
Keywords: brain injury, emotional regulation, executive function, psychological distress, assessment
Stubberud et al. Emotional Regulation in Brain Injury
INTRODUCTION
Difficulties in emotional regulation are among the most common
and debilitating consequences of acquired brain injury (ABI),
such as traumatic brain injury (TBI) and cerebrovascular
accidents (CVA), with potential deleterious effects in all life
domains [e.g., (
14)]. Indeed, impaired emotional regulation
can lead to compromised social functioning, decreased leisure
activity, increased risk of suicide, and loss of employment/failure
to return to work (3, 57). Despite its clinica l significance,
relatively little research has systematically addressed emotional
regulation in individuals with ABI. Likely contributing to the
lack of research in this area is the absence of instruments
that adequately assess the complexity of this construct among
adults with ABI. Accurate evaluation of the nature of deficits in
emotional regulation is, however, imperative in the process of
developing suitable and realist ic rehabilitation and therapeutic
intervention plans after ABI.
Emotional regulation relates to the capacity to flexibly
modulate and control subjective experience and expression of
emotions (
8, 9), and th e reduction of emotional arousal (10). In
ABI, there may be impairments in self-monitoring and control,
in addition to the ability to differentiate emotions, that a re
revealed through various symptoms of emotional dysre gulation,
including disinhibited emotion/behavior, and reduced emotional
awareness and expression (
8, 11). Further, emotional regulation
is an important aspect of executive functioning (EF) (12,
13), broadly described as inter-related top-down processes
promoting the control and regulation of cognition, behavior,
and emotion (14). In contrast to the view that brain injury
is directly responsible for emotional dysregulation, it can also
represent secondary reactions to the consequences of ABI
(15). Importantly, the experience of cognitive deficits after ABI
has been described as having a “disordered mind (16), a
situation that can be emotionally experienced as a disorganized
inner state. Adding layers of complexity, pre- and comorbid
emotional problems may also influence symptom presentation
after ABI. Nevertheless, the reactions to the psychosocial
and cognitive changes associated with having an ABI makes
it challenging to conceptualize and measure problems with
emotional regulation (
17).
Most measures addressing emotional functioning were
not specifically developed for ABI and often focus on the
phenomenology of depressive or anxiety states, rather than
the actual capacity to regulate emotion. Thus, Cattran et al.
(8) developed a questionnaire to measure emotional regulation
after ABI, the Brain Injury Rehabilitation Trust Regulation of
Emotions Questionnaire (BREQ). To our knowledge, only two
feasibility studies (
18, 19), the original study by Cattran et al.
(8) and a cognitive rehabilitation study (20), have employed t he
BREQ in the field of ABI. Also, the original study by Cattran
et al. is the only one providing BREQ data from relatives of
ABI individuals (i.e., informants) (8). Hence, there are a modest
number of empirical studies involving the BREQ. In addition,
no studies have examined its relat ionship with a comprehensive
EF questionnaire, such as the Behavior Rating Inventory of
Executive Function Adult Version (BRIEF-A; 21). Cattran
et al. (8), however, examined the association of BREQ with
the Dysexecutive Questionnaire [DEX; (21)] and demonstrated
strong correlations. Still, the DEX only contains 20 items, and
few of these address emotional functioning. In summary, the
multitude of problems related to reduced emotional regulation
after ABI, along with the lack of relevant measurement tools
that are necessary when differential diagnoses are considered,
highlight the importance of generating more knowledge about
the clinical properties of the BREQ (emotional regulation),
including establishing its association to various EF domains and
symptoms of anxiety and depression.
The present article reports on a subset of baseline data from
Tornås et al.’s (
20) randomized controlled trial (RCT; n = 70),
where the efficacy of Goal Management Training (GMT) was
examined in patients with ABI.
The main goal of the current study was to examine the
relationship between the BREQ and (a) a questionnaire measure
of EF i n daily life (BRIEF-A) and (b) symptoms of anxiety and
depression, as measured by the Hopkins Symptom Checklist 25
[HSCL-25; (
22)], in persons with ABI in the chronic phase. Based
on the sparse extant literature, it was expe ct ed that:
1. Both self- and informant reports of BREQ and BRIEF-A [i.e.,
Global Executive Composite (GEC), Behavioral Regulation
Index (BRI), and Emotional Control subscale] would be
significantly correlated (hypothesis 1).
2. Intercorrelations between BREQ and HSCL-25 would occur
(hypothesis 2).
METHOD
This study reports baseline data from a large single-center
RCT (
20). All participants provided written informed consent.
The study was approved by t h e Regional Committee for
Medical Research Ethics (2012/1436, South-Eastern Norway) and
conducted in accordance with the Helsinki De c larati on. Clinical
Trial Registration No.: NCT02692352.
Participants
An information letter was sent to 178 former patients (aged
18–67 years) at Sunnaas Rehabilitation Hospital (SRH) with a
verified ABI and self-reported executive difficulties in daily life,
at least 6 months post-injury. Any neurodegenerative disorder,
ongoing substance abuse, major psychiatric diseases, and/or
severe cognitive deficits were exclusion criteria.
Informed consent was ret urned from 90 persons who
underwent a comprehensive screening interview by phone.
Fourteen declined participation and 6 did not meet inclusion
criteria. Thus, the final sample totaled n = 70 (age 19–66 yea rs,
M
age
= 42.9, SD
age
= 13), with 69 participants returning th e
questionnaires used in the present study. Fifty-eight participants
(83%) had previously received subacute rehabilitation at SRH.
Traumatic brain injury was the dominant cause of injury (64.3%),
and a slight majority were males (52.9%). All participants were
Caucasian. Mean time since injury was 8 years (SD = 112.4
months), ranging from 10 to 575 months. The mean length
of education was 13.4 years (SD = 2.4) (Tables 1, 2). About
Frontiers in Neurology | www.frontiersin.org 2 September 2020 | Volume 11 | Article 1011
Stubberud et al. Emotional Regulation in Brain Injury
TABLE 1 | Demographic, cognitive, and brain injury characteristics of
the participants.
Total (n = 70)
Age, mean ± SD 42.89 (12.96)
Gender, M = men 38 M (54.3)
Education, years ± SD 13.4 (2.43)
WASI 104.31 (12.65)
Tower Test 10.37 (2.82)
Months since injury ± SD 97.47 (112.44)
Injury etiology n (%)
TBI 45 (64.3)
Stroke 15 (21.5)
Tumor 6 (8.6)
Anoxic 2 (2.9)
Other 2 (2.9)
Vocational status n (%)
Work (full time) 6 (8.8)
Work (part time) 7 (10)
Voc. Rehab 25 (35.7)
Sick leave 3 (4.3)
Student 6 (8.6)
Disability pension 23 (32.9)
In a relationship n (%) 44 (63)
Percentage totals may not add to 100% due to rounding. Sign, Significance; Voc. rehab,
Vocational rehabilitation; WASI, Wechsler Abbreviated Scale of Intelligence. Scaled scores
on the WASI and Tower Test.
one third (32.9%) of the sample received disability pension, and
the rest were either in vocational rehabilitation, working (part-
or full-time), students, or on sick leave. All participants were
independent in ADL.
For 56 of the participants, magnetic resonance imaging (MRI)
was obtained in the study period using a 3 Tesla scanner
(Achieva 3.0T, Philips Medica l System, Best, The Netherlands)
at the Intervention Center at Oslo University Hospital. Previous
MRI/computed tomography scans were collected from other
hospitals for five participants. For various reasons, scanning
could not be performed for nine participants. The frontal lobe
was the most affected cortical location, followed by temporal- and
parietal lobe injury. Finally , about 50% of the sample had signs of
cortical atrophy (Table 2 ).
All participants were asked to give consent for the two
questionnaires to be sent to an informant that knew them very
well. Two of the participants declined, and four informants
did not return t h e questionnaires. Therefore, 64 informants (all
Caucasian) were included, with 57 and 56 informants completing
the BREQ and the BRIEF-A, respectively. More than half of
the informants (53.1%) were spouses/partners living with the
participants, about one third (31.3%) were parents, and the
remaining informants were siblings (12.5%), adult children
(3.1%), or close friends (7.8%).
Measures
In the main study (
20), various neuropsychological tests and
questionnaires were administered to the participants. For
TABLE 2 | Radiological description of the brain injuries.
CT/MRI verified ABI at onset n (%)
Yes 36 (97.3)
No
a
1 (2.7)
MRI verified lesion at baseline n (%)
Yes
b
23 (62.2)
No 8 (21.6)
Missing
c
6 (16.2)
Injury localization n (%)
Right hemisphere 7 (18.9)
Left hemisphere 9 (24.3)
Bilateral 5 (13.5)
Frontal 11 (29.7)
Parietal 4 (10.8)
Temporal 7 (18.9)
Occipital 0
Cerebellum 2 (5.4)
Subcortical nuclei
d
1 (2.7)
Subcortical white matter 13 (35.1)
Cortical atrophy n (%) 35 (50)
a
Verified by neurological and neuropsychological evaluation.
b
MR/CT scans were
collected from other hospitals for five participants due to practical or medical reasons; the
images were interpreted by the same radiologist. All 5 scans were performed between
2011 and 2013.
c
MRI was not possible to conduct due to practical reasons for four
participants, medical reasons for four, and one participant refused to undergo repeated
scanning.
d
Striatum, basal ganglia and/or thalamus. MRI, Magnetic Resonance Imaging.
the current supplementary study, th e Wechsler Abbreviated
Scale of Intelligence [WASI; (
23)] and the Tower Test (24)
were included to characterize the cognitive functioning
[i.e., general intellectual capacity (IQ) and EF] in the
sample. Daily life EF was assessed with the BRIEF-A (25),
emotional regulation was measured with the BREQ (8), and
symptoms of anxiety and depression were assessed with the
HSCL-25 (22).
The Brain Injury Rehabilitation Trust Regulation of
Emotions Questionnaire
The BREQ is a 32-item standardized questionnaire that
aims at assessing changes and disturbances in emotional
regulation following ABI, yielding a total sum score.
Patients and a significant other are asked to rate each item’s
frequency of occurrence on a 4-point Likert scale from
1 (never) to 4 (always). The measure has demonstrated
good concurrent validity (r = 0.64–0.82) and to be
distinguishable from measures of cognitive ability and tests of
affect (
8).
The Behavior Rating Inventory of Executive Function
Adult Version
The BRIEF-A is a 75-item standardized questionnaire of
an adult’s EF or self-regulation in his or her everyday
environment. Based on 9 sub-scales, it yields a GEC score
as well as two Composite Index scores: the BRI and the
Metacognition Index (MCI). The Emotional Control scale
Frontiers in Neurology | www.frontiersin.org 3 September 2020 | Volume 11 | Article 1011
Stubberud et al. Emotional Regulation in Brain Injury
TABLE 3 | Correlations between the BREQ and the BRIEF-A and HSCL-25.
BREQ-S BREQ-I
BRIEF-S-GEC 0.55
**
0.44
**
BRIEF-S-BRI 0.77
**
0.46
**
BRIEF-S-MCI 0.21 0.32
BRIEF-I-GEC 0.30 0.71
**
BRIEF-I-BRI 0.51
**
0.84
**
BRIEF-I-MCI 0.12 0.55
**
BRIEF-S-EMO 0.74
**
0.48
**
BRIEF-I-EMO 0.54
**
0.81
**
HSCL-25 Total 0.52
**
0.29
BREQ, BIRT (Brain Injury Rehabilitation Trust) Regulation of Emotions Questionnaire;
BREQ-S, self-rated version of the BREQ; BREQ-I, informant-rated version of the
BREQ; HSCL-25, Hopkins Symptom Checklist 25; BRIEF-A, Behavior Rating Inventory
of Executive Function Adult Version; BRIEF-S/I, BRIEF self/informant version; EMO,
Emotional control; GEC, Global Executive Composite; BRI, Behavioral Regulation Index;
MCI, Metacognition Index.
**
Correlation is significant at the 0.001 level (two-tailed).
measures t he impact of EF problems on emotional expression
and assesses the ability to modulate or control emotional
responses. Patients and a significant other are asked to rate
each item’s frequency of occurrence on a 3-point Likert scale
from 1 (never) to 3 (often) (
25). The BRIEF-As reliability is
high; Cronbachs a lpha of BRI and MI has been found to
be 0.94 and 0.96, respectively (26). The BRIEF-A informant
form was administered to the same significant other informant
as the BREQ.
Hopkins Symptom Checklist 25 (HSCL-25)
The HSCL-25 is a 25-point self-report inventory of depressive
and anxiety symptoms (22). It includes a 15-item depressive
symptoms scale and a 10-item anxiety symptoms scale. Items
are scored on a Likert scale ranging from 0 (not at all) to
4 (very much). Finally, the HSCL-25 has satisfactory validity
and reliability as an instrument of anxiety and depression
symptoms (22).
Statistical Analyses
Data analyses were conducted using SPSS version 25.0 for
Windows. Frequency distributions, means, and standard
deviations (SD) were calculated for the demographic, medical,
and cognitive variables. Relationships between measures
were examined with Pearson product-moment correlation
coefficients (two-tailed test). For BRIEF-A, the GEC, BRI,
MCI, and Emotional Control subscale in both self- and
informant reports were selected as variables, while the
total scores were employed for BREQ and HSCL-25. In
determining the strength of the relationships, Cohen’s (
27)
guidelines were employed: r = 0.10–0.29 (small), r = 0.30–0.49
(medium), and r > 0.50 (large). A conservative alpha-level
of 0.01 was applied in order to take multiple comparisons
into account.
RESULTS
Descriptive Data on General Intellectual
Capacity (IQ), Executive Functioning, and
Questionnaires
The ABI group had general intellectual capacity (IQ) and
EF test performance within the normal range, relative to
the stand a rdizati on samples (Table 1). The BREQ-self mean
score was 55.7 (SD = 14.4), while the BREQ-informant mean
score was 52.5 (SD = 13.1). To our knowledge, there are no
recommendations available regarding a clinical cut-off score
on the BREQ, nor any published data from healthy controls.
However, with the rating “always (4), “often” (3), “sometimes
(2), or “never” (1), we decided to use an item mean of 2.5
with total score 80 as cut-off score. Hence, when adding up
how many got a total score 80, 10% (n = 7) self-reported
80, and 3% (n = 2) of the informants reported a score 80
in the patients. Moreover, two of the BRIEF-A (group average)
scores were equal to or above recommended clinical cut-off (
T = 65), i.e., GEC-self (M = 64.7, SD = 9.7) and MCI-self (M
= 65.3, SD = 9.8). On an individual level, a score equal to or
above recommended clinical cut-off was self-reported for 52% (n
= 36) on the GEC, 38% on the BRI (n = 26), 54% (n = 37) on the
MCI, and 41% (n = 28) on the Emotional Control scale. For the
informants, a clinical score was reported for 25% (n = 14) on the
GEC, 18% (n = 10) on the BRI, 38% (n = 21) on the MCI, and
13% (n = 9) on the Emotional Control scale. However, all BRIEF-
A-informant group scores were below cut-off (T 65). Wh ile the
group average on the HSCL-25 (M = 22.4, SD = 15.3) was below
the recommended clinical cut-off (HSCL-25 total < 25), 35% (n
=24) reported symptoms of anxiety and depression above clinical
cut-off (
28).
Relations Between BREQ and Brief-A (Self-
and Informant Reports)
All correlations between BREQ-self and BRIEF-A (GEC and BRI)
scores were large and positive, including GEC-self, r (67) = 0.55,
p < 0.001, BRI-self, r (67) = 0.77, p < 0.001, Emotional Control-
self r (67) = 0.74, p < 0.001, in addition to BRI-informant, r (54)
= 0.51, p < 0.001 and Emotional Control-informant, r (54) =
0.54, p < 0.001 (Table 3). Additionally, all correlations between
BREQ-informant and BRIEF-A (GEC and BRI) scores were
positive, including GEC-self, r (55) = 0.4 4, p < 0.001 (medium),
BRI-self, r (55) = 0.46, p < 0.001 (medium), Emotional Control-
self, r (55) = 0.48, p < 0.001 (medium), GEC-informant, r (54) =
0.71, p < 0.001 (large), BRI-informant, r (54) = 0.84, p < 0.001
(large), and Emotional Control-informant, r (54) = 0.81, p <
0.001 (large) (Table 3). Finally, for the MCI only the informant
reports of BREQ and BRIEF-A reached significance, r (54) = 0.55,
p < 0.001 (large) (Table 3).
Relations Between BREQ (Self- and
Informant Reports) and HSCL-25
There was a positive significant correlation between BREQ-self
scores and anxiety and depression scores (HSCL-25), r (61) =
Frontiers in Neurology | www.frontiersin.org 4 September 2020 | Volume 11 | Article 1011
Stubberud et al. Emotional Regulation in Brain Injury
0.52, p < 0.001 (large). However, the correlation between BREQ-
informant and patient-rated HSCL-25 scores did not reach
statistical significance, r (49) = 0.29, p = 0.03 (Table 3).
Post-hoc Analyses
In order to allow comparison of results, one sample t-tests
were conducted to determine if t here were significant differences
between the BREQ reports in our study and the BREQ reports
from Cattran et al.’s study (age 18–61 years, M = 36, SD = 12)
(
8). There was no difference between the mean BREQ-self score
from our ABI sample (M = 55.7, SD = 14.4) and the mean BREQ-
self score from the ABI cohort studied by Cattran et al. (n = 72,
M = 58.23, SD = 20.01), t (68 ) = 1.31, p = 0.196. However, the
mean BREQ-informant score from our sample (M = 52.5, SD
= 13.1) was significantly lower than the mean BREQ-informant
score from Cattran et al.’s study (M = 63.26, SD = 19.54), t (56)
= 6, p < 0.001 .
DISCUSSION
The main aim of the present study was to examine the
relationship between self- and informant perceived emotional
regulation and daily life EF, and emotional regulation and
symptoms of anxiety and depression, in persons with ABI.
Overall, several findings supported our hypotheses.
Reported Emotional Regulation and
Executive Function in Daily Life
Consistent with the first hypothesis, both self- and informant
reports of perceived emotional regulation and d aily life EF
were significantly correlated. For both BREQ versions, the
strongest associations were observed with the BRI in the
BRIEF-A. As this index is composed of scales designed to
measure the ability to maintain appropriate regulatory control of
behavior and emotional responses (i.e., Inhibit, Shift, Emotional
Control, and Self-Monitor), it is more closely related to the
domain of emotional regulation than the BRIEF-A MCI (
8, 11,
25). Of note, an association between the BRIEF-A Emotional
Control subscale and the BREQ was also found. A relationship
between BREQ and MCI informant-report was also detected.
The division between the BRI and MCI is mainly theoretical,
and some of the abilities reflected in the MCI (i.e., Initiate,
Working Memory, Plan/Organize, Task Monitor, Organization
of Materials) may also overlap with aspects of emotional
regulation. Clearly, the constructs of emotional regulation and
EF are closely connected (13), as the measures are intended
to assess everyday manifestations of emotional dysregulation
and executive dysfunction, respectiv ely. The BRIEF-A includes
behavioral and emotional aspects, such as appropriate inhibition
of thoughts and actions, flexibility in shifting problem-solving
set, modulation of emotional response, and monitoring of ones
activities, that are very important for emotional regulation
(8, 9). The findings in the present study are in accordance
with previous research (
8), showing a strong relationship
between BREQ and measures of EF. It is possible that the
BREQ represents a valuable contribution to the assessment
of emotional regulation in the ABI-population, but it is still
uncertain what additional information it adds beyond the BRIEF-
A. Due to an often observed discrepancy between objective
and subjective measures of cognition, with a generally poor
relationship between questionnaires and performance-based
neuropsychological tests (
29), one mig ht consider employing
multiple EF measures in future studies. Furthermore, as there
are no published studies that can inform on recommendations
regarding a clinical cut-off score on the BREQ, nor any published
BREQ data from healthy controls, it is difficult to know if
our sample experienced emotional dysregulation in the clinical
range, based on the BREQ. Nevertheless, only 10% of the
participants self-reported, and 7% of the informants reported a
total score at or above what we suggest as the clinical cutoff
(80). This finding is somewhat in contrast to the Emotional
Control (BRIEF-A) scores, where 41% self-reported and 13% of
the informants reported scores in the clinical range. Although
conjectural, our post-hoc analyses revealed t hat the informants
in the present study reported significantly less problems with
emotional regulation in the patients compared to the ABI sa mple
in C attra n et al.’s study (
8). The ABI-participants in the latter
study (8) were, however, slightly younger and with a lower IQ
relative to our sample. It is important to consider that several
factors might contribute to bias, and differences, in patient
and informant ratings (e.g., cognitive deficits, severe emotional
regulation dysfunction, self-awareness, social desirability bias,
informants burden, abuse, stress level, and/or personality) (30
33), suggesting t hat information should be gathered from
multiple sources. Finally, the majority of the participants chose
a spouse/partner as an informant, and the remaining informants
were parents, siblings, friends, or adult children. Due to the
variability of the informants and their relationship with the
patients, potential differences between spouse/partner reporting
and the reporting of the other informants were examined. In
our post-hoc analyses, no significant differences were, however,
detected between spouse/partner reporting and t h e reporting of
the other informants.
Perceived Emotional Regulation and
Symptoms of Anxiety and Depression
With regard to the second hypothesis, a statistically significant
relationship between scores of emotional regulation (self-
reported) and symptoms of anxiety and depression was detected.
Although emotional regulation has been given relatively little
attention in the field of ABI, it is among the most studied
phenomena in contemporary psychology, having generated a
robust body of evidence linking it to psychopathology (
34),
in addition to being recognized as a core function supporting
psychological well-being (35). In our study, both the self- and
informant-rated BREQ versions produced moderate to high
correlations with t he HSCL-25, which may suggest either that
the BREQ also measures a degree of anxiety and depression, or
that psychological distress is prevalent among those suffering
from emotional dysregulation. These findings are, however, in
accordance with Cattran et al. (
8) where moderate to h igh
correlations between the BREQ a nd the Anxiety subscale of the
Irritability, Depression, and Anxiety Scale were observed.
Frontiers in Neurology | www.frontiersin.org 5 September 2020 | Volume 11 | Article 1011
Stubberud et al. Emotional Regulation in Brain Injury
Study Limitations
Clearly, studies with larger sample sizes are needed to
more definitively examine the relationships between the
questionnaires. The current sample was likely not representative
of the entire population of individuals with ABI, as the RCT
included participants who self-reported executive deficits, and
were motivated for a cognitive rehabilitation intervention for
dysexecutive symptoms. Thus, they potentially represent a group
with high symptom awareness. In this regard, symptom validity
measures, in addition to awareness questionnaires (self- and
informant reports), should be considered for future studies.
Importantly, since we included participants ranging from 10
months to 48 years post-injury, they were at different stages in
their recovery processes, and thus had different functional status.
Further, as about one third of the sample was on a disability
pension, a majority in a relationship, and only 7% of informants
reported emotion regulation dysfunction, this likely reflects a
less severely injured segment of the ABI population (
36, 37).
Finally, a more detailed description of potentially complicating
premorbid or comorbid factors, information about treatments
received in the acute or subacute period, and symptom debut is
recommended for future studies.
CONCLUSION
This is the first study to examine the relationship between BREQ
and a comprehensive EF questionnaire. Reports of emotional
regulation and perceived EF in daily life were found to correlate
in a sample of ABI participants. Furthermore, a relationship
between scores of emotional regulation and symptoms of anxiety
and depression was also detected. These findings indicate that,
for patients with ABI, the BREQ does not add substantial
information beyond what can be assessed with t he BRIEF-A and
the HSCL-25. Considering the covariation between the measures,
and the lack of published norms for the BREQ, a preliminary
recommendation is that it is premature to employ the BREQ as a
standard measure for assessing emotional regulation in ABI.
DATA AVAILABILITY STATEMENT
The raw data supporting the conclusions of this article will be
made available by the authors, without undue reservation.
ETHICS STATEMENT
The studies involving human participants were reviewed and
approved by Regional Committee for Medical Research Eth ic s,
South-Eastern Norway. The patients/participants provided their
written informed consent to participat e in this study.
AUTHOR CONTRIBUTIONS
JS, ML, A-KSo, A-KS c , a nd ST contributed to the design and
implementation of the research and to the analysis of the results.
JS wrote the paper with input from all authors. All authors
contributed to the article and approved the submitted version.
FUNDING
This study was funded by the Norwegian ExtraFoundation
for Health and Rehabilitation through EXTRA funds (grant
number 2011/2/0204).
ACKNOWLEDGMENTS
The authors thank t h e participants and t h e staff at t he Cognitive
Rehabilitation Unit Sunnaas Rehabilitation Hospital.
REFERENCES
1. Ponsford JL, Downing MG, Olver J, Ponsford M, Acher R, Carty M, et al.
Longitudinal follow-up of patients with traumatic brain injury: outcome
at two, five, and ten years post-injury. J Neurotrauma. (2014) 31:64–
77. doi: 10.1089/neu.2013.2997
2. Konrad C, Geburek AJ, Rist F, Blumenroth H, Fischer B, Husstedt I, et al.
Long-term cognitive and emotional consequences of mild traumatic brain
injury. Psychol Med. (2011) 41:1197–211. doi: 10.1017/S0033291710001728
3. Engberg AW, Teasdale TW. Psychosocial outcome following traumatic brain
injury in adults: a long-term population-based follow-up. Brain Inj. (2004)
18:533–45. doi: 10.1080/02699050310001645829
4. Wood RL, Liossi C, Wood L. The impact of head injury neurobehavioural
sequelae on personal relationships: preliminary findings. Brain Inj. (2005)
19:845–51. doi: 10.1080/02699050500058778
5. Gordon WA, Cantor J, Ashman T, Brown M. Treatment of post-TBI executive
dysfunction: application of theory to clinical practice. J Head Trauma Rehabil.
(2006) 21:156–67. doi: 10.1097/00001199-200603000-00008
6. Neacsiu AD, Fang CM, Rodriguez M, Rosent hal MZ. Suicidal behavior and
problems with emotion regulation. Suicide Life Threat Behav. (2018) 48:52–
74. doi: 10.1111/sltb.12335
7. Testa JA, Malec JF, Moessner AM, Brown AW. Predicting family functioning
after TBI: impact of neurobehavioral factors. J Head Trauma Rehabil. (2006)
21:236–47. doi: 10.1097/00001199-200605000-00004
8. Cattran C, Oddy M, Wood R. The development of a measure of emotional
regulation following acquired brain injury. J Clin Exp Neuropsychol. (2011)
33:672–9. doi: 10.1080/13803395.2010.550603
9. Gross JJ. Emotion regulation: affective, cognitive, and social consequences.
Psychophysiology. (2002) 39:281–91. doi: 10.1017/S00485772013
93198
10. Garner PW, Spears FM. Emotion regulation in low-income preschoolers. Soc
Dev. (2000) 9:246–64. doi: 10.1111/1467-9507.00122
11. Beer JS, Lombardo MV. Insights into emotion regulation from
neuropsychology. In: Gross JJ, editor. The Handbook of Emotion Regulation.
New York, NY: The Guilford Press (2007). p. 69–86.
12. Hart T, Brockway JA, Fann JR, Maiuro RD, Vaccaro MJ. Anger self-
management in chronic traumatic brain injury: protocol for a psycho-
educational treatment with a structurally equivalent control and an
evaluation of tre atment enactment. Contemp Clin Trials. (2015) 40:180–
92. doi: 10.1016/j.cct.2014.12.005
13. Rath JF, Simon D, Langenbahn DM, Sherr RL, Diller L. Group treatment
of problem-solving deficits in outpatients with traumatic brain injury:
a randomised outcome study. Neuropsychol Rehabil. (2003) 13:461–
88. doi: 10.1080/09602010343000039
14. Cicerone K, Levin H, Malec J, Stuss D, Whyte J. Cognitive rehabilitation
interventions for executive function: moving from bench to bedside in
patients with traumatic brain injury. J Cogn Neurosci. (2006) 18:1212–
22. doi: 10.1162/jocn.2006.18.7.1212
Frontiers in Neurology | www.frontiersin.org 6 September 2020 | Volume 11 | Article 1011
Stubberud et al. Emotional Regulation in Brain Injury
15. Dams-O’Connor K, Gordon WA. Integrating interventions after traumatic
brain injury: a synergistic approach to neurorehabilitation. Brain Impairment.
(2013) 14:51–62. doi: 10.1017/BrImp.2013.9
16. Prigatano G. Disordered mind, wounded soul: the emerging role of
psychotherapy in rehabilitation after brain injury. J Head Trauma Rehabil.
(1991) 6:1–10. doi: 10.1097/00001199-199112000-00004
17. Prigatano GP. Personality disturbances associated with traumatic brain injury.
J Consult Clin Psychol. (1992) 60:360–8. doi: 10.1037/ 00 22 -0 0 6X.60 .3.3 60
18. Tsaousides T, D’Antonio E, Varb anova V, Spielman L. Delivering
group treatment via videoconference to individuals with traumatic
brain injury: a feasibility study. Neuropsychol Rehabil. (2014)
24:784–803. doi: 10.1080/09602011.2014.907186
19. Baylan S, Haig C, MacDonald M, Stiles C, Easto J, Thomson M, et al.
Measuring the effects of listening for leisure on outcome after stroke
(MELLO): a pilot randomized controlled trial of mindful music listening. Int
J Stroke. (201 9) 15:149–58.0 doi: 10.1177/1747493019841250
20. Tornås S, L øvstad M, Solbakk AK, Schanke AK, Stubberud J. Goal
management training combined with external cuing as a means to improve
emotional regulation, psychological functioning, and quality of life in patients
with acquired brain injury: a randomized controlled trial. Arch Phys Med
Rehabil. (2016) 97:1841–52.e3. doi: 10.1016/j.apmr.2016.06.01 4
21. Wilson BA, Alderman N, Burgess PW, Emslie H, Evans JJ. Behavioural
Assessment of the Dysexecutive Syndrome. Bury St. Edmunds: Thames Valley
Test Company (1996).
22. Derogatis LR, Lipman RS, Rickels K, Uhlenhuth EH, Covi L. The Hopkins
Symptom Checklist (HSCL): a self-report symptom inventory. Behav Sci.
(1974) 19:1–15. doi: 10.1002/bs.3830190102
23. Wechsler D. Manual for the Wechsler Abbreviated Scale of Intelligence. San
Antonio, TX: Psychological Corporation (1999).
24. Delis DC, Kaplan E, Kramer JH. Delis-Kaplan Executive Functioning System
(D-KEFS). San Antonio, TX: The Psychological Corporation (2001).
25. Gioia GA, Isquith PK, Guy SC, Kenworthy L. Behavior Rating Inventory
of Executive Function. Odessa, FL: Professional Manual: Psychological
Assessment Resources, Inc. (200 0).
26. Waid-Ebbs JK, Wen PS, Heaton SC, Donovan NJ, Velozo C. The
item level psychometrics of the behaviour rating inventory of executive
function-adult (BRIEF-A) in a TBI sample. Brain Inj. (2012) 26:1646–
57. doi: 10.3109/02699052.2012.700087
27. Cohen J. Statistical Power Analysis for the Behavioral Sciences. 2nd ed.
Hillsdale, NJ: L. Erlbaum Associates (1988). p. xxi, 567.
28. Ravndal E, Amundsen EJ. Mortality among drug users after discharge from
inpatient treatment: an 8-year prospective study. Drug Alcohol Depend. (2010)
108:65–9. doi: 10.1016/j.drugalcdep.2009.11.008
29. Toplak ME, West RF, Stanovich KE. Practitioner review: do performance-
based measures and ratings of executive function assess the same construct? J
Child Psychol Psychiatry. (2013) 54:131 –4 3. doi: 10.1111/jcpp.12001
30. Fleming JM, Strong J, Ashton R. Self- awareness of deficits in adults with
traumatic brain injury: how best to measure? Brain Inj. (1996) 10:1–
15. doi: 10.1080/026990596124674
31. Bogod NM, Mateer CA, MacDonald SW. Self-awareness after traumatic
brain injury: a comparison of measures and their relationship to executive
functions. J Int Neuropsychol Soc. (2003) 9:450–8. doi: 10.1017/S13556177039
30104
32. Barker LA, Morton N, Morrison TG, McGuire BE. Inter-rater reliability
of the Dysexecutive Questionnaire (DEX): comparative data from non-
clinician respondents-all raters are not equal. Brain Inj. (2011) 25:997–
1004. doi: 10.3109/02699052.2011.597046
33. Haag HL, Jones D, Joseph T, Colantonio A. Battered and brain
injured: traumatic brain injury among women survivors of
intimate partner violence-a scoping review. Trauma Violence Abuse.
(2019). doi: 10.1177/1524838019850623. [Epub ahead of print].
34. Aldao A, Nolen-Hoeksema S, Schweizer S. Emotion-regulation strategies
across psychopathology: a meta-analytic review. Clin Psychol Rev. (2010)
30:217–37. doi: 10.1016/j.cpr.2009.11.004
35. Gross JJ. E motion regulation: current status and future prospects. Psychol
Inquiry. (2015) 26:1–26. doi: 10.1080/1047840X.2014.940781
36. Tibaek M, Kammersgaard LP, Johnsen SP, Dehlendorff C, Forchhammer
HB. Long-term return to work after acquired brain injury in young danish
adults: a nation-wide registry-based cohort study. Front Neurol. (2018)
9:1180. doi: 10.3389/fneur.2018.01180
37. Kim S, Zemon V, Lehrer P, McCraty R, C avallo MM, Raghavan P, et al.
Emotion regulation after acquired brain injury: a study of heart rate
variability, attentional control, and psychophysiology. Brain Inj. (2019)
33:1012–20. doi: 10.1080/02699052.2019.1593506
Conflict of Interest: The authors declare that the research was conducted in the
absence of any commercial or financial relationships that could be construed as a
potential conflict of interest.
Copyright © 2020 Stubberud, Løvstad, Solbakk, Schanke and Tornås. This is an
open-access article distributed under the terms of the Creative Commons Attribution
License (CC BY). The use, distribution or reproduction in other forums is permitted,
provided the original author(s) and the copyright owner(s) are credited and that the
original publication in this journal is cited, in accordance with accepted academic
practice. No use, distribution or reproduction is permitted which does not comply
with these terms.
Frontiers in Neurology | www.frontiersin.org 7 September 2020 | Volume 11 | Article 1011