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Brain Injury, October 2009; 23(11): 879–887
The heterogeneity of mild traumatic brain injury:
Where do we stand?
ANDRE
´E TELLIER
1
, SHAWN C. MARSHALL
2
, KEITH G. WILSON
3
, ANDRA SMITH
4
,
MARY PERUGINI
3
, & IAN GILMOUR STIELL
5
1
Department of Psychology (Neuropsychology Ser vice), The Ottawa Hospital,
2
Department of Medicine, The Ottawa
Hospital Rehabilitation Centre,
3
Department of Psychology, The Ottawa Hospital Rehabilitation Centre,
4
School of
Psychology, University of Ottawa, and
5
Clinical Epidemiology Unit, Loeb Research Institute, University of Ottawa,
Ottawa, Ontario, Canada
(Received 17 April 2009; accepted 22 July 2009)
Abstract
Primary objective: To explore the heterogeneity of mild traumatic brain injury (mTBI).
Methods and procedures: Hospital-based prospective follow-up study of 125 patients with mTBI sub-divided into ‘severity’
sub-groups on the basis of GCS scores (GCS of 15 ¼mild sub-group; GCS of 13–14 ¼moderate sub-group). Post-
traumatic amnesia (PTA) duration (30 minutes used as a cut-off) was also used to define group membership for secondary
analyses. The follow-up assessment consisted of a brief neuropsychological battery as well as measures of neurobehavioural
functioning, community integration and post-concussive symptomatology. CT scanning was also obtained when clinically
relevant.
Main outcomes and results: The two mTBI sub-groups, as defined by GCS scores, did not differ with respect to post-
concussive symptomatology, neurobehavioural symptoms, neuropsychological performance or CT scan abnormalities. In
contrast, when group membership was redefined on the basis of PTA, the two sub-groups differed significantly with respect
to intracranial abnormalities and report of aggressive or disinhibited behaviours at the 6-month mark.
Conclusions: While the notion of heterogeneity in mTBI was not supported when severity was based on GCS scores, there
was partial support when PTA duration was used as a measure of severity.
Keywords: Glasgow Coma Scale, mild brain injury, outcome, traumatic brain injury
Introduction
Determining the severity of a traumatic brain injury
(TBI) in acute care settings is important to clinicians
as they strive to provide accurate information to
patients and family members regarding the gravity of
the injury, the expected course of recovery and the
likelihood of permanent sequelae. The most univer-
sally used index of severity consists of the Glasgow
Coma Scale (GCS) score [1], a system that is
routinely used by emergency personnel and hospital
staff. Based on the GCS scale, a TBI is deemed to be
mild if the score ranges from 13–15. Implicit in the
inclusion of all patients with GCS scores of 13–15
into the mild TBI (mTBI) group is the assumption
of homogeneity in injury severity. However, this
assumption has been challenged by reports that
patients with a GCS score of 13 and 14 present with
greater morbidity than those with a GCS score of 15
[2–5]. The present study was performed to deter-
mine the extent to which mTBI patients with a GCS
score of 13 and 14 and those with a GCS score of 15
represent sub-groups of patients with distinct clinical
profiles early on in the recovery process.
While it is true that the milder the TBI, the better
the recovery, patients with mTBI are not immune to
experiencing impairment or difficulties beyond the
Correspondence: A. Tellier, Neuropsychology Service, Psychology Department, The Ottawa Hospital, Civic Campus, 1053 Carling Avenue, Ottawa, Ontario
Canada K1Y 4E9. Tel: (613) 761-4580. Fax: (613) 761-5328. E-mail: atellier@ottawahospital.on.ca
ISSN 0269–9052 print/ISSN 1362–301X online ß2009 Informa Healthcare Ltd.
DOI: 10.1080/02699050903200555
3-month mark traditionally held out as the point
beyond which impairment does not extend. Even
though the consensus remains that good recovery is
achieved by most by 3 months post-injury [6], many
reports have shown persistent impairment beyond
that sub-acute phase [7–11]. From a neurocognitive
perspective, cognitive and functional impairments
up to 1 year post-mTBI have been reported [12–14]
and in some cases it has been possible to document
working memory difficulties more than 2 years post-
injury [15, 16]. Various post-concussive symptoms
have also been shown to persist at 6 months post-
injury [17, 18] and long-term morbidities in the form
of increased likelihood of depression and post-
concussion syndrome, under-employment and mar-
ital problems have been reported years following a
mTBI [19]. From a neuroimaging and neurofunc-
tional point of view, abnormal functional studies in
19% of patients with mTBI have been observed
more than 3 months post-injury [20] with reports of
axonal injury on MRI spectroscopy months-to-years
post-injury [21] and a high incidence of temporal
lobe abnormalities on functional imaging over a wide
follow-up period (up to 7.8 years) [22]. Reports such
as these make it clear that residual functional
impairment can arise in some mTBI cases. This
has prompted some authors to term the affected
mTBI sub-group, an estimated 10–20% of all cases,
the ‘miserable minority’ [23, 24].
In parallel to the growing recognition that
difficulties can persist in some mTBI cases, there is
mounting awareness that the aetiology of the persis-
tent difficulties is likely to be heterogeneous across
cases [25, 26]. Variability in terms of the clinical
presentation and aetiology raises interesting issues
with respect to the concept of homogeneity in the
mTBI group. It has been convincingly argued by
some that mTBI patients with lower GCS scores
represent a different mTBI sub-group than those
with a GCS of 15 given the greater likelihood of
neuroimaging abnormalities, need for surgical inter-
vention and poorer outcome associated with a lower
score [2–5]. Previous neuroimaging data also
emphasized the fact that while many patients with
mTBI are not expected to have positive neuroima-
ging findings, a significant proportion of them do
(31% of the entire study group), thus showing the
mTBI group as a whole to be far less homogeneous
than once thought [27]. The need to sub-divide
levels of ‘mild’ TBI has been raised by some [28],
while others have already proposed a different
terminology to refer to the more ‘severe’ mTBI
group (‘high risk’ or ‘complicated’ for those with
intracranial abnormalities on CT scanning) [5, 29].
Yet, others have failed to find significant correlations
between GCS scores in patients with mTBI and
their neurocognitive performance on admission or
employment status at 3 months post-injury [8, 30].
Missing from the above discussion on the vari-
ability in mTBI cases is the influence of psycholog-
ical factors. Much has been written about this topic
and a comprehensive review of this area extends
beyond the focus of this paper. Yet, its importance
warrants mention at this point. The need to consider
the role of personality factors and coping styles as
outcome determinants has been emphasized [31]
and post-traumatic stress [32] and litigation and/or
financial compensation [33–37] have been identified
as risk factors for poorer recovery following mTBI.
That the interaction between psychological factors
and recovery following mTBI is a complex one is
evidenced by reports of an association between
financial gains and slower recovery independent of
mTBI severity [38–40]. Furthermore, the finding
that patients with mTBI who have a history of sexual
abuse and ongoing emotional issues demonstrate
impairment that is different from that exhibited by
a pure mTBI group and yet unexplained by their
emotional status or PTSD symptomatology [41] has
raised the possibility that prolonged stress may result
in neuropathological changes that might predispose
certain individuals to more severe symptomatology
post-mTBI. For a comprehensive review on the
topic of prognostic factors in mTBI, please refer to
Carroll et al. [9].
The controversy surrounding the homogeneity of
the mTBI group might partially reflect the bias
inherent in certain methodological issues. For
instance, many of the studies performed to date
have been retrospective in nature, thus making it
difficult to clearly and objectively define mTBI from
the outset or to systematically record relevant
predictors. Data which were previously recorded
within the context of clinical practice and hence
likely collected by different professionals and within
different contexts, do not have the rigour of data
collected within the context of a prospective design.
Furthermore, many of the retrospective studies have
involved clinical samples of patients who presented
with clinical complaints at some point post-mTBI,
an approach that limits the ability to control for or
at the very least record variables of interest. Finally,
the inclusion of all patients with GCS scores of
13–15 in the same mTBI group is a practice that
may itself introduce variability.
The present study, which took place within the
context of a larger prospective study looking at
consecutive visits to an emergency department, was
an attempt at investigating the hypothesis that
mTBI patients with a GCS score of 13 and 14 and
those with a GCS score of 15 represent different sub-
groups of patients who present with distinct clini-
cal profiles early on in the recovery process.
880 A. Tellier et al.
More specifically, it was hypothesized that patients
with a GCS score of 15 would report fewer clinical
and functional symptoms and have less cognitive
impairment and neuroimaging deficits than mTBI
patients with a score of either 13 or 14.
Methods
Participants
Recruited over a 15-month period, the sample
consisted of 125 patients with mTBI who presented
to the Emergency Department of a lead centre for
trauma and agreed to participate after having been
contacted by phone by an Emergency nurse who
used a scripted text to inform them of the study.
Mild TBI was defined on the basis of a GCS score of
13–15 as well as a loss of consciousness of less than
30 minutes and post-traumatic amnesia (PTA) of up
to 24 hours [42]. The GCS scores that were used for
eligibility determination included scores recorded at
the scene, upon arrival to hospital or during the
period of observation prior to discharge home, with
the lowest recorded score being used. In all cases,
the GCS score was assigned by professional staff
(either the nursing staff of the Emergency depart-
ment or trained ambulance attendants at the scene).
In turn, PTA was defined retrospectively by asking
participants at the time of their initial participation,
that is 1-month post-mTBI, to estimate the duration
according to a pre-determined scale (none, less
than 1 minute, 1–5 minutes, 5–30 minutes, 30–60
minutes, 1–12 hours, or 12–24 hours).
The sample was predominantly male (68%) with a
mean age of 36.58 years (SD ¼13.90). The mech-
anism through which the mTBI was sustained was as
follows: motor vehicle collisions in 33.6%, falls in
25.6% and sports-related/direct blows to the head in
40.8% of cases. Thirty-four per cent of the sample
had sustained a previous TBI. Eighty-nine patients
(71.2% of the original sample) were sent for CT
scanning, as per the usual practice of emergency
physicians in the clinical evaluation of patients. The
majority of participants (70.4%) were assigned an
initial GCS score of 15 (labelled the ‘mild mTBI’
sub-group throughout the remainder of this manu-
script) while the remaining 29.6% of the sample
obtained a GCS score of 13 or 14 (labelled the
‘moderate mTBI’ group).
Instruments
A neuropsychological battery, administered to all
participants at 1 month post-trauma, was kept brief
to minimize the burden on participants who were
also asked to fill out a number of other question-
naires in the context of the larger prospective study.
The battery contained measures which tapped into
areas sensitive to the effects of mTBI, namely
processing speed, working memory, multi-tasking
and sustained attention in the face of perceptual
interference. More specifically, the Stroop Color and
Word Test [43], Trail-making Test [44], Consonant
Trigram Test [45, 46] and Processing Speed Index
and Working Memory Index of the Weschler Adult
Intelligence Scale-III [47] were administered. Pre-
morbid intellect was estimated with the Quick Test
[48], while test-taking attitude and effort were
assessed with the 21-item Test [49].
Subjective complaints at 1 and 6 months post-
mTBI were assessed with the Neurobehavioral
Functioning Inventory (NFI) [50], the Community
Integration Questionnaire (CIQ)–Productivity Scale
[51] and an in-house post-concussive checklist
(5-point likert scale) based on the DSM-IV research
criteria of fatigue, disordered sleep, headaches,
vertigo or dizziness, irritability and changes in
mood or personality. The NFI and CIQ were
chosen due to their ease of administration and
previous use with a mTBI population [52], although
only the Productivity score of the CIQ was used in
analyses due to its greater sensitivity than the other
two scales (Home Integration and Social
Integration) to the impact of mTBI [53, 54]. A
copy of the post-concussive checklist is shown in the
Appendix.
Finally, CT scanning was obtained at the time of
presentation to hospital. This was performed with-
out contrast and with third-generation equipment
and involved cuts of 10 mm or less from the foramen
magnum to the vertex. Both soft tissues and bone
windows were included.
Statistics
MANOVAs, t-tests, frequency distributions and
2
analyses were performed where applicable. For the
purposes of the
2
analyses, CT scanning results
were coded according to presence/absence of posi-
tive findings. When used as a dependent variable,
PTA was coded as an ordinal variable on the basis
of how it was originally recorded (i.e. less than
1 minute, 1–5 minutes, 5–30 minutes, 30–60
minutes, 1–12 hours, 12–24 hours). An alpha level
of 0.05 was used for all statistical tests with correc-
tion for multiple comparisons where appropriate.
Results
As outlined in Table I, the two mTBI sub-groups did
not differ with respect to age, education, estimated
IQ or history of previous TBI. In contrast, there was
a significant over-representation of males in the
moderate mTBI sub-group (p<0.05). In terms of
The heterogeneity of mTBI 881
initial parameters of brain injury severity such as
duration of loss of consciousness, extent of retro-
grade or post-traumatic amnesia and altered mental
state (feeling dazed, disoriented or confused just
after the injury), the two groups did not differ
significantly with the exception of the extent of
their PTA which differentiated the two groups
(
2
¼19.60, p¼0.01) with a larger percentage of
the mild mTBI sub-group reporting a PTA of 30
minutes or less (90.8% vs. 62.1%).
With respect to symptom endorsement at 1 month
post-injury, the two sub-groups did not differ with
respect to their reporting of post-concussive symp-
tomatology or other neurobehavioural symptoms or
integration difficulties commonly associated with a
brain injury (Table II). The same non-significant
group differences were obtained at the 6-month
follow-up. As far as pain is concerned, this was not
reported to any significant degree by either group
(same mean reported by both group) and, as such,
was not considered in further analyses. The two
groups also failed to differ in terms of their reporting
of acute stress disorder at the 1-month mark (8% of
the moderate group vs. 10% of the mild group
reported re-experiencing the traumatic event by way
of thoughts, dreams or flashbacks). Similarly, at the
6-month mark, 0% of the moderate group vs. 1% of
the mild group qualified for a diagnosis of post-
traumatic stress disorder, a difference that was not
significant. As such, the presence of acute or post-
traumatic stress disorder was not used in subsequent
analyses.
In turn, as outlined in Table III, neuropsycholo-
gical performance failed to differ between the two
groups on all measures (F
1,101
¼0.84, p¼0.5).
When previous history of TBI was considered in
the analyses, this variable did not exert a significant
impact on neuropsychological performance
(p¼0.5). Table IV outlines a breakdown of the
neuropsychological data on the basis of a previous
history of TBI.
With respect to the neuroimaging data, of the
71.2% of patients with mTBI who were scanned,
79 patients (i.e. 63.2% of the entire study group)
had unremarkable scans. Those with positive scans
(n¼10) had such abnormalities as contusions,
subarachnoid haemorrhage, subdural & epidural
haematoma and mild mass effect. There was an
Table I. Demographic and brain injury severity indices for the two sub-groups.
Variables
‘Moderate’ mTBI sub-
group (GCS 13–14)
(n¼37), M(SD)
‘Mild’ mTBI sub-
group (GCS 15)
(n¼88), M(SD)
Age 39.38 (15.43) 35.44 (13.16)
Gender (% of males)
a
81% 62.5%
Education (years) 14.22 (2.45) 14.06 (2.35)
IQ
b
105.88 (11.41) 103.18 (14.82)
History of previous TBI 37.8% 33.0%
Cause of mTBI
Motor vehicle collisions 37.8% 31.8%
Falls 27.1% 25.0%
Sports-related or hits to head 35.1% 43.2%
Loss of consciousness
No loss 20.0% 16.1%
5 minutes or less 48.6% 67.8%
>5 minutes 31.4% 16.1%
Retrograde amnesia
None 40.5% 51.1%
5 minutes or less 40.5% 43.2%
>5 minutes but <2 hours 19.0% 5.7%
Post-tramatic amnesia
c
None 13.5% 24.1%
5 minutes or less 16.2% 34.5%
5–30 minutes 32.4% 32.2%
>30 minutes but <24 hours 37.9% 9.2%
Altered mental state (dazed, disoriented or confused)
Not present 8.1% 12.5%
5 minutes or less 10.8% 18.2%
>5 minutes but <12 hours 56.8% 60.2%
>12 hours 24.3% 9.1%
SD ¼Standard deviation.
a
p<0.05.
b
as assessed by the Quick Test.
c
p¼0.01.
882 A. Tellier et al.
inverse relationship between initial GCS score and
the number of requested scans, indicating that the
decision to request a scan was largely prompted by
clinical presentation: 100% of those with a GCS of
13 and 89.7% of those with a GCS score of 14
(combined value of 92%) vs. only 62.5% of those
with a GCS score of 15 were sent for CT scanning.
However, there was no significant difference in terms
of abnormal scans between those with a moderate
mTBI and those with a GCS of 15 (five in each
group; p¼0.5). A listing of the CT scan abnormal-
ities is found in Table V.
Finally, as a way of determining whether or not
PTA duration was a more sensitive indicator of
severity of mTBI than GCS scores, the above
analyses were repeated using PTA duration as a
defining characteristic for group membership. The
‘mild’ PTA group consisted of those whose initial
PTA duration was 30 minutes or less while the
‘moderate’ PTA group included those with a PTA
in excess of 30 minutes. Those repeat analyses failed
to yield any significant group differences in terms of
age, gender, education, estimated IQ, neuropsycho-
logical performance and reporting of post-concussive
symptomatology or community integration com-
plaints at 1 or 6 months post-injury. The presence
of a previous TBI did not alter these findings.
In contrast, the two PTA groups differed sig-
nificantly with respect to intracranial abnormalities
(
2
¼6.35, p¼0.01; only 6% of the mild group had
abnormal scans whereas 27% of the moderate group
did). As far as their endorsement of symptoms on
the NFI at 1 month post-TBI, the two PTA groups
did not differ significantly from each other
(F
6,117
¼0.92, p¼0.14). At the 6-month mark,
however, the two PTA groups differed significantly
Table II. Symptom reporting of the two mTBI sub-groups at 1 month.
a
Variables
‘Moderate’ mTBI sub-
group (GCS 13–14) (n¼37),
M(SD)
‘Mild’ mTBI sub-group
group (GCS 15) (n¼88),
M(SD)
PCS complaints 16.11 (6.42) 17.03 (5.23)
NFI scales (T-scores)
Depression 41.27 (10.41) 40.43 (9.32)
Somatic 42.73 (11.80) 42.56 (8.35)
Memory/Attention 40.73 (11.05) 40.74 (9.89)
Communication 42.59 (10.44) 41.91 (9.91)
Aggression 44.51 (7.62) 43.74 (8.19)
Motor 40.65 (11.88) 41.40 (8.49)
Community integration
Questionnaire productivity/Work sub-scale 5.35 (1.64) 5.27 (2.06)
Pain Rating
b
2.3 (2.34) 2.3 (0.26)
Acute stress disorder reporting
c
(%)
8% 10%
SD ¼Standard deviation; PCS ¼post-concussive symptoms; NFI ¼Neurobehavioral Functioning inventory.
a
All comparisons were non-significant (p-values >0.4).
b
Based on a rating scale of 1 (no pain) to 10 (as intense as you could imagine).
c
A diagnosis of acute stress disorder was made if the patient reported having experienced a traumatic event and had
episodes of re-experiencing the event by way of thoughts, dreams or flashbacks.
Table III. Neuropsychological performance of each sub-group.
Measures
‘Moderate’ mTBI sub- group
(GCS 13–14) (n¼37), M(SD)
‘Mild’ mTBI sub- group (GCS 15)
(n¼88), M(SD)
21-item test forced recognition 17.77 (2.31) 17.88 (2.44)
Stroop interference (T-score) 47.29 (10.63) 51.38 (10.09)
Trail-making test (percentile)
Trail A
a
50.59 (26.72) 63.05 (24.71)
Trail B 60.16 (31.80) 59.48 (31.39)
Consonant trigram test (out of 60) 48.66 (5.91) 48.12 (8.62)
WAIS-III processing speed index 105.44 (16.29) 107.89 (15.63)
WAIS-III working memory index 108.94 (16.66) 108.22 (15.90)
SD ¼Standard deviation; mTBI ¼mild traumatic brain injury.
a
Approached significance at p¼0.07; all other p-values greater than 0.05.
The heterogeneity of mTBI 883
from each other (F
6,69
¼0.80, p¼0.02) and a look at
the individual sub-scales showed a significantly
greater endorsement by the moderate PTA sub-
group of aggressive and disinhibited behaviours
(such as cursing, screaming, hitting, making inap-
propriate comments and breaking things) on the
aggression sub-scale of the NFI (mean T-score of
48.13 [9.16] for the moderate PTA group vs. 41.64
[5.20] for the mild PTA group; p¼0.000). This
finding remained significant even when a previous
TBI history was included as a covariate in the
analyses (p¼0.005).
Discussion
Biases inherent in the present study design need to
be discussed so that proper conclusions can be
derived from the data. For one, the uneven sample
size for the two GCS sub-groups introduced some
bias. Second, the lack of a comprehensive neuro-
psychological battery, which was largely dictated by
a desire to minimize burden on participants, might
have resulted in an under-detection of impairment.
The absence of a control group also limited one’s
ability to rule out a possible impact of non-organic
variables and to make firm conclusions specific to a
mTBI. Furthermore, since a significant proportion
of patients with mTBI frequently fail to seek medical
attention, the present sample of individuals who
presented to hospital is not representative of the
mTBI population at large and thus affects the
generalizability of these findings. Finally, a follow-
up study that could incorporate some of the newer
neuroimaging techniques that can detect the post-
mTBI white matter abnormalities detailed in a
recent review [55] would allow for a more compre-
hensive assessment of the heterogeneity in mTBI.
The results of this prospective study failed to
support the notion of heterogeneity in mTBI when
severity was based on GCS scores but did reveal
partial support when PTA duration was used as a
measure of severity. Whereas those with lower GCS
scores did not differ from those with a GCS of 15
with respect to post-concussive symptomatology,
neurobehavioural symptoms, re-integration difficul-
ties, neuropsychological performance or neuroima-
ging abnormalities, individuals with mTBI who had
experienced a PTA duration greater than 30 minutes
were more likely to have intracranial abnormalities
and to report symptoms suggestive of disinhibition
at 6 months post-mTBI. As such, as defined by PTA
Table IV. Neuropsychological performance on the basis of previous history of TBI.
‘Moderate’ mTBI sub-group (GCS 13–14) ‘Mild’ mTBI sub-group (GCS 15)
Measures No previous TBI TBI Hx No previous TBI TBI Hx
21-item Test 19.00 (1.30) 17.09 (2.30) 17.90 (2.71) 17.77 (1.88)
Stroop interference (t-score) 50.07 (9.52) 49.91 (9.44) 49.96 (9.29) 54.88 (10.69)
Trail-making test (percentile)
Trail A 52.21 (25.58) 56.82 (27.04) 64.87 (25.54) 62.00 (22.96)
Trail B 60.36 (32.97) 66.55 (33.91) 60.23 (29.80) 63.69 (33.39)
Consonant trigram
Test (out of 60) 49.00 (5.50) 49.00 (7.56) 48.35 (8.16) 47.96 (9.64)
WAIS-III PSI 106.86 (16.98) 107.45 (17.57) 108.42 (14.75) 107.35 (18.50)
WAIS-III WMI 110.71 (11.94) 106.64 (18.62) 107.71 (15.24) 109.69 (17.50)
SD ¼Standard deviation; mTBI ¼mild traumatic brain injury; Hx ¼history; PSI ¼Processing speed index; WMI ¼Working memory
index.
Table V. Computerized tomography scan abnormalities.
Number of occurrences by scanned sub-group
a
CT findings
‘Moderate’ mTBI sub-
group (GCS 13–14) (n¼34)
‘Mild’ mTBI sub- group
(GCS 15) (n¼55)
Cerebral contusions 3 3
Subarachnoid haemorrhage 2 2
Subdural haematoma 1 1
Epidural haematoma 1
Mild mass effect 1
a
Total number of abnormalities (14) exceeds the actual number of patients who had abnormal scans (n¼10; 5 in each
group) as many patients had more than one structural abnormality.
884 A. Tellier et al.
duration, mTBI sub-groups did present as distinct
groups with respect to a limited number of clinical
parameters.
That PTA duration should turn out to be a more
sensitive index of severity and a better predictor of
outcome than GCS scores is not unexpected, as
others before have found it to be a significant
predictor of post-concussion syndrome [56] and to
also correlate with outcome in more severe cases.
Not only was group membership based on PTA
more sensitive to the presence of intracranial
abnormalities, it was also sensitive to symptomatol-
ogy reported at 6 months post-mTBI, namely
disinhibited behaviours. PTA duration was thus a
good predictor of the presence of some symptoms
beyond the acute phase.
The ability of PTA duration to identify mTBI sub-
groups and to predict difficulties 6 months post-
injury is welcome news for the clinician hoping to
deal efficiently with the large number of patients
with mTBI who present with often mild and ill-
defined complaints. This is particularly true in a
society where clinical demands far outstrip the
available resources, a reality that makes investigating
or following every patient with mTBI impossible. As
such, knowing that patients with a mTBI who have
experienced a PTA duration greater than 30 minutes
might be more vulnerable to experiencing persistent
symptomatology at 6 months post-injury allows the
clinician to follow or counsel this particular ‘at risk’
sub-group more closely, thus resulting in a more
judicious deployment of limited resources.
The fact that the endorsement of aggressive and
disinhibited behaviours was the only significant
difference between the mild and moderate PTA
group at 6 months post-injury raises interesting
issues with respect to clinical expectations in the sub-
acute phases. For one, it reinforces the position that
some individuals with mTBI are still experiencing
behavioural issues beyond the 3-month mark.
Furthermore, the nature of the complaints implies
disruption of the orbitofrontal system which, if not
properly assessed, might be missed clinically. For
instance, subtle involvement of that system does not
result in gross cognitive or behavioural impairment.
The lack of appropriate tools to detect persistent
difficulties in the sub-acute phases may partially
account for the variability in the extent to which
researchers have claimed good or poor recovery
following a mTBI.
From a neuropsychological point of view, the
inability to find sub-group differences in neurocog-
nitive performance at 1 month post-TBI is consis-
tent with results obtained by others [30]. Yet, the
fact that measures of working memory and multi-
tasking did not differentiate between the two mTBI
sub-groups was quite unexpected, particularly as far
as the inability of the Consonant Trigram Test to
distinguish the two groups is concerned. This is a
measure that is particularly sensitive to the presence
of cognitive impairment in the context of a mTBI
and represents one of the tests that is routinely used
in our centre to investigate mild cases. In fact, a
qualitative look at the neuropsychological data
reveals this measure to be the only one to show
mildly reduced performance. The data also clearly
show the mild reduction in performance to be
virtually the same across both sub-groups. While it
might be tempting to view the Consonant Trigram
Test as insensitive to the effects of TBI given its
failure to differentiate the sub-groups, the global
reduction in performance rather suggests that its
sensitivity is such that it detects impairment in the
mildest of cases. This highlights the need to use the
right marker when investigating impairment in
mTBI cases.
Acknowledgement
This research was supported by funding from the
Ontario Neurotrauma Foundation.
Declaration of Interest: The authors report no
conflicts of interest. The authors alone are respon-
sible for the content and writing of the paper.
References
1. Teasdale G, Jennett B. Assessment of coma and impaired
consciousness: A practical scale. Lancet 1974;2:81–84.
2. Borg J, Holm L, Cassidy JD, Peloso PM, Carroll LJ, von H,
Ericson K. Diagnostic procedures in mild traumatic brain
injury: Results of the WHO collaborating centre task force
on mild traumatic brain injury. Journal of Rehabilitation
Medicine 2004;43(Suppl):61–75.
3. Culotta VP, Sementilli ME, Gerold K, Watts CC.
Clinicopathological heterogeneity in the classification of mild
head injury. Neurosurgery 1996;38:245–250.
4. Go
´mez PA, Lobato RD, Ortega JM, De La Cruz J. Mild
head injury: Differences in prognosis among patients with a
Glasgow Coma Scale score of 13 to 15 and analysis of factors
associated with abnormal CT findings. British Journal of
Neurosurgery 1996;10:453–460.
5. Hsiang JNK, Yeung T, Yu ALM, Poon WS. High-risk mild
head injury. Journal of Neurosurgery 1997;87:234–238.
6. Kashluba S, Paniak C, Blake T, Reynolds S, Toller-Lobe G,
Nagy J. A longitudinal, controlled study of patient complaints
following treated mild traumatic brain injury. Archives of
Clinical Neuropsychology 2004;19:805–816.
7. Bailey BN, Gudeman SK. Minor head injury. In: Becker DP,
Gudeman SK, editors. Textbook of head injury. Philadelphia:
W.B. Saunders; 1989. pp 308–318.
8. Rimel RW, Giordani B, Barth JT, Boll TJ, Jane JA. Disability
caused by minor head injury. Neurosurgery 1981;9:221–228.
9. Carroll LJ, Cassidy JD, Peloso PM, Borg J, von Holst H,
Holm L, Paniak C, Pe
´pin M. Prognosis for mild traumatic
brain injury: Results of the WHO collaborating centre task
force on mild traumatic brain injury. Journal of Rehabilitation
Medicine 2004;43(Suppl):84–105.
The heterogeneity of mTBI 885
10. Middelboe T, Andersen HS, Birket-Smith M, Friis ML.
Minor head injury: Impact on general health after 1 year.
A prospective follow-up study. Acta Neurologica Scandinavia
1992;85:5–9.
11. Wrightson P. Management of disability and rehabilitation
services after mild head injury. In: Levin HS, Eisenberg HM,
Benton AL, editors. Mild head injury. New York: Oxford
University Press; 1989. pp 245–255.
12. Deb S, Lyons I, Koutzoukis C, Neuropsychiatric sequelae
one year after a minor head injury. Journal of Neurology,
Neurosurgery and Psychiatry 1998;65:899–902.
13. Stalnacke BM, Elgh E, Sojka P. One-year follow-up of
mild traumatic brain injury: Cognition, disability and life
satisfaction of patients seeking consultation. Journal of
Rehabilitation Medicine 2007;39:405–411.
14. Van der Naalt J, van Zomeren AH, Sluiter WJ,
Minderhoud JM. One year outcome in mild to moderate head
injury: The predictive value of acute injury characteristics
related to complaints and return to work. Journal of
Neurology, Neurosurgery and Psychiatry 1999;66:207–213.
15. Chen SHA, Kareken DA, Fastenau PS, Trexler LE,
Hutchins GD. A study of persistent post-concussion symp-
toms in mild head trauma using positron emission tomo-
graphy. Journal of Neurology, Neurosurgery and Psychiatry
2003;74:326–332.
16. Vanderploeg RD, Curtiss G, Belanger HG. Long-term
neuropsychological outcomes following mild traumatic
brain injury. Journal of Clinical and Experimental
Neuropsychology 2005;11:228–236.
17. Gerber DJ, Schraa JC. Mild traumatic brain injury: Searching
for the syndrome. Journal of Head Trauma Rehabilitation
1995;10:28–40.
18. Kraus J, Schaffer K, Ayers K, Stenehjem J, Shen H, Afifi AA.
Physical complaints, medical service use, and social and
employment changes following mild traumatic brain injury: A
6-month longitudinal study. Journal of Head Trauma
Rehabilitation 2005;20:239–256.
19. Vanderploeg RD, Curtiss G, Luis CA, Salazar AM. Long-
term morbidities following self-reported mild traumatic
brain injury. Journal of Clinical and Experimental
Neuropsychology 2007;29:585–598.
20. Abu-Judeh HH, Parker R, Singh M, El-Zeftawy H, Atay S,
Kumar M, Naddaf S, Aleksic S, Abdel-Dayem HM. SPET
brain perfusion imaging in mild traumatic brain injury
without loss of consciousness and normal computed tomo-
graphy. Nuclear Medicine Communications 1999;20:
505–510.
21. Cohen BA, Inglese M, Rusinek H, Babb JS, Grossman RI,
Gonen O. Proton MR spectroscopy and MRI-volumetry
in mild traumatic brain injury. American Journal of
Neuroradiology 2007;28:907–913.
22. Umile EM, Sandel E, Alavi A, Terry CM, Plotkin RC.
Dynamic imaging in mild traumatic brain injury: Support for
the theory of medical temporal vulnerability. Archives of
Physical Medicine and Rehabilitation 2002;83:1506–1513.
23. Ruff R. Two decades of advances in understanding of
mild traumatic brain injury. Journal of Head Trauma
Rehabilitation 2005;20:5–18.
24. Ruff RM, Crouch JA, Tro
¨ester AI, Marshall LF,
Buchsbaum MS, Lottenberg S, Somers LM. Selected cases
of poor outcome following minor brain trauma: Comparing
neuropsychological and positron emission tomography
assessment. Brain Injury 1994;8:297–308.
25. Ruff RM, Camenzuli L, Mueller J. Miserable minority:
Emotional risk factors that influence the outcome of a mild
traumatic brain injury. Brain Injury 1996;10:551–565.
26. Binder L. A review of mild head trauma. Part II: Clinical
implications. Journal of Clinical and Experimental
Neuropsychology 1997;19:432–457.
27. Tellier A, Della Malva CL, Cwinn A, Grahovac S,
Morrish W, Brennan-Barnes M. Mild head injury: A misno-
mer. Brain Injury 1999;13:463–475.
28. Kennedy RE, Livingston L, Marwitz JH, Gueck S,
Kreutzer JS, Sander AM. Complicated mild traumatic brain
injury on the inpatient rehabilitation unit: A multicenter
analysis. Journal of Head Trauma Rehabilitation 2006;21:
260–271.
29. Williams DH, Levin HS, Eisenberg HM. Mild head injury
classification. Neurosurgery 1990;27:422–428.
30. Sadowski-Cron C, Shneider J, Senn P, Radanov BP,
Ballinari P, Zimmermann H. Patients with mild traumatic
brain injury: Immediate and long-term outcome compared to
intra-cranial injuries on CT scan. Brain Injury 2007;20:
1131–1137.
31. Finlayson MAJ. Psychotherapy and psychological aspects of
recovery from brain injury. In: Lovell MR, Echemendia RJ,
Barth JT, Collins MW, editors. Traumatic brain injury in
sports. Lisse: Swets & Zeitlinger Publishers; 2004.
pp 417–434.
32. Friedland JF, Dawson DR. Function after motor vehicle
accidents: A prospective study of mild head injury and
posttraumatic stress. Journal of Nervous Mental Disease
2001;189:426–434.
33. Bazarian JJ, Wong T, Harris M, Leahey N, Mookerjee S,
Dombovy M. Epidemiology and predictors of post-concus-
sive syndrome after minor head injury in an emergency
population. Brain Injury 1999;13:173–189.
34. Binder LM, Rohling ML. Money matters: A meta-analytic
review of the effects of financial incentives on recovery
after closed head injury. American Journal of Psychiatry
1996;153:7–10.
35. Feinstein A, Ouchterlony D, Somerville J, Jardine A. The
effects of litigation on symptom expression: A prospective
study following mild traumatic brain injury. Medicine,
Science and the Law 2001;41:116–121.
36. Miller LJ, Donders J. Subjective symptomatology after
traumatic head injury. Brain Injury 2001;15:193–202.
37. Rutherford W, Merrett JD, McDonald JR. Sequelae
of concussion caused by minor head injuries. Lancet
2002;1:1–4.
38. Cassidy JD, Carroll LJ, Co
ˆte
´P, Holm L, Nygren A. Mild
traumatic brain injury after traffic collisions: A population-
based cohort study. Journal of Rehabilitation Medicine
2004;43(Suppl):15–21.
39. Paniak C, Reynolds S, Toller-Lobe G, Melnyk A, Nagy J,
Schmidt D. A longitudinal study of the relationship between
financial compensation and symptoms after treated mild
traumatic brain injury. Journal of Clinical and Experimental
Neuropsychology 2002;24:187–193.
40. Paniak C, Toller-Lobe G, Melnyk A, Nagy J. Prediction of
vocational status three to four months after treated mild
traumatic brain injury. Journal of Musculoskeletal Pain
2000;8:193–200.
41. Raskin SA. The relationship between sexual abuse and mild
traumatic brain injury. Brain Injury 1997;11:587–603.
42. American Congress of Rehabilitation Medicine Mild
Traumatic Brain Injury Committee of the Head Injury
Interdisciplinary Special Interest Group. Definition of mild
traumatic brain injury. Journal of Head Trauma
Rehabilitation 1993;8:86–87.
43. Golden CJ. Stroop color and word test. Wood Dale, IL:
Syoelting Company; 1978.
886 A. Tellier et al.
44. Reitan RM. Validity of the Trail Making Test as an indication
of organic brain damage. Perceptual Motor Skills 1958;8:
271–276.
45. Brown J. Some tests of the decay theory of immediate
memory. Quarterly Journal of Experimental Psychology
1958;10:12–21.
46. Peterson LR, Peterson MJ. Short-term retention of individual
verbal items. Journal of Experimental Psychology 1959;58:
193–198.
47. Wechsler D. Wechsler adult intelligence scale. 3rd edn.
New York: Psychological Corporation; 1997.
48. Ammons RB, Ammons CH. The Quick Test (QT):
Provisional manual. Psychological Reports 1962;11:111–162.
49. Iverson GL. 21-item test research manual. University of
British Columbia. Vancouver, BC: University Press; 1998.
50. Kreutzer J, Seel R, Marwitz J. The Neurobehavioral
Functioning Inventory. San Antonio: The Psychological
Corporation; 1999.
51. Willer B, Rosenthal M, Kreutzer JS, Gordon WA, Rempel R.
Assessment of community integration following rehabilitation
for traumatic brain injury. Journal of Head Trauma
Rehabilitation 1993;8:75–87.
52. Paniak C, Toller-Lobe G, Reynolds S, Melnyk A, Nagy J.
A randomized trial of two treatments for mild traumatic brain
injury: 1 year follow-up. Brain Injury 2000;14:219–226.
53. Paniak C, Phillips K, Toller-Lobe G, Durand A, Nagy J.
Sensitivity of three recent questionnaires to mild traumatic
brain injury-related effects. The Journal of Head Trauma
Rehabilitation 1999;14:211–219.
54. Sta
´lnacke BM. Community integration, social support and
life satisfaction in relation to symptoms 3 years after mild
traumatic brain injury. Brain Injury 2007;21:933–942.
55. Bigler E. Neuropsychology and clinical neuroscience of
persistent post-concussive syndrome. Journal of the
International Neuropsychological Society 2008;14:1–11.
56. Meares S, Shores EA, Taylor AJ, Batchelor J, Bryant RA,
Baguley IJ, Chapman J, Gurka J, Dawson K, Capon L, et al.
Mild traumatic brain injury does not predict acute post-
concussion syndrome. Journal of Neurology, Neurosurgery
and Psychiatry 2008;79:300–306.
Appendix: Post-concussional disorder questionnaire
Never Rarely Sometimes Often Always
Becoming fatigued easily 1 2 3 4 5
Disordered sleep 1 2 3 4 5
Headache 1 2 3 4 5
Vertigo or dizziness 1 2 3 4 5
Irritability or aggression on little or no provocation 1 2 3 4 5
Anxiety, depression or affective liability 1 2 3 4 5
Changes in personality (social or sexual inappropriateness) 1 2 3 4 5
Apathy or lack of spontaneity 1 2 3 4 5
The heterogeneity of mTBI 887