European Journal of Neurology 2012
doi:10.1111/j.1468-1331.2012.03813.x
Does head CT scan pathology predict outcome after mild
traumatic brain injury?
M. Lannsjöa,b, M. Backhedenc, U. Johanssonb, J. L. af Geijerstamd and J. Borge
a
Department of Rehabilitation Medicine, Institute of Neuroscience, University of Uppsala, Uppsala, Sweden; bCentre for Research and
Development, Uppsala University/County Council of Gavleborg, Gavleborg, Sweden; cMedical Statistics Unit, Department LIME, Karolinska Institutet, Stockholm, Sweden; dClinical Epidemiology Unit, Department of Medicine, Karolinska Institutet, Stockholm, Sweden;
and eDepartment of Clinical Sciences, Rehabilitation Medicine, Karolinska Institutet, Danderyd Hospital, Stockholm, Sweden
Keywords:
brain concussion, head
CT scan, mild traumatic
brain injury, prediction
Received 3 April 2012
Accepted 12 June 2012
Background: More evidence is needed to forward our understanding of the key
determinants of poor outcome after mild traumatic brain injury (MTBI). A large,
prospective, national cohort of patients was studied to analyse the effect of head CT
scan pathology on the outcome.
Methods: Thousand two hundred and sixty-two patients with MTBI [Glasgow
Coma Scale (GCS) score 15] at 39 emergency departments completed a study
protocol including acute head CT scan examination and follow-up by the
Rivermead Post Concussion Symptoms Questionnaire (RPQ) and the Glasgow
Outcome Scale Extended (GOSE) at 3 months after MTBI. Binary logistic
regression was used for the assessment of prediction ability.
Results: In 751 men (60%) and 511 women (40%), with a mean age of 30 years
(median 21, range 6–94), we observed relevant or suspect relevant pathologic
findings on acute CT scan in 52 patients (4%). Patients aged below 30 years
reported better outcome both with respect to symptoms and GOSE as compared to
patients in older age groups. Men reported better outcome than women as regards
symptoms (OR 0.64, CI 0.49–0.85 for 3 symptoms) and global function (OR 0.60,
CI 0.39–0.92 for GOSE 1–6).
Conclusions: Pathology on acute CT scan examination had no effect on selfreported symptoms or global function at 3 months after MTBI. Female gender and
older age predicted a less favourable outcome. The findings support the view that
other factors than brain injury deserve attention to minimize long-term complaints
after MTBI.
Introduction
Traumatic brain injury (TBI) is a recognized public
health problem with annual incidence rates around
250 per 100 000 or more [1,2]. Most patients have a
mild TBI with a presenting Glasgow Coma Scale
(GCS) score of 13–15 [3]. A majority of these patients
present with a GCS score of 15 [4] and are clinically
diagnosed with a brain concussion.
Evidence-based guidelines for the acute management
of patients with mild TBI (MTBI) specify criteria for
routine use of CT scan examination as part of the
diagnostic set-up [5,6]. In patients presenting with a
GCS score of 15, around 5% exhibits trauma-related
Correspondence: M. Lannsjö, Rehabilitation Medicine, Sandviken
Hospital, SE-81189 Sandviken, Sweden (tel.: +4626278529 or
+ 46703264259; fax: +4626255997; e-mail: [email protected]).
© 2012 The Author(s)
European Journal of Neurology © 2012 EFNS
CT scan abnormalities [7,8] and acute CT scan
examination allows safe and cost-effective triage of this
large MTBI population [9].
In contrast, evidence-based guidelines for cost-effective prevention and treatment of post-traumatic,
‘post-concussional’ problems are lacking, although
such problems have long been recognized in a
subgroup of patients [10,11]. Some evidence indicates
that early, educational information [12,13] and teambased follow-up [14] may be beneficial but identification of patients at risk for poor outcome remains a
challenge. Whilst previous studies of patients
with MTBI have demonstrated that older age [15,16],
female gender [17], premorbid health problems [18,19],
co-morbidities [19,20] and other injuries [16,18],
financial incentives and litigation [21,22], may be
associated with poor outcome, the impact of brain
lesions remains unclear and a matter of debate
1
2
M. Lannsjö et al.
[16,23,24]. Two recent studies indicate that demographic and other variables [16,18] are stronger
predictors than CT scan pathology. These studies
included patients seen at a level I Trauma centre and
presenting with a GCS score of 13–15. More evidence
is needed to forward our understanding of the key
determinants of poor outcome after MTBI and thus
identify relevant targets for preventive and therapeutic
interventions and to guide clinical management.
Patients with the mildest form of MTBI, who
present with a GCS score of 15, constitute the largest
proportion of all patients with TBI and are managed
in both regional and local hospitals. Hence, using
acute head CT scan examination, we investigated the
effect of traumatic pathology on the outcome
after MTBI in a large, prospective national cohort of
patients with MTBI and a presenting GCS score
of 15.
Methods
During the period May 2001–January 2004, 39 of 75
emergency departments in Sweden participated in a
randomized controlled trial comparing effects and
costs of two acute management strategies for MTBI
[9]. Participating departments were representative
according to hospital size and geographical distribution. Eligible were patients 6 years and with a
history of head trauma within the last 24 h, confirmed
or suspected loss of consciousness (LOC) and/or
amnesia, normal neurological examination and a GCS
score of 15, and no associated injuries that required
admission. A total of 2602 persons were recruited and
randomized either to inpatient care (1286) or to head
CT scan and early discharge if CT findings were
normal (1316). Patients, who were randomized to
head CT scan and discharge, formed the study sample. Scans were reported and interpreted according to
local clinical practice at each study site.
Follow-up at 3 months post-injury was by mailed
questionnaires to assess symptoms outcome by the
Rivermead Post Concussion Symptoms Questionnaire
(RPQ) [25] and global outcome by the Glasgow
Outcome Scale Extended (GOSE) [26,27].
The RPQ consists of 16 items asking the patient to
rate symptoms on a scale from 0 to 4 (0 = not experienced at all, 1 = no more of a problem, 2 = a mild
problem, 3 = a moderate problem and 4 = a severe
problem). Questionnaires were received from 97% of
the participants. Frequency of missing data in the
questionnaires was <1.5% for each of the 16 items.
Poor symptom outcome was defined as three symptoms or more according to RPQ. We also analysed
outcome of symptoms belonging to each of four
factors (somatic, cognitive, emotional and audiovisual) identified in a previous study [28].
The GOSE is an ordinal scale with eight steps
(1 = dead, 2 = vegetative state, 3 = lower severe
disability, 4 = upper severe disability, 5 = lower moderate disability, 6 = upper moderate disability,
7 = lower good recovery, 8 = upper good recovery).
Statistical methods
Binary logistic regression was used to analyse data.
Predictor variables in the statistical models were
findings at head CT scan, age and gender. Outcome
variables were GOSE score dichotomized to 1–6 and
7–8 and RPQ reporting dichotomized into having or
not having 3 symptoms. Age was entered in the
model as a factor with the age groupings, 6–14.9, 15–
29.9, 30–59.9, 60–79.9 and 80 years. Pair wise comparisons between age groups were performed in case
of a significant overall age effect. The overall model
was checked with tests of the global null hypothesis.
Type 3 analyses for each predictor variable were
carried out as well as odds ratios with 95% confidence
intervals. The type 3 analysis gives a result that is independent of the variables order in the model. A significance level of 5% was used for all tests performed.
Binary logistic regression model fit was assessed with
the Hosmer Lemeshov test. The area under the Receiver Operating Characteristic Curve (ROC curve),
AUC, was calculated to estimate discrimination ability. Bivariate associations were assessed with Spearman rank correlation and log linear models. The
statistical analyses were carried out in the statistical
package SAS 9.2 (SAS Institute Inc., Solna, Sweden).
Ethics
No financial incentives were offered. Oral and written
information was provided for written consent. All
regional research ethics committees in Sweden
approved the study. The Swedish national health and
pharmaceutical insurance plan covered all patients
included in the study.
Results
The study sample comprised 1262 patients, 751 men
(60%) and 511 women (40%) after exclusion of 24
patients with missing head CT scan data and 30 with
pathology on CT scan not associated with the acute
injury. Table 1 presents baseline data.
Mean age was 30 years (median, 21; range, 6.0–93.6).
The sample was divided into five age groups (Table 1)
according to homogenous frequencies of symptoms
© 2012 The Author(s)
European Journal of Neurology © 2012 EFNS European Journal of Neurology
Head CT and outcome after MTBI
Table 1 Age, gender and result of head CT scan
Base line data
Age
Gender
CT
% (No.)
6–14.9
15–29.9
30–59.9
60–79.9
80
Male
Female
Normal
Pathology, total
Haemorrhage/contusion
Haematoma
Fracture, no other pathology
Oedema/other
32
31
24
10
3
60
40
96
4
(394)
(389)
(304)
(128)
(39)
(751)
(511)
(1210)
(52)
(27)
(10)
(7)
(8)
within these groups. Relevant or suspected relevant
pathology was observed in 52 of 1262 (4%) CT scans
and comprised haemorrhage/contusions in 27 (52%),
fractures in 10 (19%), haematomas in 7 (14%), oedema
or other in 8 (15%). We found no significant interactions between gender and CT results or between age
and gender.
Effect of age, gender and CT pathology on symptoms
at 3 months post-injury
Poor symptom outcome was defined as reporting 3
symptoms. When individual symptoms were dichotomized into no current problems with symptoms (RPQ
scores 0–1) versus little, moderate or severe problems
with symptoms (RPQ scores 2–4), 23% (n = 279) of
the participants reported three or more symptoms
after 3 months (6% missing data). All symptoms
except double-vision showed satisfying likelihood
ratio. However, “double vision” had no significant
influence on the results and was kept in the analysis.
Table 2 presents results of the binary logistic regression analysis.
Age had an effect on symptoms at 3 months.
Patients in age groups below 30 years had
significantly lower OR for reporting three or more
symptoms. Gender also had an effect. Males had
significantly lower OR for reporting three or more
symptoms. Head CT scan results had no effect on
symptom outcome (Table 2). Area under the ROC
curve was 0.654.
3
Table 2 Effect of age, gender and CT scan pathology on symptoms
at 3 months after mild traumatic brain injury. The table shows
regards symptoms (OR) for having problems with three or more
symptoms (poor outcome)
Factor
Age
a
Gender
CT
Comparison
OR
95% CI
Lower Upper
P-value
6.0–14.9 15.0–29.9
6.0–14.9 30.0–59.9
6.0–14.9 60.0–79.9
6.0–14.9 80.0–99.9
15.0–29.9 30.0–59.9
15.0–29.9 60.0–79.9
15.0–29.9 80.0–99.9
30.0–59.9 60.0–79.9
30.0–59.9 80.0–99.9
60.0–79.9 80.0–99.9
Male/Female
Normal/Pathologic
0.52
0.30
0.32
0.22
0.58
0.62
0.42
1.07
0.73
0.69
0.64
0.68
0.35
0.20
0.19
0.10
0.41
0.39
0.20
0.67
0.35
0.31
0.49
0.36
0.001
0.000
0.000
0.000
0.002
0.041
0.022
0.772
0.411
0.352
0.002
0.241
0.77
0.44
0.52
0.47
0.82
0.98
0.88
1.70
1.53
1.51
0.85
1.32
Overall test for age, P < 0.001.
a
of these analyses corresponded well to the results of
the analysis for all symptoms and added no more
information.
Effect of age, gender and CT pathology on global
function at 3 months post-injury
At 3 months, four patients (0.3%) had a score of 1
(dead), no patient had a score of 2 (vegetative state),
101 had a score of 1–6 (8%) and 1125 had a GOSE
score 7–8 (89%); data were missing in 3%. Good outcome was defined as GOSE scores of 7–8 and poor
outcome as GOSE scores of 1–6. Table 3 presents the
results of the binary regression analysis.
Age had an effect on GOSE at 3 months with in
the main, significantly lower OR for poor outcome
for younger ages compared to older. We found no
significant differences between the two youngest age
groups (6–14.9 and 15–29.9), between age groups 15–
29.9 and 30–59.9 and between age group 30–59.9 and
60–79.9. Gender also had an effect. Men had significantly lower OR for a poor outcome. Head CT scan
results had no effect on the outcome according to
GOSE. Area under the ROC curve was 0.669.
Analyses with Spearman rank correlations showed
no significant correlations between GOSE scores and
remaining symptoms (correlation value 0.014).
Discussion
Effects on symptoms by symptom factors
Somatic, cognitive, emotional or audio-visual factors,
respectively, were examined for two levels of
unfavourable outcome, that is, one symptom or more
and two symptoms or more, respectively. The results
The main finding of this study is that traumatic head
CT scan pathology has no effect on self-reported outcome at 3 months after MTBI. Study patients had a
presenting GCS score of 15 in the emergency room,
and thus represent the largest subgroup of patients
© 2012 The Author(s)
European Journal of Neurology © 2012 EFNS European Journal of Neurology
4
M. Lannsjö et al.
Table 3 Effect of age, gender and CT scan pathology on Glasgow Outcome Scale Extended (GOSE) at 3 months. The table shows regards
symptoms (OR) for having a GOSE score of 1–6 (poor outcome)
Factor
Age
a
Gender
CT
Comparison
6.0–14.9
6.0–14.9
6.0–14.9
6.0–14.9
15.0–29.9
15.0–29.9
15.0–29.9
30.0–59.9
30.0–59.9
60.0–79.9
Male/Female
Normal/Pathologic
15.0–29.9
30.0–59.9
60.0–79.9
80.0–99.9
30.0–59.9
60.0–79.9
80.0–99.9
60.0–79.9
80.0–99.9
80.0–99.9
0.60
0.52
OR
95% CI
Lower
Upper
P-value
0.65
0.41
0.34
0.11
0.63
0.52
0.16
0.83
0.26
0.31
0.39
0.23
0.35
0.22
0.17
0.05
0.36
0.27
0.07
0.43
0.12
0.13
0.92
1.16
1.23
0.77
0.70
0.25
1.10
1.03
0.37
1.59
0.58
0.76
0.018
0.114
0.194
0.005
0.004
0.000
0.106
0.059
0.000
0.566
0.001
0.010
Overall test for age, P < 0.001.
a
with traumatic brain injuries [4]. Patients from
different hospital settings were included, and the
attrition rate was low. Hence, the findings add to our
understanding of outcome prediction after MTBI and
support the view that factors other than brain injury,
as defined by head CT scan pathology, are key
predictors. The findings also indicate that more
sensitive methods than CT scan are needed to detect
relevant brain abnormalities in this group of patients.
We defined a poor symptoms outcome as a report
of three symptoms or more, which is in accordance
with most previous studies and suggested criteria sets
for related ICD-10 and DSM IV diagnoses [29,30].
Outcome was measured at 3 months after the event
because previous studies indicate that when symptoms resolve after MTBI, this occurs within this
time-period [22] and the risk for intervening events
that may confound the outcome increases by time.
The proportion of patients with a poor symptoms
outcome (23%) is in agreement with previous
reports, although some studies including patients
within the whole MTBI spectrum report larger proportions [19,23,31,32]. The RPQ symptoms questionnaire is a widely used measure that has recently been
subject to factor analysis [28,33] and Rasch analysis
[34,35]. Based on findings in these previous studies,
we dichotomized data for each symptom (having or
not having symptoms) instead of using total, summary scores.
Glasgow Outcome Scale Extended is an established
instrument to assess global outcome after TBI, covers
aspects on personal care and social functioning and
relates consistently with other measures of selfreported health and disability [27]. We defined poor
outcome as a GOSE score of 1–6, which complies
with the instructions of the scale a recent study in the
area [16]. The observed proportion of patients report-
ing a GOSE score below 7 (8%) was lower than
reported in some previous studies including patients
with GCS scores of 13–15 [15,16].
The rate of relevant or suspect relevant pathology
on head CT scan was 4%, most of which was attributed to haemorrhage or brain contusion. The CT scan
results rely on routine evaluation by radiologists at
each of the hospitals where patients were recruited,
and consequently, the validity of these data may be
questioned. However, the observed frequency and type
of CT scan abnormalities are in agreement with previous reports on patients presenting with a GCS score
of 15 [8], but lower than observed in more selected
study samples recruited at trauma-level centres [16,36].
Thus, the CT scan findings reflect routine evaluation
of these patients in clinical practice and give our
results high external validity. This information should
form the basis on which to guide patients and plan
further interventions.
CT scan pathology had no effect on self-reported
symptoms in total, or on somatic, cognitive, emotional or audio-visual symptoms as previous defined
by factor analysis [28,33]. This does not exclude brain
pathology as a factor at play in patients with a poor
outcome after MTBI. First, our study allows conclusions only for patients presenting with a GCS score of
15, and with no need of surgical or other specific
interventions. However, these patients constitute the
large majority of patients with MTBI, or brain concussion [4]. Second, CT scans may not be sensitive to
relevant functional or structural abnormalities, for
example, diffuse axonal injury [37]. Some previous
studies indicate that a substantial proportion of
patients with MTBI and a normal head CT scan
might have brain pathology according to MRI scans
[38] but the impact of such brain pathology on the
long-term outcome after MTBI remains to be
© 2012 The Author(s)
European Journal of Neurology © 2012 EFNS European Journal of Neurology
Head CT and outcome after MTBI
demonstrated. Thus, further studies, utilising new
neuroimaging methods, will hopefully clarify the possible role of structural or functional abnormalities for
long-term outcome after the most common, mildest
injuries [39]. Third, although clinically relevant, selfreported outcomes might not be very specific, and no
consensus has yet been reached on how to define a
poor outcome [24].
The impact of age and gender on the outcome after
MTBI has been subject to several previous studies.
Most previous reports on the impact of age indicate
that young persons have better outcome [15,16,22].
The present study provides strong evidence that age
has an effect on the self-reported outcome after MTBI
and that young persons have a better outcome. Most
previous reports on the impact of gender indicate that
women report more remaining symptoms after MTBI
[17], whilst some studies found no such relationship
[18,22]. The present study provides strong evidence
that gender has an effect on self-reported outcome
after MTBI and that women are at greater risk for
poor outcome than men are.
The key finding of this study has some practical
implications. There is some evidence that the early
provision of educational and reassuring information
as well as team-based follow-up may reduce long-term
problems after MTBI [8,12–14]. Our findings indicate
that a similar approach is relevant also for patients
presenting with a GCS score of 15 after blunt head
trauma and with head CT scan abnormalities that do
not require surgery or other acute intervention.
Instead, pre-injury factors, co-morbidities and social
problems deserve more attention and some of these
may be available for intervention. Further studies with
other diagnostic tools including new brain imaging
methods [39] may help clarify the potential role of
abnormal brain function or structure for persisting
problems and if these may be targeted by MTBI-specific treatments.
Limitations of study
The study design did not allow control for other
relevant baseline factors, for example, psychosocial
conditions or co-morbidities, or for intervening
events or interventions during the follow-up period.
However, we controlled for two strong predictors
identified also in previous studies, and it appears
less likely that other factors would change the main
finding. The predictor variables discrimination ability, as assessed by the estimated AUC, was only
modest, which probably reflects the difficulty to find
strong predictors in a complexity of causes in this
context.
5
Conclusions
Acute head CT scan pathology does not predict symptoms or global function at 3 months after MTBI with
a presenting GCS score of 15, but female gender and
older age are associated with poor outcome. The findings support the view that factors other than brain
injury deserve attention to minimize long-term complaints after MTBI and also that more sensitive imaging methods than CT scan are needed to clarify the
possible impact of brain abnormalities on long-term
outcome after MTBI.
Acknowledgements
Grants from the Centre for Research and Development Uppsala University/County Council of Gavleborg, the Stockholm County Council and AFA
Insurance. Authors declare no conflicts of interest.
References
1. Cassidy JD, Carroll LJ, Peloso PM, et al. Incidence,
risk factors and prevention of mild traumatic brain
injury: results of the WHO Collaboration Centre Task
Force On Mild Traumatic Brain Injury. J Rehabil Med
2004; Feb(Suppl. 43): 28–60.
2. Tagliaferri F, Compagnone C, Korsic M, Servadei F,
Kraus J. A systematic review of brain injury epidemiology in Europe. Acta Neurochir 2006; 148: 255–268.
3. Teasdale GM, Jennett B. Assessment of coma and
impaired consciousness. Lancet 1974; 13: 81–84.
4. Kay A, Teasdale GM. Head injury in the United Kingdom. World J Surg 2001; 25: 1210–1220.
5. National Institute for Clinical Excellence Head Injury.
Triage, Assessment, Investigation and Early Management
of Head Injury in Infants, Children and Adults. Clinical
Guideline 4. Developed by the National Collaborating
Centre for Acute Care. London: NICE, 2007.
6. Vos PE, Alekseenko Y, Battistin L, et al. Mild traumatic brain injury. Eur J Neurol 2012; 19: 191–198.
7. Stiell IG, Clement C, Rowe BH, et al. Comparison of
the Canadian CT head rule and the New Orleans criteria in patients with minor head injury. JAMA 2005; 294:
1511–1518.
8. Borg J, Holm L, Cassidy JD, et al. Diagnostic procedures in mild traumatic brain injury: results of the
WHO Collaborating Centre Task Force On Mild Traumatic Brain Injury. J Rehabil Med 2004; Feb(Suppl. 43):
61–75.
9. Geijerstam JL, Oredsson S, Britton M. Medical outcome
after immediate computed tomography or admission for
observation in patients with mild head injury: randomised controlled trial. Br Med J 2006; 333: 465.
10. Ruff RM, Camenzuli L, Mueller J. Miserable minority:
emotional risk factors that influence the outcome of a
mild traumatic brain injury. Brain Inj 1996; 10: 551–565.
11. Iverson GL. Outcome from mild traumatic brain injury.
Curr Opin Psychiatry 2005; 18: 301–317.
12. Paniak C, Toller-Lobe G, Reynolds S, Melnyk A, Nagy
J. A randomized trial of two treatments for mild trau-
© 2012 The Author(s)
European Journal of Neurology © 2012 EFNS European Journal of Neurology
6
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
M. Lannsjö et al.
matic brain injury: 1 year follow-up. Brain Inj 2000; 14:
219–226.
Ponsford J, Willmott C, Rothwell A, et al. Impact of
early intervention on outcome following mild head
injury in adults. J Neurol Neurosurg Psychiatry 2002; 73:
330–332.
Wade DT, King NS, Wenden FJ, Crawford S, Caldwell
FE. Routine follow up after head injury: a second
randomised controlled trial. J Neurol Neurosurg Psychiatry 1998; 65: 177–183.
Mosenthal AC, Livingston DH, Lavery RF, et al. The
effect of age on functional outcome in mild traumatic
brain injury: 6-month report of a prospective multicenter
trial. J Trauma 2004; 56: 1042–1048.
Jacobs B, Beems T, Stulemeijer M, et al. Outcome prediction in mild traumatic brain injury: age and clinical
variables are stronger predictors than CT abnormalities.
J Neurotrauma 2010; 27: 655–668.
Bazarian JJ, Blyth B, Mookerjee S, He H, McDermott
MP. Sex differences in outcome after mild traumatic
brain injury. J Neurotrauma 2010; 27: 527–539.
Stulemeijer M, van der Werf S, Borm GF, Vos PE.
Early prediction of favourable recovery 6 months after
mild traumatic brain injury. J Neurol Neurosurg Psychiatry 2008; 79: 936–942.
Faux S, Sheedy J, Delaney R, Riopelle R. Emergency
department prediction of post-concussive syndrome following mild traumatic brain injury – an international
cross-validation study. Brain Inj 2011; 25: 14–22.
Lange RT, Iverson GL, Rose A. Depression strongly
influences postconcussion symptom reporting following
mild traumatic brain injury. J Head Trauma Rehabil
2011; 26: 127–137.
Binder LM, Rohling ML. Money matters: a metaanalytic review of the effects of financial incentives on
recovery after closed-head injury. Am J Psychiatry 1996;
153: 7–10.
Carroll LJ, Cassidy JD, Peloso PM, et al. Prognosis for
mild traumatic brain injury: results of the WHO Collaborating Centre Task Force on Mild Traumatic Brain
Injury. J Rehabil Med 2004; Feb(Suppl. 43): 84–105.
Meares S, Shores EA, Taylor AJ, et al. The prospective
course of postconcussion syndrome: the role of mild
traumatic brain injury. Neuropsychology 2011; 25: 454–
465.
Ruff RM. Mild traumatic brain injury and neural recovery: rethinking the debate. NeuroRehabilitation 2011; 28:
167–180.
King NS, Crawford S, Wenden FJ, Moss NEG, Wade
DT. The Rivermead Post Concussion Symptoms Questionnaire: a measure of symptoms commonly experienced after head injury and its reliability. J Neurol 1995;
242: 587–592.
26. Teasdale GM, Pettigrew LEL, Wilson JTL, Murray G,
Jennett B. Analyzing outcome of treatment of severe
brain injury: a review and update on advancing the use
of the Glasgow outcome scale. J Neurotrauma 1998; 15:
587–597.
27. Wilson JTL, Pettigrew LEL, Teasdale GM. Emotional
and cognitive consequences of head injury in relation to
the Glasgow outcome scale. J Neurol Neurosurg Psychiatry 2000; 69: 204–209.
28. Lannsjö M, af Geijerstam JL, Johansson U, Bring J,
Borg J. Prevalence and structure of symptoms at three
months after Mild Traumatic Brain Injury in a national
cohort. Brain Inj 2009; 23: 213–219.
29. World Health Organization. The ICD-10 Classification
of Mental and Behavioural Disorders: Diagnostic Criteria
for Research. Geneva: World Health Organization,
1993.
30. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders, 4th edn. Washington,
DC: American Psychiatric Association, 1994.
31. Ponsford J, Willmott C, Rothwell A, et al. Factors influencing outcome following mild traumatic brain injury in
adults. J Int Neuropsychol Soc 2000; 6: 568–579.
32. Røe C, Sveen U, Alvsåker K, Bautz-Holter E. Post-concussion symptoms after mild traumatic brain injury:
influence of demographic factors and injury severity in a
1-year cohort study. Disabil Rehabil 2009; 31: 1235–
1243.
33. Potter S, Leigh E, Wade D, Fleminger S. The Rivermead Post Concussion Symptoms Questionnaire; a
confirmatory factor analysis. J Neurol 2006; 253:
1603–1614.
34. Eyres S, Carey A, Gilworth G, Neumann V, Tennant A.
Construct validity and reliability of the Rivermead PostConcussion Symptoms Questionnaire. Clinical Rehabilitation 2005; 19: 878–887.
35. Lannsjö M, Borg J, Björklund G, af Geijerstam JL,
Lundgren-Nilsson Å. Internal construct validity of the
Rivermead Post-concussion Symptoms Questionnaire.
J Rehabil Med 2011; 43: 997–1002.
36. Hsiang JNK, Yeung T, Yu ALM, Poon WS. High-risk
mild head injury. J Neurosurg 1997; 87: 234–238.
37. Povlishock JT, Katz DI. Update of neuropathology and
neurological recovery after traumatic brain injury.
J Head Trauma Rehabil 2005; 20: 76–94.
38. Bazarian JJ, Blyth B, Cimpello L. Bench to bedside: evidence for brian injury after concussion – looking beyond
the computed tomography scan. 2006 by the Society for
Academic Emergency Medicine. Acad Emerg Med 2006;
13: 199–214.
39. Gonzales PG, Walker MT. Imaging modalities in mild
traumatic brain injury and sports concussion. Am Acad
Physical Med Rehabil 2011; 3: 413–424.
© 2012 The Author(s)
European Journal of Neurology © 2012 EFNS European Journal of Neurology