Case study
a r t i c l e i n f o a b s t r a c t
Article history: Traumatic brain injury (TBI) is an important cause of death and disability worldwide. The prognosis eval-
Received 24 October 2016 uation is a challenge when many variables are involved. The authors aimed to develop prognostic model
Accepted 5 March 2017 for assessment of survival chances after TBI based on admission characteristics, including extracranial
injuries, which would allow application of the model before in-hospital therapeutic interventions. A
cohort study evaluated 1275 patients with TBI and abnormal CT scans upon admission to the emergency
Keywords: unit of Hospital das Clinicas of University of Sao Paulo and analyzed the final outcome on mortality. A
Brain injury
logistic regression analysis was undertaken to determine the adjusted weigh of each independent vari-
Prognostic
Survival
able in the outcome. Four variables were found to be significant in the model: age (years), Glasgow
Coma Scale (315), Marshall Scale (MS, stratified into 2,3 or 4,5,6; according to the best group positive
predictive value) and anysochoria (yes/no). The following formula is in a logistic model (USP index to head
injury) estimates the probability of death of patients according to characteristics that influence on mor-
tality. We consider that our mathematical probability model (USP Index) may be applied to clinical prog-
nosis in patients with abnormal CT scans after severe traumatic brain injury.
2017 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.jocn.2017.03.012
0967-5868/ 2017 Elsevier Ltd. All rights reserved.
J.R. Junior et al. / Journal of Clinical Neuroscience 42 (2017) 122128 123
known clinical models are not significant. The purpose of this 3.3. Computed tomography findings
model is to be applied before in-hospital therapeutic interventions.
Marshall degree is statistically associated with mortality
(p < 0.001). Midline deviation is a significant factor in increasing
2. Methods mortality (p < 0.001). Despite exclusion of analysis Marshall I
patients, any category above Marshall II increases the risk of death.
Our cohort study evaluated 1275 patients with TBI and abnor- This was especially observed in Marshall VI when compared with
mal CT scans upon admission to the emergency unit of Hospital Marshall V patients (Table 2). When grouped the overall mortality
das Clinicas of University of Sao Paulo between September 1, of Marshall II and III was 12% and Marshall IV, V and VI was 26%
2003 and December 31, 2009. The primary objective was to ana- (p < 0.001).
lyze the final outcome on mortality. Clinical and radiographic data
were prospectively collected and entered into our database. The
3.4. Glasgow Coma Scale and anisocoria
demographic data, mechanism of cranial trauma, Glasgow Coma
Scale, anisocoria, presence of thoracic lesions, abdominal injuries,
The average Glasgow Coma Scale of patients who die is statisti-
upper limbs fractures, lower limbs fractures, hip fractures and neu-
cally lower than the patients who survived (p < 0.001) (table 3).
rosurgical intervention were compiled. The Marshall scale and
The 1-point increase in Glasgow scale causes a 19% reduction in
midline deviation were documented. Sedation before neurological
the chance of mortality of the patient. Pupillary abnormalities were
assessment, hemodynamic instability or CT scan without abnor-
associated with higher mortality (p < 0.001). The mortality of
malities (Marshall I patients) were excluded from our analysis.
anisocoric patients was 38% and 16% for isocoric patients
Multivariate logistic regression analysis, chi-square test or the
(p < 0.001). Patients with anisocoria have 67% higher chance of
likelihood ratio tests were used to evaluate the effects of patients
mortality (Table 2).
demographics, type of TBI, and extracranial injuries in mortality.
Age, ethnics, gender, etiology of trauma, spinal fractures, thoracic
trauma, abdominal lesions, upper and lower extremities fractures, 3.5. Neurosurgical intervention
GCS score, fixed pupillary response on hospital admission, Marshall
classification, midline shift deviation were included in our analysis. Patients (n = 601) were operated on following current literature
The influence of age and Glasgow Coma Scale on mortality was recommendations for the neurosurgical management of patients
estimated with the use of summary measures (mean, standard with traumatic brain injury. For lesions with more than 50 cm3,
deviation, median, minimum and maximum) and Students t-test. the decision were easier, and usually in favor of surgery. For lesions
Logistic regression analysis was used to analyze the adjusted with volume less than 25 cm3 the conservative management were
weigh of each independent variable in the outcome. According to prefered. When the lesion volume was between 25 and 50 cm3
our results in the multivariate analysis and adjusted weight, four associated factors, as midline shift, cisterns aspects, and Glasgow
variables were found to be significant in the model: age (years), Coma Scale were considered for surgical indication.
Glasgow Coma Scale (315), Marshall Scale (MS, stratified into
2,3 or 4,5,6; according to the best group positive predictive value) 3.6. Multivariate analysis
and anysochoria (yes/no).
After interpretation of the adjusted weight of significant vari- A logistic regression analysis was undertaken to define the
ables a mortality probability calculator was developed using as adjusted weigh of each independent variable in the outcome. Four
input the logit (p) obtained from the analysis applying those four variables were found to be significant in the model: age (years),
independent variables. The tests were performed at a significance Glasgow Coma Scale (315), Marshall Scale (MS, stratified into
level of 5%. 2,3 or 4,5,6; according to the best group positive predictive value)
and anysochoria (yes/no). Data from the regression analysis, odds
ratio with IC 95%, beta-coefficients and p-values from the four
3. Results independent variables included in the model are presented in
Table 4.
3.1. General characteristics The following formula is in a logistic model (we call it USP index
to head injury) estimates the probability of death of patients
Baseline data is presented in Table 1. Most patients were men according to characteristics that influence on mortality:
(81%). More than half (75%) of participants were caucasians. Road Logistic regression equation: logit (p) = 1.36 + (age * 0.03)
traffic crashes represented the most common cause of injury + (GCS * 0.2) + (MS 4,6 or 6 * 0.72) + (anysochoria * 0.58). Proba-
(54%). Young people (less than 30 years) were involved in 39% of bility = 1/1 + elogit (p).
hospital admission. The general mortality was 19.1%. The mortality Constant: 2.04. Hosmer and Lemeshow test: p = 0.24, area
increases with increasing age of the patient (p < 0.001). Ethnics under the curve (AUC): 0.77 ( 0.740.79).
were statistically associated with mortality, 26% of Caucasian peo- Based on this logistic equation, a mortality probability calcula-
ple died versus 16% of others (p = 0.03). tor (Supplementary material) was developed using as input the
logit (p) obtained from the analysis applying those four indepen-
3.2. Extracranial injuries and mortality dent variables. As shown in the example (Fig. 1), the death proba-
bility of a patient aged 65, with a GCS of 7, a MS of 4, with no
The presence of spinal fracture was associated with lower mor- anysochoria is estimated to be around 47.7%. The significance level
tality in the univariate analysis. Of 169 spinal fractures in this ser- of 5% was considered.
ies only 8 patients (5%) died, while 21% of patients without spinal
fractures died (p < 0.001). Spinal fractures were detected in 20% of 4. Discussion
patients classified as Marshall 4, 5 or 6 and 6% of patients classified
as Marshall 2 or 3 (p < 0.001). Thoracic, abdominal, pelvic lesions Neurotrauma is an expressive public health problem. It is a
and upper or lower limbs fractures were not associated with higher heterogeneous disease and outcomes for individual patients are
mortality in these patients (Table 2). very difficult to predict. There are many variables as mechanism
124 J.R. Junior et al. / Journal of Clinical Neuroscience 42 (2017) 122128
Table 1
Demographic data.
Death Total p
No Yes
n % n %
Sex 0.650
Female 199 81.9 44 18.1 243
Male 832 80.6 200 19.4 1032
Age (years) <0.001
<20 158 89.3 19 10.7 177
2029 280 85.9 46 14.1 326
3039 195 81.3 45 18.8 240
4049 153 84.1 29 15.9 182
5059 82 69.2 44 30.8 143
6069 73 77.7 21 22.3 94
7079 46 73.0 17 27.0 63
>80 27 54.0 23 46.0 50
Ethnia 0.034
Caucasian 763 79.3 199 20.7 962
Mixed 203 86.4 32 13.6 235
Black 50 80.6 12 19.4 62
Oriental 15 93.8 1 6.3 16
Causes <0.001
Running over 233 74.2 81 25.8 314
Car accident 116 89.2 14 10.8 130
Motorcycle accident 213 89.5 25 10.5 238
Bike accident 31 86.1 5 13.9 36
Fall from a height 220 79.7 56 20.3 276
Fall from own height 93 75.0 31 25.0 124
Others 125 79.6 32 20.4 157
Total 1031 80.9 244 19.1 1275
Chi-square test.
Table 2
Relationship between extracranial injuries, Marshall classification, midline deviation anisocoria and mortality.
Chi-square test.
# Likelihood ratio test.
J.R. Junior et al. / Journal of Clinical Neuroscience 42 (2017) 122128 125
Table 3
Relationship between Glasgow Coma Scale and Age on mortality.
t-Student test.
Bold values represent p < 0.05.
Table 4
Variables included in the model: adjusted weigh of each independent variable in the outcome.
OR IC 95% Coefficient p
Age (years) 1.03 1.021.03 0.03 0.0001
Glasgow Coma Scale (315) 0.81 0.770.84 0.2 0.0001
Marshall Scale 4, 5, 6 (0: no; 1: yes) 2.07 1.502.85 0.72 0.0001
Anysochoria (0: no; 1: yes) 1.79 1.172.72 0.58 0.006
of injury, patients comorbidities, pre-hospitalar assistance and 4.1. Glasgow Coma Scale
several others factors that should be analyzed jointly in a prognos-
tic model [68,11,13,1618]. Since the pioneering study of Jennett Glasgow Coma Scale (GCS) is applied to assess the clinical
et al. [12], for the prediction of functional outcome and mortality severity of intracranial injury [20]. The verification of GCS should
after severe TBI, manifold prognostic models have been developed. be performed in the first hour, usually after respiratory and hemo-
The main objective of these models is to afford an unbiased mea- dynamic stabilization, although, it could be confounded by medical
sure of the precocious individual outcome in the hospital admis- sedation, paralysis or intoxication [21]. In our study, GCS assess-
sion. Despite great prediction models (actually there are more ment was carried out after initial stabilization, in patients without
than one hundred prediction models for neurotrauma patients sedation. When sedation was necessary for transportation, the pre-
published in the literature) only few have been developed in large hospitalar team GCS scores were used for analysis. The average
groups of TBI [9]. The flaws of small samples studies are related to Glasgow Coma Scale of patients who die was statistically lower
poor statistical power what prevents accurate determination of than the patients who survived (p < 0.001). The 1-point decrease
outcomes. in Glasgow scale lead to a 19% increase in the chance of mortality
Recently, based on large and generalizable populations, the of the patient. Confirming our data there are many studies demon-
International Mission for Prognosis and Analysis of Clinical Trials strating a relation between low score on GCS and poorer outcomes
in TBI (IMPACT) [16] and the Medical Research Council Corticos- [21,22]. According to Narayan et al. the GCS score (the sum score
teroid Randomization After Significant Head Injury (CRASH) [19] and the motor component score) has been shown to have a signif-
study groups were included to formulate the prediction models, icant correlation with outcome following severe TBI. The predictive
which are currently used. value for poor outcome in patients with initial GCS 68 was 26%
In the IMPACT model, which lay emphasis on in severe TBI and for patients with GCS 53 was 77% [23]. Another study by Gale
patients, the data were collected from eight clinical trials and three et al. found that the mortality rate was 88% for those with a GCS
observational series. The Glasgow Coma Scale motor score, age and score of 35 [24].
pupillary reactivity were the best predictors of mortality and 6- One of the difficulties of GCS is the poor interobserver reliability
month outcome [16]. However, the patients monitored were from and imprecise assignment of score in prehospital and emergency
126 J.R. Junior et al. / Journal of Clinical Neuroscience 42 (2017) 122128
departments [7,25,26]. A simple measure of neurological examina- which is recognized as prognostic factors were inadequate
tion have been considered by some authors According to Healey markers of extracranial injuries. In this context, the Injury Severity
et al. the motor component (from Glasgow Coma Scale) preserves Score (ISS) is more appropriate for extracranial injury assessment
the predictive values of the complete GCS [26]. The simplified [35]. In our paper the presence of extracranial injury, not assessed
motor score (SMS) which is a three-point measure based upon by ISS, was associated with poorer outcome in patients with low
the GCS motor response have been studied also [27]. According Glasgow Coma Scale in the univariate analysis and the tomo-
to Caterino et al. SMS has the same predictive value for neurolog- graphic aspects were not significant in the first moment. This
ical outcomes as the entire GCS [25]. However, in a recent meta- adventitious association was observed only in patients with low
analysis that compared the complete GCS and simplified motor GCS, it was not proper to include in our prognostic model, since
score, it was observed that in the prediction of outcome both scales we have included patients with higher GCS also.
were similar. However, GCS better predicted the mortality [28]. In
our study, despite of criticisms related to interrater reliability we
do not consider entire GCS as a complex scale since it is used 4.4. Age
worldwide.
According to Chesnut et al., age is a stronger predictor of func-
4.2. Anisocoria tional outcome and mortality in TBI [30]. Many studies demon-
strated that older age is associated with poorer outcome and the
Usually pupillary diameter and reactivity is not influenced from threshold values varying between 30 and 60 years. The chance of
sedation or paralysis. It is well recognized that pupillary reactivity an adverse outcome increases with patient age in a stepwise man-
suggest brainstem lesion or compression and are related with ner, especially after the 60 years [7,17,18]. According to Ono et al.
adverse outcome [29]. In our series, the presence of anisocoria [14], the threshold of 40 years was used as distinction between
was related to 38% of mortality. According to Balestreri et al. poor and good outcomes when the intracranial injuries were sep-
patients who present with anisocoria have 67% higher chance of arated in epidural, subdural and parenchymal haematomas. One
mortality. The presence of anisocoria may be reliable to predict of the criticisms of this paper, made by the own authors, was the
mortality and the presence of intracranial lesion [22]. As demon- small sample size (272 patients). In the same way, in pediatric
strated by Chesnut et al. 43% of patients with pupillary asymme- patients (<15 years) with GCS = 3 and bilaterally fixed and dilated
try > 3 mm had intracranial mass lesions [30]. Recently Sobuwa pupils, the mortality is lower and functional outcome is better than
et al. developed a predictive model for severe TBI and pupil reactiv- adults with same neurological status [14]. Luerssen et al. [38] pub-
ity was independently significant predictor of outcome. In their lished a relevant study that compared the impact of age on patients
study, the odds ratio for good outcome in cases of bilateral pupil- with severe TBI and pediatric patients had lower mortality when
lary reactivity was 4.40 [31]. In a retrospective cohort of 24.115 compared to adults (28% versus 47%).
patients the best accuracy for outcome prediction was found for The observation that poorer survival was associated with
GCS motor component and pupil reactivity. When both (pupil reac- increasing age beyond a certain threshold has been published for
tivity and GCS motor component) were combined the predictive age cut off points of either 40 or 55 years, and requires further
accuracy of GCS alone was outmatched [32]. Majdan et al. observed interpretation [7]. Our results were quite different since our higher
the same results, in which 445 patients were analyzed and the GCS mortality occurred between 5059 years and after 80 years old.
motor score and pupillary reactivity obtained the best prognostic There were no positive linear correlation between age and mortal-
value to predict 6-month mortality in patients with severe TBI. In ity. However young people (<20 years), who suffered TBI, the mor-
pediatric patients, non-reactive pupils are also related to higher tality reached approximately 10%.
mortality but in lower percentage than adults [33]. In our study
the patients under 20 were not analyzed as a separate group.
The significance of extracranial injury in TBIs patients is contro- The association of gender and outcome is described in many
versial. There were studies which demonstrated that the presence studies, however there are discrepancies between them [7,19,39].
of major extracranial injuries was associated with poorer outcome, It should be observed that men are more likely to have severe
however in others, the outcome depends on the severity of the pri- TBI in road traffic accidents and assaults. Interestingly there is evi-
mary cerebral damage and is not worsened by the presence of dence that women who survived after severe TBI have poorer qual-
extracranial injuries [34,35]. According to Van Leeuwen et al. the ity of life and worse functional outcomes when compared with
prognostic effect of extracranial injury relates to brain injury sever- men [7]. Despite this, gender has not been well established as a
ity, and the larger effects are observed milder TBI patients [36]. prognostic factor [7,39]. In our series we did not find any associa-
Confirming this data in the POCON [37] study (507 patients), tion between sex and outcome (p = 0.65).
Lingsma et al. [38] demonstrated that extracranial injury did not
added prognostic value in the general patient population. Never-
theless, in patients with less severe intracranial injury (Marshall 4.6. Ethnics
CT Classification I or II or higher GCS), the extracranial injury adds
some prognostic value. So, in severe TBI patients the brain injury Ethnics were statistically associated with mortality, 26% of Cau-
itself was responsible for poor prognosis and in less severe TBI casian people died versus 16% of other ethnias (p = 0.03). It was not
the presence of extracranial injury was the fundamental cause of included in our prognostic model since is difficult to define what is
poor outcome [38]. This has been observed when patients classi- a particular ethnia in our series because of the mixed races
fied as Marshall 4, 5 or 6 were diagnosed with more spinal frac- observed. According to Sorani et al. [40] the ethnic origin has an
tures than patients classified as Marshall 2 or 3. In this situation association with outcome after TBI. They demonstrated that black
probably the mortality was related to the brain injury and the people have a worse outcome than Caucasian or Asian people. The
spinal fracture was not a protective factor. In a study that reasons for this relation can be speculative and may include access
enrolled 683 patients, hypotension and hypoxemia on admission to emergency and rehabilitation care.
J.R. Junior et al. / Journal of Clinical Neuroscience 42 (2017) 122128 127
One criticism of our series, which can be extended to IMPACT Disclosures of funding received
[16] and CRASH [19] models, is that secondary injuries (mainly rep-
resented by hypoxia, hyperglycemia, fever and coagulopathy) is None.
linked to worse outcome and has not been included in the analyi-
sis. On the other hand, treatments that are promptly implemented Acknowledgements
(represented as ICP monitoring, multimodal monitoring, surgical
intervention which includes also decompressive craniectomy) We would like to thank to all staff neurosurgeons from Hospital
have been associated with better outcome and lower mortality das Clnicas of University of Sao Paulo involved in the care of
[7]. It should be highlighted that the CRASH model overestimates patients.
mortality and poor outcome in patients who are submitted to neu-
romonitoring and management of elevated intracranial pressure
Appendix A. Supplementary data
after TBI. However, the CRASH prognostic model overrates the
probability of adverse outcome in patients who are submitted to
Supplementary data associated with this article can be found, in
decompressive craniectomy.
the online version, at http://dx.doi.org/10.1016/j.jocn.2017.03.012.
The application of models to earlier predicts individual outcome
and the use of prognostic models to define patient populations and
to compare different patient series should be distinguished. An References
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