Mild traumatic brain injury defined by Glasgow Coma Scale: Is it really mild?

http://informahealthcare.com/bij ISSN: 0269-9052 (print), 1362-301X (electronic) Brain Inj, Early Online: 1 6! 2014 Informa UK Ltd. DOI: 10.3109/02699052.2014.945959 ORIGINAL ARTICLE Mild traumatic brain injury defined by Glasgow Coma Scale: Is it really mild? Bellal Joseph, Viraj Pandit, Hassan Aziz, Narong Kulvatunyou, Bardiya Zangbar, Donald J. Green, Ansab Haider, Andrew Tang, Terence O Keeffe, Lynn Gries, Randall S. Friese, & Peter Rhee Division of Trauma, Critical Care, Emergency Surgery, and Burns, Department of Surgery, University of Arizona, Tucson, AZ, USA Abstract Introduction: Conventionally, a Glasgow Coma Scale (GCS) score of 13 15 defines mild traumatic brain injury (mtbi). The aim of this study was to identify the factors that predict progression on repeat head computed tomography (RHCT) and neurosurgical intervention (NSI) in patients categorized as mild TBI with intracranial injury (intracranial haemorrhage and/or skull fracture). Methods: This study performed a retrospective chart review of all patients with traumatic brain injury who presented to a level 1 trauma centre. Patients with blunt TBI, an intracranial injury and admission GCS of 13 15 without anti-platelet and anti-coagulation therapy were included. The outcome measures were: progression on RHCT and need for neurosurgical intervention (craniotomy and/or craniectomy). Results: A total of 1800 patients were reviewed, of which 876 patients were included. One hundred and fifteen (13.1%) patients had progression on RHCT scan. Progression on RHCT was 8-times more likely in patients with subdural haemorrhage 10 mm, 5-times more likely with epidural haemorrhage 10 mm and 3-times more likely with base deficit 4. Forty-seven patients underwent a neurosurgical intervention. Patients with displaced skull fracture were 10-times more likely and patients with base deficit 44 were 21-times more likely to have a neurosurgical intervention. Conclusion: In patients with intracranial injury, a mild GCS score (GCS 13 15) in patients with an intracranial injury does not preclude progression on repeat head CT and the need for a neurosurgical intervention. Base deficit greater than four and displaced skull fracture are the greatest predictors for neurosurgical intervention in patients with mild TBI and an intracranial injury. Introduction More than 1.5 million Americans suffer from traumatic brain injury (TBI) each year, of which 75% are categorized as mild TBI, having a Glasgow Coma Scale (GCS) of 13 15 on presentation [1, 2]. Although GCS is an important clinical tool which is routinely used for assessment and monitoring of TBI patients for clinical deterioration, categorization of patients as mild TBI based on GCS carries a low risk (1%) of life-threatening intracranial haemorrhage requiring an emergency neurosurgical intervention [3, 4]. The standard management plan for these patients consists of a neurosurgical consultation, period of observation or admission and repeat imaging [3, 5 7]. However, there is only a sub-set of patients that have radiographic progression on repeat head computed tomography (RHCT) or that benefit from an emergent neurosurgical intervention. Correspondence: Bellal Joseph, MD, University of Arizona, Department of Surgery, Division of Trauma, Critical Care, Burns, and Emergency Surgery, 1501 N. Campbell Ave, Room.5411, PO Box 245063, Tucson, AZ 85727, USA. Tel: 520-626-5056. Fax: 520-626-5016. E-mail: bjoseph@surgery.arizona.edu Keywords Glasgow Coma Scale, mild brain injury, outcome trauma, traumatic brain injury History Received 28 January 2014 Revised 30 April 2014 Accepted 15 July 2014 Published online 11 August 2014 Defining mild TBI based on GCS is misleading as it doesn t rule out serious intracranial injuries nor does it preclude the progression of the initial intra-cranial haemorrhage and the need for a neurosurgical intervention. The New Orleans study and the Canadian Computed Tomography (CT) head rule have demonstrated 100% sensitivity in identifying patients who require an initial head CT; however, both of these guidelines fail to predict the progression of the initial intra-cranial haemorrhage on the repeat head CT scan [8, 9]. A recent study from the National Trauma Data Bank (NTDB) showed older age, male gender, ethnicity and mechanism of injury are significant predictors for the need for neurosurgical procedures [10]. However, this study did not assess the combined effects of patient s history (intoxication (alcohol and drug), anti-platelet (aspirin or clopidogrel) and anticoagulation therapy (warfarin)), physiological parameters (systolic blood pressure, heart rate), laboratory data (platelet count, lactate, base deficit) and findings on the initial head CT scan for progression of the initial insult and need for neurosurgical intervention. Early recognition of high risk clinical factors may help to identify a sub-set of

2 B. Joseph et al. Brain Inj, Early Online: 1 6 patients who are likely to progress and require a neurosurgical intervention [6, 7]. The aim of this study was to identify factors that predict progression on repeat head computed tomography (RHCT) and neurosurgical intervention (NSI) in patients categorized as mild TBI with an intracranial injury (skull fracture and/or intracranial haemorrhage) on initial head computed tomography (CT) scan. Methods A 3-year (2009 2012) retrospective cohort analysis was performed of all patients with blunt traumatic brain injury who presented to a level 1 trauma centre. Patients with age 18 years, isolated TBI (head Abbreviated Injury Scale (AIS) score 3 and other body region AIS score53), GCS score of 13 15 on presentation (mild traumatic brain injury) and an intracranial injury (skull fracture or intracranial haemorrhage) on initial head CT scan and a routine repeat head CT scan were included. Patients on anti-platelet (aspirin or clopidogrel therapy) or anti-coagulation therapy (warfarin therapy), patients transferred from other institutions and patients that underwent emergent neurosurgical intervention were excluded from the study. This study excluded patients on anti-platelet or anti-coagulation therapy as the presence of these medications is known to be associated with worse outcomes after TBI. This study defined mild TBI (mtbi) as patients with a GCS score of 13 15 on presentation. Intra-cranial injury was defined as presence of skull fracture and/or intra-cranial haemorrhage. The patient s electronic medical records were reviewed and the following data points were collected: patient demographics including age, gender, race and ethnicity, mechanism of injury, vitals on presentation, which included systolic blood pressure (SBP), heart rate (HR), temperature (Temp) and Glasgow Coma Scale (GCS) score, laboratory data on presentation (complete blood count, serum lactate and base deficit), initial and repeat head CT scan findings, neurosurgical intervention, hospital and Intensive Care Unit (ICU) length of stay and in hospital mortality. The Abbreviated Injury Scale score (AIS) and the Injury Severity Score (ISS) were obtained from the trauma registry. These scores are well defined established markers for severity of injury. The higher the scores, the more severely injured the patient. While ISS score is the sum of the squares of the injured body regions (head, chest, thorax, abdomen or extremities), head-ais denotes the severity of head injury. These data points were reported as each of these parameters have been shown to affect outcomes in patient with TBI. Patients with low platelet count (5100 000 mm 3 ) are more likely to have progression on routine RHCT. Similarly, base deficit and lactate assess the perfusion of the individual which, when elevated, is known to be associated with mortality. The initial and repeat head CT scan (RHCT) were reviewed by a single investigator (trauma surgeon) for type of skull fracture and size and type of intra-cranial haemorrhage. The findings of repeat head CT scan were categorized as progressed or unchanged. Progression on RHCT was defined as development of a new intra-cranial haemorrhage or increase in the size of the initial haemorrhage. All patients underwent a routine RHCT within 6 hours of the initial head CT scan. The primary outcome measure was progression on RHCT. The secondary outcome measure was need for neurosurgical intervention. Neurosurgical intervention was defined as craniectomy or craniotomy. Data are reported as the mean ± standard deviation (SD) for continuous variables, median (range) for ordinal variables and the proportion for categorical variables. A Univariate analysis was performed to identify factors that predict progression on RHCT and the need for neurosurgical intervention. Factors with p 0.2 were selected for the multivariate logistic regression. A multivariate logistic regression was then performed to identity the strongest predictors of progression on RHCT and determine the need for neurosurgical intervention. Factor with p 0.05 in the multivariate regression model were considered significant. All statistical analyses were performed using Statistical Package for Social Sciences (SPSS, Version 20; SPSS, Inc., Chicago, IL). Results A total of 1800 patients with blunt TBI were identified, of which 876 patients met the inclusion criteria. The mean age was 54.3 ± 21.5 years, 65.5% (n ¼ 574) were male; median GCS score was 15 (range ¼ 13 15) and median head AIS was 2 (range ¼ 2 3). Table I demonstrates the demographics of the study population. Table II demonstrates the findings of the initial head CT scan in the study population. In total, 91.3% (n ¼ 800) patients had an intra-cranial haemorrhage (ICH) and 33.3% (n ¼ 292) patients had skull fractures; 66.7% (n ¼ 584) patients had isolated ICH and 8.4% (n ¼ 74) had isolated skull fracture. Subdural (n ¼ 359) followed by intra-parenchymal haemorrhage (n ¼ 299) were the most common type of ICH among the patients of the study population. Table I. Demographics and outcomes. Variables n ¼ 876 Age, y, (mean ± SD) 54.3 ± 21.5 Males, % (n) 65.5% (574) Whites, % (n) 83% (727) Injury type Falls, % (n) 42% (368) MVA, % (n) 30% (263) GCS, median [IQR] 15 [14 15] ISS, median [IQR] 15 [10 17] Head AIS, median [IQR] 2 [2 3] ED SBP (mean ± SD), mm of Hg 141.8 ± 25.1 ED HR (mean ± SD), min 1 88 ± 18.7 Haemoglobin (mean ± SD), g dl 1 13.5 ± 6.2 Platelet count 10 3 (mean ± SD) 182 ± 61 Lactate (mean ± SD) 2.2 ± 1.4 Base deficit 44, % (n) 4.1% (36) Hospital LOS, days (mean ± SD) 3.6 ± 4.6 ICU LOS, days (mean ± SD) 1.2 ± 2.2 Mortality, % (n) 8.2% (72) MVA, Motor Vehicle Accidents; GCS, Glasgow Coma Scale; ISS, Injury Severity Score; AIS, Abbreviated Injury Scale; ED, Emergency Department; SBP, Systolic Blood Pressure; HR, Heart Rate; LOS, Length of stay.

DOI: 10.3109/02699052.2014.945959 Mild traumatic brain injury 3 Table II. Findings on initial CT. n ¼ 876 Skull Fracture, % (n) 33.3% (292) Displaced, % (n) 16.3% (143) Intra-cranial haemorrhage 91.3% (800) SDH, % (n) 41% (359) SDH 10 mm, % (n) 15% (131) EDH, % (n) 6.7% (59) EDH 10 mm, % (n) 2.4% (21) SAH, % (n) 2.8% (25) IVH, % (n) 4% (35) IPH, % (n) 34.1% (299) Fx, Fracture; SDH, Subdural haematoma; EDH, Epidural haematoma; SAH, Subarachnoid haemorrhage; IVH, Intra-parenchymal haemorrhage; IVH, Intra-ventricular haemorrhage. Factors associated with progression on repeat head CT One hundred and fifteen (13.1%) patients had progression on RHCT. On Univariate analysis, age 65 years (p ¼ 0.07), loss of consciousness (p ¼ 0.2), displaced skull fracture (p ¼ 0.02), subdural haematoma 10 mm (p ¼ 0.004), epidural haematoma 10 mm (p ¼ 0.01), base deficit 4 (p ¼ 0.02), lactate 2.5 (p ¼ 0.18) and platelet count 5100 000 (p ¼ 0.04) were significant factors associated with progression on RHCT. After adjusting for factors in a multivariate logistic regression model, subdural haematomas 10 mm (p ¼ 0.007), epidural haematoma 10 mm (p ¼ 0.001) and base deficit 4 (p ¼ 0.01) were independent predictors for progression on RHCT in patients with mild TBI. Table III demonstrates the findings of the Univariate and multivariate regression analysis for progression on RHCT. Factors associated with neurosurgical intervention Forty-seven (5.4%) had a neurosurgical intervention, of which 49% (n ¼ 23) had a progression on RHCT. On Univariate analysis, male gender (p ¼ 0.19), loss of consciousness (p ¼ 0.19), displaced skull fracture (p ¼ 0.01), subdural haematoma 10 mm (p ¼ 0.001), epidural haematoma 10 mm (p ¼ 0.03), base deficit 4 (p50.001) and lactate 2.5 (p ¼ 0.12) were significant predictors for neurosurgical intervention. After adjusting for all confounding factors in a multivariate logistic regression model, base deficit 4 (p50.001), displaced skull fracture (p50.001), subdural haematomas 10 mm (p50.001) and epidural haematoma 10 mm (p ¼ 0.006) were independent predictors for neurosurgical intervention. Table IV demonstrates the findings of Univariate and multivariate regression analysis for factors associated with neurosurgical intervention. In total, 50.6% (n ¼ 443) had a GCS of 15, 29.7% (n ¼ 260) had a GCS of 13 and the remaining (n ¼ 173) had a GCS of 13 on admission. Figure 1 demonstrates the distribution of progression on RHCT and neurosurgical intervention rate after stratifying patients based on GCS. There was no difference in the proportion of patients that progressed on RHCT (p ¼ 0.23) and required neurosurgical intervention (p ¼ 0.12) after stratifying patients based on admission GCS. Table III. Univariate and multivariate analysis for progression on RHCT. Univariate analysis Multivariate analysis Variables p Value OR [95% CI] p Value OR [95% CI] Pre-injury parameters Age 65 years 0.07 1.5 [0.9 2.5] 0.3 1.4 [0.7 2.7] Male gender 0.8 1.1 [0.6 1.7] Intoxication 0.9 1.3 [0.3 4.7] Hypotension 0.35 1.3 [0.45 1.9] (SBP 90 mm Hg) LOC 0.2 1.2 [0.6 2] 0.8 1.1 [0.5 2] Mechanism of injury 0.5 1.1 [0.3 2.8] Heart rate 4100 min 1 0.7 1.1 [0.6 1.8] CT scan findings Displaced skull Fx 0.02 1.9 [1.1 3.3] 0.08 2.3 [0.9 3.5] SDH 410 mm 0.004 3.4 [1.5 8] 0.007 4.8 [1.9 9.6] EDH 410 mm 0.01 3.8 [ 1.2 7.6] 0.001 7.9 [2.4 12.6] Laboratory parameters Hgb 10 g dl 1 0.4 1.5 [0.76 3.1] Platelet 100 000 0.04 1.6 [1.1 3.9] 0.1 1.3 [0.98 3.6] Lactate 2.5 0.18 2.6 [1.2 5.5] 0.2 2.1 [0.89 2.5] Base deficit 44 0.02 3.1 [1.2 7.6] 0.01 2.8 [1.6 4.1] Fx, Fracture; SDH, Subdural haematoma; EDH, Epidural haematoma; RHCT, Repeat Head Computed Tomography; LOC, Loss of Consciousness; Hgb, Haemoglobin. Table IV. Univariate and multivariate analysis for neurosurgical intervention. Univariate analysis Multivariate analysis Variables p Value OR [95% CI] p Value OR [95% CI] Pre-injury parameters Age 65 years 0.3 1.08 [0.8 1.3] Male gender 0.19 1.2 [0.5 1.9] 0.1 1.6 [0.8 2.1] Intoxication 0.3 1.8 [0.9 3.4] Hypotension 0.35 1.3 [0.45 1.9] (SBP 90 mm Hg) LOC 0.19 1.4 [0.7 3.2] 0.3 1.2 [0.5 1.9] Mechanism of injury 0.34 1.2 [0.4 1.8] Heart Rate 4100 min 1 0.26 1.5 [0.9 2.8] CT scan findings Displaced skull Fx 0.01 16 [7.6 19.6] 50.001 10 [6.7 12] SDH 410 mm 0.001 3.9 [2.4 5.1] 50.001 3.4 [2.1 4.46] EDH 410 mm 0.03 4.8 [2.9 5.6] 0.006 3.5 [1.4 5.5] Laboratory parameters Hgb 10 g dl 1 0.51 1.2 [0.6 2.5] Platelet 100 000 0.031 2.5 [1.15 5.1] 0.09 1.6 [0.98 4.8] Lactate 2.5 0.12 3.6 [0.7 6.5] 0.21 1.9 [0.62 3.1] Base deficit 44 0.01 23 [1.4 31] 0.001 21 [1.6 27] Fx, Fracture; SDH, Subdural haematoma; EDH, Epidural haematoma; RHCT, Repeat Head Computed Tomography; LOC, Loss of Consciousness; Hgb, haemoglobin. The mean hospital length of stay was 3.6 ± 4.6 days and the mean ICU length of stay was 1.2 ± 2.2 days. The overall mortality rate was 8.2% (n ¼ 72). Discussion Historically, Glasgow coma scale (GCS) is the most often used system for grading severity of brain injury [3 10]. This study found that GCS score 13 15 does not preclude progression on repeat head CT and the need for a neurosurgical intervention in patients TBI and an intracranial injury. Base deficit 4 and extra-axial bleeds 10 mm were the only

4 B. Joseph et al. Brain Inj, Early Online: 1 6 Figure 1. GCS stratified progression on repeat head CT scan and neurosurgical intervention. 20% 18% 16% 14% 12% 10% 8% 6% 4% 2% 0% 11% Progression on RHCT p=0.23 4.00% 13.80% Neurosurgical Interven on p=0.12 6.10% 17.90% GCS 15 GCS 14 GCS 13 7.50% significant predictors for progression of initial intra-cranial haematoma and need for neurosurgical intervention in patients with mild TBI. In patients with TBI and an intracranial injury, Glasgow coma scale score should not be used as a criterion to define mild injury. The definition of mild TBI based on GCS is very convenient for hospital-based epidemiological studies. However, the large spectrum of clinical and radiological findings in patients with GCS 13 15 leads to poor specificity of this definition [11, 12]. GCS has been used to rapidly identify patients with TBI at triage [8, 9] but, sole reliance on GCS may result in under-triage of patients. It is understood that GCS is devised as a scale to assess the neurological conditions of the patient at any given point of time and its true value is in the repeated assessment of patients over time to assess any potential change, particularly deterioration; however, categorizing patients into mild category based on this scale needs further evaluation as these patients are likely to progress and require intervention. This study demonstrates the clinical and radiographical findings that predict both progression on RHCT and the need for neurosurgical intervention in patients with mild head injury. The result of this study identifies patient injury characteristics that can help risk stratification of patients, even with mild head injury. In this study, it was found that patients with mild head injury with base deficit of greater than 4 were 3-times more likely to have progression on RHCT and 21-times more likely to have a neurosurgical intervention. Siegel [13] found that base deficit had a variable significance in the prediction of oxygen requirement in patients with head trauma. Rixen et al. [14] concluded that base deficit is an early available important indicator to identify trauma patients with haemodynamic instability, high transfusion requirements, metabolic and coagulatory decompensation, as well as a high probability of death. It is believed that base deficit is an important clinical indicator for worse outcomes in patients with mild TBI and consideration should be made to routinely measure this marker on admission or even in pre-hospital setting. Presence of skull fracture and extra cerebral haematomas are known indicators for progression of initial insult in patients with traumatic brain injury [3, 4, 15, 16]. In this study it was found that patients with a subdural haemorrhage 10 mm, epidural haemorrhage 10 mm and displaced skull fracture were independent predictors for progression of initial intra-cranial haemorrhage in patients with mild head injury. The findings of this study are similar to Velmahos et al. [15], who demonstrated that patients with multiple findings on initial head CT were 11-times more likely to have worsening on a repeat head CT scan. Similarly, in another study, Mendelow et al. [16] demonstrated an association between skull fracture and progression of the intra-cranial injury. However, both these studies included patients on anti-platelet and anti-coagulation therapy which are known to be at a higher risk for progression of the initial intracranial injury. The incidence of neurosurgical intervention in mild TBI patients was 5.4% (n ¼ 47) and it was found that patients with a subdural haemorrhage 10 mm were 3.4-times and patients with epidural haemorrhage 10 mm were 3.5-times more likely to have a neurosurgical intervention. Mendelow et al. [16] concluded that 21% of the patients with mild TBI have a skull fracture with an underlying haematoma, prompting the need of neurosurgical intervention. Carlson et al. [17] reported that both epidural haematoma and subdural haematoma were found to be significantly associated with the need for surgery. This study questions the role of GCS as an indicator of mild head injury, given the high incidence of neurosurgical intervention in patients categorized as mild injury based on GCS score. Studies have linked male gender, age, mechanism of injury, loss of consciousness, pre-hospital anti-coagulation use for progression of initial intra-cranial haemorrhage and the need for neurosurgical intervention [10, 18 20]. Kisat et al. [10], in an analysis of the National Trauma Database (NTDB), showed male gender to be a predictor for the presence and progression of ICH in patients with mild head trauma. Velmahos et al. [15] showed that age 65 years was a predictor for progression on RHCT and also demonstrated that, of the seven patients with mild TBI that underwent surgical intervention, all but one were older than 70 years and three of them were on warfarin. The European Federation of Neurological Societies 2002 guidelines advocate a mandatory head CT in mild head injury patients with a dangerous mechanism [19]. This study did not find age, gender or mechanism of injury to predict the need for neurosurgical intervention. Additionally, it excluded patients on anticoagulation and anti-platelet therapy to select an homogenous

DOI: 10.3109/02699052.2014.945959 Mild traumatic brain injury 5 patient population, given the fact these patients are more likely to progression radiographical and require intervention [20 22]. From the data presented in this manuscript and also from previous work, it has been shown that all patients with mild TBI do not benefit from a routine RHCT and a neurosurgical consultation [3, 4]. This manuscript highlights a sub-set of patients with mild TBI and a positive head CT scan that would benefit from a RHCT scan and a neurosurgical consultation. It advocates the use of RHCT and neurosurgical consultation only in patients with a displaced skull fracture, extra axial bleed 10 mm or a base deficit 4. The findings of the paper should be interpreted keeping in mind its limitations. It is a retrospective data study from a single centre with a smaller number size. Second, this study did not assess for change in GCS score as a predictor for progression or neurosurgical intervention. Third, although all patients got a repeat head CT scan, this study did not have a protocol for when to do a RHCT. Fourth, this study did not assess the neurological examination in these patients at the time of progression or intervention. Despite these limitations, it is believed that the findings of this study stress upon the importance of CT scan findings and base deficit 4 in evaluation of patients with mild TBI with a positive head CT scan. The positive predictors in the study need further validation. However, it is believed that physicians must rely on their clinical intuition and knowledge to guide their decisions. Conclusion In patients with intra-cranial injury (skull fracture and intracranial haemorrhage) a mild GCS score (GCS 13 15) does not preclude the progression of the initial insult and the need for a neurosurgical intervention. Epidural and subdural haemorrhage greater than 10 mm are the strongest predictors for progression on repeat head CT. Base deficits greater than 4 and displaced skull fracture are the greatest predictors for neurosurgical intervention in patients with mild TBI and an intra-cranial injury. This study identifies patient injury characteristics that may warrant an early transfer to a level 1 trauma centre. Acknowledgements Poster Presentation at the Annual Trauma Association of Canada Scientific Conference, 11 13 April 2013, Whistler, British Columbia, Canada. Declaration of interest This study has not been supported by anyone. The authors have no financial or proprietary interest in the subject matter or materials discussed in the manuscript. References 1. Faul M, Xu L, Wald MM, Coronado VG. Traumatic brain injury in the United States: Emergency department visits, hospitalizations, and deaths. Atlanta, GA: Centers for Disease Control and Prevention, National Center for Injury Prevention and Control; 2010. 2. 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