Blast-Induced Traumatic Brain Injury: the Experience from a Level I Trauma Center in Southern Thailand

NEUROSURGICAL FOCUS Neurosurg Focus 45 (6):E7, 2018

Blast-induced traumatic brain injury: the experience from a level I trauma center in southern Thailand

Thara Tunthanathip, MD, Kanutpon Khocharoen, MD, and Nakornchai Phuenpathom, MD

Neurosurgical Unit, Department of Surgery, Faculty of Medicine, Prince of Songkla University, Hat Yai, Songkhla, Thailand

OBJECTIVE In the ongoing conflict in southern Thailand, the improvised explosive device (IED) has been a common cause of blast-induced traumatic brain injury (bTBI). The authors investigated the particular characteristics of bTBI and the factors associated with its clinical outcome. METHODS A retrospective cohort study was conducted on all patients who had sustained bTBI between 2009 and 2017. Collected data included clinical characteristics, intracranial injuries, and outcomes. Factors analysis was conducted using a forest plot. RESULTS During the study period, 70 patients met the inclusion criteria. Fifty individuals (71.4%) were military personnel. One-third of the patients (32.9%) suffered moderate to severe bTBI, and the rate of intracerebral injuries on brain CT was 65.7%. Coup contusion was the most common finding, and primary blast injury was the most common mechanism of blast injury. Seventeen individuals had an unfavorable outcome (Glasgow Outcome Scale score 1–3), and the overall mortality rate for bTBI was 11.4%. In the univariate analysis, factors associated with an unfavorable outcome were preoperative coagulopathy, midline shift of the brain ≥ 5 mm, basal cistern effacement, moderate to severe TBI, hypotension, fixed and dilated pupils, surgical site infection, hematocrit < 30% on admission, coup contusion, and subdural hematoma. In the multivariable analysis, midline shift ≥ 5 mm (OR 29.1, 95% CI 2.5–328.1) and coagulopathy (OR 28.7, 95% CI 4.5–180.3) were the only factors predicting a poor outcome of bTBI. CONCLUSIONS bTBIs range from mild to severe. Midline shift and coagulopathy are treatable factors associated with an unfavorable outcome. Hence, in cases of bTBI, reversing an abnormal coagulogram is required as soon as possible to improve clinical outcomes. The management of brain shift needs further study. https://thejns.org/doi/abs/10.3171/2018.8.FOCUS18311 KEYWORDS traumatic brain injury; blast injury; blast-induced traumatic brain injury; prognostic factors

rauma from war has been part of the human condi- resulting in a primary blast injury. Secondary blast in- tion since the beginning of civilization. In histori- juries are found in victims who are further away from cal conflicts, gunshot injuries were responsible for the center of detonation, often sustaining injuries from mostT of the damage. Currently, the improvised explosive penetrating flak. Victims can be thrown against a fixed device (IED) is the handmade weapon used to demoralize object, causing acceleration-deceleration injuries.3,9 Be- victims, even in the conflict in southern Thailand. As of cause explosive injuries are found in particular situations, 2018, this conflict has been ongoing in the southern border there are a few reports about common clinical character- provinces for more than 10 years (https://en.wikipedia.org/ istics of bTBI victims. wiki/South_Thailand_insurgency; Fig. 1).8,17 Blast injury About 80% of IED-induced injuries are fatal, and the has occurred most commonly during events such as strikes most commonly injured regions are the lower extremities on military convoys, attacks with mines, and IEDs con- (24.6%–28%), upper extremities (16%–24%), and head cealed in motorcycles. These handmade weapons cause (2%–34%). About 88% of the fatal cases involve bTBI.1,26 unique patterns of injuries, especially brain injuries.4 The clinical details and management of bTBI in war situ- The general mechanisms of blast-induced traumatic ations have been reported.1,12,26 However, our experience brain injury (bTBI) are an explosion that generates im- with civilian cases has revealed certain differences. There- mediate blast energy and a wave that impacts the head, fore, in this study, we aimed to explore the clinical infor-

ABBREVIATIONS bTBI = blast-induced traumatic brain injury; DCNS = damage control neurosurgery; GCS = Glasgow Coma Scale; GOS = Glasgow Outcome Scale; IED = improvised explosive device. SUBMITTED June 18, 2018. ACCEPTED August 29, 2018. INCLUDE WHEN CITING DOI: 10.3171/2018.8.FOCUS18311.

©AANS 2018, except where prohibited by US copyright law Neurosurg Focus Volume 45 • December 2018 1

Unauthenticated | Downloaded 10/05/21 12:06 PM UTC Tunthanathip et al.

FIG. 3. A 32-year-old military person with a secondary blast injury. Axial (A) and coronal (B) CT scans showed a bone fragment that penetrated into the deep parietal lobe. FIG. 1. Map showing the southern conflict region, composed of three southern border provinces (gray) and four districts of the Songkhla province. saturation < 92% or partial pressure of oxygen < 80 mm Hg.15,22,23 According to Wu et al. and clinical practice at mation associated with such cases, including the clinical our institute, coagulopathy was defined as thrombocyto- characteristics, intracranial injuries, treatment, and out- penia (platelet count < 100,000/μl) or elevated internation- comes of bTBI, and to analyze the factors associated with al normalized ratio > 1.2 or prolonged activated partial clinical outcomes. thromboplastin time > 40 seconds at admission.30 Surgical treatments and outcomes were reviewed from Methods computer-based medical records. Patients were divided This study was a retrospective review of patient re- into five groups according to their Glasgow Outcome cords from our institution’s trauma registry. We reviewed Scale (GOS) at the time of hospital discharge: 1 (death), 2 (persistent vegetative state), 3 (severe disability), 4 (moder- the medical records of blast injury patients who had been 10 admitted to Songklanagarind Hospital in the years 2009– ate disability), and 5 (good recovery). Finally, the GOS scores were dichotomized into favorable (GOS scores 4 2017. Data collected for analysis included demographics, 2,28 intracranial injuries, other associated injuries, treatment, and 5) and unfavorable (GOS scores 1–3) categories. and outcomes. Additionally, patients were divided into The study was performed with the approval of the Ethics three groups according to their initial Glasgow Coma Committee of the Faculty of Medicine, Songklanagarind Scale (GCS) score: mild TBI (GCS score 13–15), moder- Hospital, Prince of Songkla University. ate TBI (GCS score 9–12), and severe TBI (GCS score 3–8). Statistical Analysis Neuroimaging studies were reviewed to evaluate in- Patient characteristics, intracranial injuries, and treat- tracranial injuries. Following the definitions outlined by ments were analyzed using descriptive analysis and were Rosenfeld and colleagues, we categorized the intracra- presented as proportions or the means ± standard devia- nial injuries as primary, secondary, and tertiary blast ef- tion. Binary logistic regression was used to analyze corre- fects.20,21 Moreover, we also documented illustrative cases lation and magnitude of associations between several fac- demonstrating the mechanisms of bTBI (Figs. 2–4). tors and intracranial injuries. In the multivariable analysis, Anemia was defined as a hemoglobin level below 9 logistic regression was used to determine which variables g/dl at admission, and hypoxia was defined as oxygen were included in the model and stratification. We proposed

FIG. 2. A 29-year-old military person with a primary blast injury. A: Axial CT scan showed diffuse brain swelling with an obliterated basal cistern. B: Sagittal CT scan showed focal hemorrhages at the parasagittal white matter. C: Coronal CT scan showed mi- crohemorrhage at the gray and white matter located in both parasagittal areas. Acute subdural hematoma along the left convexity was observed.

2 Neurosurg Focus Volume 45 • December 2018

Unauthenticated | Downloaded 10/05/21 12:06 PM UTC Tunthanathip et al.

TABLE 1. Clinical characteristics of 70 patients with bTBI Factor No. (%) Age group in yrs <20 2 (2.9) 20–40 42 (60) 41–60 24 (34.3) >60 1 (1.4) Sex Male 64 (91.4) Female 6 (8.6) FIG. 4. A 27-year-old military person with a tertiary blast injury. A: Axial Military personnel CT scan showed a coup scalp hematoma at the impact site and contra- Military 50 (71.4) coup left temporal contusion. B: Coronal CT scan showed a compound depressed left parietal bone fracture at the impact site and contracoup Nonmilitary 20 (28.6) temporal contusion. Signs & symptoms Scalp injury 49 (70.0) Alteration of consciousness 20 (28.6) the odds ratio and 95% confidence interval of binary lo- Loss of consciousness 14 (20.0) gistic regression analysis by forest plot. A p value < 0.05 was considered statistically significant. Statistical analyses Hypotension 15 (21.4) were performed with the R program, version 3.4.1 (The R Bleeding per nose/ear 3 (4.3) Foundation). Headache 2 (2.9) Weakness 8 (11.4) Results Visual problem 8 (11.4) In the study period between 2009 and 2017, 70 patients Initial GCS score met the inclusion criteria. Table 1 shows the clinical char- 15–13 47 (67.1) acteristics of the study population. The mean age was 35 ± 12–9 7 (10.0) 10.8 years (range 19–61 years). More than 90% of the pa- 8–3 16 (22.9) tients were male, and more than two-thirds were military Pupil reactivity personnel. Secondary brain injuries, especially hypotension and hypoxia, accounted for 21.4% and 4.3% of all in- Both eyes reactive 58 (82.9) juries, respectively. Among the victims, 67.1% had a mild Unequal 7 (10.0) TBI and 22.9% had a severe TBI. Both eyes nonreactive 3 (4.3) Almost two-thirds (65.7%) of imaging studies revealed Laboratory significant intracranial injuries. The overall injury charac- Anemia 13 (18.6) teristics are shown in Table 2. The most common findings Coagulopathy 11 (15.7) were coup contusion (63.0%), subarachnoid hemorrhage (54.3%), and subdural hematoma (47.8%). According to the Hypoxia 3 (4.3) definitions of Rosenfeld and colleagues,20,21 the most com- Acidosis 4 (5.7) mon mechanism was primary blast injury (48.6%), while secondary blast injury was found in 37.1% of patients. The mean Injury Severity Score was 24.6 ± 11.4, and almost a quarter (24.3%) of the patients had an unfavor- more than two-thirds of the Abbreviated Injury Scale able outcome. Surgical site infection occurred in 5.7% of scores for the head were severe injury. The most common the patients and was significantly associated with an ex- associated injuries were orbit (28.6%), lower extremities ternally exposed scalp wound and retained foreign body (24.3%), and upper extremities (22.9%). Anemia and co- in penetrating injuries. agulopathy were observed on admission in about 18.6% Binary logistic regression was used to analyze factors and 15.7% of patients, respectively. Blood loss injuries predicting outcome. Glasgow Outcome Scale scores were significantly associated with anemia were basilar skull dichotomized into favorable and unfavorable categories fracture, coup contusion, and upper and lower extremity for binary analysis. In the univariate analysis, the signifi- trauma, whereas injuries associated with coagulopathy cant factors were preoperative coagulopathy, midline shift were basilar skull fracture, coup contusion, subarachnoid ≥ 5 mm, basal cistern effacement, moderate to severe TBI, hemorrhage, and retroperitoneal hematoma (p < 0.05, chi- hypotension, fixed and dilated pupils, surgical site infec- square test). tion, hematocrit < 30% on admission, coup contusion, and Table 3 shows the treatments and outcomes in this subdural hematoma. In the multivariable analysis, the only study. Surgical treatment was used in all severity levels factors associated with an unfavorable outcome were mid- of TBI, with the depressed skull fracture and coup contu- line shift ≥ 5 mm (OR 29.1, 95% CI 2.5–328.1) and coagu- sion significantly related to surgical treatment (p < 0.05, lopathy (OR 28.7, 95% CI 4.5–180.3). Figure 5 shows the chi-square test). The overall mortality rate was 11.4%, and odds ratios of factors as a forest plot.

Neurosurg Focus Volume 45 • December 2018 3

Unauthenticated | Downloaded 10/05/21 12:06 PM UTC Tunthanathip et al.

TABLE 2. Injury characteristics of patients with bTBI » CONTINUED FROM PREVIOUS COLUMN Factor No. TABLE 2. Injury characteristics of patients with bTBI Mean Injury Severity Score (SD) 24.6 (11.4) Factor No. Abbreviated Injury Scale score, head (%) Associated injury (%) (continued) 2 20 (28.6) Retroperitoneal 6 (8.6) 3 16 (22.9) Burn 5 (7.1) 4 24 (34.3) Mediastinum 4 (5.7) 5 10 (14.3) Thoracic spine 3 (4.3) Intracranial injury characteristic, n = 46 (%) Rib fracture 3 (4.3) Linear skull fracture 7 (15.2) Bowel perforation 3 (4.3) Depressed skull fracture 20 (43.5) Pelvis 2 (2.9) Basilar skull fracture 8 (17.4) Larynx/tracheal 2 (2.9) Epidural hematoma 10 (21.7) Liver 1 (1.4) Subdural hematoma 22 (47.8) Splenic 1 (1.4) Coup contusion 29 (63.0) SD = standard deviation. Contracoup contusion 2 (4.3) Brainstem injury 1 (2.2) Subarachnoid hemorrhage 25 (54.3) Discussion Intraventricular hemorrhage 1 (2.2) Explosive injuries occur in specific conditions such as Diffuse brain edema 7 (15.2) war, terrorist events, or conflicts. Injuries from IEDs in the Lateralization, n = 46 (%) conflict in southern Thailand have been common in recent 3 Bilat 8 (17.4) years because of the insurgency. In the present study, we Unilat 38 (82.6) found that bTBIs are serious and unique events. Mortality and morbidity in our study were lower than those reported Lt 15 (32.6) in previous papers1,9,20,31 because the fatal events were the Rt 23 (50.0) result of a civilian conflict in which victims injured by Location of major injury, n = 46 (%) an explosion were transferred to nearby hospitals where Frontal lobe 24 (52.2) medical devices and medications were suitable for initial Temporal lobe 12 (26.1) evaluation and resuscitation. Moreover, we found that the Parietal lobe 8 (17.4) factors associated with a poor outcome after treatment included subfalcine herniation > 5 mm and coagulopathy on Occipital lobe 5 (10.9 admission. Various other studies have found that midline Brainstem 1 (2.2) shift of the brain and basal cistern effacement are related Thalamus/hypothalamus 1 (2.2) to increased intracranial pressure and a worse progno- Other 1 (2.2) sis.2,9,19 We also found that patients with bTBI had a poor Mechanism of injury, n = 70 (%) Primary blast 34 (48.6) TABLE 3. Treatments and outcomes in 70 patients with bTBI Secondary blast 26 (37.1) Tertiary blast 10 (14.3) Factor No. (%) Pressure effect on CT, n = 70 (%) Treatment Basal cistern effacement 61 (87.1) Conservative treatment 42 (60.0) Midline shift Decompressive craniectomy 7 (10.0) <5 mm 64 (91.4) Craniotomy 18 (25.7) >5 mm 6 (8.6) Other 3 (4.3) Associated injury (%) GOS score at hospital discharge Orbit 20 (28.6) Death 8 (11.4) Lower extremities 17 (24.3) Vegetative status 4 (5.7) Upper extremities 16 (22.9) Severe disability 5 (7.1) Pneumothorax/hemothorax 15 (21.4) Moderate disability 5 (7.1) Maxillofacial 11 (15.7) Good recovery 48 (68.6) Tympanic membrane perforation 11 (15.7) GOS score at last follow-up Lumbar spine 10 (14.3) Vegetative status 2 (2.9) Cervical spine 7 (10.0) Moderate disability 4 (5.7) Good recovery 44 (62.9) CONTINUED IN NEXT COLUMN »

4 Neurosurg Focus Volume 45 • December 2018

Unauthenticated | Downloaded 10/05/21 12:06 PM UTC Tunthanathip et al.

FIG. 5. Forest plot of univariate and multivariable analysis of factors associated with an unfavorable outcome. BE = both eyes; Di = diameter; EDH = epidural hematoma; fx = fracture; MLS = midline shift; SDH = subdural hematoma; SSI = surgical site infection; TSAH = traumatic subarachnoid hemorrhage.

outcome when their injuries included midline shift of the a scalp laceration, and had a compound skull fracture on brain and/or basal cistern effacement.5,13,16 brain CT performed at the provincial hospital. Initially, he In our experience, patients injured by blast waves fre- underwent debridement and craniectomy by the neurosur- quently develop diffuse brain swelling and clinical brain geon at the provincial hospital. Then, he was transferred herniation. Moreover, extracranial injuries cause hem- to our hospital via ambulance to have the bone fragment orrhagic shock and hypoxia that precipitate more brain removed. In the mass casualty situation, bTBI patients did swelling and herniation. Damage control neurosurgery not need a life-saving operation, and they were transferred (DCNS) is urgent neurosurgery performed to treat ma- directly to our hospital via helicopter (Fig. 4). lignant brain edema or large intracranial hematomas in a Coagulopathy is a frequent event in traumatic injury remote, rural, or military situation.14,18,27,29 It includes rapid due to blood loss. The guideline for field management of surgery to stop major bleeding, evacuate hematomas, de- combat-related head trauma is the application of early de- compress brains with extensive craniectomy, and obtain tection and prevention of coagulopathy and hypotension watertight dural closures.7,19,20 In the combat field, DCNS in bTBI.12 In our experience, intraabdominal injury and can be immediately performed by a general physician to basilar skull fracture were common sources of bleeding improve survival in patients with GCS score 3–8 and posi- that should be concerning. Bleeding from a basilar skull tive signs of herniation after resuscitation; however, surgi- fracture influxed massively into the oropharynx, whereas cal outcome data remain limited. Few published papers intraabdominal bleeding will accumulate in the peritoneal have focused on the clinical outcomes of bTBI.12 cavity. The prevalence of coagulopathy is significantly In the differential situation, victims injured from an ex- higher in patients with TBI and is associated with a poor plosion in civilian cases were transferred from the event clinical outcome.6,11,24,25 field to the nearest hospitals. Patients were resuscitated, After injuries, various molecules and pathways such as and visualized sources of bleeding were immediately se- platelet-activating factors, tissue factors, microparticles, cured. Patients who suffered serious injuries were trans- and brain phospholipids are activated, causing a hypoco- ferred to provincial hospitals, which have a surgeon and agulable state.31 Also, coagulopathy should be reversed neurosurgeon. The bTBI patients underwent neuroimaging immediately with the transfusion of blood products such at provincial hospitals, and if clinical signs of brain hernia- as fresh frozen plasma, platelets, and cryoprecipitate to tion were observed, DCNS was performed in order to save improve clinical outcome. the patient’s life. Then, when their vital signs were stable, The present study may be limited by the size of the patients were transferred to our hospital via helicopter or sample, which resulted in a wide confidence interval. This ambulance. For example, the patient whose neuroimages paper presents initial research on the clinical outcomes of appear in Fig. 3 sustained a secondary blast injury, had patients with bTBI and the analysis of factors predicting

Neurosurg Focus Volume 45 • December 2018 5

Unauthenticated | Downloaded 10/05/21 12:06 PM UTC Tunthanathip et al. outcome according to our knowledge. Additional multi- explosive blast traumatic brain injury. Curr Neurol Neurosci variable analyses were used to control confounding fac- Rep 12:570–579, 2012 tors arising from limitations of our research methodology. 15. Manley G, Knudson MM, Morabito D, Damron S, Erickson V, Pitts L: Hypotension, hypoxia, and head injury: frequency, duration, and consequences. Arch Surg 136:1118–1123, 2001 Conclusions 16. Marshall LF, Toole BM, Bowers SA: The National Traumatic Coma Data Bank. Part 2: patients who talk and deteriorate: Blast injury causes TBI ranging from mild to severe. implications for treatment. J Neurosurg 59:285–288, 1983 Midline shift and coagulopathy are treatable factors as- 17. Nanuam W: Engagement of Malaysia and Indonesia on sociated with an unfavorable outcome. Hence, reversing Counterinsurgency in the South of Thailand. Honolulu: an abnormal coagulogram is required immediately to im- Asia Pacific Center for Security Studies, 2015 (http://apcss. prove outcomes, but the management of brain shift needs flywheelsites.com/wp-content/uploads/2015/08/AP-Wassana- further study. counterinsurgency-Aug2015.pdf) [Accessed October 4, 2018] 18. Risling M, Davidsson J: Experimental animal models for studies on the mechanisms of blast-induced neurotrauma. Front Neurol 3:30, 2012 References 19. Rosenfeld JV: Damage control neurosurgery. Injury 35:655– 660, 2004 1. Arul GS, Reynolds J, DiRusso S, Scott A, Bree S, Templeton 20. Rosenfeld JV: Neurosurgical injury related to terror, in P, et al: Paediatric admissions to the British military hospital Shapira SC, Hammond JS, Cole LA (eds): Essentials of at Camp Bastion, Afghanistan. Ann R Coll Surg Engl Terror Medicine. New York: Springer, 2009, pp 313–336 94:52–57, 2012 21. Rosenfeld JV, McFarlane AC, Bragge P, Armonda RA, 2. Brazinova A, Mauritz W, Leitgeb J, Wilbacher I, Majdan M, Grimes JB, Ling GS: Blast-related traumatic brain injury. Janciak I, et al: Outcomes of patients with severe traumatic Lancet Neurol 12:882–893, 2013 brain injury who have Glasgow Coma Scale scores of 3 or 22. Salim A, Hadjizacharia P, DuBose J, Brown C, Inaba K, 4 and are over 65 years old. J Neurotrauma 27:1549–1555, Chan L, et al: Role of anemia in traumatic brain injury. J Am 2010 Coll Surg 207:398–406, 2008 3. Cernak I: Blast-induced neurotrauma, in Winn HR (ed): 23. Samuel J, Franklin C: Hypoxemia, and hypoxia, in Myer Youmans Neurological Surgery, ed 7. Philadelphia: WB JA, Milikan KW, Saclarides TJ (eds): Common Surgical Saunders, 2017, Vol 4, pp 2934–2942 Diseases: An Algorithmic Approach to Problem Solving. 4. Chaiphrom N, Kanchanaroek K, Khumwattana M: New York: Springer, 2008, pp 391–394 Characteristics and distribution of blast and firearm injuries 24. Sun Y, Wang J, Wu X, Xi C, Gai Y, Liu H, et al: Validating in Thai military personnel during conflict in southern the incidence of coagulopathy and disseminated intravascular Thailand. J Med Assoc Thai 92 (Suppl 1):S47–S52, 2009 coagulation in patients with traumatic brain injury—analysis 5. Eisenberg HM, Gary HE Jr, Aldrich EF, Saydjari C, Turner of 242 cases. Br J Neurosurg 25:363–368, 2011 B, Foulkes MA, et al: Initial CT findings in 753 patients with 25. Talving P, Benfield R, Hadjizacharia P, Inaba K, Chan LS, severe head injury. A report from the NIH Traumatic Coma Demetriades D: Coagulopathy in severe traumatic brain Data Bank. J Neurosurg 73:688–698, 1990 injury: a prospective study. J Trauma 66:55–62, 2009 6. Franschman G, Boer C, Andriessen TM, van der Naalt 26. Thompson DC, Crooks RJ, Clasper JC, Lupu A, Stapley J, Horn J, Haitsma I, et al: Multicenter evaluation of the SA, Cloke DK: The pattern of paediatric blast injury in course of coagulopathy in patients with isolated traumatic Afghanistan. J R Army Med Corps [epub ahead of print], brain injury: relation to CT characteristics and outcome. J 2017 Neurotrauma 29:128–136, 2012 27. Toklu HZ, Yang Z, Oktay S, Sakarya Y, Kirichenko N, 7. Freeman JL, Winston KR, Byers JT, Beauchamp K: Damage- Matheny MK, et al: Overpressure blast injury-induced control neurosurgery: packing to halt relentless intracranial oxidative stress and neuroinflammation response in rat bleeding. J Trauma Acute Care Surg 79:865–869, 2015 frontal cortex and cerebellum. Behav Brain Res 340:14–22, 8. Funston J: Conflict in Southern Thailand: Causes, 2018 Agents and Trajectory. Carlton, Victoria: Melbourne 28. Tunthanathip T, Phuenpathom N: Impact of road traffic injury Law School, 2008 (https://www.webcitation.org/query. to pediatric traumatic brain injury in Southern Thailand. J php?url=http://www.law.unimelb.edu.au/files/dmfile/ Neurosci Rural Pract 8:601–608, 2017 funstonfinalforwebsite2.pdf) [Accessed October 4, 2018] 29. Wang JM, Chen J: Damage of vascular endothelial barrier 9. Gean AD (ed): Brain Injury: Applications from War and induced by explosive blast and its clinical significance. Chin Terrorism. Philadelphia: Lippincott Williams & Wilkins, J Traumatol 19:125–128, 2016 2014 30. Wu X, Du Z, Yu J, Sun Y, Pei B, Lu X, et al: Activity of 10. Jennett B, Bond M: Assessment of outcome after severe brain factor VII in patients with isolated blunt traumatic brain damage. Lancet 1:480–484, 1975 injury: association with coagulopathy and progressive 11. Kim YJ: A systematic review of factors contributing to hemorrhagic injury. J Trauma Acute Care Surg 76:114– outcomes in patients with traumatic brain injury. J Clin Nurs 120, 2014 20:1518–1532, 2011 31. Zhang J, Jiang R, Liu L, Watkins T, Zhang F, Dong 12. Knuth T, Letarte PB, Ling G, Moores LE, Rhee P, Tauber JF: Traumatic brain injury-associated coagulopathy. J D, et al: Guidelines for Field Management of Combat- Neurotrauma 29:2597–2605, 2012 Related Head Trauma. New York: Brain Trauma Foundation, 2005 (https://braintrauma.org/uploads/02/09/ btf_field_management_guidelines_2.pdf) [Accessed October 4, 2018] 13. Lipper MH, Kishore PR, Enas GG, Domingues da Silva AA, Choi SC, Becker DP: Computed tomography in the Disclosures prediction of outcome in head injury. AJR Am J Roentgenol The authors report no conflict of interest concerning the materi- 144:483–486, 1985 als or methods used in this study or the findings specified in this 14. Magnuson J, Leonessa F, Ling GS: Neuropathology of paper.

6 Neurosurg Focus Volume 45 • December 2018

Unauthenticated | Downloaded 10/05/21 12:06 PM UTC Tunthanathip et al.

Author Contributions Correspondence Conception and design: Tunthanathip. Acquisition of data: Tun- Thara Tunthanathip: Prince of Songkla University, Songkhla, thanathip, Khocharoen. Analysis and interpretation of data: Tun- Thailand. [email protected]. thanathip. Drafting the article: Tunthanathip. Critically revising the article: Tunthanathip. Reviewed submitted version of manuscript: Tunthanathip, Khocharoen. Approved the final version of the manuscript on behalf of all authors: Tunthanathip. Statistical analysis: Tunthanathip. Administrative/technical/material support: Tunthanathip, Khocharoen. Study supervision: Phuenpathom.

Neurosurg Focus Volume 45 • December 2018 7

Unauthenticated | Downloaded 10/05/21 12:06 PM UTC