Explosive Blast Neurotrauma

Geoffrey Ling,1,2 Faris Bandak,1,5 Rocco Armonda,2 Gerald Grant,3 and James Ecklund2,4

Abstract

Explosive blast traumatic brain injury (TBI) is one of the more serious wounds suffered by United States servicemembers injured in the current conflicts in Iraq and Afghanistan. Some military medical treatments for blast TBIthat have been introduced successfully in the war theater include decompressive craniectomy, cerebral angi-ography, transcranial Doppler, hypertonic resuscitation fluids, among others. Stateside neurosurgery, neuro-critical care, and rehabilitation for these patients have similarly progressed. With experience, military physicianshave been able to clinically describe blast TBI across the entire severity spectrum. One important clinical findingis that a significant number of severe blast TBI victims develop pseudoaneurysms and vasospasm, which canlead to delayed decompensation. Another is that mild blast TBI shares clinical features with post-traumatic stressdisorder (PTSD). Observations suggest that the mechanism by which explosive blast injures the central nervoussystem may be more complex than initially assumed. Rigorous study at the basic science and clinical levels,including detailed biomechanical analysis, is needed to improve understanding of this disease. A comprehensiveepidemiological study is also warranted to determine the prevalence of this disease and the factors that con-tribute most to the risk of developing it. Sadly, this military-specific disease has significant potential to become acivilian one as well.

Key words: clinical management of CNS injury; decompressive craniectomy; military injury; penetrating ballistic-like brain injury; traumatic brain injury

Introduction

Because of the ongoing Global War on Terror, thereare increasing numbers of patients afflicted with trau-

matic brain injury (TBI). Many of these patients are injured byan explosive blast (bTBI). From this mounting clinical expe-rience, bTBI is becoming recognized as a disease distinct frompenetrating TBI (pTBI) and closed head TBI (cTBI). In thisarticle the prevailing understanding of the basic mechanismsof injury and common approaches to clinical managementwill be presented.

In Operation Enduring Freedom in Afghanistan (OEF) andOperation Iraqi Freedom (OIF), explosive blast accounts forover 60% of combat casualties. For these wars, the most com-mon explosive weapon is an improvised explosive device orIED (Shanker, 2007). Historically, the head is frequently in-jured in battle, accounting for about 20% of all combat-relatedinjuries in past modern wars (Bellamy et al., 1986; Bellamy,1992; Carey, 1996; Carey et al., 1998). The epidemiological

data are still evolving for OIF and OEF. However, evidence todate from the Joint Theater Trauma Registry shows that injurypatterns from OIF and OEF are similar to those noted previ-ously (Shanker, 2007).

A distinct feature of OIF and OEF compared to wars of the20th century is the high survival of combat-injured warfigh-ters, even those who suffer TBI. An important contributor tothis survival is the use of body armor. In the past, the severityof bTBI was thought to be related to pTBI from fragments orcTBI from the head striking an object after the victim wasthrown (Bellamy, 1995; Carey, 1996). The modern combathelmet is preventing many fragments from causing pTBI. Italso affords some protection against impact, but may not beoptimized for this particular purpose. However, it is nowknown that bTBI can manifest at all severity levels, indepen-dent of a penetrating wound or being bodily thrown. Thus,unfortunately even this effective protective equipment can-not fully prevent all aspects of bTBI ( Jaffe, 2004; Shanker,2007).

1Department of Neurology, and 2Department of Surgery, F. Edward Hebert School of Medicine, Uniformed Services University of theHealth Sciences, Bethesda, Maryland.

3Department of Neurosurgery, Duke University Medical Center, Durham, North Carolina.4Department of Neuroscience, Inova Fairfax Hospital, Fairfax, Virginia.5Integrated Services Group, Inc., Potomac, Maryland.

JOURNAL OF NEUROTRAUMA 26:815–825 (June 2009)ª Mary Ann Liebert, Inc.DOI: 10.1089=neu.2007.0484

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Advances in military medical care have also contributed tothe lowest killed:wounded ratio (less than 1 in 10 patients die)in modern history. There have been a number of battlefieldand in-theater medical innovations. Important clinical im-provements used for treating TBI are early decompressivecraniectomy, neuro-critical care, cerebral angiography, tran-scranial Doppler, hypertonic saline, TBI clinical managementguidelines (battlefield and in-hospital), and others (Knuthet al., 2005; Ling and Ecklund, 2007; Ling et al., 2008). As aresult, morewarfighters are survivingwhat previouslywouldhave been fatal injuries. This growing number of veteranswith serious disabilities necessitates new opportunities foradvancing medical care (Zoroya, 2005).

Prevalence of Blast Traumatic Brain Injury

The lay press and other popular media outlets report theprevalence of bTBI as approaching 40–60% of deployed U.S.warfighters (Zoroya, 2005; Shanker, 2007; Zoroya, 2007a,2007b). A recent RAND report estimates that 320,000 servicemembers or 20% of the deployed force potentially suffer fromTBI (Tanielian and Jaycox, 2008). The supporting evidencefor these claims is limited. A comprehensive scientificallyrigorous epidemiological study of bTBI has not yet been done.Instead, the data used to support these assertions are fromextrapolations from limited sample sizes, self-reported data,single centers and=or narrow inclusion criteria (Okie, 2005;Zoroya, 2006; Hoge et al., 2008; Tanielian and Jaycox, 2008).Importantly, the relationship between bTBI and post-traumaticstress disorder (PTSD) is incompletely understood (Hoge et al.,2008). As these two separate and distinct diseases share com-mon clinical symptoms, which may affect accurate diagnosis,caution must be taken when trying to generalize such data.There are active efforts to elucidate the true epidemiology ofthis injury. Some of these efforts include the Joint TheaterTraumaRegistry, theDefense andVeterans Brain Injury Centerstudy, and a new comprehensive database effort supportedby the Hugh and Carolyn Shelton Military NeurotraumaFoundation.

Explosive Blast Traumatic Brain Injury,a New Type of TBI

TBI has classically been divided into two groups, pTBI andcTBI. Blast TBI shares clinical features of both pTBI and cTBI,but also has unique aspects.

In pTBI, a foreign object penetrates the bony skull and thentraverses through the brain parenchyma. This leads to phys-ical disruption of neurons, glia, and fiber tracts, all of whichare exacerbated by ischemia and hemorrhage. Clinically, pa-tients usually have an impaired level of consciousness withneurological deficits referable to parenchyma injured by theforeign body tract of travel. If the object enters at very highvelocity, the severity of clinical impairment may greatly ex-ceed what one would expect from the size of the object (e.g., arifle bullet). This is due to cavitation of brain tissue. Thecharacteristic surface lesion is a breach in the skull where theforeign body entered. There may also be another skull defectwhere the foreign body exited. CSF leaks and an extrudingbrain are often observed emerging from the defect. CT scanstypically reveal blood along the path of travel. Hemorrhage,cerebral edema, and macerated tissue are all hallmarks ofpTBI.

In cTBI, disruption of brain function can occur from brainmotion and deformation within the cranium, resulting in thetypically observed injuries to the brain parenchyma, bloodvessels, and fiber tracts (Bandak et al., 1996). A patient’sclinical presentation can be related to the severity of the me-chanical insult the brain experiences. Focal impactsmay resultin localized lesions and neurological deficits. The clinicalsyndrome worsens sub-acutely due to secondary injury pro-cesses of inflammation, ischemia, and free radical formation.

In bTBI, primary injury to the brain occurs when thephysical forces emanating from detonation couple to the headand brain. The exact forces that contribute to the injury are notfully understood, but pressure transient appears to play animportant but possibly not exclusive role. Furthermore, inbTBI the calvarium may or may not be breached, and thuspatients may have findings ascribable to cTBI, pTBI, or both.

There may be secondary, tertiary, and quaternary blasteffects that may also contribute to a patient’s particular pre-sentation. As described by the Centers for Disease Controland Prevention (CDC), primary blast injury is from physicalforces emanating from the explosive (Centers for DiseaseControl and Prevention, 2006). Secondary injury occurs frommatter thrown by the explosion, including fragments from theweapon casing and environmental debris. Tertiary injury re-sults when the patient is thrown by the explosive blast andstrikes an object such as a wall or the ground. Quaternaryinjury is from factors not included in the first three, such asburns or toxic fume inhalation.

Clinically, a patient’s condition may be as mild as a briefperiod of confusion to as severe as a coma. One apparentcharacteristic of severe bTBI is how commonly patients havediffuse cerebral edema and hyperemia. This develops rapidly,often within just an hour or so following blast injury. Thepresence of subarachnoid hemorrhage indicates amore severeinjury and often heralds acute severe brain edema and hy-peremia, and delayed vasospasm. This vasospasm is often thecause of delayed neurological deterioration (Armonda et al.,2006). This presentation seems to be more common followingblast than the other types of TBI, and has led military neu-rosurgeons to perform decompressive craniectomies moreoften than commonly done for pTBI or cTBI (Grant, 2007;Schlifka, 2007; Ling et al., 2008).

There is a challenge in confirming or refuting a uniquesignature clinical description for bTBI. It is difficult usingepidemiologic data alone to separate the less understood ex-plosive blast injury signs and symptoms from other betterunderstood components attributable to classic cTBI or pTBI.Further complicating this effort is that these patients fre-quently have other serious injuries beyond TBI (such astraumatic limb amputation and hemorrhagic shock) that re-quire aggressive resuscitation and other systemic therapies.The effects of such therapies on the clinical picture of bTBIneed clarification.

Mechanisms of Explosive Blast Traumatic Brain Injury

The precise causes and mechanisms of primary bTBI re-main unknown and the current understanding is incomplete.Specifically, the ‘‘cause’’ is the action generated by the ex-plosive blast, and the ‘‘mechanism’’ is the process by whichthe interaction of the explosive blast with the body producesinjury (i.e., the wounding process or how the body is injured).

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In trauma, there are primary and secondary injury mecha-nisms. Primary injury mechanisms are those which can beattributed directly to the cause (i.e., periorbital vascular dis-ruption from a blow to the eye). Secondary injurymechanismsconstitute the physiological response to the primary injury(i.e., the inflammatory swelling associated with the ‘‘blackeye’’). For bTBI, it is probable that more than one primaryinjury mechanism exists and that there are potentially severalcoupled mechanisms.

Blast produced by an explosive device is a transient pres-sure wave disturbance that travels through a medium like airor water. This is accomplished through detonation of an en-ergetic material such as a conventional explosive. An explo-sive is a material capable of storing high molecular bindingenergy in a relatively small volume, but has the importantcharacteristic of relative instability. Thus this quiescent storedchemical energy can be released very rapidlywhen a chemicalreaction is induced. This energy release leads to a phasechange that generates rapidly expanding gas. This in turntransfers mechanical, thermal, and electromagnetic energyinto the surrounding medium as well as into objects or peoplewithin the blast proximity. The extent and intensity of thisprocess depends on several factors such as charge size, che-mical composition, and confinement. This rapid, chemicallydriven process is referred to as a ‘‘detonation.’’

A critical aspect of a detonation is the rapid pressure wavesthat can travel faster than the characteristic wave speed of thehost medium, and therefore compress to become shockwaves. Figure 1 schematically shows a steepening pressurewave becoming a shockwave. For a typical explosion in a freefield environment (i.e., out in the open), the blast wave con-tains a shock wave, which is the leading element of thepressure disturbance. The shock wave is followed by pressuredecay with varying peak amplitudes as shown in Figure 2.The free field pressure-time relationship has been describedby Friedlander as an initial rapid rise in pressure, followed byslow decay which may rebound below the ambient pressureand produce a negative pressure phase, thereafter rising backto baseline (Baker, 1973). Figure 3 shows an idealized waveform with amplitudes of pressure at different times and dif-ferent points as the wave travels in the free field away fromthe point of detonation.

An explosive blast wave induces localized particle motionin the medium it is passing through. Any object, such as the

head, in the path of a blast wave will experience forces thatwill move it and deform it. Given the short duration of anexplosive blast shock wave, the force effects on the head willbe relatively localized and the deformation non-uniform. Therapid time onset of the shock as well as associated pressuregradients are likely to be a cause of brain injury. The magni-tude of these effects will vary at different points along andwithin the head.

The non-free field or enclosed condition (i.e., inside astructure) is more complex. In an enclosure, blast pressurewaves reflect off walls, ceilings, barriers, and other objects,creating a ‘‘complex wave field.’’ Under such conditions, eachexplosive blast must be analyzed on an individual basis andcannot be generalized by a single relation as was done byFriedlander for the free field example. For a complex blastwave, the contributions from the shape and the peak of theinitial blast wave as well as each reflected wave need to beaccounted for spatially and temporally in the assessment ofinjury.

The assumption that the cause of bTBI is dependent only onpeak pressure and not the shock wave may not be valid. Thisoriginal assumption is based on the work of Bowen andRichmond, who described a relationship between peak pres-sure and lethality in a sheep model (Bowen et al., 1968;Richmond et al., 1968). The impression is that high pressureslead to air-filled organ failure (i.e., lung and bowel) (Phillipsand Richmond, 1991). If the lung is themost susceptible organthen a high prevalence of blast lung injury is to be expected.However, the OIF and OEF clinical experience reveals thatblast lung injury occurs infrequently. Acute respiratory dis-tress syndrome (ARDS) is reported, but only in conjunctionwith other severe injuries such as traumatic amputation andmassive hemorrhagic shock. ARDS is rarely, if ever, seen inisolation (Holcomb, 2005). The bowel has not been found to beinjured by explosive blast unless there is shrapnel penetration.In contrast, bTBI is much more common. The brain is not anair-filled organ and so other mechanisms such as those fromshock wave effects must be responsible. Brain injury was notstudied in the earlier studies (Bowen et al., 1968; Richmondet al., 1968). One consideration is that the interceptor bodyarmor vest may be protecting the lungs and bowel from blastforces. Another possibility is that other physical forces maycontribute or play a more prominent role in explosive blastinjury.

FIG. 1. Schematic of the steepening process that a pressure wave front experiences in the formation of a shock wave. Theshock wave represents a very rapid and steep rise in the pressure and can be a direct mechanism of injury in the brainexposed to blast.

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An explosive detonation produces effects other than justpressure waves. Conventional military ordnance also releaseslight, acoustic, thermal, and electromagnetic energies, some ofwhich can be injurious to the CNS. In addition, there are toxicfumes. The relative contribution of each of these forces to bTBIis uncertain. The evidence is lacking for including or exclud-ing them as potential causes of bTBI.

Categories of Severity for bTBI

Blast TBI is presently categorized similarly as TBI from cTBIand pTBI. Military providers use the same criteria as theircivilian counterparts. The TBI definition from the Mild Trau-matic Brain Injury Committee of the American Congress ofRehabilitation Medicine (1993) applies to bTBI when explo-sive blast is the etiology of loss of consciousness, loss ofmemory preceding or following injury (amnesia), alteration inmental status at the time of injury, and=or focal neurologicaldeficit. The level of bTBI severity is based mainly on the du-ration of altered mental status. Mild bTBI is associated withbrief (<5min) loss of consciousness or awareness. As in classiccTBI,mild bTBI can lead to headache, confusion, and amnesia,as well as other symptoms such as difficulty concentrating,mood alteration, sleep disturbance, and anxiety. After injury,these symptoms often resolve within a few hours or days.Very troubling to patients is post-concussive syndrome,which may develop up to days later (Ling and Maher, 2006).

A joint Veterans Administration and Department of Defensecommittee is developing guidelines for management of thiscondition. In general, this syndrome usually responds to re-assurance and specific symptomatic treatment such as non-narcotic analgesics, anti-migraine medication for headache,and antidepressants. As with civilian cTBI, it may last only afew weeks, but in some cases can persist for up to a year ormore ( Jarrell and Ecklund, 2003; Ryan and Warden, 2003;Ling and Maher, 2006).

Again using civilian criteria, moderate bTBI is associatedwith a presenting Glasgow Coma Scale (GCS) score of 9–13,often with prolonged loss of consciousness and=or neuro-logical deficit (Geocadin, 2004). Combat-injured patientssuffering frommoderate bTBI will require prompt evacuationto an echelon 3medical treatment facility (i.e., combat supporthospital), and may require neurosurgical care. They too maydevelop post-concussive syndrome ( Jarrell and Ecklund,2003; Ling and Maher, 2006; Ling et al., 2008).

Severe bTBI occurs when the injury causes the patient to beobtunded or comatose (i.e., presenting with a GCS score of 8or less). Such injury is typically associated with significantneurological injury, often with abnormal neuroimaging (e.g.,head CT scan revealing skull fracture, intracranial hemor-rhage, and early diffuse cerebral edema). These patients re-quire advanced medical care while still on the battlefield. The‘‘Guidelines for Field Management of Combat-Related HeadTrauma’’ is an effort to optimize far-forward medical care of

FIG. 2. Pressure-time history for a free field explosive blast showing the steep pressure rise of the shock wave followed by apositive pressure phase and a negative pressure phase.

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TBI (Knuth et al., 2005). After initial stabilization, these pa-tients must be evacuated to the nearest combat support hos-pital that has neurosurgical capability. Such patients will mostlikely need airway protection, mechanical ventilation, neu-rosurgical intervention, intracranial pressure monitoring, andneuro-critical care in an intensive care unit setting. Recoveryis prolonged and usually incomplete if at all. Based on thecivilian TBI experience, it is expected that a significant per-centage of severe bTBI patients will not survive to 1 year post-injury (Geocadin, 2004; Ling et al., 2008; Multi-Society TaskForce on PVS, 1994a, 1994b).

Explosive blast TBI can also lead to concussion. bTBI con-cussion is considered by some investigators as a subtype ofcTBI (Warden, 2006). It too can be classified as mild (grade 1),moderate (grade 2), or severe (grade 3), using the same criteriaestablished for civilian concussion. Mild concussion is definedas brief confusion lasting less than 15min, but with no loss ofconsciousness. At the moderate level, confusion lasts longerthan 15min, but consciousness is maintained. Severe con-cussion is whenever there is any loss of consciousness.

Recognizing that applying criteria developed for classiccivilian TBImay be inappropriate, a new classification specificfor bTBI is being proposed (Okie, 2005; Warden and French,2005). Mild bTBI is defined as loss of consciousness <1 h andpost-traumatic amnesia <24 h after exposure to an explosiveblast. Moderate bTBI is loss of consciousness for >1 but lessthan 24 h and amnesia lasting >1 but <7 days. Severe bTBI isloss of consciousness >24 h and amnesia >7 days. It needs tobe emphasized that this classification is a proposal and has notyet gained wide acceptance in the medical community.

Post-traumatic Stress Disorder and Blast TraumaticBrain Injury

PTSD is a well-defined clinical syndrome. According to theDiagnostic and Statistical Manual of Mental Disorders, FourthEdition, Text Revision (2000), patients who experience eventsthat threatened life or health and feel intense fear or help-lessness may develop this disease. The disease is manifestedas re-experiencing the traumatic event, avoidance of stimuli

associated with the event, and a number of other symptoms.These symptoms include difficulty concentrating, sleep dis-turbance, bursts of anger, irritability, hypervigilance, and in-creased startle response, all of which interfere with thepatient’s ability to lead a normal life. Mild bTBI shares manyof these clinical features, such as difficulty concentrating,sleep disturbance, and mood alteration, but there are somedifferences. For example, headache is probablymore commonin TBI, whereas hypervigilance and increased startle are moreoften associated with PTSD.

PTSD and bTBI can occur in the same individual (Wardenet al., 1997; Ropper and Gorson, 2007; Hoge et al., 2008). Thisis not surprising given the inherently violent nature of anexplosive blast. Because of the similarities between these twodiseases, there is the potential for misdiagnosis. Soldiers whoare outside the blast zone may suffer psychological injury.This is due both to the personal experience of being close tothe explosion, andwitnessing severe injury inflicted on fellowsoldiers. The result may be PTSD symptoms misattributed tobTBI (Hoge et al., 2008). The converse can also be true. Asoldier may be within the blast zone and suffer a cTBI form ofbTBI. In the absence of overt physical signs, the woundedsoldier may be misdiagnosed as having PTSD. In eithercase, the consequences can be tragic, as the misdiagnosedpatient will receive the wrong types of therapy. Thus extremecare must be taken to ensure that the proper diagnosis isrendered.

Clinical Management

Clinical care for TBI begins on the battlefield and is carriedout in accordance with the ‘‘Guidelines for Field Managementof Combat-Related Head Trauma’’ (Knuth et al., 2005). Thecombat medic’s first responsibility is to protect the patientfrom further harm. After this, the ABCs of airway, breathing,and circulation are attended to. During this initial stabiliza-tion, the patient’s GCS score should be determined. The GCSscore can be helpful in making triage decisions, especially inisolated head injury. If the GCS score is low, the patientshould be evacuated to higher echelons of care. If GCS score is

FIG. 3. Idealized shock wave pressure and magnitude decay at several time points after explosion as the shock wave travelsaway from the source.

EXPLOSIVE BLAST NEUROTRAUMA 819

13 or less, this should be done by helicopter or in anotherexpeditious manner. Typically, IED blast injuries result inmultiple injuries to the same patient, all requiring simulta-neous management.

Once at the combat support hospital, a more detailedclinical assessment should be made. Neuroimaging with CTshould be done as soon as possible to identify lesions such asintracranial hemorrhage, skull fracture, or cerebral edema. Itis crucial that such conditions are diagnosed so that earlyneurosurgical intervention can be rendered. Military TBI pa-tients receive the same standard of care in a combat sup-port hospital as they would in a civilian hospital (The BrainTrauma Foundation, 2007). Important issues to attend to in-clude maintaining adequate oxygenation, controlling intra-cranial pressure (ICP), and ensuring proper cerebral perfusionpressure. Intracranial hypertension is common in severe bTBI.One frequent observation among operating neurosurgeons isthe presence of hyperemia and severe edema in the acuteperiod (Fig. 4A). This tends to occur more frequently when atraumatic subarachnoid hemorrhage is noted on CT (Fig. 4B).The presence of blood in the basilar cisterns may be onemarker for higher severity of blast injury. Patients have alsobeen noted to develop delayed increased ICP, sometimes 14–21 days after severe bTBI. This phenomenonmay be related toother insults such as vasospasm (Armonda et al., 2006). Onemedical therapy that has been usedwith great success in thesetypes of injuries is hypertonic saline (Ling andMarshall, 2008;Ling et al., 2008). Intravenous boluses of 23% NaCl can beused for acute elevations of ICP with continuous IV infusionsof 2% and 3%NaCl solutions tomaintain ICP control (Qureshiand Suarez, 2000; Geocadin, 2004). The benefit of hypertonicsaline solutions is that serum osmolality may be increasedwithout compromising intravascular volume. This is critical,as severely injured warfighters are often suffering fromhemorrhagic shock. Other therapies that have been promisingin mitigating delayed intracranial hypertension are mild hy-pothermia (34–368C) and early decompressive craniectomy(Ling et al., 2008). Presently, factor VIIa is not used to treatintracranial hemorrhage. However, some TBI patients mayreceive factor VIIa for the clinical indication of systemichemorrhage (Holcomb, 2005).

Decompressive craniectomy is commonly used in severebTBI patients (Okie, 2005; Grant, 2007; Schlifka, 2007; Linget al., 2008). A decompressive craniectomy permits theswelling brain to avoid compression by the skull andmay alsoprovide local brain cooling. From a practical military stand-point, craniectomy provides an additional measure of safetyfor ICP control during the evacuation process where, at times,ICP management can be challenging. The other benefit ofearly decompressive craniectomy is that it may obviate theneed to usemore conventional methods of ICP control such aspharmacological coma. Barbiturate coma is difficult to exe-cute in the deployed setting due to the limited number ofneuro-critical-care specialists and lack of EEG support. Thusfor many reasons, decompressive craniectomy is the mostpractical, if seemingly aggressive, approach. Cranioplasty isdelayed for at least 3months from the time of the patient’s lastinfection. The availability of computer-generated cranial flapsmade from methyl methacrylate has improved cosmetic re-sults, shortened operative times, and reduced the need forsubcutaneous placement of the bone flap with its attendantrisks (Fig. 5A and 5B).

IED blast injuries are complex. There are frequently asso-ciated injuries, including traumatically amputated limbs,multiple penetrating wounds, and severe hemorrhage. Man-agement is multidisciplinary and rapid with several sub-specialists treating the patient simultaneously under thedirection and coordination of a trauma surgeon. There is oftenextensive soft-tissue loss from the blast with possible severefacial and scalp burns (Fig. 6). The helmet provides excellentprotection so penetrating objects usually enter through theface, orbit, or skull base (i.e., areas not covered by the helmet).Prevention of CSF leakage and good tissue coverage are ofparamount importance. When the helmet stops a fragment,

FIG. 4. This patient was exposed to a close-range IED blastwhile riding in an open vehicle approximately 2 h prior tothis intraoperative photo. (A) Photo taken after a decom-pressive craniectomy and dural opening that reveals the se-vere brain hyperemia and edema often associated with theseinjuries. (B) Photo of CT image from the same patient,showing traumatic subarachnoid hemorrhage in the basilarcisterns.

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there can also be an associated cTBI ranging from mild con-cussion to severe contusions and skull fractures from the re-sulting helmet deformation (Fig. 7A and 7B).

The kinetic energy imparted by a penetrating projectile andthe location of the injury tract are important. Low-velocityprojectiles may penetrate the skull but cause little underlying

parenchymal damage (Fig. 8), whereas high-velocity projectilescan cause massive tissue damage from a large secondary cav-ity. The cavity creates large volumes that can be of such pres-sure that skull fracture occurs with fragments expanding in anoutward displacement fashion. Fragments from explosionstravel at low velocity and thus do not result in significantcavitation. The decisions with regard to removal of shrapneldebris or bone fragments lodged in the brain have evolvedsince the Vietnam and Korea Wars. Previously, surgeons ag-gressively sought to remove all foreign bodies including bonefragments in an effort to reduce infection risk and risk of de-veloping post-traumatic epilepsy. Longitudinal studies oftreated Vietnam War patients and other more recent studiesfrom other conflicts have shown that aggressive removal of allfragments is unnecessary, but removal of gross contaminationwithdebridement of large injury tracts is beneficial (Carey et al.,1970; Carey et al., 1972; Carey et al., 1974; Carey et al., 1974;Carey, 1987; Carey et al., 1998). Currently, any accessiblefragments are removed if they can be safely debrided along thetract, but fragments that may be deep or subcortical, contra-lateral, or otherwise inaccessible are left in place (Grant, 2007;Schlifka, 2007; Ling et al., 2008). The reconstruction of the duraand scalp closure are important to reduce the incidence of CSFleakage and meningitis. A soldier who presents with a goodneurological status, no significant mass effect, and small pen-etrating fragments in the brainwill likely get local debridementand scalp closurewith an emphasis on preventingCSF leakage.On the contrary, a soldier who presents with significant tissuedestruction, mass effect, and=or an extensive wound tract withlarge penetrating fragments will likely undergo a large de-compressive craniectomy, debridement of the tract, and re-moval of the fragments (Carey et al., 1972; Carey et al., 1998;Grant, 2007; Schlifka, 2007).

If bodily thrown by the explosion, the patient’s head canstrike a solid object resulting in tertiary blast injury. As a re-sult, there can be skull base injuries to the middle fossa,temporal bone, or frontal sinus, which should be suspectedif patients have otorrhea or rhinorrhea. There is also a

FIG. 5. (A) Photo of a computer-generated cranioplastyflap produced from a cranial model based on a patient’s CTscan. (B) Intraoperative photo showing the same flap beingimplanted in a patient several months after his decom-pressive craniectomy performed in-theater after a blast in-jury. Note the excellent fit despite the complex orbital andzygomatic arch involvement. The frequency of transfacialand orbital wounds leads to complex reconstructive re-quirements that are well served by this computer-generatedtechnique.

FIG. 6. This is the presenting injury of the patient describedin Figure 4. Note the extensive soft-tissue loss and orbitalinvolvement.

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heightened concern for Acinetobacter and other infections,many of which are prevalent in Iraq and are often drug-resistant. Due to the high incidence of concomitant skull basetrauma and CSF leaks following blast injuries, patients may

have complex Le Fort fractures, as well as a ventriculostomy,lumbar drain, or both in place. Early maxillofacial fixation isperformed, even in the setting of a head injury. The com-pounded morbidity of drug-resistant Acinetobacter baumanniimeningitis with external drains in place is much greater thanthat of early surgical intervention. Anecdotal reports suggestthat early reduction of facial fractures has been effective inminimizing CSF leaks.

Finally, there can be critical vascular effects on both arteriesand veins, such as sagittal sinus injury and lacerated corticalarteries. Blast injuries appear to have a high risk for traumaticpseudoaneurysm formation. Our recent work revealed a 35%incidence of pseudoaneurysms in 47 blast-injured patientswho underwent cerebral angiography at the National NavalMedical Center during the first 2 years of OIF (Armonda et al.,2006). Patients who underwent angiography were those whosustained an injury tract near a vascular territory or had anunexplained decompensation in neurological status or ICUmonitoring indicators. Blast-related pseudoaneurysms havebeen observed to expand and rupture, and require treatmentby appropriate endovascular or open surgical techniques.

Vasospasm is a particularly common finding after bTBI.Our study revealed that 47% of the patients who underwentangiography developed cerebral vasospasm (Armonda et al.,2006). Early transcranial Doppler studies in-theater demon-strate that this vasospasm can develop early, often within 48 hof injury. Not surprisingly, this occurs with moderate andsevere bTBI, and is worse with higher injury severity (Lingand Ecklund, 2007). Vasospasm can also present later in thecourse of this disease, typically 10 or more days after initialinjury, and does appear to be more prevalent when traumaticsubarachnoid hemorrhage is also present acutely.

Many moderate and severe bTBI victims arrive intubatedand medicated from the field and have severe facial traumathat prevents a reliable neurological examination, especiallyof pupillary reaction. CT can reveal tight basilar cisterns andpoor sulcal definition indicative of diffuse edema, withoutany apparent penetrating brain fragments or intracranial

FIG. 7. Fractures and brain contusions can be seen evenwhen the helmet provides protection from projectile pene-tration into the brain. (A) CT scan showing a small contusionin a patient who presented with a grade 3 concussion after agunshot wound to the helmet. (B) This image reveals a largercontusion and depressed fracture in a patient whose helmetdeflected a fragment from an IED.

FIG. 8. In addition to their munition casings, blasts canenergize surrounding objects, which in turn act as projectiles.This figure shows a rock that was propelled by an IED andlodged in a patient’s skull. Surgical exploration revealed adural laceration with minimal underlying parenchymaldamage.

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hemorrhage (Fig. 9). Difficult triage decisions in such situa-tions can be aided by adjunctive tools such as transcranialDoppler. For example, flow reversal in all insonated vesselsprovides supportive evidence that aggressive care is futileand inappropriate in this environment. Conversely, normali-zation of flow with early interventions such as placement ofan external ventricular drainage device may indicate thatsurgical or aggressive medical intervention is warranted.

It must be recognized that wartime clinical decisionmakingcan be challenging. Triage is especially difficult for medicalproviders who are used to caring for patients in medical cen-ters in the U.S., where there are adequate resources, man-power, and other hospitals nearby. In a war environment,decisions have to be made based on the existing realities.Some of these are the expectation that several severely injuredpatients will arrive simultaneously, the number of providersare few, critical resources such as operating rooms, CT scan-ners, and blood products, are limited, and evacuation assetsmay be unavailable. The goal of proper triage is to use thelimited resources to help the largest number of patients (Pesiket al., 2001).

Blast Concussive Injury

Diagnosis of concussion or mild TBI is particularly vexing.It is critical to recognize early that a warfighter has suffered aconcussion. This is so that patients who are diagnosed canreceive appropriate medical care, and more importantly, so

that they do not return to duty with compromised mentalstatus, which at times can be quite subtle. In the war theater,the first providers are generally medics, who typically do nothave sufficient training in recognizing the subtleties of mildTBI. This is exacerbated by the lack of overt evidence oftrauma (e.g., lacerations or hematoma). The patient may notrecognize that she or he has suffered an injury. Some patientswill knowingly try to hide their injury so that they can remainwith their unit (Zoroya, 2007a, 2007b). Thus, for medics andother medical providers, there needs to be increased suspicionthat bTBI may have occurred in any warfighter who has beenexposed to an explosive blast so that an appropriate clinicalwork-up can be initiated. If necessary, the patient should bereferred to higher echelons of care, ideally to a neurologist,neurosurgeon, or emergency medicine physician (Ling andMaher, 2006; Warden, 2006).

After their first blast exposure, many soldiers do not rec-ognize that they may have been injured and thus will not seekmedical care. It may take two or more blast exposures beforethey realize that they may have been injured. The first indi-cation of injury may be persistent post-concussive symptoms,such as headaches, vertigo, short-term memory loss, anddifficulty concentrating or multi-tasking (Ryan and Warden,2003; Okie, 2005; Ropper and Gorson, 2007). As these symp-toms can be subtle, these patients should undergo a detailedmental status evaluation by a physician or psychologist. Partof this evaluation should be objective neuropsychologicaltesting, even though it may consist only of limited bedsidetesting. There are efforts underway to develop neuropsy-chological tests that can be automated on a laptop computeror are easy enough for use by less-trained providers (Zoroya,2007a, 2007b).

If a patient is suspected of having PTSD, a combat stressteam provider or psychiatrist should be consulted. It cannotbe overemphasized that bTBI and PTSD can occur alone ortogether and may be difficult to differentiate.

If TBI is suspected, the patient must be removed fromcombat-related duties. This may mean garrison or light dutyfor a period of time until symptoms fully resolve, or evacua-tion out of theater where advanced neuroimaging (such asMRI) and more detailed evaluation may be instituted.

One important clinical condition to be avoided is second-impact syndrome (SIS). SIS is a disease that can develop if asubsequent head injury occurs before full recovery (McQuil-len et al., 1988; Ling, 2007). This can lead to a worse clinicaloutcome, especially in the young, inwhommortality rates canreach 50%. In order to allow for sufficient recovery, militarymedical providers use established civilian practice guidelines,such as The American Academy of Neurology’s ‘‘Guidelinesfor Concussion Management,’’ that includes recommendedperiods of recovery (Quality Standards Subcommittee of theAmerican Academy of Neurology, 1997). There are otherguidelines that can also be used, such as the Cantu gradingsystem and the Colorado Medical Society Guidelines (Bailesand Cantu, 2001; Bleiberg et al., 2004). Although developedfor sports-related TBI, these are still useful tools for militaryhealth care providers (Ling, 2007; Ropper and Gorson, 2007).

Conclusion

Blast TBI is a disease afflicting many combat-injured war-fighters, and it potentially constitutes a new category of TBI.

FIG. 9. This patient was exposed to an IED blast injury andhad extensive soft-tissue wounds in the nasion region whichlimited a reliable pupillary examination. His CT scan shownhere reveals compressed basilar cisterns with subarachnoidhemorrhage; there was no intracranial penetration. A tran-scranial Doppler examination was performed as part of thetriage process and was consistent with brain death.

EXPLOSIVE BLAST NEUROTRAUMA 823

Clinically it shares many features with traditional TBI, butthere are unique aspects. In its mild form, bTBI also sharesmany features with PTSD, but here again it has distinct as-pects. Although military medical providers depend on civil-ian standard-of-care TBI guidelines when managing bTBI,they are continually adapting their medical practice in orderto optimize the treatment of this disease, particularly in atheater of war. It is clear that further rigorous scientific studiesof bTBI at both the basic science and clinical levels are needed.This research must include improved understanding of thecauses andmechanisms bywhich explosive blast leads to TBI.Also needed are comprehensive epidemiological studies todetermine the prevalence of this disease, and the factors thatcontributemost to the risk of developing it. Awidely acceptedunambiguous clinical description of bTBI with diagnosticcriteria would greatly improve diagnosis. It is hoped thatthrough appropriate research, meaningful prevention, miti-gation, and treatment strategies for bTBI can be realizedquickly. It should be recognized that although bTBI is cur-rently a disease suffered largely by soldiers, there is the un-fortunately high likelihood that it may become a civiliandisease as well.

Author Disclosure Statement

The views and opinions expressed herein are solely those ofthe authors. They do not represent, and should not be inter-preted as, stated or implied endorsement by the UniformedServices University of the Health Sciences, U.S. Army, U.S.Air Force, Department of Defense, or the U.S. government.

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Address reprint requests to:Geoffrey Ling, M.D., Ph.D.

Colonel, Medical Corps, U.S. ArmyDepartment of Neurology

Uniformed Services University of the Health Sciences4301 Jones Bridge Road

Bethesda, MD 20814

E-mail: gling@usuhs.mil

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