Imaging for the Diagnosis and Management of Traumatic Brain Injury
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To understand the role of imaging in traumatic brain injury (TBI), it is important to appreciate that TBI encompasses a heterogeneous group of intracranial injuries and includes both insults at the time of impact and a deleterious secondary cascade of insults that require optimal medical and surgical management. Initial imaging identifies the acute primary insult that is essential to diagnosing TBI, but serial imaging surveillance is also critical to identifying secondary injuries such as cerebral herniation and swelling that guide neurocritical management. Computed tomography (CT) is the mainstay of TBI imaging in the acute setting, but magnetic resonance tomography (MRI) has better diagnostic sensitivity for nonhemorrhagic contusions and shear-strain injuries. Both CT and MRI can be used to prognosticate clinical outcome, and there is particular interest in advanced applications of both techniques that may greatly improve the sensitivity of conventional CT and MRI for both the diagnosis and prognosis of TBI.
Key WordsTBI hemorrhage subdural epidural contusion traumatic shear injury
Traumatic brain injury (TBI) is a significant cause of morbidity and mortality worldwide, with substantial associated economic costs to the healthcare system. It is estimated that 10 million people sustain TBI each year worldwide, and the Centers for Disease Control and Prevention in the USA estimates that 1.7 million people suffer TBI annually . The cost of TBI in the USA, including direct medical costs and indirect costs of lost productivity, is estimated to total >60 billion dollars annually . Over the long term, TBI patients also suffer functional and cognitive changes and develop medical conditions, such as epilepsy, that require long-term or lifelong supportive and medical care.
The primary causes of TBI vary according to patient age. Falls are the leading cause of TBI in children up to 4 years of age and elderly individuals >75 years of age. Among adolescents, motor-vehicle accidents are the chief cause of TBI. Sports and recreation-related injuries, assaults and firearm use, and blast injuries for active duty military personnel are other common causes of TBI.
PATHOPHYSIOLOGY OF TBI
The damage to the brain from TBI is traditionally divided into primary and secondary injuries. Primary injuries, such as hematomas and traumatic axonal injury (TAI), occur as a direct result of the traumatic impact. Secondary injuries develop minutes to days after the primary trauma and include a complex biochemical cascade of events leading to cerebral swelling and herniation that is triggered by the primary traumatic event. This classification highlights that TBI is not a one-time event but rather a continuous and progressive injury that necessitates optimal medical and surgical management of cerebral oxygenation, intracranial pressure (ICP) and cerebral perfusion pressure (CPP) to maximize patient recovery and prevent successive injury.
Primary traumatic injuries, such as intracranial hemorrhage, can trigger secondary insults by raising the ICP. CPP (i.e., the pressure gradient driving oxygen and nutrient delivery to the brain) is the difference between mean arterial pressure and ICP. CPP is used as an index of cerebral blood flow. When the ICP increases due to TBI (or systemic blood pressure falls), the CPP will fall, and the brain will become ischemic unless intact cerebral autoregulation induces compensatory cerebrovascular vasodilatation to maintain adequate blood flow to the brain. However, normal cerebral autoregulation is frequently disrupted in patients with TBI, particularly in young patients. Also, at low CPP values (below a threshold of ~50–60 mm Hg), autoregulation seems to be impaired, and the brain is likely to become ischemic [2, 3]. With ischemia and the resultant decreased oxygen and glucose delivery to the brain, complex biochemical and cellular pathways are triggered that further aggravate injury to the brain. Excitatory neurotransmitters (primarily glutamate) are released into the tissue that initiate various pathophysiologic processes, including excessive calcium influx into cells, resulting in mitochondrial dysfunction, cellular swelling, free radical production, and eventual neuronal death.
PRINCIPLES OF MANAGEMENT OF TBI
Current management of TBI in the neurointensive care unit is focused on preventing or mitigating the above-mentioned cascade of secondary injuries by maintaining adequate perfusion to the brain. This approach requires vigilant neuromonitoring and control of blood pressure and oxygenation to avoid both hypotension and hypoxemia, which can increase morbidity and mortality [4, 5, 6]. TBI patients in whom autoregulation is severely impaired depend entirely on blood pressure to maintain cerebral blood flow to the brain, a condition termed “pressure-passive” flow. Adequate blood pressure support is therefore critical.
ICP is also monitored in all patients with severe TBI as defined by a Glasgow Coma Scale (GCS) score of 3–8, and an abnormal computed tomography (CT) scan [7, 8]. ICP is conventionally measured by an external ventricular drainage catheter, though parenchymal, subarachnoid, subdural, and epidural devices can also be used. As increased ICP may portend cerebral herniation or potentially compromised CPP and is associated with a worse prognosis, rigorous measures to lower the ICP are used. These includes both medical treatment with hyperosmolar therapy, cautious hyperventilation, and appropriate sedation/analgesia, as well as surgical treatment with cerebrospinal fluid (CSF) drainage via the external ventricular drainage catheter, intracranial hematoma evacuation and, if necessary, decompressive craniectomy [9, 10, 11].
Finally, ensuring that CPP is maintained at an adequate level to avoid ischemic injury is important; again, threshold values for CPP are ~50–60 mm Hg, as cerebral ischemia may occur below this range [2, 3].
A large number of neuroprotective agents that modulate the deleterious biochemical cascade triggered by cerebral ischemia to further compound injury have been studied. Numerous neuroprotective strategies, including the use of agents to antagonize excessive excitotoxic glutamate activity, block voltage-gated calcium channels and intracellular calcium influx, reduce mitochondrial dysfunction, and limit free radical damage, have been evaluated in both experimental animal models and clinical trials [12, 13, 14]. Unfortunately, none of these agents have shown convincing benefit in randomized control trials to date. This lack of an efficacious outcome may reflect a number of factors, including the heterogeneity of TBI patients in these trials and the difficulty in knowing whether the pathophysiologic mechanisms targeted in these patients are indeed active at the time of drug delivery.
ROLE OF IMAGING IN DIAGNOSIS AND MANAGEMENT OF TBI
Imaging is critical to both the diagnosis and management of TBI. For diagnosis of TBI in the acute setting, noncontrast CT is the modality of choice as it quickly and accurately identifies intracranial hemorrhage that warrants neurosurgical evacuation. CT readily identifies both extra-axial hemorrhage (epidural, subdural, and subarachnoid/intraventricular hemorrhage) and intra-axial hemorrhage (cortical contusion, intraparenchymal hematoma, and TAI or shear injury). While CT is the mainstay of TBI imaging in the acute setting, magnetic resonance imaging (MRI) has better diagnostic sensitivity for certain types of injuries that are not necessarily hemorrhagic, including cortical contusions and nonhemorrhagic traumatic axonal injuries.
For the management of TBI patients, noncontrast CT readily identifies the progression of hemorrhage and signs of secondary injury relevant to neurocritical care, such as cerebral swelling, herniation, and hydrocephalus.
In this review, we discuss each type of primary and secondary brain injury in turn, with an emphasis on the imaging features that are of particular relevance to medical and surgical management and decision-making.
PRIMARY INJURIES IN TBI PATIENTS
Acute Epidural Hematoma, Management Considerations 
Surgical evacuation if:
GCS ≤8 with anisocoria, or
Any GCS with EDH volume >30 cm3*
Nonoperative monitoring if:
GCS >8, and
No focal neurologic deficit, and
EDH volume <30 cm3*, and
EDH thickness <15 mm, and
Midline shift <5 mm
A subdural hematoma (SDH) can occur either at the coup or contrecoup site, although the latter is more common. Injury to superficial bridging veins results in bleeding between the meningeal layer of the dura and arachnoid, and blood may continue to accumulate in this space as bridging veins are progressively stretched and injured. SDHs commonly occur over the cerebral convexities, along the tentorium cerebelli, and along the falx cerebri, in descending order of frequency .
Acute Subdural Hematoma, Management Considerations 
Surgical evacuation in all patients regardless of GCS, if:
SDH thickness >10 mm, or
Midline shift >5 mm
Nonoperative monitoring in patients with GCS ≤8, if:
SDH thickness <10 mm, and
Midline shift <5 mm, and
ICP <20 mm Hg, and
Neurologically stable, and
No pupillary abnormalities
Subarachnoid hemorrhage (SAH) occurs in ~40% of patients with moderate to severe head injury and is commonly associated with other types of intracranial hemorrhage . SAH may result from direct laceration of the small cortical vessels traversing the subarachnoid space, redistribution of intraventricular hemorrhage exiting the fourth ventricular outflow foramen, or direct extension from cortical contusion/hematoma. Patients with traumatic SAH have a significantly worse outcome than those without SAH: 41% of patients without traumatic SAH achieved a level of good recovery compared with only 15% of patients with SAH, according to the results of a large study conducted by the European Brain Injury Consortium .
Acute SAH is readily identified on noncontrast CT scans as linear areas of high attenuation in the cerebral sulci at the convexities, Sylvian fissures, or basilar cisterns. It is important to examine areas such as the interpeduncular cistern, which may contain subtle SAH that is easily missed without conscious attention to this area. In ~5% of patients with TBI, SAH may be the only abnormal finding on a noncontrast CT scan .
Hydrocephalus is a common complication of traumatic SAH and may develop acutely or in a delayed fashion. Intraventricular hemorrhage or inflammatory arachnoiditis may result in hydrocephalus in the acute setting, while decreased resorption of CSF by arachnoid villi is responsible for chronic hydrocephalus.
Cortical contusions in closed head injury result when the brain is bruised by the irregular inner surfaces of the skull at the time of impact. They can occur at the coup site when a depressed skull fracture or transient calvarial deformity from a blow to the stationary head grazes the underlying cortex. More commonly, however, they occur at the contrecoup location when the moving head collides against a stationary object. These contrecoup contusions are frequently of greater severity than the injuries at the coup site. The precise mechanism of contrecoup contusions and the explanation for their greater severity are subjects of considerable debate. A recent explanation proposes that when a moving skull collides against a stationary object, such as when a person falls and strikes the back of his head against the ground, the buoyant brain is displaced by CSF in the opposite direction from impact, causing injury opposite the blow .
With greater severity of head trauma, microhemorrhages associated with a contusion may coalesce into an intracerebral hematoma (ICH), reflecting that contusions and ICH represent a spectrum of injury rather than discrete, independent entities. ICHs may also develop in delayed fashion in a part of the brain that was previously seen to be radiographically normal, an entity known as the “delayed traumatic intracerebral hematoma.” Similar to contusions, ICHs represent a dynamic process of injury. According to one study, only 56% of ICH >3 cm in diameter developed within 6 h of injury, and only 84% of ICH reached maximal size by 12 h,  underscoring again the importance of intensive clinical monitoring and serial imaging.
The specific indications for craniotomy and surgical evacuation in patients with contusion or ICH have not been established. Generally, a combination of clinical and radiologic factors is felt to be important, including hemorrhage location and volume, extent of mass effect on CT (cisternal effacement or midline shift), GCS score, ICP, and neurological deterioration [29, 30, 31, 32]. Patients with contusions/ICH and progressive neurological decline, medically refractory increased ICP, or radiographic evidence of mass effect tend to have poor outcome without surgical treatment, although specific surgical criteria have not been established.
Traumatic axonal injury
Traumatic axonal injury (TAI) is also commonly referred to as diffuse axonal injury or shear injury. The term TAI is preferred by the authors of this review as injuries are not distributed diffusely throughout the whole brain, but occur in characteristic, discrete locations, including the parasagittal white matter near the cerebral cortex, corpus callosum, and brainstem. Mild (grade I) TAI involves the gray–white junction of the lobar white matter, particularly the parasagittal frontal lobes; moderate (grade II) TAI involves the fibers of the corpus callosum, particularly the splenium, in addition to the subcortical white matter; severe (grade III) TAI involves the dorsolateral midbrain, in addition to the subcortical white matter and corpus callosum.
The mechanism of injury is one of cytoplasmic shear-strain of the axonal cytoskeleton due to sustained acceleration/deceleration, such as that which occurs with a high-speed motor vehicle crash or prolonged shaking . Damage to the neurons occurs not only at the time of mechanical injury but in the hours, days, and weeks, even years, following the traumatic event due to a deleterious cascade of biochemical events and Wallerian-type degeneration with progressive neuronal loss. Changes associated with TAI are thought to be responsible for the majority of global cognitive defects seen after TBI, particularly with regard to difficulties with memory and information processing.
SECONDARY INJURIES IN TBI PATIENTS
There is an ongoing debate in the literature as to whether cerebral edema or cerebral hyperemia with increased blood volume is the underlying cause of cerebral swelling. Both mechanisms may be at play. A generally held premise is that cerebral hyperemia due to dysautoregulation with vascular engorgement and increased cerebral blood volume is the principal mechanism of cerebral swelling, although recent data suggest that blood volume may actually be decreased following trauma and that cerebral edema may be the major fluid component of brain swelling [38, 39]. There are two types of cerebral edema: vasogenic, due to disruption of the blood–brain barrier allowing accumulation of extracellular water, and cytotoxic, due to the failure of cell membrane pumps, resulting in intracellular water leakage. Of these two types of edema, cytotoxic edema may be primarily responsible for cerebral swelling, as demonstrated by the increased water content and reduced apparent diffusion coefficient values in one MRI study .
Children are particularly susceptible to diffuse cerebral swelling following TBI, with the incidence of diffuse swelling being approximately twofold higher in children than in adults . Children and young adults are more prone to post-traumatic dysautoregulation, which leads to vasodilatation, hyperemia, and cerebral swelling. When swelling is severe, ICP increases and CPP falls, resulting in infarction and cerebral damage.
Medical strategies to combat the deleterious effects of cerebral swelling and lower ICP include head elevation, moderate hyperventilation, hyperosmolar therapy with mannitol, and the appropriate use of sedatives and analgesics (barbiturates) to prevent pain or agitation from exacerbating elevated ICP. However, when ICP is refractory to maximal medical therapy, decompressive craniectomy has been used in an attempt to lower ICP. Studies on the efficacy of decompressive craniectomy generally suggest that it can lower ICP and may improve functional outcome [42, 43, 44]. Decompressive craniectomy also results in radiologic improvement, with better visualization of basilar cisterns and decreased midline shift, both of which correlate with improved outcome . However, the specific clinical criteria and context for decompressive surgery have yet to be established.
Cerebral herniation is a result of unmitigated increased ICP. These patients typically undergo decompressive craniectomy with mass lesion evacuation.
Subfalcine herniation or midline shift occurs when the cingulate gyrus herniates under the falx cerebri; uncal herniation results when the medial temporal lobe herniates through the tentorial incisura and compresses the ipsilateral suprasellar cistern; descending transtentorial herniation occurs with downward herniation of both temporal lobes through the tentorial incisura, compressing the basilar cisterns; upward transtentorial herniation occurs in the opposite direction, with the cerebellum extending through the tentorial incisura and effacing the quadrigeminal cistern; tonsillar herniation results when the cerebellar tonsils herniate into the foramen magnum.
Cerebral ischemia and infarction
Other potential causes of ischemia and infarction in patients with TBI include vasospasm, which has been angiographically documented in patients following head trauma.47 Also, extra-axial hematomas that exert a significant mass effect on the adjacent cortex may compress cortical veins and result in venous infarction. Finally, direct vascular injury, such as dissection, occlusion, or pseudoaneurysm from a skull base fracture, may also result in ischemia.
ROLE OF IMAGING IN THE PROGNOSTICATION OF OUTCOME FOLLOWING TBI
In addition to diagnosing and guiding the management of TBI, imaging modalities can be used to predict clinical and functional outcome after head injury. Because noncontrast CT has been the mainstay of imaging acute TBI given its speed, accessibility, and sensitivity to hemorrhage, attention has historically focused on identifying CT predictors of clinical outcome. The widely used Marshall classification and Rotterdam score (discussed below) relate imaging findings on noncontrast CT scans to mortality and patient outcome. However, with the development of novel CT techniques, such as CT perfusion, there is considerable interest in investigating these modalities to better treat and prognosticate TBI patients. As with CT, continued innovations in MRI technology have led to developments such as susceptibility-weighted and diffusion tensor imaging that may also help to better prognosticate outcome in TBI patients.
Routine noncontrast CT
Individual predictors of poor outcome on conventional CT include compressed or absent basilar cisterns, the presence of subarachnoid hemorrhage, midline shift, and intracranial hemorrhagic lesions (e.g., subdural or epidural hematomas, shear injury, and contusions). Compressed or absent basilar cisterns indicate a threefold higher risk of increased ICP and are associated with a two- to threefold increase in mortality . Traumatic subarachnoid hemorrhage is associated with a twofold increase in mortality, and hemorrhage in the basilar cisterns has a 70% positive predictive value for poor outcome . Midline shift indicates increased ICP and is similarly associated with a poor clinical outcome, although this association is somewhat complicated by the fact that midline shift is caused by intracranial hemorrhage that also negatively impacts outcome. Finally, intracranial hemorrhage has an approximately 80% positive predictive value for poor functional outcome, with prognosis worsening as the hematoma volume increases in size . Of note, mortality is higher in patients with acute subdural hematomas compared with those with epidural hematomas.
Marshall Classification of Head Injury (Trauma Coma Data Bank)
Diffuse injury I (no visible pathology)
No visible intracranial pathology on CT scan
Diffuse injury II
Cisterns present with midline shift ≤5 mm and/or lesion densities present, no high- or mixed-density lesion >25 cc, may include bone fragments and foreign bodies
Diffuse injury III
Cisterns compressed or absent with midline shift ≤5 mm, no high- or mixed-density lesion >25 cc
Diffuse injury IV
Midline shift >5 mm, no high- or mixed-density lesion >25 cc
Evacuated mass lesion
Any lesion surgically evacuated
Nonevacuated mass lesion
High- or mixed-density lesion >25 cc, not surgically evacuated
Rotterdam Score for Probability of Mortality in Patients with Traumatic Brain Injury
No shift or shift ≤5 mm
Shift >5 mm
Epidural mass lesion
Intraventricular or subarachnoid hemorrhage
Advanced CT techniques
While noncontrast CT is invaluable for the diagnosis, management and prognosis of patients with TBI, it is limited to displaying only anatomic information. Physiologic derangements in cerebral perfusion, blood flow, and oxygenation related to the deleterious cascade of secondary traumatic brain injuries that significantly impacts functional outcome are not captured on conventional noncontrast CT scans. Perfusion CT is a new imaging tool that utilizes dynamic scanning during intravenous contrast injection to illustrate physiologic parameters of cerebral blood volume (CBV), cerebral blood flow (CBF), and mean transit time (time for blood to perfuse a region of tissue).
Evidence of normal brain perfusion or hyperemia (high CBV and CBF) on perfusion CT scans in TBI patients has been associated with a favorable clinical outcome, while oligemia (low CBV and CBF) has been associated with unfavorable outcome . These findings on perfusion CT scans have been postulated to reflect the status of cerebrovascular autoregulation: patients with relatively minor head trauma and intact autoregulation maintain or even slightly increase cerebral perfusion, while patients with severe head injury have impaired autoregulation and pressure-passive flow, which often results in oligemia and decreased perfusion. The excitement of using perfusion CT to better understand the physiology of TBI patients is tempered by concerns of increased radiation exposure, particularly in young patients who are often the victims of head injury.
Advanced MRI techniques
While CT is useful for the diagnosis and prognostication of outcome in patients with hemorrhagic injuries such as subdural and epidural hematomas, patients with subarachnoid hemorrhage and contusions, a subset of TBI, have normal CT scans without hemorrhage yet still fare poorly. TAI patients can suffer significant post-traumatic symptoms and may be profoundly comatose, with cognitive impairment and poor functional outcome despite normal results on conventional CT or MR images. As such, there is considerable interest in developing more sensitive diagnostic tests for TAI and for correlating these tests with long-term functional outcome. Unfortunately, as there are no good treatment options for TAI patients at this time, the value of improved imaging diagnosis currently lies in the potential to better prognosticate clinical outcome.
Diffusion tensor imaging (DTI) is one investigative MRI technique that maps out the microstructural characteristics of the brain based on the intrinsic diffusion properties of neurons. Unlike conventional diffusion weighted imaging, which encodes diffusion in 3 basic directions, DTI assesses diffusion in at least 6 but typically 25–30 directions, yielding a more complete set of diffusivity information that can be used to deduce axonal orientation and create maps of white matter tracts in the brain. TAI interrupts the cytoskeletal network and impairs axoplasmic transport, causing changes in tissue diffusivity that can be visualized and quantified on DTI . DTI has been shown to be more sensitive than conventional 3T MRI in detecting TAI, and results from recent studies suggest that the extent of damage to white matter structures on DTI may correlate with the extent of cognitive impairment and functional outcome following TBI [53, 54].
SWI is another relatively new MRI technique that increases sensitivity for the detection of TAI. SWI utilizes a high-resolution, velocity-compensated, 3-dimensional GRE sequence based on both magnitude and phase data [55, 56]. It is exquisitely sensitive to susceptibility effects due to microhemorrhages, small veins, and changes in iron content, and more sensitive than conventional GRE sequences for the detection of hemorrhagic TAI, revealing four- to sixfold more microhemorrhages than conventional GRE imaging [57, 58]. Initial studies also suggest that lesion burden on SWI correlates with clinical outcome, including the duration of coma and long-term functional disability [59, 60].
Magnetoencephalography is a functional imaging technique that measures the magnetic field generated by neuronal activation. Unlike normal brain tissue that generates α-waves with a frequency of 8–13 Hz, injured neurons produce δ-waves with a low frequency of 1–4 Hz. This magnetic signal can be measured and localized with high spatial (2–3 mm) and temporal (<1 ms) resolution. In TBI patients, magnetoencephalography “slow waves” can be seen in cortical gray matter that is functionally and structurally connected to white matter fiber tracts with axonal shear injury, as demonstrated on DTI, and may be more sensitive than DTI in diagnosing mild TBI .
Functional MRI (fMRI) is another functional imaging technique that relies on the relationship between physiologic function, energy consumption, and blood flow to depict brain activity. Most brain fMRI studies rely on a blood oxygen level-dependent signal to demonstrate cerebral function. It is thought that neuronal activity causes an increase in cerebral flood flow and local blood oxygenation with a relative decrease in the amount of deoxyhemoglobin, a product of oxygen consumption. Deoxyhemoglobin is paramagnetic, generating field inhomogeneities that result in signal loss on GRE sequences sensitive to susceptibility effects. Thus, as the relative concentration of deoxyhemoglobin decreases within a region of neuronal activity, an increased signal within this area is seen on GRE images. Blood oxygen level-dependent fMRI studies performed in patients with mild TBI and structurally normal imaging studies have shown differences in brain activation during various tasks as compared with healthy control subjects [62, 63].
To understand the role of imaging in TBI, it is important to appreciate that TBI encompasses a heterogeneous group of intracranial injuries and includes both insults at the time of impact and a deleterious secondary cascade of insults that require optimal medical and surgical management. Initial imaging identifies the acute primary insult that is essential to diagnosing TBI, but serial imaging surveillance is also critical to identifying secondary injuries, such as cerebral herniation and swelling, that guide neurocritical management. CT is the mainstay of TBI imaging in the acute setting, but MRI has better diagnostic sensitivity for nonhemorrhagic contusions and shear-strain injuries. Both CT and MRI can be used to prognosticate clinical outcome, and there is particular interest in advanced applications of both techniques that may greatly improve the sensitivity of conventional CT and MRI for both the diagnosis and prognosis of TBI.
The authors have no financial interests in the discussed subject matter to disclose.
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