Imaging of pediatric head trauma

Neuroimag Clin N Am 12 (2002) 271 – 294

Imaging of pediatric head trauma Tina Young Poussaint, MD*, Karen K. Moeller, MD Department of Radiology, Harvard Medical School, Boston, MA 02115, USA Division of Neuroradiology, Department of Radiology, Children’s Hospital, Boston, MA 02115, USA

Pediatric head trauma is one of the leading causes of injury, mortality, and morbidity in childhood, accounting for 95,000 hospital admissions and 600,000 emergency department visits in the United States per year, with an incidence from 0.2% to 0.3% [1 – 4]. Neuroimaging as an aid in the diagnosis and treatment of intracranial injury has revolutionized the management and care of these patients, improving outcome and prognosis. The mechanisms of injury in children vary depending on age. In children below age two, nonaccidental trauma accounts for more than 80% of deaths [1,5]. The younger the child, the higher the risk of injury [6], and the risk for asymptomatic intracranial injury is highest for infants younger than six months [7], because of their large heads, weak neck musculature, and relatively thin calvaria [8]. As the age of the child increases, falls become a less frequent cause of accidental trauma, whereas bicycle injuries and motor vehicle accidents become more common [8].

Imaging evaluation Computed tomography Computed tomography (CT) is the modality of choice for the evaluation of acute neurologic presentations or hemorrhage in the child with trauma. It is rapid, widely available, and inexpensive. CT can accommodate life support equipment, traction and

* Corresponding author. Division of Neuroradiology, Department of Radiology, Children’s Hospital, 300 Longwood Avenue, Boston, MA 02115. E-mail address: [email protected] (T. Poussaint).

monitoring devices, and is easy to obtain. It is useful for the detection of acute or subacute hemorrhage, scalp injury, and pneumocephalus, as well as other neurosurgically significant conditions—hydrocephalus, midline shift, masses and mass effect, ischemia, and herniation—that require rapid detection for potential treatment. CT helps to demonstrate linear calvarial skull fractures that are not in the plane of scanning, depressed, and basilar skull fractures as well as facial fractures. Limitations of CT are related to beam hardening streak artifact in the posterior fossa, patient motion, partial volume averaging, and detection of small extraaxial hematomas. Magnetic resonance imaging Magnetic resonance imaging (MRI) provides multiplanar capability, and superior sensitivity and specificity to abnormal brain anatomy and function in the injured pediatric brain. It is helpful for characterization and timing of hemorrhage and for anatomic localization in the extraaxial space or brain parenchyma [9,10]. MRI has increased sensitivity for detection of intraparenchymal injury such as edema, hematoma, contusion, diffuse axonal injury, and brain edema. It provides superior visualization of the brainstem and posterior fossa components, aiding in the detection of injuries there. The sequelae of head trauma are better evaluated with MR than CT imaging [9 – 12]. In addition to standard T1- and T2-weighted multiplanar imaging, gradient echo images with long echo times are sensitive for detecting blood products and should be performed in any patient with a history of head trauma [13,14]. Fluid attenuated inversion recovery (FLAIR) sequences have been reported to be sensitive to the detection of subarachnoid hemorrhage (SAH) [15 – 17], although CT remains the initial

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screen for SAH. Magnetic resonance angiography (MRA) can provide information about the involvement of major vascular structures, such as the circle of Willis or the dural venous sinuses, after head trauma. MRA is used for the diagnosis of vascular injury such as dissection, occlusion, or pseudoaneurysm, which may be corroborated with conventional angiography, depending on the clinical setting. MR perfusion and diffusion MR perfusion can assess cerebral perfusion dynamics by analyzing hemodynamic parameters, including relative cerebral blood volume, relative cerebral blood flow, and transit time. Using echoplanar or line-scan spin echo techniques, diffusion imaging (DI) provides information based upon differences in the rate of diffusion of water molecules, and is especially sensitive to intracellular changes in patients with head trauma. The rate of diffusion, or apparent diffusion coefficient (ADC), is higher for free or pure water than for macromolecular bound water. The ADC varies according to the microstructural or physiologic state of a tissue. A particularly important application of DI is in the early detection of diffuse and focal ischemic injury [18,19]. Diffusion imaging within one to two hours of injury [20] in the patient with head trauma has been found to detect more lesions than conventional MR images [21 – 23]. In a study of children with nonaccidental head injury, early DI was found to reveal diffusion abnormalities in approximately 90% of the children, and was helpful in early detection of infarction, revealing more extensive brain injury or injury that had not been seen on conventional MRI [24]. The severity of the abnormalities on DI correlated with poor outcome (P < 0.005). Diffusion tensor imaging (DTI) has been found to provide information about brain ultrastructure by quantifying isotropic and anisotropic water diffusion. Measuring water diffusion anisotropy can yield information about structures such as white matter tracts [25]. Changes in diffusion anisotropy in traumatic brain injury and diffuse axonal injury have been reported [23,26]. In a study of 20 adult patients, changes in diffusion anisotropy within the white matter correlated with acute Glasgow coma scale and Rankin score at discharge (Thierry A.G.M. Huisman, MD, personal communication, 2001). There was a statistically significant correlation between fractional anisotropy values and severity of head injury in both the acute setting (Glasgow coma score) and long-term prognosis (Rankin score) in different predilection sites of diffuse axonal injury. Future studies using this

application in the pediatric population will likely yield more important information about head trauma severity and outcome in children who have had accidental or nonaccidental trauma. Magnetic resonance spectroscopy Magnetic resonance spectroscopy (MRS) offers a noninvasive approach to biochemical analysis and provides quantitative information regarding cellular metabolites, since signal intensity is linearly related to steady-state metabolic concentration. Elevated lactate has been found in cerebral contusions and regions of brain infarction in pediatric head trauma [27]. In babies who were shaken, a decrease in N-acetylaspartate (NAA) and increase in lactate between five and seven days after injury indicated poor prognosis and significant brain damage [28]. In adults with traumatic brain injury, proton MR spectroscopic findings have been found to correlate with neuropsychological function with reduced NAA in white matter, which suggests neuronal injury and inflammation [29,30]. Thus, MRS can predict patient outcome and has the capability to assess severity of brain injury in older pediatric patients. Functional MRI Functional MRI (fMRI) is the term applied to brain activation imaging in which local or regional changes in cerebral blood flow that accompany stimulation or activation of sensory (eg, visual, auditory), motor, or cognitive centers are displayed. One fMRI study involved the effects of trauma on cognition, neural circuitry, learning and memory [31], with the aim of using fMRI as an assessment and prognostic tool to evaluate trauma patients. In mild traumatic brain injury (TBI) in adults [32], fMRI has demonstrated effects on working memory. In other adult patient studies, impairment of working memory was associated with alterations in functional cerebral activity in moderate to severe TBI [33] and was used to predict brain function in a comatose head-injury [34]. Thus, fMRI should be useful to evaluate brain function and prognosis in nonresponsive brain trauma patients of any age. Magnetic source imaging Magnetic source imaging (MSI) integrates anatomic data from conventional MRI with electrophysiological data from magnetoencephalography. Magnetoencephalography is a technique that measures magnetic fields associated with intracellular cur-

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rent flows within neurons [35] and has demonstrated brain dysfunction in patients with postconcussive symptoms [36]. It apparently has greater sensitivity for this purpose than conventional MR or electroencephalography (EEG). Magnetization transfer imaging Magnetization transfer imaging relies upon the large difference between the relaxation properties of free water and water bound to macromolecules and macromolecular protons [37]. The exchange of magnetization between these two pools has been applied to patients with traumatic brain injury. Abnormal magnetization transfer ratios were found in normal appearing white matter on conventional MRI prone to axonal injury and are an apparent predictor of poor outcome [38]. Nuclear medicine Single photon emission computed tomography (SPECT) imaging may demonstrate focal, multifocal, or regional areas of hypoperfusion in patients with brain injury in the acute (< 24 hours) and chronic phases when compared to CT [39 – 41]. In a study of SPECT, CT, and MRI, SPECT was compared to CT in the acute phase and showed slightly more abnormalities. However, MR showed more abnormalities than SPECT [42]. F-18 fluorodeoxyglucose positron emission tomography (FDG-PET imaging) has demonstrated a decrease in the regional cerebral metabolic rate of glucose in traumatic brain injuries [43]. Oxygen-15 positron emission tomography (O-15 PET) imaging in severely brain-injured patients demonstrated alterations in substrates in verbal recall. Frontal regional cerebral blood flow was decreased during free recall and enhanced during recognition in these patients compared with controls [44]. Ultrasonography Ultrasonography (US), with its real-time capabilities and ready access, has been used in the evaluation of extracerebral fluid collections in infants and in critically ill patients who are not able to be transported for CT or MR. Distinction of the subarachnoid spaces over the convexities from subdural collections is accomplished using standard and color Doppler techniques [45,46]. Transcranial doppler techniques have been used to correlate resistive indices with elevated intracranial pressure in patients with head trauma [47].

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Birth trauma Scalp injury Three patterns of extracranial hemorrhage associated with birth trauma are: caput succedaneum, subgaleal hemorrhage, and cephalohematoma [48]. Caput succedaneum is the most common scalp injury during the birth process, frequently occurring following vaginal delivery. It consists of hemorrhage and edema within the fibrofatty layer just beneath the skin, localized at the vertex with associated molding. These hemorrhages are soft to palpation, are selflimited and typically resolve over days. Although imaging is not necessary to make the diagnosis, caput succedaneum is often demonstrated incidentally and appears as focal soft tissue swelling on CT or MRI. Subgaleal hemorrhage occurs between the epicranial aponeurosis (galea) and the periosteum of the calvaria. It remains superficial to the temporalis muscle in this region of the skull [49]. This space contains small veins and is also crossed by emissary veins that connect the dural sinus with the superficial veins of the scalp. These hemorrhages are firm to palpation and typically asymptomatic. The anatomy of the subgaleal space may allow pooled blood to become very large and extensively extend around the cranium leading to significant blood loss. This type of injury can occur following instrumentation used during delivery, especially vacuum extraction [50]. Subgaleal hematomas appear on imaging studies as diffuse soft tissue swelling that crosses suture lines. The hematoma typically resolves over two to three weeks. Cephalohematoma is subperiosteal in location and occurs in up to 1% of live births [51]. Cephalohematomas may lie beneath the temporalis muscle. They may occur following vaginal delivery, but they have an increased incidence in deliveries that employ forceps or use vacuum extraction. Because of the subperiosteal location of the hemorrhage, they are bounded by the sutures where the periosteum is firmly attached. These hemorrhages present as a palpably firm, tense mass that resolves over weeks to months and can calcify as they age and become incorporated in periosteal new bone. They are most common in the parietal region and can be unilateral or bilateral [49]. On imaging, cephalohematomas have a crescentic shape and are bound by sutures. Curvilinear peripheral calcification can develop within 14 days (Fig. 1). The appearance on MRI varies depending on the age of the hematoma. Cephalohematomas are usually hyperintense on T1-weighted imaging, and a hematocrit effect may be visualized on T2weighted imaging [52]. Rarely, cephalohematomas

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delivery accompanied by instrumentation [12]. The most frequent site for depressed skull fractures in the neonate is the parietal bone, followed by the frontal bone. The degree of depression of the involved bone is best evaluated by CT, which may also show an underlying injury. The depressed fracture is often referred to as the ‘‘ping-pong’’ fracture, because of the inward buckling of the bone, which may be present without loss of bony continuity and resembles the same deformity in a ping-pong ball. Intracranial injury Intracranial injury can occur during delivery secondary to cephalopelvic disproportion, breech presentation, or from instrumentation involving forceps or vacuum extraction. The rate of intracranial hemorrhage is higher in infants delivered by vacuum extraction, forceps, or cesarean section during labor than among those delivered spontaneously [54] (Fig. 2). The four most common intracranial injuries associated with birth trauma with subdural hemorrhage are: tentorial laceration, occipital osteodiastasis, falcine laceration, and rupture of bridging cortical and meningeal veins [55]. A large tear in the tentorium can result in rupture of the vein of Galen, straight sinus, or transverse

Fig. 1. Cephalohematoma in a 4-month old infant with a left parietal bump. (A) AP scout CT tomogram and (B) axial CT bone window images demonstrate calcified left parietal cephalohematoma.

may become infected, leading to complications such as subdural empyema, epidural abscess and osteomyelitis [53]. Skull injury A type of skull injury unique to newborns is the overlapping of calvarial bones at the sutures. Often, the degree of overlap is minor and of no clinical significance. The calvarial deformity resolves over time with growth. On CT, overlapping of adjacent bones at the sutures is best visualized on the bone window images. Depressed skull fractures are rare in neonates, but can be encountered following vaginal

Fig. 2. Subdural hemorrhage after forceps and vacuum delivery. Axial CT image demonstrates acute subdural blood along the right tentorium and cerebral convexity with mass effect on the right lateral ventricle and midline shift to the left.

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sinus, leading to large posterior fossa subdural hematomas (SDH) (Fig. 3). These hematomas can become massive, leading to brain stem compression and even death [56,57]. Smaller posterior fossa subdural hematomas are being recognized more frequently with the increased utilization of MRI. These hematomas result

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from smaller tears in the tentorium or rupture of small infratentorial veins. On CT, these subdurals present as increased attenuation and thickening along the tentorium. The SDH can also extend laterally along the cerebellar hemispheres. Follow-up imaging is recommended to ensure that hydrocephalus does not occur secondary to fourth ventricle compression. Occipital osteodiastasis occurs when there is a traumatic tear and separation along the synchondrosis between the squamosal and the exo-occipital portions of the occipital bone [58]. It is probably secondary to pressure on the occipital bone from the pubic symphysis of the mother during breech delivery, or results from forced engagement of the fetal head. Feto-pelvic disproportion is probably also an important factor contributing to this injury [59]. There also may be displacement of the anterior margin of the squamosal portion of the occipital bone into the posterior fossa, which may result in a tear of the dural sinuses or inferior cerebellar veins. Lateral skull films show overriding of the squamosal portion of the occipital bone on the condylar portions of the occipital bone. On CT, large subdural hemorrhages may be visualized in the posterior fossa. Parenchymal hemorrhage and cerebellar edema may also occur. The SDH usually occurs along the inferior aspect of the tentorium, with extension laterally along the cerebellar hemispheres. These hemorrhages can be seen on US as extraxial collections that are mild to moderately echogenic. The MR appearance varies depending on the age of the hematoma, with coronal imaging helpful for demonstrating these SDHs. Laceration of the falx is less common than laceration of the tentorium. This injury often occurs at the junction of the falx and tentorium, with bleeding occurring from a tear in the inferior sagittal sinus, which leads to SDH along the inferior aspect of the interhemispheric fissure adjacent to the corpus callosum. SDH over the cerebral convexity may occur from rupture of superficial cortical veins that bridge the dura. These SDHs are often unilateral and can be accompanied by subarachnoid hemorrhage (SAH) or adjacent cerebral contusion.

Skull fractures

Fig. 3. Tentorial laceration. (A,B) Axial CT images demonstrate severe hydrocephalus, blood in the fourth ventricle, along the tentorium, and in the region of the vein of Galen and straight sinus.

The calvarium in a child is softer and thinner than an adult’s and is therefore susceptible to fracture. Skull fractures from minor trauma are more common in children than adults, especially in children less than two years old [60]. In addition, under the age of four, the calvarium is unilaminar and lacks diploe [49]. Therefore the skull offers less protection to the

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child’s brain than it does in the adult, and children with skull fractures are at increased risk of having intracranial injury [6]. Skull fractures may be diagnosed by CT or plain radiography. Skull fractures in neonates may be of the following types: linear, diastatic, depressed, compound, or buckled. Older children may sustain comminuted fractures as the skull becomes more rigid with age. Linear fractures are by far the most common type of fracture in all age groups. Most linear fractures are associated with an overlying hematoma or scalp soft-tissue swelling. These fractures are more often diastatic in newborns and in infants that are less than six months old. On plain films, these are seen as lucent linear defects that tend to stop at the suture. They may be seen only on one view and are often better visualized on the lateral view of the skull. If a child is less than six months old, the central portion of the fracture line can be wider. Linear skull fractures may also be detected on CT but may be missed, especially if the fracture line is parallel to the plane of scanning. In this situation, three-dimensional (3D) CT maximum intensity projections (MIP) of the calvarium may be helpful to better visualize the fracture [61]. In infants and older children approximately 30% of patients with a depressed skull fracture have an associated brain injury [6,62] (Fig. 4). Complications from depressed skull fractures include dural tear, cerebral contusion, retained osseous fragments, and cosmetic deformity. The degree of depression correlates with underlying brain injury, so that if the outer portion of the depressed fragment is not depressed beyond the inner table of the adjacent calvarium, the fracture is considered less serious. Leptomeningeal cyst is a unique pediatric lesion that occurs as a delayed complication in approximately 0.05% to 1.6% of infants and children with skull fractures [63,64]. Ninety percent of these lesions (also called growing fractures) occur in children who are younger than three [65]. These are skull fractures that widen over time secondary to the torn meninges, becoming interposed between the fracture fragments. Cerebral spinal fluid (CSF) pulsation causes increased herniation of the meninges and progressive widening of the skull defect. There are three factors that are probably responsible for the increased incidence of this complication in children: an actively growing skull, dura that is more tightly adherent to the calvaria, and decreased thickness of the pediatric calvaria [63,66,67]. A leptomeningeal cyst may complicate any skull fracture, but is often associated with a diastatic parietal fracture. A dural tear occurs at the fracture site and arachnoid herniates into the defect [68]. This prevents

Fig. 4. Depressed skull fracture with underlying contusion. (A) Lateral scout CT tomogram (B) demonstrates depressed comminuted right parietal skull fracture with underlying contusion.

osteoblasts from migrating across the fracture line, with subsequent impaired healing. CSF pulsations lead to further herniation of the arachnoid into the defect. CSF becomes entrapped within the defect secondary to fibrosis and adhesions. Pathologically, the wall of the cyst consists of a fibrocollagenous membrane. Finally, slow erosion of the skull occurs at the site of the growing cyst. To recognize this complication, follow-

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up imaging is recommended in all young children with diastatic skull fractures. Risk factors for the development of a leptomeningeal cyst include age less than three and fracture diastasis of 4 mm or greater [63]. On plain films, leptomeningeal cysts appear as oval areas of bone erosion. The margins of the lesion are smooth and the inner table is eroded more than the outer table. The edges of the defect are elevated and thickened. CT (Fig. 5) and MRI confirm the skull defect and demonstrate the cyst, which parallels CSF in attenuation and signal characteristics [69]. In some cases, there is

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herniation of brain tissue at the defect. Underlying encephalomalacia and ipsilateral hemiatrophy may also occur. Early diagnosis of these lesions is important because brain damage is progressive. Surgery is the treatment of choice. Since the main factor responsible for leptomeningeal cyst formation is a dural tear, some authors recommend US at the initial time of injury in patients thought to be at risk for this complication. US in experienced hands can be used to diagnose a dural tear [70]. Normally, the dura appears as an echogenic line

Fig. 5. Leptomeningeal cyst. (A) Axial CT image (B) demonstrates comminuted left parietal fracture with contusion. (C) Lateral CT scout tomogram 2 months later demonstrates fracture with leptomeningeal cyst (white arrow). (D) Axial CT image (E) demonstrates left parietal encephalomalacia and bulging of intracranial contents through bony defect.

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shape, and does not cross suture lines. There may be an associated fracture (Fig. 6). The appearance on MR

Fig. 5 (continued).

on ultrasonography and is not visualized if there is a defect. The fracture itself is used as an acoustic window. Color Doppler sonography has been helpful for demonstrating arterial flow through the defect [71].

Extraaxial hemorrhage Epidural hematoma Epidural hematomas (EDH) occur between the inner table of the skull and the outer layer of the dura. Epidural hematomas are less common in infants and young children than in adults and are seen in 1 to 3% of children with head trauma [72,73]. In children, the dura is more firmly adherent to the inner table of the skull and the groove for the middle meningeal artery is shallow, allowing for more mobility of the vessel. For these reasons EDH is less common, and when it does occur, is more often from venous bleeding than arterial. The source of the blood can be in the diploe or the dura [49]. Skull fractures are less commonly associated with EDH in children because of the increased plasticity of the child’s skull. Since the bleeding is often venous, these hematomas evolve slowly, and the clinical presentation of acute EDH in the young child can be less dramatic than in an adult. Often, there is an asymptomatic interval followed by rapid deterioration. Aggressive early imaging is recommended when this injury is suspected. On imaging, EDH appears identical to the findings seen in adults. The EDH appears hyperdense on CT, has a biconvex

Fig. 6. Epidural hematoma in an 11-month-old infant who fell from a walker. (A) Axial CT image (B) demonstrates epidural hematoma, midline shift to right, mass effect on left lateral ventricle, and associated nondisplaced left parietal skull fracture.

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varies with the age of the hematoma, with acute hematomas appearing isointense on T1-weighted images and dark on T2-weighted images. There have been recently described cases of epidural hematomas decompressing into the subgaleal space through a skull fracture. These were shown to resolve as the hematoma redistributed into the subgaleal space [74].

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subarachnoid spaces associated with macrocephaly, thought to be secondary to immature CSF absorption at the level of the arachnoid villi (Fig. 7). Often vessels can be seen traversing the extra-axial space, confirming the subarachnoid location. This condition often resolves by age two without sequelae [76,77]. These patients may be predisposed to extra-axial hemorrhage after minor head trauma [78] (Fig. 8).

Subdural hematoma Subarachnoid hemorrhage Subdural hematomas are collections of blood located between the inner dural layer and the arachnoid. These may occur following accidental trauma, but are also associated with child abuse. Other predisposing factors include prematurity and blood dyscrasias. These collections are more common in infants and younger children than in adolescents. In infants, the cortical veins are more easily torn, because of the plasticity of the skull, the softness of the underlying unmyelinated brain, and the expanded extraaxial space, which places more tension on the bridging cortical veins when trauma occurs. Unlike in adults, where the SDH is often unilateral, SDH in children is bilateral in up to 80% of cases [51]. In addition, interhemispheric SDH is more common in children than in adults. Often SDH in the pediatric age group is extensive, with involvement of the temporal, frontal and parietal regions. This results from the lack of adhesions in the subdural space that are present in the adult. Imaging findings in children with subdural hematoma are similar to those in adults. In the acute phase (< 3 days) a crescentic shaped, high-attenuation extraaxial collection is visualized on CT. In 1 to 3 weeks, the hematoma gradually becomes isodense relative to the adjacent brain. Gradually, after two to three weeks the SDH decreases to an attenuation that is similar to CSF. On MR, the SDH appearance will vary depending on the age of the blood products within the hematoma. The evolution of blood products in an extraxial collection is similar to that of an intraparenchymal hematoma, but tends to occur over a longer time span because of differences in oxygen tension in the subdural space [12]. In addition, unlike parenchymal hematomas, ferritin and hemosiderin are not deposited in the wall of a chronic SDH [75]. This is because the blood-brain barrier inhibits resorption of the blood products in intraparenchymal hematomas. Chronic SDH can develop outer and inner membranes that enhance following contrast medium administration. Varying ages of blood products may appear as fluid-fluid levels. In infants, a mimic of chronic subdural hematoma is benign external hydrocephalus. These are prominent

Subarachnoid hemorrhages frequently accompany head injury and the imaging findings are identical to adults. The sylvian fissure and interpeduncular cistern are common sites for SAH to be visualized on imaging. CT is the imaging modality of choice for detecting acute SAH. If MRI is being performed, FLAIR sequences are more sensitive in detecting SAH than other routine MR sequences. SAH will appear as high signal within the sulci, whereas normal cerebrospinal fluid will be low in signal intensity [15 – 17]. Intraventricular hemorrhage Intraventricular hemorrhage may be associated with parenchymal hematomas, contusions, and diffuse axonal injury (DAI). DAI involving the corpus callosum is often associated with intraventricular hemorrhage from rotational forces that lead to tearing of the subependymal veins on the ventral surface of the corpus callosum [79].

Intraaxial hemorrhage Parenchymal injuries encountered during childhood include contusions, DAI, and intracerebral hematomas. Cortical contusions occur when there is direct impact of the brain against bone during a deceleration force and represent  45% of intra-axial injuries [80]. Contusions often occur in the inferior frontal lobes and anterior temporal lobes, where the adjacent inner table of the skull is irregular. Because the inner table of the skull is relatively smooth in children compared with adults, contusions are less common in them. Contusions can be adjacent to the point of impact (coup) or on the opposite side of the head (contracoup). They involve the superficial gray matter and usually spare the underlying subcortical white matter unless large. On CT, contusions appear as illdefined regions of high attenuation in characteristic locations, namely the anterior inferior frontal lobe

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Fig. 7. External hydrocephalus. (A) Sagittal T1 MR image demonstrates prominent subarachnoid spaces with displacement of vessels away from cortex. (B) Axial proton density and (C) T2 MR images demonstrate prominent subarachnoid spaces that follow CSF on all sequences.

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Fig. 8. External hydrocephalus with subdural hematoma. (A) Sagittal T1 MR image demonstrates prominent subarachnoid spaces and hyperintense left subdural hematoma. (B) Axial proton density MR image demonstrates hyperintense left subdural hematoma and enlarged subarachnoid spaces. (C) Axial T2 MR image demonstrates left subdural hematoma hypointense to CSF.

and the anterior temporal lobe. MRI is more sensitive than CT in detecting nonhemorrhagic contusions. If a trauma patient is being evaluated by MRI, gradient echo images are an important sequence also, because of increased sensitivity for detecting hemorrhage [13,14].

Intracerebral hemorrhages may be difficult to distinguish from hemorrhagic contusions or diffuse axonal injury. They are commonly seen in the frontotemporal white matter or basal ganglia [73]. On MRI, the appearance of the intraparenchymal hemorrhage varies with the age of the lesion. Acute hema-

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tomas will appear isointense to the brain on T1weighted images and hypointense on T2-weighted images, because of the presence of deoxyhemoglobin

in the red blood cells. With time, deoxyhemoglobin is converted to intracellular methemoglobin and the hematoma will appear bright on T1-weighted images

Fig. 9. Diffuse axonal injury. A 15-year-old boy with traumatic brain injury 2 months prior. (A,B) Axial T2 MR images demonstrate bilateral chronic subdural hematomas and abnormal hyperintense signal in the periventricular white matter and left midbrain. (C,D) Axial gradient echo images demonstrate numerous hypointense lesions in the left cerebral peduncle, bilateral frontal, parietal and temporal lobe white matter, and splenium of corpus callosum.

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and dark on T2-weighted images. High signal develops later on the T2-weighted images as the red blood cells lyse and the methemoglobin becomes extracellular. Chronic hemorrhage appears hypointense on T1-weighted images and T2-weighted images as hemosiderin and ferritin accumulate in macrophages. Subcortical gray matter injury is relatively uncommon. It consists of petechial hemorrhages in the thalami, basal ganglia, and regions around the third ventricle and likely occurs because of injury to the small perforating blood vessels [80]. Diffuse axonal injury follows severe head injury when there is sudden acceleration and deceleration combined with rotational forces. It is one of the most common types of severe head injury [73]. With this mechanism, portions of the brain move relatively slowly compared to adjacent areas, which leads to a shearing stress with subsequent axonal injury. This pattern of injury involves the subcortical white matter, the corpus callosum, the brainstem, and the internal capsule. Pathologically, there is extensive damage, with multiple torn and retracted white matter tracts (retraction balls) and perivascular hemorrhage [81]. Compared to older children and adults, infants are more susceptible to this injury, because of their relatively large heads, weaker neck musculature, increased CSF spaces, and increased compliance of the calvarium [49]. It is most often associated with high-velocity motor vehicle accidents, but may also be seen in blunt trauma and nonaccidental trauma. CT in the setting of DAI may be normal or may only show small foci of high attenuation. These patients may have profound impairment of consciousness that suggests the diagnosis even with a near normal CT. MRI is more sensitive for the detection of DAI lesions that can be hemorrhagic or nonhemorrhagic [10,80] (Fig. 9). On gradient echo images, these lesions appear hypointense. They may be round or elliptical in shape, and parallel to the axonal tracts involved. Milder forms of DAI consist of lesions near the gray – white junction. More severe injury results in lesions in deeper structures within the brain, such as the centrum semiovale and corpus callosum, particularly the posterior body and splenium [79]. Severe DAI may affect the brain stem, including the dorsolateral midbrain, pons, and cerebellar peduncles. [82] As mentioned earlier, diffusion tensor imaging may be helpful in the evaluation the brain parenchyma DAI [23,26].

Sequelae of trauma Sequelae of traumatic injury may include vascular injury, diffuse cerebral edema, hydrocephalus,

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hypoxic-ischemic injury, developmental delay, posttraumatic seizures, cognitive deficits, encephalomalacia, infection, cranial nerve injury, and pituitary/ hypothalamic injury. Vascular injury, diffuse cerebral edema, and hydrocephalus will be discussed below. Vascular injury Vascular injuries that may occur in traumatic head injury are similar to those found in adults and include arterial dissections, venous occlusions or ruptures, and carotid-cavernous fistula. Dissections of the carotid artery or vertebral artery may occur as a result of penetrating or blunt trauma to the neck [83]. In children, carotid dissections may also result from falls when pencils or similar objects are in the mouth [84,85]. Carotid artery dissection may also be associated with fractures involving the skull base and extending into the carotid canal [86]. These vascular injuries have also been described in the setting of seemingly trivial traumatic forces, such as sudden flexion or extension of the neck [87]. In this situation, the dissection is often classified as being spontaneous, although usually a history of minor trauma or sudden neck movement can be elicited. In extracranial carotid dissection, the internal carotid artery (ICA) is often involved just distal to its bifurcation, with cephalad extension to the skull base. Intracranial carotid dissection may involve the supraclinoid ICA. In nonpenetrating trauma, vertebral artery dissection usually occurs at the C1 – C2 level or at the site of cervical spine fractures [88]. Cerebral infarction demonstrated on conventional or diffusion MR images results from emboli or arterial occlusion. On MRI, narrowing or occlusion of the vessel may be present, characterized by narrowing of the vascular flow void or abnormal signal within the lumen of the vessel (Fig. 10). In addition, intramural hemorrhage may be seen in the wall of the vessel, causing a periarterial collar of abnormal signal that may be asymmetric on one side of the lumen [89,90]. The intramural hematoma may be better demonstrated using T1-weighted imaging with fat saturation through the neck and skull base of the affected vessel [91]. MRA may also demonstrate lumen narrowing, vessel occlusion, or pseudoaneurysm characterized by bright signal projecting beyond the lumen of the artery [92]. Conventional angiography, which may demonstrate stenosis, occlusion, or pseudoaneurysm formation, may serve as an adjunct to MRA. Carotid-cavernous fistulas may present with pulsatile exopthalmos or cranial nerve palsies. Conventional angiography is the imaging modality of choice for diagnosis, because it demonstrates the fistula

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Fig. 10. Carotid dissection. A 9-year-old girl who suffered laceration of her right oropharynx when a handlebar entered her mouth as she fell from a bicycle. (A) Axial CT image demonstrates right MCA sign with increased attenuation in the right middle cerebral artery (white arrow) and (B) infarct in the right posterior basal ganglia. (C) Diffusion MR image demonstrates restricted diffusion in right subinsular region, basal ganglia, and posterior limb of internal capsule. (D) 2D-time of flight (TOF) MRA image of the neck and (E) 3D-TOF MRA image of the circle of Willis demonstrate occlusion of RICA from carotid dissection.

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and blood flow, and restricted diffusion in brain regions with neuronal injury [51]. As in adults, transtentorial herniation and subfalcine herniation may occur in children from increased ICP. Transtentorial herniation may be complicated by posterior cerebral infarcts secondary to compression of the posterior cerebral artery by the free edge of the tentorium in the ambient cistern. The anterior cerebral artery may be similarly compressed during subfalcine herniation. Hydrocephalus Hydrocephalus frequently develops after intracranial injury, and may be related to adhesions forming after SAH that likely block CSF absorption at the arachnoid villi. It may not be possible to differentiate post-traumatic hydrocephalus from cerebral atrophy, which may also occur following trauma [96,97]. Correlation with head circumference may aid in distinguishing the two entities in young children.

Fig. 10 (continued).

between the cavernous ICA and cavernous sinus. CT findings include prominence of the cavernous sinus and superior opthalmic vein on the affected side. Diffuse cerebral edema Post-traumatic cerebral swelling is more common in the pediatric population than in adults. Loss of autoregulation of blood flow to the brain following injury in children may lead to hyperemic cerebral swelling [93 – 95]. Because children also have a lower mean arterial pressure, this can lead to decreased blood flow to the brain as swelling becomes more severe. Cerebral swelling may also occur in the setting of DAI. Accurate diagnosis is important to begin therapy for treatment of increased intracranial pressure (ICP). On imaging, diffuse cerebral swelling is usually manifested 24 to 48 hours following the initial traumatic event. CT and MRI demonstrate compressed lateral ventricles and sulci, loss of grey/ white differentiation, and effacement of the basilar cisterns. Acutely, it may not be possible to distinguish cerebral edema related to increased blood flow from that secondary to DAI. Follow-up imaging should demonstrate atrophy in children with neuronal damage. Diffusion imaging may also be useful in distinguishing these two forms of cerebral edema. Diffusion imaging demonstrates increased diffusion in areas of the brain with increased intersititial edema

Nonaccidental head injury The incidence of child abuse in the United States is estimated to be 42 per one thousand children. The Third National Incidence Study of Child Abuse and Neglect estimated that 2,815,600 children were victims of child abuse [98]. The number of children seriously harmed by abuse or neglect was approximately 569,000 in 1993. These estimates are likely low, for it is generally accepted that many cases of child abuse go unreported [46]. Head trauma is the leading cause of morbidity and mortality in abused children less than two years old [5,46,99]. The incidence is even greater in infants that are less than one year old. Over 95% of life-threatening head injuries in infants are the result of abuse. On clinical followup, the majority of infants who are victims of abuse have significant neurologic impairment. Child abuse is a known cause of mental retardation, developmental delay, behavorial disturbances, learning disabilities, and cerebral palsy. Abused children are also at increased risk for the development of depression and anxiety disorders. The clinical presentation in infants who have sustained nonaccidental head injury (NAHI) includes decreased consciousness, irritability, apnea, respiratory difficulty, and seizures. Caretakers may describe a history of lethargy or decreased appetite. Nonaccidental injury should be suspected in the infant or young child who presents with no history of injury; with a discrepancy between the explanation

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and nature of lesions; with injuries of different ages or multiple injuries; with associated retinal hemorrhages; or with a change or inconsistency in the history, delay in medical care, repeated injuries, or evidence of overall poor care [6,46].

Mechanisms associated with abuse that may lead to head injury include direct impact, shaking, asphyxia, or nutritional deprivation. Whiplash or shaking is a specific and well known mechanism of injury that was initially described by Guthkelch and later defined more

Fig. 11. Nonaccidental head injury in a 3-month-old infant shaken by the father. (A,B) Axial CT images demonstrate interhemispheric (black arrow) and right convexity subdural hematomas and diffuse cerebral edema. (C) Axial T2 MR image demonstrates mild loss of cortical ribbon in the parieto-occipital regions. (D) Axial MR diffusion image and apparent diffusion coefficient (ADC) image (E) demonstrate restricted diffusion in the parietooccipital regions bilaterally, consistent with infarction.

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Fig. 11 (continued).

specifically by Caffey [100 – 102]. It occurs when an infant is held by the caretaker, usually with two hands, and violently shaken. A wide variety of head injuries associated with child abuse may be demonstrated on CT, MRI, and skull radiographs. Some of these injuries are specific and others overlap with injuries sustained during accidental trauma. The injuries specific for child abuse will be discussed in detail here.

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regarded as one of the most characteristic CNS lesions encountered in nonaccidental head trauma [106]. In patients under the age of two, subdural hematomas are more strongly associated with inflicted head injury than with accidental trauma [107,108]. SDH is much more common than EDH in the setting of child abuse. Angular rotation of the brain within the calvarium is the mechanism of injury that has been widely accepted as the cause of subdural hematoma in whiplash-shaking injury. These hematomas most often occur posteriorly along the interhemispheric fissure [109] or in the parietooccipital region (Fig. 11A,B). Anterior interhemispheric and SDH along the tentorium may also occur. An interhemispheric hematoma appears as increased attenuation along the falx on CT imaging. Features which aid in distinguishing these lesions from the normally hyperdense falx include asymmetric thickening of the falx, and collections that are flat medially and convex laterally. In patients with an interhemispheric hematoma, MRI often shows that the hematoma extends laterally along the convexity. Large acute SDH is easily demonstrated on CT, because the hematoma appears hyperdense. It is important to recognize that in infants and children the hyperacute/acute SDH appears as a mixed high

Skull fractures The incidence of skull fractures is approximately 45% in known child abuse cases [99]. Nonaccidental skull fractures can be linear, depressed, diastatic, or complex. The parietal bone and occipital bone are most commonly involved [103]. In a comparison of fractures from abuse with fractures from accidental trauma, child abuse may be indicated by multiple or complex fractures, bilateral fractures, and fractures that cross suture lines or involve more than one bone [104,105]. Conventional radiographs are still considered the gold standard for the diagnosis of skull fractures in children; therefore skull films should still be routinely obtained as part of the radiographic skeletal survey in suspected child abuse cases. Subdural hematoma Since Caffey’s original description of SDH in the setting of child abuse in 1946, SDH has come to be

Fig. 12. Shaken baby with subdural hematomas of different ages. Axial FLAIR MR image demonstrates bilateral subdural hematomas of different signal intensities, which was confirmed on gradient echo imaging (not shown).

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indicate injuries of different ages [46] (Fig. 12). On CT, chronic SDH in the setting of nonaccidental trauma, is demonstrated by bifrontal collections that are isodense to CSF. MRI is more sensitive in the detection of small hematomas and nonacute hematomas because of its multiplanar capabilities and lack of artifact from the adjacent calvarium. MRI and ultrasound with color Doppler (Fig. 13) are superior to CT in distinguishing chronic SDH from prominent subarachnoid spaces as seen in benign external hydrocephalus. Subarachnoid hemorrhage Subarachnoid hemorrhages can be seen in patients who were shaken [101]. In the context of nonaccidental trauma, the most common location for SAH is along the sulci focally within the cerebral hemispheres or along the falx [46]. The hemorrhages along the falx can usually be distinguished from SDH by noting extension into the adjacent sulci. As previously mentioned, CT is the imaging modality of choice for SAH, although FLAIR imaging may be helpful for their detection on MR images.

Fig. 13. Ultrasound in a shaken infant with prominent extraaxial spaces on CT. (A) Coronal ultrasound images without and (B) with color Doppler are helpful in distinguishing subdural collections from enlarged subarachnoid (a) spaces.

and low density collection on CT. The high-density portion of the hematoma represents clotted blood and the low attenuation portion, unclotted blood. Reasons for this appearance may include active hemorrhaging, or an arachnoid tear with CSF extrusion into the subdural space. Until recently these SDH were presumed to be chronic with acute rebleeding, a pattern frequently seen in adults [110]. Subdural collections may have areas of different density and intensity characteristics with levels, loculations, or septations on CT and MR that may

Fig. 14. A 9-month-old strangled and shaken infant. Axial CT image demonstrates large right cerebral hemisphere and left frontal infarct with right convexity subdural hematoma and mild mass effect on the right lateral ventricle.

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Fig. 15. Nonaccidental head injury in a 4-month-old infant shaken by the mother’s boyfriend. (A,B) Axial CT images demonstrate cerebral edema with ‘‘white cerebellar sign’’ and interhemispheric (white arrow) and tentorial subdural hematoma. (C) Axial T2 MR image demonstrates loss of gray-white differentiation in parieto-occipital regions. (D) Axial MR diffusion and (E) ADC images demonstrate restricted diffusion in frontal and parieto-occipital regions.

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with NAHI [24] (Figs. 11 and 15). In the study of Suh et al, diffusion abnormalities were noted in 90% of children with NAHI, and were multifocal or involved multiple lobes in > 90% of those patients. These injuries involved the posterior aspects of the cerebral hemispheres and spared the anterior temporal lobes and frontobasal frontal lobes (see Figs. 11C – E, 15C – E). This pattern differed from the accidental trauma group, in which there were more white matter shearing injuries or injuries that were focal or unilateral, restricted to a vascular distribution, or associated with an overlying fracture. Cerebral edema

Fig. 15 (continued).

Intra-axial injuries Intra-axial injuries that can be seen in NAHI include contusions, hematomas, infarcts, DAI, and white matter shear injuries. The location and appearance of cortical contusion do not differ significantly from those seen in accidental trauma. Contusions tend to occur in the inferior frontal lobes and anterior temporal lobes. Although DAI and intraparenchymal hematoma may occur in NAHI, they are more often present in accidental head injury [111]. Cerebral infarction may occur secondary to numerous mechanisms, including shaking; however, when the mechanism of injury includes strangulation, it is likely secondary to occlusion of the carotid artery in the neck (Fig. 14). Smothering is also a known mechanism of injury in NAHI. It can lead to cerebral infarction and hypoxic-ischemic injury. Infarctions can also occur when cerebral swelling leads to transfalcine or transtentorial herniation that compresses the anterior or posterior cerebral arteries respectively. Cerebral infarction unrelated to strangulation is a complication in NAHI that is likely underestimated [112]. Diffusion imaging compared to conventional MRI, as previously mentioned, shows increased sensitivity in the early detection of infarct in children

Cerebral edema is an important injury that commonly occurs in the setting of NAHI. Cerebral edema may be diffuse or focal. Younger infants are more likely to develop diffuse cerebral edema in the setting of trauma than older children and adults. The exact cause and pathologic events leading to diffuse cerebral edema are poorly understood. In children, the brain often responds to injury with an increase in cerebral blood flow [93]. This posttraumatic cerebral hypertension often occurs within hours of the traumatic episode. Brain swelling may subsequently lead to decreased blood flow and hypoxic-ischemic injury can ensue. Tissue hypoxia leads to cytotoxic edema, because adenosine triphosphate (ATP) is needed in order to maintain the sodium potassium pump and cell membrane homeostasis. Apnea and hypotension occuring in the immediate postinjury period are also thought to be factors that contribute to hypoxia and the development of cerebral edema in the setting of severe inflicted head injury [112,113]. Early CT findings in cerebral edema include loss of the graywhite differentiation and decreased conspicuity of the CSF spaces. The ventricles also may appear small. Over time, diffuse low attenuation is visualized, with loss of the gray – white junction in both cerebral hemispheres. Often the cerebellum appears hyperdense relative to the rest of the brain. This has been called the ‘‘CT reversal sign’’ or the ‘‘white cerebellar sign’’ [99,114] (see Fig. 14A). The pathogenesis of this sign is not completely understood, but probably correlates with less edema in these regions. Infants with diffuse cerebral edema may subsequently develop border zone infarctions and cortical necrosis. The border zone infarctions occur most commonly between the anterior and middle cerebral arteries [112]. In addition, children with more focal cerebral swelling often demonstrated ipsilateral to an acute SDH may develop cortical necrosis in the involved hemisphere.

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Mimickers of child abuse Certain disorders have been recognized as diseases that may mimic child abuse. These include skeletal dysplasias such as osteogenesis imperfecta, which may present clinically with multiple long bone fractures or skull fractures. Other skeletal dysplasias with an increased tendency for fractures include Schmidlike metaphyseal chondrodysplasia and Menke’s disease (copper deficiency) [115]. The radiographic skeletal survey usually contributes to the diagnosis of these disorders. Accidental trauma in infants that may result in significant head trauma and may mimic child abuse includes injuries associated with walkers, stairway falls, and improper immobilization in car seats [46]. In these settings, obtaining a careful clinical history may help distinguish between accidental and nonaccidental trauma. Patients with coagulation disorders may develop repeated intracranial hemorrhages that may be confused with nonaccidental head injury. Other conditions that have raised the suspicion of child abuse include diffuse fulminant encephalitides and mitochondrial diseases that simulate diffuse hypoxia-ischemia [115], as well as metabolic diseases such as glutaric aciduria type 1 that have been associated with subdural hemorrhage [116].

Acknowledgments We would like to thank Virginia Grove for manuscript preparation and Donald Sucher for photography.

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