It is not usually possible to morphologically establish the existence of diffuse axonal injury in young children by demonstrating the classic pathologic changes of retraction bulbs, tissue tears, or intraparenchymal hemorrhages, although these findings may be demonstrated on occasion (33,54). Many of these children die too soon after injury for these pathologic changes to be established. For this reason, it is important to appreciate the markers of shearing injury to identify these cases as diffuse axonal injury.
Shearing injuries in young children are accompanied by various degrees of brain swelling. The swelling may not be apparent at autopsy in infants with brief survival intervals. Initially, CT may demonstrate progressive brain swelling and decreased ventricular size without other lesions being visible. The swelling is probably related both to direct injury to the axonal processes, causing localized edema, and to generalized swelling caused by changes in vascular permeability and autoregulation (5). Some investigators have postulated that hypoxia occurring when a child is shaken and becomes apneic accounts for the underlying cerebral insult and brain swelling (55). However, hypoxia does not explain why the injury is sometimes more unilateral than bilateral, the atrophy that develops in the brains in children who survive, or that the appearance of these brains at autopsy is not typical of hypoxic injury.
Children who sustain repetitive episodes of mild diffuse brain injury may gradually accumulate brain damage and acquire neurologic deficiencies (14). The exact timing of such mild additive injuries is not possible. There is no reason to believe that remote shearing lesions would make the brain more susceptible to new shearing injury. Mild injuries unaccompanied by loss of consciousness are not usually brought to medical attention. Some mild shearing injuries are manifested as seizures and clinically present difficult diagnostic problems, because there is no currently available method to demonstrate the underlying pathologic changes of the shear injury until more severe degrees of diffuse axonal damage have been sustained and can be recognized by the markers of subdural or subarachnoid hemorrhage on CT or MRI (38).
Rebleeding after trivial injury or spontaneous rebleeding from a preexisting chronic subdural hematoma should not be offered as an explanation for the presence of acute subdural blood lacking obvious demonstration of such an old subdural membrane (57). The pathogenesis of subdural bleeding has become better delineated after more than 20 years’ experience with CT. The classic multilayered chronic subdural hematoma is currently considered a unique type of hemorrhage for several reasons. A chronic subdural hematoma very rarely follows severe head injury in a previously normal person, in whom an acute subdural hemorrhage transforms by aging to become a chronic subdural membrane. Instead, the blood of the acute subdural hemorrhage in these head injuries is readily resolved or rapidly organized (58–60). The resorption of subdural blood tends to be even more rapid and more complete in children than in adults (19). The development of the classic multilayered chronic subdural hematoma results from venous bleeding under low pressure and requires the potential for the subdural space to enlarge without a significant increase in pressure. The factors that promote such a development within a low-pressure intracranial space exist only in specific categories of people, such as those with brain atrophy (i.e., the elderly and those with alcoholism), those with hydrocephalus who have been treated by placement of a ventricular shunt, or those with traumatic encephalomalacia (59). In children with glutaric aciduria type 1, frontotemporal atrophy develops, and occasionally subdural hemorrhage without trauma develops on that basis (61). Minor trauma in these specific categories of patients may result in tearing of bridging veins and small amounts of subdural hemorrhage, which induces an ingrowth of granulation tissue from the dura. This granulation tissue contains fragile capillaries, which may produce microbleeds leading to enlargement of the hematoma. The further evolution of these hematomas is determined mostly by the nature of the vascular neomembrane formed in these patients. The expansion of these hematomas also appears to be related to the excessive activation of both the clotting and the fibrinolytic systems in the subdural fluid (62–64). A young child whose subdural hemorrhage subsequently organizes into a membrane composed of large vascular channels at risk for rebleeding would have been symptomatic before the time of rebleeding, because there would have been a preexisting brain abnormality. The signs and symptoms that would be expected before rebleeding include seizures, macrocephaly, anorexia, lethargy, headache, and apnea (60).
About 20% to 30% of asymptomatic neonates have small amounts of subarachnoid and subdural hemorrhage during delivery. The resolution of this blood may result in the presence of small numbers of dural macrophages containing hemosiderin and, sometimes, small fibrous patches consisting of a few layers of granulation tissue on the dura. These patches of thin membrane or scattered macrophages are not at risk of rebleeding with trivial trauma. Proof of rebleeding of a chronic subdural membrane should be based on the demonstration of a chronic subdural membrane that is grossly evident at autopsy, followed by microscopic confirmation of the vascularized membrane, and should not be based solely on the microscopic finding of fragments of fibrous tissue or a few macrophages containing hemosiderin.
The dura is a tough, fibrous, bilayered membrane overlying the arachnoid. It consists of an inner layer (menigeal) and an outer layer (periosteal). The periosteal layer serves as the periosteum of the inner table of the skull. The dura of young children, particularly along the basilar skull sutures, is a very cellular structure, which contains growing fibrous tissue along with numerous hematopoietic cells, including macrophages, many of which normally contain hemosiderin. The appearance of the normal young dura may be misinterpreted as having a thin chronic subdural membrane by microscopists who are not familiar with looking at these young duras, who may not be able to tell the inner from the outer dural surface, and who may incorrectly believe a chronic membrane to be the cause of acute subdural hemorrhage.
It is essential that a meticulous autopsy examination be performed in all cases of possible injury to children. When subdural and/or subarachnoid hemorrhage is found at autopsy, the brain must be thoroughly examined to exclude the possibility of other causes of bleeding in these spaces. Although berry aneurysms are uncommon in young children, they may occur. Vascular malformations may also occur in young children and cause hemorrhage in intracerebral and intracerebellar subarachnoid and subdural areas. The distribution of bleeding in aneurysms and arteriovenous malformations is unlikely to resemble that of head injury, but these malformations need to be excluded by careful examination of the brain (72,73).
Anatomic and developmental differences of the brain and skull of children under the age 4 or 5 years make the head injuries and mechanisms of injury that affect these children different in certain respects from those occurring after that age. Inflicted head injuries in these young children usually create shearing injuries of the brain and blood vessels, resulting in diffuse axonal injury and subdural, subarachnoid, and retinal hemorrhages. The pathologic findings of subdural and subarachnoid hemorrhages and very, frequently, retinal hemorrhages are the most common findings by which these rotational head injuries in young children are identified at autopsy. Recognition of the underlying mechanism of the rotational brain or shearing injury is important to an understanding of the clinical course of these children, particularly with respect to the decrease in the level of consciousness and respiratory distress demonstrated after injury.
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