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Inflicted Childhood Neurotrauma (The Shaken Baby Syndrome): Ophthalmic Findings
Brian J. Forbes, PhD, MD · Cindy W. Christian, MD · Alexander R. Judkins, MD · Marino Saveri, BS
Half of infant homicides occur during the first 4 months of life1,2 and 80% of infant homicides are thought to represent infant child abuse. More than three children die each day in the United States as a result of child abuse. The majority of these deaths are caused by inflicted neurotrauma, which results from violent, nonaccidental shaking or blunt impact to the head, or both. Historically, the injuries resulting from repetitive unrestrained head and neck movements from shaking were termed the whiplash shaken infant syndrome, which currently is referred to as shaken baby syndrome.3 The term shaken baby syndrome has biomechanical implications that are difficult and controversial. Although confessions are obtained in a minority of cases and the reliability of such confessions must be considered suspect, the prominence of repetitive violent shaking as the key element in generation of the shaken baby syndrome is supported.
A landmark study suggested that impact trauma in addition to shaking was required to generate the level of force required for an infant to sustain brain injury.4 The majority of infants with severe brain injury due to abuse have clinical or autopsy evidence of blunt impact trauma, and biomechanical data suggest that impact is necessary for injury. Ultimately, the contributions of shaking versus impact in the pathogenesis of this syndrome are debated; leading clinicians and researchers favor more generic terms for the injuries identified from inflicted head trauma. Some have suggested the syndrome be renamed the shaken impact syndrome while others have suggested inflicted traumatic brain injury or inflicted childhood neurotrauma. As inflicted childhood neurotrauma was the preferred term at a recent National Institutes of Health conference of leading investigators in the field, this term will be used throughout the course of this tutorial.
Inflicted Childhood Neurotrauma
Clinical findings in affected infants include subdural hemorrhage, hypoxic-ischemic brain injury, retinal hemorrhages, skeletal injuries, and cutaneous or other injuries. The frequency with which noncranial injuries are identified varies by age and presentation, and skeletal or cutaneous injuries are not necessary for diagnosis. Unlike most other forms of ocular trauma, minimal external ocular signs of injury are usually present with no evidence of direct blows to the eye. Skeletal fractures are found in 30% to 70% of injured children, and retinal hemorrhages are seen in approximately 80% of injured children.5-14
Victims of inflicted childhood neurotrauma are generally younger than 3 years of age, and the majority of victims are infants. The clinical presentation reflects the severity of the injury, and this ranges from mild lethargy or irritability to acute life-threatening events, unexplained seizures, or coma. Falls in childhood are the most common reason for emergency department visits and hospital admissions. The most common reasons for children eventually diagnosed with inflicted childhood neurotrauma presenting to a physician are outlined in Table 1.15
| Common Presentations of Children with Inflicted Childhood Neurotrauma |
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In a review of missed cases of inflicted childhood neurotrauma, viral gastroenteritis was the most common incorrect diagnosis made followed by unintentional injury. When physicians misdiagnose inflicted injury as either unintentional trauma or a medical disease, approximately 25% of infants sustain further injury before the correct diagnosis is made. Under-diagnosis and over-diagnosis have unacceptable consequences for the children and families.
Approximately one third of injured infants are misdiagnosed at the time of initial presentation, have mild injuries, or live in nonminority, two-parent households.16 Victims of inflicted childhood neurotrauma are younger (mean 12.8 months versus 27.5 months), are more likely to have history of medical problems (53% versus 14.1%), and are seven times more likely to be ex-preemies (2.2% versus 0.07%) than children with accidental neurotrauma.17,18
In an effort to improve early identification of abused infants, fundoscopy to look for retinal hemorrhages has been advocated in the hospital setting to evaluate infants who
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A detailed eye examination is necessary to completely assess the presence and extent of intraocular injury in this syndrome and to differentiate it from other medical problems.
In 2001, an estimated 903,000 children were abused or neglected. Common characteristics of these children and what type of abuse occurred are outlined in Slide 1, Slide 2, Slide 3, and Slide 4.21 The perpetrators in criminal cases of abusive head trauma are outlined in Slide 4.22
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Autopsy and in vivo studies of the acute ocular findings in infants and toddlers younger than 3 years with nonaccidental head injury from inflicted childhood neurotrauma have described a consistent clinical picture. Characteristic ophthalmic findings include intraocular hemorrhage with a reported frequency of 50% to 100% with most papers reporting approximately 80%.6-14 Retinal hemorrhage occurs at all levels of the retina, including blot, flame-shaped and preretinal hemorrhage, and vitreous hemorrhage. Retinal hemorrhages can be few in number, exclusively intraretinal, and confined to the posterior pole. However, retinal hemorrhages are often too numerous to count, present at all layers, and extend to the ora serrata (Slide 5). Dense preretinal or
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Retinoschisis may occur, most often in the macular area but also peripherally. Through an ophthalmoscope, there is a dense central hemorrhage surrounded by a pale, elevated retinal fold in a circular shape. These lesions, seen histopathologically and clinically, have also been called hemorrhagic macula cysts and perimacular circular folds,25-28 and have a unique and characteristic appearance seen rarely in other types of head trauma.26 Macular retinoschisis with or without perimacular folds has been well-documented clinically, at postmortem examination, and by electroretinography as a distinctive finding that has not been reported due to any other cause in children younger than 5 years old.28
In contrast to the dramatic and relatively specific acute findings, late changes associated with inflicted childhood neurotrauma are neither consistent nor specific to inflicted childhood neurotrauma. Permanent visual impairment is frequent and central visual impairment related to the hypoxic ischemic brain injury from inflicted childhood neurotrauma
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The age of intraocular hemorrhage is difficult to assess clinically. It is assumed that the hemorrhages occur immediately at the time of injury. Some evolution including darkening of the retinal hemorrhages, organization of vitreous hemorrhages, and disappearance of the retinal hemorrhages occurs gradually over 2 to 4 weeks after the acute injury.
Prognostic Value of Ophthalmic Findings
In addition to the diagnostic significance of acute and late ophthalmic manifestations of inflicted childhood neurotrauma, several eye findings have prognostic significance. The extent of intraocular hemorrhage, presence of macular retinoschisis lesions, and presence of pupillary abnormalities have been correlated with fatal outcome and permanent neurologic impairment.28,31-36 The correlation between severity of ocular injury and neurologic outcome suggests a relationship between the brain injury and the ocular injury in inflicted childhood neurotrauma.
Differential Diagnosis of Retinal Hemorrhages in Infancy
Many systemic and ocular conditions may be associated with retinal hemorrhages, although the absence of supportive findings on ocular examination, physical examination, history, or laboratory evaluation makes their consideration equivocal. The incidence of retinal hemorrhages in children with the following conditions is known to be rare if at all possible and characterized by retinal hemorrhages that are few in number and confined to the posterior pole or with other recognizable unique features. Many of these entities are readily excluded from the differential diagnosis on the basis of history or physical examination.
Idiopathic retinal hemorrhages of newborns related to obstetrical and perinatal hemodynamic changes are frequent. Retinal hemorrhages secondary to normal birth have been extensively studied retrospectively and prospectively in tens of thousands of babies. From these data, researchers concluded that superficial retinal hemorrhages resolve by 1 week postpartum and deeper retinal hemorrhages resolve by 6 weeks. However, these small, relatively few nerve fiber layer hemorrhages are present for only the first 2 to 3 weeks of life and are distinguished by an exclusively posterior location and small size and number.37,38
Retinal hemorrhages also have been reported in association with severe accidental injury. Because many patients with nonaccidental injury present with a history of minor trauma, the threshold for retinal hemorrhage in accidental head trauma is important in consideration of the differential diagnosis. Multiple clinical and postmortem studies of eyes in patients with severe head injury suggest that the rate of retinal hemorrhage is less than 3% of instances.39-42 When retinal hemorrhages occur, they are confined to the posterior pole, few in number, and rarely subretinal. Even with severe head injury and severe brain injury sufficient for hospitalization, retinal hemorrhage is uncommon.36,39-42
Many infants with severe abusive head injury undergo cardiopulmonary resuscitation (CPR) including chest compressions and artificial ventilation. Retinal hemorrhages have rarely been seen after prolonged CPR, but never as numerously or extensively as seen in inflicted childhood neurotrauma.43-46 From case reports and prospective studies, it can be concluded that retinal hemorrhages only rarely occur from CPR and, when they do, they are few in number and confined to the posterior pole.
Purtscher’s retinopathy may occur after acute compression injuries to the thorax or head with characteristic manifestations including cotton wool spots, retinal hemorrhages, and retinal edema most commonly surrounding the optic disc. Purtscher’s retinopathy, which may be caused by mediated leukoembolization, is uncommon in inflicted childhood neurotrauma and the retinal hemorrhages in inflicted childhood neurotrauma do not appear to be correlated to the presence or absence of rib fractures, which are a sign of severe chest compression.47
Terson syndrome, which involves a retinal hemorrhage associated with subarachnoid hemorrhage, is well-recognized in adults although it appears to be uncommon in children. The lack of correlation between the side of involvement of the subarachnoid hemorrhage and ocular hemorrhage suggests that this is not a sufficient explanation for the retinal hemorrhages seen in inflicted childhood neurotrauma. Retinal hemorrhage has been found to be uncommon in children with intracranial hemorrhage of causes other than inflicted childhood neurotrauma and the retinal hemorrhages are not in a pattern or quantity consistently found in inflicted childhood neurotrauma.48,49 No evidence exists to support a link between immunizations and retinal hemorrhages in children.50,51
Coagulopathies and other bleeding disorders, including thrombocytopenia, anemia, leukemia, factor deficiencies, vitamin K deficiency, as well as metabolic diseases such as glutaric acidemia must be considered in the differential diagnosis of intraocular hemorrhage in infants. Generally, retinal hemorrhages related to hematologic abnormalities are less numerous and less extensive and do not extend peripherally in the retina. However, infants with bleeding disorders such as vitamin K deficiency have been incorrectly diagnosed as victims of abuse. Retinoschisis lesions have not been reported in these conditions. Basic hematologic evaluation, including complete blood count and coagulation studies, should be performed in all patients suspected of having inflicted childhood neurotrauma.52 Other ocular syndromes associated with retinal hemorrhage in childhood, including Norrie’s disease, Coats’ disease, persistent hyperplastic primary vitreous, hypotony retinopathy, cytomegalovirus retinitis, toxoplasmosis, and retinopathy of prematurity, are easily distinguished from nonaccidental head injury by the distinctive clinical appearance, as well as the clinical setting.
Pathophysiology of Retinal Hemorrhages
Theories as to the cause of retinal hemorrhages in inflicted childhood neurotrauma continue to be debated in the literature. One postulates that venous obstruction in the retina occurring from increased intracranial pressure due to cerebral edema and subdural hemorrhage is the source of retinal hemorrhages. Sudden increases in chest or head pressure may be contributing factors as well. Another theory postulates that traction of the vitreous on the retina during the acceleration and deceleration of shaking and impact causes circular retinal folds and hemorrhagic retinoschisis cavities, as well as smaller hemorrhages. Subdural hemorrhages in inflicted childhood neurotrauma are thought to be caused by the shearing of small vessels from inertial injury, most likely due to rapid acceleration/deceleration movements. The correlation between the severity of intraocular and intracranial injury and histopathological evidence suggests that similar inertial trauma may lead to shearing within the retina and at areas of the retina-vitreous attachment, leading to the fundoscopic lesions seen. The role of vitreous shaking in the generation of macular retinoschisis and perimacular folds has strong support in theory and in autopsy findings. The high frequency of hemorrhages at the vitreous base supports a theoretical link to vitreous traction. Orbital shaking injury, including disruption of autonomic supply to the retinal vessels, may play a role. Literature suggests that the shaking, with resultant shearing injury, is the primary factor in the generation of retinal hemorrhages seen in inflicted childhood neurotrauma. The optic atrophy often seen in survivors is best explained by direct optic nerve injury within the orbit. The role of vitreous traction and tissue shearing must be further explored. Postmortem orbital findings suggest a role for autonomic dysregulation and direct vessel damage that is yet to be explored. The compounding effects of anoxia/hypoxia, anemia, thrombocytopenia, mild coagulopathy, obstruction of retinal venous flow, or possible age-related anatomic variations in the retinal vasculature are not well understood. The adjunctive role of increased intracranial pressure needs further exploration. Although the role of vitamin C deficiency has been suggested exclusively in lay and legal literature, this has not been formally explored, and vitamin C deficiency is rare at this time. The minimal forces required to generate retinal hemorrhages and, more specifically, the reason why shaking seems to be unique in the generation of severe retinal hemorrhages, are unknown.
Controversies in the Diagnosis and Management
The most difficult and controversial aspect of the diagnosis of inflicted childhood neurotrauma is the reliability of this diagnostic designation. Physicians are rarely in the position to make a diagnosis with such profound significance to patients and their families. Ascertainment of child abuse is critical to prevent potentially fatal recurrence in victims. Extensive intraocular hemorrhage in young infants in the setting of acute brain injury and in the absence of a history of severe accidental trauma or underlying medical cause must be considered to be nonaccidental injury until proven otherwise.
The management of acute intraocular hemorrhages is primarily supportive. Gradual resolution is generally seen in 2 to 6 weeks, although dense preretinal and vitreous hemorrhage may persist much longer. With prolonged vitreous clouding, young children have a risk of deprivational amblyopia. In rare cases of prolonged vitreous opacity, surgical vitrectomy may be necessary to allow normal visual development. Survivors of inflicted childhood neurotrauma must be re-examined for amblyopia, refractive errors, and other late complications that require treatment.
The Role of the Ophthalmologist in the Diagnosis and Management
Inflicted childhood neurotrauma is a clinical pattern of nonaccidental injury including intracranial and intraocular hemorrhage, occurring in infants and toddlers younger than 3 years of age. Examination of the eye through undilated pupils with a direct ophthalmoscope is inadequate for complete evaluation for the eye findings of inflicted childhood neurotrauma. The primary role of the ophthalmologist in the care of young children is to provide complete evaluation of the intraocular hemorrhages. Ophthalmic consultation allows complete assessment and documentation of the eye findings frequently with retinal photography, an essential component of the diagnosis of inflicted childhood neurotrauma. In addition to establishing the diagnosis, examination provides prognostic information related to the eye findings. Ophthalmologists are able to coordinate long-term management of the frequent visual complications. In case of a fatal outcome, postmortem examination must include gross and histopathologic evaluation of the eyes and optic nerves. Finally, physicians who treat infants and children are mandated to report suspected child abuse to child welfare agencies for investigation, and ophthalmologists who encounter children with ophthalmic manifestations of abuse need to ensure that the proper steps are taken to protect patients from further harm. Ophthalmologists are in a crucial position to detect signs of child abuse.
