17.1  Introduction

In 1971, Guthkelch reported on 23 children, of whom 22 were less than 18 months old, presenting with various combinations of subdural hemorrhage, fractures, parenchymal brain injury, and retinal hemorrhages [1] (Fig. 17.1). He was the first to recognize the important role of repeated acceleration–deceleration forces – shaking – as a form of abusive injury. In 1972 and 1974, Caffey expanded on this topic and coined the term whiplash-shaken infant syndrome [2]. Both the authors recognized the frequent absence of external signs of trauma and the role of torn bridging vessels in the brain as the cause of the intracranial hemorrhage. With the advent of computerized tomography, the diagnosis of traumatic brain injury became easier to ascertain, but the basic definition of whiplash-shaken infant syndrome did not change.

Using autopsy evidence and a rudimentary dummy model, Duhaime and coworkers in 1987 suggested that blunt impact trauma might be a prerequisite to generate sufficient deceleration forces for the characteristic injuries to occur [3]. Although it has since been shown that shaking alone can be injurious, if not lethal, some authors still prefer to designate the clinical presentation as “shaken impact syndrome”particularly when there is clear evidence (e.g., skull fracture) of blunt

B.J. Forbes (*)

Department of Ophthalmology, The University of Pennsylvania School of Medicine, The Children’s Hospital of Philadelphia, 34 th and Civic Center Blvd, Philadelphia PA 19104, USA e-mail: forbesb@email.chop.edu

A.V. Levin

Department of Ophthalmology, Jefferson Medical College of

Thomas Jefferson University, 840 Walnut Street, Philadelphia,

PA 19107-5109, USA

Fig. 17.1  Photographs of the fundi of a victim of the Shaken Baby syndrome showing marked asymmetry in the degree of hemorrhaging present in up to 28% of such children. Subretinal, intraretinal, and preretinal hemorrhages are visible on the top fundus photo, while the bottom shows only an isolated retinal hemorrhage along the inferior arcade

impact. Evidence now also suggests that the rapid rise in gravitational forces brought on by an impact may be induced either by the impact against a soft surface, for example if the child is thrown down upon a mattress, or by the impact of the chin on the chest or the occiput of the upper back during shaking [4]. The relative contributions of shaking vs. impact in the pathogenesis of this syndrome are still debated leading some clinicians

and researchers to favor more generic terms such as abusive head injury, inflicted head trauma, inflicted traumatic brain injury, or inflicted childhood neurotrauma [5]. While the term shaken baby syndrome is prominent in the ophthalmic literature, and repetitive acceleration–deceleration appears to be a key factor in generating the characteristic injuries, the less descriptive and generally accepted term by experts in the field as of 2009, abusive head trauma (AHT), will be used throughout the course of this chapter.

Confessions are obtained in only 10–15% of cases and although the reliability of such confessions may be considered suspect, those perpetrators who do confess indicate the prominence of repetitive violent shaking as the key [6]. Over 97% of perpetrators who do confess relate that they were present when the patient became symptomatic. This suggests that in most cases, particularly those with more severe neurological manifestations, it is unlikely for the child to be asymptomatic for a lucid interval, for sufficient time to allow transfer of care. Victims of AHT are typically not physically battered, and show little external evidence of the trauma, and accompanying sexual assault is particularly uncommon.

Homicide is the leading cause of injury and death in infancy, and half of infant homicides occur during the first 4 months of life [7, 8]. Eighty percent of infant homicides are thought to be due to child abuse. Each day in the United States more than 3 children die as a result of abuse. The majority of these deaths are caused by AHT. Infants and young children are particularly vulnerable because of their relatively large head, weak cervical musculature, and immature, incompletely myelinated brain. In addition, the unfused sutures and relatively high volume of cerebrospinal fluid allow for greater movement of the brain within the cranial vault [9].

Characteristic brain injuries include subdural and/or subarachnoid hemorrhage, parenchymal brain contusion and shearing injury, cerebral edema, and hypoxiaischemia [10]. Skeletal injuries may include skull fracture, rib fractures induced as the perpetrator violently grasps and compresses the child’s thorax, and long bone injury, in particular, periosteal stripping and metaphyseal chip fractures if a child is grasped by a limb during the event [11]. Fractures are not required for diagnosis, and cutaneous injuries are usually absent even when the bones are broken. Retinal hemorrhages are a cardinal feature of AHT and are the most common ocular manifestation of child abuse [12–19].

Unlike most other forms of ocular trauma, there are usually minimal external ocular signs of the injury and usually no evidence of direct blows to the eye.

Although some believe that a single severe shake may be sufficient to cause significant injury, confessions of perpetrators implicate that the violent forces which results in AHT injuries or death are extreme and repetitive [20]. Even when single impact head injury rises to the level of a multistory fall or motor vehicle accident, the classic brain, skeletal, and ocular manifestations of AHT are usually not mimicked. The repetitive acceleration–deceleration mechanism of AHT is not seen in most forms of accidental trauma. The amount of violence and the nature of the action that is required to induce AHT are beyond that which any reasonable person would consider acceptable and in a range that even the most distraught person would recognize as injurious.

The clinical presentation reflects the severity of the injury, and ranges from mild lethargy or irritability to acute life-threatening events, unexplained seizures, coma, or death. Some children may even present with no symptoms, except perhaps an increasing head circumference due to chronic subdural effusions with or without retinal hemorrhages. In a review of missed cases of AHT, viral gastroenteritis was the most common incorrect diagnosis followed by accidental injury [21]. When physicians misdiagnose inflicted injury as either accidental trauma or a medical disease, approximately 25% of infants will sustain further injury before the correct diagnosis of abuse is eventually made [22]. The consequences of missing abuse are perhaps more dangerous to a child than incorrectly diagnosing abuse, though underdiagnosis and overdiagnosis have unacceptable consequences for both the children and families. Approximately, one third of injured infants are misdiagnosed at the time of initial presentation, especially those who are very young and have mild injuries, or live in Caucasian, two parent households [18]. There is also the suggestion that racial differences do exist in the evaluation and reporting of patients with fractures for child abuse, particularly in toddlers with accidental injuries [23]. The need for early recognition is underscored by the fact that 39–71% of victims of AHT have had a prior episode of abuse, neglect, or shaking [24]. In one study, 45% of children had brain atrophy at presentation suggesting prior episodes of brain injury that had gone undiagnosed [25]. In an effort to improve early identification of abused infants,

funduscopy to look for retinal hemorrhages is recommended for all infants who present with unexplained acute life-threatening events [26, 27].

Falls in childhood are the single most common form of trauma resulting in emergency department visits and hospital admissions [21]. A history of a fall is the most common story offered at presentation of children later diagnosed to be AHT victims. The modern medical literature regarding falls in childhood begins in the 1960s when investigators began analyzing falls from beds, cribs, changing tables, infant seats, tables, or strollers suggesting a prevalence rate of approximately 1.8 million falls annually [28, 29]. From 1975 through 2001, the overwhelming preponderance of literature indicated that short falls (less than six feet) very rarely result in serious or life-threatening head injuries. A retrospective review of U.S. Consumer Product Safety Commission National Clearing House Data uncovered only 18 deaths secondary to short playground falls from the more than 75,000 cases reviewed [30]. There were no infant deaths reported in the study. An even larger and comprehensive review calculated that the risk of death from a short fall is less than 0.5 per million [31].

17.2  Age of Victims

Infant victims are usually less than 3 years old with most victims being less than 1 year (mean 5–10 months)[32]. Long-term severity seems to be inversely correlated with the age of presentation [33]. There are several reports of victims up to at least 15 years and one reported case of an adult torture victim who sustained fatal shaking injuries including retinal hemorrhages although the eye findings were not fully detailed [34]. Victims of AHT are generally younger, more likely to have a history of medical problems, and seven times more likely to have been born prematurely than children with accidental neurotrauma [35].

17.3  Epidemiology of Abusive

Head Trauma

AHT is the most common type of child abuse resulting in death, although it represents only 2.9–4.9% of all cases referred to child abuse teams [24]. Assault

represents over half of all traumatic brain injury in the first year of life and 90% of brain injuries from 1 to 4 years of age [36]. The mortality rate of AHT based on the studies of more than ten patients is approximately 8–61% with most studies finding a rate of 14–25% [37]. While males are more often victims of AHT, not all studies agree and the proportions are equal for children who die. First-born children are also more likely to be victims (62–92%), although this may be a reflection, in part, of separation or imprisonment of perpetrators after the first incident [24]. Like all other forms of child abuse, no social class, religion, ethnicity, or culture are spared from AHT. Some studies have identified low socioeconomic class as a risk factor, while others have found that middle class families are more often affected or under reported [25].

17.4  Perpetrators

The most common perpetrators of AHT are biological fathers and biologically unrelated paramours of biological mothers [6]. Babysitters, females 4.4 times more than males, are the perpetrators in 4–20% of cases [6]. Biological mothers commit this crime in 5–12% of cases [6]. Males are more often perpetrators although the proportions are equal for male vs. female perpetrators of AHT homicide [38]. In approximately 25% of cases, the perpetrator remains unknown.

17.5  Brain Injury

The most common brain lesions are subarachnoid and/ or subdural hemorrhage and cerebral edema. Subdural hemorrhage is typically bilateral and often extends into the posterior interhemispheric fissure. The subdural hematomas may be thin and scant, often resulting in no significant mass effect. However, larger lesions are usually associated with serious brain injury that can be rapidly fatal and, in these cases, may be associated with mass effect, cerebral edema, ischemia, and herniation [39]. One cause of brain injury is diffuse axonal injury caused by stretching and shearing of neurons, with or without contributions from ischemia and the metabolic cascade involved in brain injury [40]. Although not required for diagnosis, localized traumatic axonal

injury in the area of the caudal brain stem/rostral cervical cord with or without hemorrhage around the chord, lends support to the concept that the whiplash action is of critical importance. One study of long-term survivors found at presentation the following incidence statistics­ for AHT victims: subarachnoid hemorrhage 31%, subdural hemorrhage 23%, intrahemispheric blood 15%, infarction 15%, parenchymal hemorrhage 8%, and parenchymal tears 8% [24]. These figures are at the low end of the reported values at presentation without regard to survival: 10–72, 10–80, 20–100, 25–50, 5–30, and 0–100% respectively [11, 24, 41].

A significant number of long-term survivors will experience neurological impairment, and in one study, only 28% of children had normal neurological examinations at discharge from the hospital [6]. In moderate length follow-up studies, 20–30% of survivors are neurologically normal, whereas long-term studies show that only 8–14% are neurologically normal [37, 38]. Early findings include quadriplegia, diplegia, and hemiplegia with or without severe mental retardation. With continued follow-up, other findings may become evident including microcephaly, late hemiparesis, developmental delay, or learning disabilities [42].

To assess brain injuries, CT scan remains the initial procedure of choice although MRI is helpful in dating the findings and often in visualizing findings that may be missed on CT. In up to 20% of cases, initial CT scan may be normal with abnormalities becoming apparent on repeat films taken within the first week. MRI is superior in detecting cervical cord injuries.

17.6  Skeletal Injuries

The incidence of skull fractures in AHT varies in the literature, from 9 to 57% [43]. The parietal and occipital bones are most often affected. In shaken babies, skull fractures may be linear, diastatic, depressed, single, or multiple. Accidental short falls in childhood can rarely result in simple linear fractures, but more complicated fractures are extremely uncommon [41]. Rib fractures are the most common type of bony injury seen in AHT, appearing in up to one half of cases with many children showing both old and new fractures [44]. Injuries seen in AHT, but rarely found in accidental injury include hemorrhagic stripping of the periosteum, multiple fractures, fractures of different ages,

corner or bucket handle fracture at the metaphyses of long bones, spinal fractures in nonmobile children, and nonsupracondylar fractures.

17.7  Acute Ophthalmic Findings

Autopsy and in vivo studies of the acute ocular findings in infants and children less than 3 years old with head injury from AHT have described a consistent clinical picture. Retinal hemorrhages are seen in 50–100% with most papers reporting approximately 85% [12–19]. The frequency of RH is the highest in autopsy cases and the lowest in children who become neurologically normal survivors. The eye findings of the two largest reported series are summarized in Table 17.1. Typically, the hemorrhages are present in both eyes, although asymmetry and unilaterality are

Table 17.1  Retinal hemorrhages in abusive head trauma [1, 2]

Morad et al. [14] (all clinical examinations, n = 75)

Kivlin et al. [19] (clinical examinations only, n = 96 except for total [row 1, n = 111])

NA not applicable; NR not reported; ILM internal limiting membrane

well recognized [12–19, 45]. In approximately two thirds of cases, retinal hemorrhage occurs at all levels of the retina, including dot/blot, flame-shaped, preretinal hemorrhage, and less commonly, subretinal and vitreous hemorrhage. Retinal hemorrhages can be few in number, exclusively intraretinal, and confined to the posterior pole, though in approximately two thirds of cases, the hemorrhages are too numerous to count and extend to the ora serrata. Dense preretinal or vitreous hemorrhages may obscure the underlying retinal hemorrhage. Retinal hemorrhage may occur in AHT withoutintracranialhemorrhageorwithnormalneuroimaging [46, 47].

The distribution of hemorrhages in the eye of an AHT victim has significant implications in terms of both diagnosis and pathophysiology. Gilliland has reported that peripheral retinal hemorrhages are indicative of repetitive acceleration–deceleration injury and such hemorrhages are statistically more common in abusive vs. accidental head injury [48]. She did not observe peripheral retina hemorrhages in the absence of central nervous system disease. As the vitreous is attached to the peripheral retina, the role of vitreo-ret- inal traction is evident.

The vitreous is also firmly attached to the macula in young children. Macular retinoschisis, and less commonly peripheral schisis, is a further evidence of the importance of acceleration–deceleration induced vit- reo-retinal traction. Both peripheral and macular traumatic retinoschisis may be associated with worse neurological injury and death [49] (Fig. 17.2). The lesion appears as a dense macular hemorrhage within the schisis cavity often with a meniscus demarcating the red blood cells below from the serum above. Most commonly, only the internal limiting membrane (ILM) and/or nerve fiber layer is pulled away by the vitreous and this has been demonstrated by electroretinogram and ultrasound. Deeper schisis and even focal macular detachment can also occur. The schisis cavity is usually surrounded by a hypopigmented or hemorrhagic circumlinear line or elevated retinal fold. These lesions have also been called “hemorrhagic macula cysts.” “Perimacular (or paramacular) circular folds” may be seen at the edge of the schisis. Histologically, one might also observe vitreous still attached at the edges of the lesion and depigmentation of the retinal pigment epithelium underlying the folds, and a similar finding has been reported on a live patient by Sturm et al. [50] and Gaynon et al. [51]. It is critical

a

b

Fig. 17.2  (a) A traumatic retinoschisis in a victim of Shaken Baby syndrome. Note the white circular paramacular fold that delineates the borders of the lesion. Blood is found beneath the internal limiting membrane with some extending through into the vitreous. (b) Another Shaken Baby syndrome victim shows histopathology of truamatic retinoschisis. Arrow indicates vitreous attached to the edge of the lesion. Note the increased width of the retina due to shearing of the layers as well as a focal retinal detachment

that the circumlinear edge abnormalities be recognized clinically as these distinguish retinoschisis from subhyaloid hemorrhage, particularly when only the ILM is elevated. Blood may break through the schisis wall into the subhyaloid space or vitreous obscuring the edge changes of a cavity, which may become apparent only when the blood resolves. The fold may be continuous for 360°, discontinuous, or represent just an arc. It may encompass just the macula or surround the entire posterior pole including the optic nerve. Schisis cavities over the blood vessels, usually representing only the elevation of the ILM, have less diagnostic significance and may be seen in many conditions. However, with perhaps the exception of two reported cases of fatal crush head injury [52, 53], traumatic macular retinoschisis in children less than 5 years has been observed only in AHT and therefore has great diagnostic significance. Crush head injury is a rare