Unusual eye injury related to abusive head trauma

Ophthalmological examination is an essential component in clinically diagnosing abusive head trauma (AHT). Typical of AHT injuries is retinal bleeding, with other parts of the eye sometimes also being affected. Visual impairment and blindness are long-term complications in this context. We present a case with unusual eye injuries after a diagnostically confirmed AHT. The ophthalmological findings on admission day showed a massive subhyaloid hemorrhage at the posterior pole and extensive flame-shaped intraretinal hemorrhages accented on the right side., A centrally localized vitreous hemorrhage appeared on both sides 3 weeks later, obscuring the optic disc and macula most probably due to a breakthrough of a sub-internal limiting membrane (ILM) hemorrhage into the vitreous cavity. Follow-up 4 weeks later revealed a dense and organized vitreous hemorrhage occupying the optic disc and macula so that a pars plana vitrectomy was performed on both eyes. The bilateral bleeding in different retinal layers, the vitreous hemorrhage and the proliferative vitreoretinal reaction (PVR) indicated massive damage caused by a significant acceleration-deceleration trauma. A two-phase vitreous hemorrhage in a child with AHT does not yet appear to have been described in the literature.


Introduction
An immediate ophthalmological examination is an indispensable element in medical evaluation of suspected abusive head trauma (AHT) in children under 2 years old [1] or 5 years old [2,3]. The main ophthalmological finding after child AHT is retinal hemorrhaging, which occurs in 50-100% of cases [4][5][6][7][8][9], whereby retinal hemorrhage severity is proportional to the severity of the neurological injury [10,11]. Retinal hemorrhages mostly occur in both eyes [9]. Patterns of retinal hemorrhages are diagnostically important, but they can be barely visible when preretinal or vitreous hemorrhages are simultaneously present [12]. Scientific consensus on the etiology of retinal hemorrhages in AHT is that repetitive acceleration-deceleration forces lead to vitreoretinal traction [4].
The damage caused by retinal hemorrhaging depends on how much the fovea is involved and is generally not the reason for blindness itself [13]. Nevertheless, visual impairment and blindness are present in long-term survivors of AHT [4], mostly caused by vitreous hemorrhage, retinal scarring or fibrosis [13].

Initial clinical findings
The 3-month-old infant was admitted to the emergency department by the rescue service due to a first afebrile seizure and breathing pauses. The parents reported fiddling (German: fäusteln), mouth movements and twisting of the eyes occurring out of sleep. Afterwards, the infant was no longer able to adequately react.
Inthe clinical admissionreport, the infant showed reduced general and proper nutritional condition. Fontanel tension was slightly above normal. The infant was hyperexcitable and showed shrill screaming and intermittent apathy with low spontaneous motor activity. Muscle tone was normal to increased. The skin colour was pale. Further clinical examination showed no abnormalities.
Due to suspected acute cerebral pressure, a brain computed tomography (CT) (. Fig. 1) was performed, which showed bilateral chronic subdural hematoma and a fresh parafalxine-accentuated subdural hematoma with a maximum width of 0.9 cm and different density values. Bilaterally a reduced delineable furrow relief was also found.
The ophthalmological findings on the day of admission showed a sluggish pupil reaction. There was a hesitant light reaction. The anterior segment of both eyes showed no irritation, with clearly refractive media. Ophthalmoscopy revealed massive subhyaloidal hemorrhages at the posterior pole and extensive flameshaped intraretinal hemorrhages accented on the right side.
Due to the strong suspicion of nonaccidental head trauma, radiographs of the upper arms, the spine and the whole legs were taken, in which there was no evidence of a fresh or older consolidated bone injury. Thorax and lower arms were not radiologically included.
A metabolic diagnosis to exclude glutaraciduria was inconspicuous. There were also no laboratory indications of a relevant coagulation disorder.

Forensic medical course
During a forensic medical examination 1 day after the suspected incident, only a 2 cm large, greenish fading hematoma on the right cheek was visible. Following the examination, further written forensic medical reports were prepared. One report covered two related question on whether the findings could have been caused by possible cramping or by a minor accident about 3 months before admission to the clinic; both questions were answered negatively. Another medical report was prepared on the question of whether there was mortal danger, which was answered positively.

Early clinical course
The clearly space-consuming character of the bleeding indicated an emergency hematoma evacuation. The neurosurgeons performed a minihole retraction on both sides, an extensive irrigation and subsequent drainage.
One day after the neurosurgical procedure, a discrete anisocoria appeared on the left side, larger than that on the right side, and a deviation of the gaze to the left side was observed. A cranial magnetic resonance imaging (cMRI) (. Fig. 2) was therefore performed. It showed a new delimitable cortical diffusion disturbance on the right occipital pole, most likely ischemic. The ophthalmological findings were stable.
Multiple ophthalmological checks were then performed. Since the pupil reaction to light was still as sluggish and hesitant as on admission day and there was no pupil reaction during the checks, there appeared to be no changes in the   Fig. 3) were absent so a cortical visual impairment was also discussed.

Later clinical course
A new, centrally localized vitreous haemorrhage appeared on both sides 3 weeks after hospital admission, obscuring the optic disc and macula most probably due to a breakthrough of sub-internal limiting membrane (ILM) hemorrhage into the vitreous cavity. The peripheral retina was covered with persistent intraretinal hemorrhages. Since the occipital cortical ischemia diagnosed by MRI initially led to the assumption of a mainly central visual disturbance, no therapeutic indication was given at the time.
Follow-up 4 weeks later revealed neither monocular nor binocular fixation and a pendular nystagmus with mixed pattern jerk waves. Pupils were still in moderate mydriasis and neither direct nor indirect light reaction was detectable. Ophthalmoscopy revealed a dense and organized vitreous hemorrhage occupying the optic disc and macula. The peripheral retina was attached with resolving intraretinal haemorrhages. An interdisciplinary team decided to promptly perform a pars plana vitrectomy to remove the hemorrhage obstructing vision and avoid deprivation amblyopia. A 23gauge pars plana vitrectomy was per-formed first on the right eye (. Figs. 4 and 5) and soon after on the left eye. During surgery, epiretinal membranes were found on both sides as a sign of proliferative vitreoretinal reaction (PVR), which indicated a massive damage to the retinal barrier. Subsequently, the left eye developed aggressive proliferative vitreoretinopathy with retinal detachment, so that further retinal surgery became necessary. In the right eye, repeated pars plana vitrectomyhad tobe performed due to postoperative hemorrhage and PVR.
Due to a relocation, further operations were performed at a different eye centre. Due to increasing lens opacity, a pars plana lensectomy without implantation of an alloplastic lens was necessary on the left eye. Ultimately a sulcus-fixed posterior chamber lens was implanted in the left eye.
The last examination was performed at the age of 21 months. No image fixation or reaction to visual stimuli could be detected. There was a horizontal pendular nystagmus of very variable amplitude and an anisocoria larger on the right than on the left pupil. Light reaction was neither directly nor indirectly triggerable. Retinal findings were described as stable.

Legal course
During the criminal proceedings at court, a forensic medical expert was heard on the question of the origin of the injury. In the course of the proceedings, a minor accident was indicated as an alternative cause, but this did not provide a plausible explanation for the injuries.
Only the child's mother could be considered a suspect, as she was a single parent and stated that the child had not been cared for by others. She was initially charged on suspicion of grievous bodily harm, then, in the course of the investigation, she was charged with grievous bodily harm ( §226 Strafgesetzbuch, StGB, German Penal Code). The trial took place first at the local court, later at the regional court, as it was established during the first main hearing at the local court that a manslaughter conviction would also be possible. In the main hearing, the accused did not comment on the substance of the case; only in the course of previous investigations had she repeatedly stated that she had not shaken the child.
On the basis of the evidence, not least due to several medical and forensic expert opinions, she was sentenced to 3 years and 6 months for aggravated bodily harm in the commission of a crime involving dangerous bodily injury. A petition for review was dismissed as inadmissible.

Discussion
The present case is an example of the course of an unusually pronounced ophthalmological involvement in a case of AHT. When the infant was first presented at the eye clinic, both eyes showed massive subhyaloidal preretinal hemorrhages at the posterior pole and massive disseminated intraretinal hemorrhages on the entire fundus. These pronounced bilateral multilayer retinal hemorrhages are often described after child abuse [14]. Besides a complexity of retinal hemorrhages, it is also suspicious if the posterior pole and theperiphery of the retina are involved [14], as in the present case.
Retinal hemorrhage diagnoses that should be considered are either of a traumatic nature, such as birth trauma related to birth modality, or high-impact accidental traumas, such as car accidents [15] or they are from critical illness, such as infections and septicemia, vasculitis, leukemia, Henoch-Schonlein purpura, endocarditis and many others [12,[16][17][18]. The latter cases are rare in the AHT age range [12]. Reports also indicate that an AHT can cause unilateral retinal hemorrhaging [18,19].
An overview of vitreous hemorrhages in the pediatric age group is given by Naik et al. [20]. The proportion of patients with bilateral vitreous hemorrhaging and the most common causes differ between different studies [20]. In the western literature [21] nonaccidental trauma or the battered baby syndrome appears to be the most common cause [20], followed by anecdotal reports of various ocular and systemic conditions such as vasculitis [22] or low platelet levels [23,24]. Also, the age on presentation varies depending on the diagnosis, with

Unusual eye injury related to abusive head trauma Abstract
Ophthalmological examination is an essential component in clinically diagnosing abusive head trauma (AHT). Typical of AHT injuries is retinal bleeding, with other parts of the eye sometimes also being affected. Visual impairment and blindness are long-term complications in this context. We present a case with unusual eye injuries after a diagnostically confirmed AHT. The ophthalmological findings on admission day showed a massive subhyaloid hemorrhage at the posterior pole and extensive flame-shaped intraretinal hemorrhages accented on the right side., A centrally localized vitreous hemorrhage appeared on both sides 3 weeks later, obscuring the optic disc and macula most probably due to a breakthrough of a sub-internal limiting membrane (ILM) hemorrhage into the vitreous cavity. Follow-up 4 weeks later revealed a dense and organized vitreous hemorrhage occupying the optic disc and macula so that a pars plana vitrectomy was performed on both eyes. The bilateral bleeding in different retinal layers, the vitreous hemorrhage and the proliferative vitreoretinal reaction (PVR) indicated massive damage caused by a significant acceleration-deceleration trauma. A two-phase vitreous hemorrhage in a child with AHT does not yet appear to have been described in the literature.

Schlüsselwörter
Netzhautblutung · Blindheit · Mehrstufig · Glaskörperblutung · Prolifertive vitreoretinale Reaktion shaking trauma (mean age = 0.6 years) and birth trauma (mean age = 0.1 years) for the youngest and pars planitis (mean age = 10.0 years), nonpenetrating trauma (mean age = 10.8 years) and penetrating trauma (mean age = 9.9 years) for older children [21]. According to Spirn et al. 2006, the most common diagnosis with bilateral presentation was an AHT in the sense of a shaking trauma. All patients with an AHT were diagnosed with bilateral hemorrhage and, conversely, 50% of cases with bilateral hemorrhage were diagnosed with an AHT [21].
Uncommon in this case was the new, centrally localized vitreous hemor-   rhage, which appeared on both sides 3 weeks after hospital admission. A search (PubMed) did not reveal any published case describing a two-phase vitreous hemorrhage in a child with AHT. There was no evidence of a second trauma. We suggest that the second vitreous hemorrhage might have been caused by the PVR. Spontaneous vitreous hemorrhage is most commonly caused by proliferative diabetic retinopathy, retinal tear, proliferative retinopathy after retinal vein occlusion and posterior vitreous detachment without retinal tear [25]. Vitreous hemorrhaging can be caused by the pathologic mechanisms of disruption of normal retinal vessels, bleeding from diseased retinal vessels or abnormal new vessels, and extension of hemorrhaging through the retina from other sources [25]. As PVR is known to be a risk factor for developing vitreous hemorrhage and other differential diagnosis could be excluded, PVR is the most likely cause for the second vitreous hemorrhage. Resulting blindness is a rare complication, especially when caused by factors in the eye itself and not by occipital cortical damage or optic nerve injury, which is more common [2].
The bilateral bleeding in different retinal layers, the vitreous hemorrhage and the PVR reaction indicate massive damage caused by a significant accelerationdeceleration trauma. With overwhelming probability, a massive accelerationdeceleration trauma was the cause of the bleeding in both eyes and the cause of lasting blindness. 4 The bilateral bleeding in different retinal layers, the vitreous hemorrhage and the PVR reaction indicate massive damage caused by a significant acceleration-deceleration trauma. 4 Two-phase vitreous hemorrhaging in a child with AHT does not appear to have been described in the available literature. 4 PVR is known to be a risk factor for developing vitreous hemorrhage. 4 Resulting blindness is a rare complication, especially when caused by factors in the eye itself and not by occipital cortical damage or optic nerve injury, which is more common.