|Year : 2018 | Volume
| Issue : 2 | Page : 104-107
Is rotational trauma the only relevant pathogenic mechanism in hemorrhagic retinopathy of shaken baby syndrome?
B S Arushi Tripathy1, Stephanie Dean2, D O Joyce L de Jong1, Carl J Schmidt3, Rudy J Castellani1
1 Department of Pathology, Western Michigan University Homer Stryker MD School of Medicine, Kalamazoo, USA
2 Office of the Chief Medical Examiner, Baltimore, Maryland, USA
3 Department of Pathology, University of Michigan, Detroit, Michigan, USA
|Date of Web Publication||29-Jun-2018|
Dr. B S Arushi Tripathy
300 Portage Street, Kalamazoo, MI 49007
Source of Support: None, Conflict of Interest: None
The pathogenesis of ocular hemorrhage in abusive head trauma/shaken baby syndrome (AHT/SBS) is complex. Whereas severe hemorrhagic retinopathy has a robust association with AHT/SBS, mild disease is less specific. We report the ocular and cerebral findings in an 8-month-old girl with spastic torticollis who presented following confessed, violent sagittal plane acceleration-deceleration with impact. Autopsy revealed subdural hemorrhage over the convexities, ischemic brain injury, and preexisting polymicrogyria. Ocular examination showed extensive but unilateral retinal hemorrhage, extending broadly to the ora serrata, with perimacular retinal folds and retinoschisis. The retina of the right globe was entirely normal. The findings in this case, suggest that movement of the globe within the orbit with acceleration-deceleration, in this case greater on one side due to torticollis, may be the primary factor for severe hemorrhagic retinopathy associated with AHT/SBS. The findings argue against putative global mechanisms, such as intracranial hypertension.
Keywords: Abusive head trauma, forensic neuropathology, forensic science, hemorrhagic retinopathy, retinal hemorrhage, retinoschisis, shaken baby syndrome
|How to cite this article:|
Tripathy B S, Dean S, de Jong D O, Schmidt CJ, Castellani RJ. Is rotational trauma the only relevant pathogenic mechanism in hemorrhagic retinopathy of shaken baby syndrome?. J Forensic Sci Med 2018;4:104-7
|How to cite this URL:|
Tripathy B S, Dean S, de Jong D O, Schmidt CJ, Castellani RJ. Is rotational trauma the only relevant pathogenic mechanism in hemorrhagic retinopathy of shaken baby syndrome?. J Forensic Sci Med [serial online] 2018 [cited 2022 Jul 4];4:104-7. Available from: https://www.jfsmonline.com/text.asp?2018/4/2/104/235439
| Introduction|| |
Retinal hemorrhage (RH) has a strong statistical association with abusive head trauma/shaken baby syndrome (AHT/SBS) in infants and young children. One systematic review identified RHs in 78% of AHT/SBS cases compared to only 5% in non-AHT/SBS, with an odds ratio of 14.7 and a 91% probability of abuse. Where recorded, RH was bilateral in 83% of cases. Of nonabuse cases, RHs were few, located in the posterior pole, with only 10% extending to the periphery. The extent of hemorrhage was also emphasized in the prospective analysis by Vinchon et al., in which severe RH in the absence of ocular impact trauma was 100% specific for abuse. Although accidental trauma occasionally produced RH, the scarcity of RH even with major accidental trauma was noteworthy in this study, suggesting that repetitive abusive acceleration-deceleration, i.e., repetitive shaking with or without impact, was more relevant than the magnitude of monophasic blunt force trauma to the head. In another systematic review, RH showed a 75% sensitivity and 94% specificity for abuse, compared to 72% and 71% for optic nerve sheath hemorrhages, respectively. In the same review, traumatic retinoschisis and perimacular retinal folds were reported in 8% and 14% of AHT/SBS, respectively.
Although RH not otherwise specified can be caused by a long list of conditions, it is difficult to deny the strong association between severe RH and child abuse in a clinical context outside of obvious major accidental trauma (e.g., motor vehicle accidents and accidental crush injuries to the head). The severity of RH seen in child abuse is generally not described in natural disease processes, including neurovascular disease, major coagulopathies, and sepsis, or is described only anecdotally. On the other hand, the pathophysiologic mechanism of hemorrhagic retinopathy in the setting of pediatric head trauma is unresolved. Also unresolved is whether the severity of RH is, in part, an artifact of survival time, although at present there are no data to support such a relationship, whereas severe RH in our anecdotal experience is known to occur in infants found dead from AHT.
While data from some experimental models have supported vitreoretinal traction as a likely pathogenic factor, extrapolation to AHT/SBS and the complexities of action sequences in diverse and unwitnessed abusive injury scenarios remains conjectural. Data from human cases, including case reports, remain valuable for developing hypotheses or stimulating new research paradigms. We present the interesting case of severe but unilateral hemorrhagic retinopathy in an infant with confessed shaking impact by the caretaker. Particularly noteworthy in this case was co-existing, severe migration disorder and spastic torticollis (head permanently rotated to the left), emphasizing the role of rotational trauma over other mechanisms in the etiology of hemorrhagic retinopathy, retinoschisis, and retinal folds.
| Case Report|| |
An 8-month-old female infant presented to the emergency department in cardiovascular collapse immediately following traumatic brain injury inflicted by her father. The infant had a history of cerebral palsy, non-compaction cardiomyopathy, global developmental delay, hypertonia, and spastic torticollis with the head constantly rotated to the left in the horizontal plane. It was reported that the infant would forcefully and continuously cry during nearly all hours, which frustrated the father and precipitated the assault. Antemortem workup revealed changes on MRI suggestive of neuronal migration disorder, although no genetic or metabolic etiology was identified or has been identified to date. Imaging studies for the emergency admission revealed a subdural hematoma over both convexities (including mixed density collections), suggesting both recent and remote trauma. Investigation by law enforcement elicited a confession from the father, with videotaped doll reconstruction of a violent assault. The father did not admit to inflicting head trauma prior to the confessed occurrence. In the account provided including doll re-enactment, the infant was picked up and raised over the father's head, facing the father, and slammed with considerable force onto a sofa, with the head and posterior torso impacting the sofa. No specific information on the firmness of the sofa was provided. When asked if the demonstration accurately reflected the injury scenario, the father affirmed the question, but added that the actual event was more severe than demonstrated. The decedent became apneic and unresponsive immediately following the assault and was pronounced brain dead after 1.5 days of hospitalization. Life support was withdrawn shortly thereafter and an autopsy was performed. Poor neurological status was evident throughout the hospital course, precluding neurosurgical intervention and pressure monitoring, so antemortem data with respect to intracranial pressure were not available.
General autopsy revealed focal contusions of the head, face, and chest, healing abrasions of the extremities, and bilateral, patchy acute bronchopneumonia. Gross neuropathology showed bilateral acute subdural hemorrhages, a subdural neomembrane involving the majority of the left convexity calvarial dura [Figure 1], multifocal acute subarachnoid hemorrhage, and focal traumatic axonal injury microscopically. Acute, transient global ischemia and diffuse polymicrogyria with status marmoratus were also present [Figure 2], the latter a substrate for the underlying neurodevelopmental delay. Some edema was evident over the cerebral convexities, although there were no herniation phenomena, evidence of midline shift, or otherwise evidence of mass effect. Some discussion of the role of the decedent's migration disorder and potential effects on injury thresholds for subdural hematoma and parenchymal brain injury was explored during trial testimony, where it was suggested that brain atrophy may increase the vulnerability to traumatic subdural collections. Whether atrophy increases susceptible to parenchymal brain injury is less clear, although some biomechanical data suggest that acceleration required to injure the brain is inversely proportional to its mass, suggesting that an atrophic brain is not necessarily damaged more easily.
|Figure 1: Gross photograph of the subdural aspect of the calvarial dura shows fresh subdural blood clot with a preexisting subdural neomembrane on the left|
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|Figure 2: A coronal section of the cerebral hemispheres at the level of the thalamus shows polymicrogyria, in addition to dusky discoloration of the cortical ribbon due to acute ischemia|
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Ophthalmic pathology examination was performed after fixation in 10% neutral buffered formalin. After examination of the optic nerve and orbital connective tissues, the globe was sectioned in the horizontal plane and examined directly with a lens attachment that permitted close-up examination of the retina along with digital photography. The left globe revealed extensive, acute, subhyaloid hemorrhage, sub-internal-limiting membrane hemorrhage with retinoschisis, multilayered intraretinal and sub-RH, and a circumferential perimacular retinal fold. Hemorrhage suffused the left retina, extending to the ora serrata. The right retina was entirely normal [Figure 3] and [Figure 4]. Optic nerve sheath hemorrhage was present to a similar extent bilaterally, and hemosiderin deposits involving the right optic nerve sheath were noted.
|Figure 3: Section of the left globe in the horizontal plane shows extensive retinal hemorrhage with perimacular retinal folds. Horizontal section of the right globe is entirely unremarkable|
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|Figure 4: H and E-stained section of the left retina shows multilayered intraretinal hemorrhages with retinoschisis and sub-internal-limiting membrane hemorrhage (scale bar = 200 μm). A representative microscopic field of the right retina shows normal retinal histology (scale bar = 100 μm)|
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| Discussion|| |
Burhans and Gerstenberger were among the first to associate RH with subdural hematoma, at a time when subdural hematoma was only beginning to be understood as a traumatic lesion. Sherwood  and Ingraham and Matson  also noted ocular hemorrhage with subdural hematoma. Caffey (1974) suggested an association with inflicted abuse in his seminal article on shaking and whiplash trauma, which has been substantiated in numerous studies since., Indeed, no study to date concludes otherwise. It is important to note that RH as a binary data point is overly simplistic, since isolated or few posterior pole hemorrhages are nonspecific, while extensive RHs and involvement of the anterior aspect of the retina, associated macular folds, and schisis cavities have few alternative explanations apart from severe trauma. Peripapillary intrascleral hemorrhage, caused by rupture of the small arteries of the Circle of Zinn-Haller, is found in about 40% of AHT/SBS victims, and has yet to be described in infants and young children outside of AHT/SBS. This finding “may be pathognomonic” according to one study  and is “characteristic if not pathognomonic” according to another study. In the largest study to date examining peripapillary intrascleral hemorrhages, these hemorrhages were graded in terms of extent and relationship to the subchoroidal region and appeared to be distinct from optic nerve sheath hemorrhage.
In this case, we noted cardinal manifestations of AHT/SBS, with subdural hematoma of different ages, encephalopathy with acute ischemic brain injury, cerebral edema, and severe hemorrhagic retinopathy with retinoschisis and circumferential perimacular retinal folds. An unusual feature of this case was that the retinal findings were unilateral - very severe on the left and completely absent on the right. Such a markedly distinct difference has not been described to date. This case was also unusual in that the decedent had a preexisting, severe developmental malformation, with diffuse polymicrogyria involving both cerebral hemispheres, and associated developmental delay with unremitting spastic torticollis, the head constantly torsed horizontally to the left. When combined with the action sequence of the assault provided by the adult father – forceful rotational acceleration of the decedent in the sagittal plane, starting from an upright position facing the father and above his head, and slamming of the decedent onto a couch – an interesting biomechanical scenario is raised whereby the right globe is relatively supported by the orbit and the left globe is not. It is reasonable to suggest that greater movement and traction of the left globe compared to the right was the primary factor for the ocular complications in this scenario. Edema and increased pressure, increased intrathoracic pressure, coagulopathy, sepsis, and ischemia-reperfusion, had they been present, would have exerted essentially equal effects on both globes as they are diffuse and systemic. It would be difficult to explain why they had affected one eye more than the other.
Sometimes mentioned in medicolegal proceedings are selected citations that support the theory that RHs are simply the manifestation of increased intracranial pressure.,,, If true, this would undermine the significance of hemorrhagic retinopathy since RH may then complicate the intracranial compartment in anyone who dies of increased intracranial pressure. Such a theory, however, would have to discount the majority of individuals with fatal increased intracranial pressure and no RHs, and the overwhelming majority of such individuals with no hemorrhages beyond the peripapillary region. Moreover, papilledema, a surrogate for increased intracranial pressure, is present in <10% of patients with SBS., Experimentally, increased intracranial pressure fails to produce extensive RHs, and only rarely produces RHs at all, while rotational trauma reproducibly elicits RH in a porcine model. Empirically, severe RH offers few, if any, differential diagnostic considerations apart from obvious severe trauma and life-threatening illness, and even then is seen in only a minority of cases apart from AHT/SBS.,, It is also difficult to explain the acute mechanical disruption of the retina in terms of circumferential folds and schisis cavities, apart from mechanical trauma; the relevant question in young children is not whether trauma was present with such findings, but rather its severity and whether the provided clinical scenario plausibly supports the ocular findings. In contrast, it is interesting that optic nerve sheath hemorrhage was bilateral and symmetric. This suggests that optic nerve sheath hemorrhage has more diverse pathogenic mechanisms and is in line with the frequent finding of optic nerve sheath hemorrhage in decedents with sudden intracranial hypertension.
| Conclusion|| |
We report severe but unilateral hemorrhagic retinopathy in a case of fatal AHT, in a decedent with spastic torticollis, and therefore asymmetrical biomechanical forces applied to the globes. This supports the concept that rotational trauma is the primary factor for ocular findings in AHT/SBS.
This case is exempted from IRB review at Western Michigan University School of Medicine, and the ethics committee has approved this study.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4]