To demonstrate the severity of ocular findings in young children who died of injuries due to motor vehicle crashes.
Case series of 10 children younger than 3 years who were fatally injured in motor vehicle crashes between January 1, 1994, and December 31, 2002. All children underwent autopsy that included eye examination. All available medical and autopsy records, pathology slides and photographs, and police and traffic department reports were reviewed for each case.
Eight patients had retinal hemorrhages, which extended into the periphery in 13 eyes and were bilateral in 7 patients. Three patients had elevated circular retinal folds. Six patients had hemorrhages below the internal limiting membrane, but no patients had deeper splitting of the retina. Nine patients had optic nerve sheath hemorrhages.
The association of extensive, sometimes severe, ocular hemorrhages with fatal accidental trauma, compared with previous reports of accidental trauma with no or few hemorrhages, indicates the severity of injury required to cause hemorrhages of this magnitude.
Innumerable severe, multilayered retinal hemorrhages that extend to the far periphery are commonly associated with nonaccidental head injury in infants and young children.1,2
While there are many other causes of retinal hemorrhages, few result in hemorrhages of this severity. When a child is assessed for abusive neurotrauma, it is important to note the size, shape, number, and distribution of the hemorrhages. In addition, it is helpful to be aware of the types of force required to produce hemorrhages with a similar distribution and degree of severity that result from accidental traumatic mechanisms where the injury is known.
The cases reported herein were collected by the Department of Ophthalmology at the Medical College of Wisconsin from January 1, 1994, through December 31, 2002, and were taken from autopsies performed by the Medical Examiner of Milwaukee County on children younger than 3 years who died in motor vehicle crashes (MVCs). Autopsies, which may include the eyes, are performed by medical examiners in patients who died of sudden, unexpected, or suspicious circumstances, according to Wisconsin law. Enucleations are performed from behind, inside the skull, unroofing the orbital plates and dissecting from behind. The orbits are not exenterated or examined for signs of trauma. In cases of MVCs, the decision to remove the eyes is left to the individual pathologist.
Institutional review board approval for the study was obtained. All available medical and autopsy records, pathology slides and photographs, and police and traffic department reports were reviewed for each case. Many of these records are in the public domain. In addition to documentation of the specific type and location of the retinal hemorrhaging, details were also recorded regarding each child's injuries and the traumatic event leading to the injuries.
During the study period, 10 children underwent autopsies that included the eyes. Details of the incidents and the patients' findings are summarized in the Table. Six other children underwent autopsies without eye examinations and were not included.
Improper restraints and direct blows in automobile-pedestrian accidents contributed to the severity of the injuries in 6 patients. All patients had severe head injuries, but 3 did not have skull fractures. Autopsy findings did not raise any suspicion of earlier abuse of the children. Eight patients had retinal hemorrhages, which extended into the periphery in 13 eyes and were bilateral in 7 patients. Two children had no hemorrhages, and another had only a few peripapillary hemorrhages in 1 eye. Nine patients had optic nerve sheath hemorrhages, which were bilateral in 8. Three patients had elevated circular retinal folds. Six patients had dome-shaped hemorrhages just below the internal limiting membrane (ILM), but no patients were found to have deeper splitting of the retinal layers.
The most common traumatic mechanism associated with retinal hemorrhaging of any severity—but particularly the most severe forms where the hemorrhages extend to the ora serrata—is rotational acceleration/deceleration type injury. This is the mechanism involved in nonaccidental childhood neurotrauma (also known as shaken baby syndrome).
Multiple reports including children of all ages have demonstrated the infrequency of retinal hemorrhaging with known accidental trauma of various mechanisms, even with skull fractures. In prospective, possibly overlapping, studies of accidentally injured nonnewborn children, only 69 of at least 776 children examined (8.9%) had retinal hemorrhages.2-32 Retrospective studies have shown similar results.33-39 Other than the certainty that the injury was accidental, details have been sparse regarding the type of accident, mortality, and the number, extent, and laterality of the retinal hemorrhages.
Of patients described in the literature, 38 had mild hemorrhages that did not extend to the ora serrata.2,5-8,10,11,13,14,17,21 Reports concerning an additional 23 patients did not include enough description of their hemorrhages to determine whether the hemorrhages were mild or severe.3,8,16,20,21,23,25,27,30,32,39 The 7 patients known to have hemorrhages extending to the ora serrata died of their injuries.4,7-9,21 Three patients died of high-energy, rotational forces similar to those seen in nonaccidental childhood neurotrauma.8,21 Four other patients died of crush injuries to the head caused by toppling television sets, the fall of another child onto the head of the victim, or an MVC.4,7-9 Plunkett38 retrospectively reported 4 children with retinal hemorrhages who died of playground injuries. Their hemorrhages were found by a neurosurgeon or by pediatric intensivists40; details regarding the extent, type, and number of hemorrhages are uncertain compared with the autopsy findings reported herein. In each investigation, a best estimate was that the injuries were accidental rather than inflicted, although some were not witnessed, particularly by an adult. That the accidents were fatal indicates the severity of the forces delivered to the children's heads; that two-thirds of those examined had retinal hemorrhages is consistent with severe injury.
The most commonly suggested mechanisms for retinal hemorrhages in children younger than 3 years, particularly in nonaccidental head trauma, are mechanical vitreous traction on the retina and a sudden increase in venous pressure in the retinal vessels.41 The mechanical theory suggests that traction on the retina due to the motion of the vitreous body during violent rotational acceleration/deceleration forces causes direct damage to the retina and its blood vessels.41 The attachment of the vitreous body in children is strongest at the posterior pole, along the vessels, and at the periphery, which may explain the distinctive distribution often seen in the most severe retinal hemorrhaging and retinal detachment in nonaccidental neurotrauma, similar to Figure 1.41-43 The observed attachment of the ILM to the peak of the circular retinal fold41 and the finding of orbit tissue injury during autopsy examination of children with nonaccidental neurotrauma and accidental death5 have also been cited as evidence of mechanical forces.
Some well-documented cases of abusive neurotrauma have shown no sign of direct head impact on careful autopsy examination of the layers of the head.44-46 Perpetrator confessions have corroborated the shaking mechanism suspected.47 The children we studied had severe acceleration/deceleration injuries consistent with the mechanical theory for retinal hemorrhages. Patient 7 had an elevated retinal fold but did not have skull fractures.
Most elevated retinal folds reported in children have been associated with abusive neurotrauma.41,44,48,49 These children had a higher mortality rate, indicating that they had more severe injury. Three children who died of accidental crush injuries to the head were reported to have elevated retinal folds.3,4,9 The occurrence of these folds in an uncertain number of patients with nontraumatic Terson syndrome has raised the possibility that the hemorrhage itself rather than traction of the vitreous on the retina plays a role,50,51 but this possibility has been questioned by Levin.41 In at least 1 trauma patient, a very large, dome-shaped sub-ILM hemorrhage has been found spanning the macular region encompassed by the circular retinal fold.4 The 3 children reported herein to have elevated circular retinal folds did not have this large sub-ILM hemorrhage (patients 2, 7, and 8) (Figure 2). Emerson and coauthors52 have proposed that sustained venous stasis and leakage from retinal vessels can lead to elevated circular retinal folds in nonaccidental neurotrauma. Our patients demonstrated that abrupt injury can cause these folds as well.
A sudden increase in venous pressure in the eye is the other primary mechanism proposed to cause retinal hemorrhages in nonaccidental neurotrauma. Less evidence supports this, however, because Terson syndrome is rarely seen in children. A study of the eyes in children with intracranial hemorrhage of various causes found only 5 small hemorrhages in 1 patient who had been in an MVC.13 Increased venous pressure secondary to Valsalva maneuvers or chest compression53-55 does not seem to be a likely cause of intraocular hemorrhage because these processes cause very few or no retinal hemorrhages in children.56-61 Crush injuries may cause retinal hemorrhages because of increased intracranial and intraocular venous pressure. However, 9 patients who died of their crush injuries did not have retinal hemorrhages or had only a few posterior hemorrhages,5,7 and 11 survivors did not have any hemorrhages.7
Three accidentally crushed children were reported to have large hemorrhages and retinoschisis.3,4,9 In our patients, there were sub-ILM hemorrhages and no deeper splitting of the retina. In 3 patients who underwent vitrectomies for large dome-shaped macular hemorrhages associated with a retinal fold or pigmentary changes around the macula, the excised anterior wall of the cyst contained ILM.62 These patients included a 17-year-old and 4-year-old with Terson syndrome of unknown cause and a 5-month-old with shaken baby syndrome. A postmortem examination in a 7-month-old with shaken baby syndrome also showed a hemorrhagic cyst enclosed by ILM.44
Many abused children with retinal hemorrhages have skull fractures that must have been caused by impact injuries but rarely to the point of classifying them as crush injuries.21,63 Seven of the patients reported herein had skull fractures (patients 1, 2, 5, 6, 8, 9, and 10), and 5 (patients 1, 6, 8, 9, and 10) had depressed skull fractures or fractures with brain lacerations. In the police reports, there was no indication that the children were crushed between 2 surfaces, as has been the case in patients reported to have an object or person fall on their head.3,4,9 Three patients had no skull fractures (patients 3, 4, and 7); their injuries largely resulted from acceleration/deceleration mechanisms. Impact and acceleration/deceleration mechanisms can combine to cause retinal hemorrhage, as in the tin ear syndrome64 and nonaccidental childhood neurotrauma.41
Our patients had injuries that involved acceleration/deceleration mechanisms, but they also had sudden head injuries and intracranial bleeding; thus, both proposed mechanisms for retinal hemorrhages could apply. Patient 9, who died of severe brain injury on the day of the accident, had only optic nerve sheath hemorrhage. Patient 4, who had only mild peripapillary hemorrhages in the left eye, died 7 days after the injury. Retinal hemorrhages were noted by the intensive care attending physician 1 day before death, but the extent and laterality of the hemorrhages were not noted. Some retinal hemorrhages could have resolved before death.
It is not clear why some patients who were fatally injured by accident or intent do not have retinal hemorrhages. Some of these patients died immediately, negating the possibility that hemorrhages had been present but resolved before death. The particular type of trauma and where the forces were sustained must account for the variation in retinal findings.
All of our patients died after being subjected to extremely severe forces involving rapid deceleration with a rotational (whiplashlike) component, similar to that described in nonaccidental childhood neurotrauma. The extent and severity of the retinal hemorrhages, when compared with the rare and mild hemorrhages in other less severely accidentally injured patients, indicate that more severe trauma causes more severe eye findings. These were all extremely high-force injury mechanisms that far exceed those involved in common (or even uncommon) household accidents. This supports previous conclusions2,8,21,65 that, in the absence of a known major accidental injury involving severe intracranial trauma, such as a crush injury or high-force MVC, extensive retinal hemorrhages are highly indicative of occult, severe intentional injury.
Correspondence: Jane D. Kivlin, MD, Department of Ophthalmology, Medical College of Wisconsin, 925 N 87th St, Milwaukee, WI 53226 (firstname.lastname@example.org).
Submitted for Publication: May 16, 2007; final revision received September 13, 2007; accepted September 17, 2007.
Financial Disclosure: None reported.
Funding/Support: This study was supported in part by an unrestricted grant from Research to Prevent Blindness, Inc.
et al. Update from the Ophthalmology Child Abuse Working Party: Royal College ophthalmologists. Eye
795- 798PubMedGoogle Scholar
P Accidental and nonaccidental head injuries in infants: a prospective study. J Neurosurg
380- 384PubMedGoogle Scholar
P Are there any pathognomic signs in shaken baby syndrome? J AAPOS
99- 10010.1016/j.jaapos.2007.01.031Google Scholar
R Perimacular retinal folds simulating nonaccidental injury in an infant. Arch Ophthalmol
1782- 1783PubMedGoogle Scholar
et al. Postmortem orbital findings in shaken baby syndrome. Am J Ophthalmol
233- 240PubMedGoogle Scholar
C Retinal hemorrhages in accidental and nonaccidental injury [reply]. Pediatrics
et al. Ocular manifestations of crush head injury in children. Eye
5- 10PubMedGoogle Scholar
DF A population-based comparison of clinical and outcome characteristics of young children with serious inflicted and noninflicted traumatic brain injury. Pediatrics
633- 639PubMedGoogle Scholar
Jr Perimacular retinal folds from childhood head trauma. BMJ
754- 756PubMedGoogle Scholar
P Traumatismes crâniens accidentels ou non du nourrisson: étude prospective de 88 cas. Presse Med
1174- 1179PubMedGoogle Scholar
M Traumatic retinal hemorrhages [abstract]. Childs Nerv Syst
et al. Ophthalmologic findings in suspected child abuse victims with subdural hematomas. Ophthalmology
1718- 1723PubMedGoogle Scholar
et al. Retinal findings in children with intracranial hemorrhage. Ophthalmology
1472- 1476PubMedGoogle Scholar
P Infantile subdural hematomas due to traffic accidents. Pediatr Neurosurg
245- 253PubMedGoogle Scholar
D Delayed sudden death in an infant following an accidental fall: a case report with review of the literature. Am J Forensic Med Pathol
371- 376PubMedGoogle Scholar
VF Orthopaedic injuries in children secondary to airbag deployment. J Bone Joint Surg Am
895- 898PubMedGoogle Scholar
AC Retinal hemorrhages caused by accidental household trauma. J Pediatr
125- 127PubMedGoogle Scholar
et al. Neuroimaging, physical, and developmental findings after inflicted and noninflicted traumatic brain injury in young children. Pediatrics
(2, pt 1)
300- 307PubMedGoogle Scholar
W Morphometrical analysis of retinal hemorrhages in the shaken baby syndrome. Forensic Sci Int
71- 80PubMedGoogle Scholar
P The association of vision-threatening ocular injury with infant walker use. Arch Pediatr Adolesc Med
1275- 1276PubMedGoogle Scholar
TC Systemic and ocular findings in 169 prospectively studied child deaths: retinal hemorrhages usually mean child abuse. Forensic Sci Int
117- 132PubMedGoogle Scholar
C Inflicted versus accidental head injury in critically injured children. Crit Care Med
1328- 1332PubMedGoogle Scholar
D Accidental head trauma and retinal hemorrhage. Neurosurgery
231- 235PubMedGoogle Scholar
et al. Retinal findings after head trauma in infants and young children. Ophthalmology
1718- 1723PubMedGoogle Scholar
et al. Head injury in very young children: mechanisms, injury types, and ophthalmologic findings in 100 hospitalized patients younger than 2 years of age. Pediatrics
(2, pt 1)
179- 185PubMedGoogle Scholar
GL Retinal haemorrhage in accidental head trauma in childhood. J Paediatr Child Health
286- 289PubMedGoogle Scholar
et al. Retinal hemorrhages, seizures, and intracranial hemorrhages: relationships and outcomes in children suffering traumatic brain injury. Martin
AE Concepts in Pediatric Neurosurgery.
11 Basel, Switzerland S Karger AG1991;87- 94Google Scholar
L The eyes of child abuse victims: autopsy findings. J Forensic Sci
741- 747PubMedGoogle Scholar
et al. Do retinal hemorrhages occur with accidental head trauma in young children [abstract]? AJDC
RN Autopsy findings in the eyes of fourteen fatally abused children. Forensic Sci Int
293- 299PubMedGoogle Scholar
RK Retinal hemorrhage after cardiopulmonary resuscitation or child abuse. J Pediatr
430- 432PubMedGoogle Scholar
GD Fatal falls in childhood: how far must children fall to sustain fatal head injury? report of cases and review of the literature. Am J Forensic Med Pathol
201- 207PubMedGoogle Scholar
RM Child abuse and unintentional injuries. Arch Pediatr Adolesc Med
16- 22PubMedGoogle Scholar
PA Serious head injury in infants: accident or abuse? Pediatrics
340- 342PubMedGoogle Scholar
MS Epidural hemorrhage: is it abuse? Pediatrics
664- 668PubMedGoogle Scholar
R Childhood head injuries: accidental or inflicted? Arch Pediatr Adolesc Med
11- 15PubMedGoogle Scholar
J Fatal pediatric head injuries caused by short-distance falls. Am J Forensic Med Pathol
1- 12PubMedGoogle Scholar
L Ocular findings at autopsy of child abuse victims. Ophthalmology
1519- 1524PubMedGoogle Scholar
J Author's response to Drs. Spivack and Levin [reply]. Am J Forensic Med Pathol
417- 419PubMedGoogle Scholar
AV Retinal hemorrhage and child abuse. David
TJ Recent Advances in Paediatrics.
New York, NY Churchill Livingstone Inc2000;151- 219Google Scholar
J Age-related differences in the human vitreoretinal interface. Arch Ophthalmol
966- 971PubMedGoogle Scholar
MA Ocular and cerebral trauma in non-accidental injury in infancy: underlying mechanisms and implications for paediatric practice. Br J Ophthalmol
282- 287PubMedGoogle Scholar
MW Vitreoretinal traction and perimacular retinal folds in the eyes of deliberately traumatized children. Ophthalmology
1124- 1127PubMedGoogle Scholar
R Shaken babies—some have no impact injuries. J Forensic Sci
114- 116PubMedGoogle Scholar
A The infant whiplash–shake injury syndrome: a clinical and pathological study. Neurosurgery
536- 540PubMedGoogle Scholar
P Analysis of perpetrator admissions to inflicted traumatic brain injury in children. Arch Pediatr Adolesc Med
454- 458PubMedGoogle Scholar
MS Shaken baby syndrome. Ophthalmology
1246- 1254PubMedGoogle Scholar
M Funduscopic lesions associated with mortality in shaken baby syndrome. J AAPOS
67- 71PubMedGoogle Scholar
CD Hemorrhagic macular cysts [letter]. Ophthalmology
C Frequency of ocular hemorrhages in patients with subarachnoidal hemorrhage. Graefes Arch Clin Exp Ophthalmol
859- 862PubMedGoogle Scholar
WR Ocular autopsy and histopathologic features of child abuse. Ophthalmology
1384- 1394PubMedGoogle Scholar
MS Valsalva and Purtscher's retinopathy with optic neuropathy in compressive thoracic injury: case report. Eye
914- 915PubMedGoogle Scholar
R Optical coherence tomography findings in Valsalva retinopathy. Am J Ophthalmol
134- 136PubMedGoogle Scholar
RD Does valsalva retinopathy occur in infants? an initial investigation in infants with vomiting caused by pyloric stenosis. Pediatrics
1658- 1661PubMedGoogle Scholar
MW Are retinal hemorrhages found after resuscitation attempts? a study of the eyes of 169 children. Am J Forensic Med Pathol
187- 192PubMedGoogle Scholar
HE Retinal haemorrhages and convulsions. Arch Dis Child
449- 451PubMedGoogle Scholar
B Retinal hemorrhage after cardiopulmonary resuscitation in children: an etiologic reevaluation. Pediatrics
585- 588PubMedGoogle Scholar
et al. Prevalence of retinal hemorrhages in pediatric patients after in-hospital cardiopulmonary resuscitation: a prospective study. Pediatrics
M Severe cough and retinal hemorrhage in infants and young children. J Pediatr
835- 836PubMedGoogle Scholar
P Vitrectomy for premacular hemorrhagic cyst in children and young adults. Graefes Arch Clin Exp Ophthalmol
824- 828PubMedGoogle Scholar
HL Neuropathology of inflicted head injury in children, I: patterns of brain damage. Brain
1290- 1298PubMedGoogle Scholar
G Tin ear syndrome: rotational acceleration in pediatric head injuries. Pediatrics
618- 622PubMedGoogle Scholar
et al. Characteristics that distinguish accidental from abusive injury in hospitalized young children with head trauma. Pediatrics
165- 168PubMedGoogle Scholar