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Keywords:

  • child abuse;
  • head trauma;
  • retinal haemorrhage;
  • shaken baby syndrome

Abstract

  1. Top of page
  2. A
  3. Introduction
  4. Clinical presentation
  5. Ocular findings
  6. Pathogenesis of ocular findings
  7. Differential diagnosis of ocular findings
  8. Outcome
  9. The role of the ophthalmologist
  10. Future directions
  11. References

Paediatric abusive head injury may have grave consequences, especially when characterized by repetitive acceleration–deceleration forces (shaken baby syndrome). Death occurs in approximately 30% and permanent neurologic damage in up to 80% of the victims. Retinal haemorrhages are a cardinal sign seen in approximately 85% of cases. In most cases haemorrhages are preretinal, intraretinal and subretinal, too numerous to count, and involving the entire retinal surface extending to the ora serrata. Traumatic macular retinoschisis is a lesion with important diagnostic significance. Vitreoretinal traction appears to be the mechanism of haemorrhage and schisis formation along with a possible role of orbital tissue trauma from repetitive acceleration–deceleration forces. Ophthalmologists must carefully document ocular findings. Appropriate autopsy examination should include ocular and orbital tissue removal. Although there is a wide differential diagnosis for retinal haemorrhages, clinical appearance, when considered in the context of systemic and laboratory findings, usually leads to the correct diagnosis.


Introduction

  1. Top of page
  2. A
  3. Introduction
  4. Clinical presentation
  5. Ocular findings
  6. Pathogenesis of ocular findings
  7. Differential diagnosis of ocular findings
  8. Outcome
  9. The role of the ophthalmologist
  10. Future directions
  11. References

Although scattered reports on suspected child abuse have existed in the medical literature since the 19th century,1 child abuse was first brought to widespread medical attention in the early 60s.2 The form of abusive head injury characterized by repeated acceleration–deceleration forces with or without blunt head impact, which would later be termed shaken baby syndrome (SBS), was first described by Guthkelch in 1971 as a syndrome characterized by intracranial and intraocular bleeding together with characteristic fractures.3 Several aspects of this syndrome were likely reported earlier as ‘chronic’ subdural haematoma in infants in 19304 and in association with long bones fractures in 19465 although the abusive nature of the injuries was not recognized. The first author to unknowingly describe retinal haemorrhage as part of this syndrome was probably Aikman in 1928,6 and it was Gilkes who first reported a relationship to child abuse in 1967.7 Following the Guthkelch report, it was Caffey who further delineated the syndrome in 1972 and 1974 as the Whiplash Shaken Infant syndrome.8,9

About 1.7% of all children hospitalized for physical injury in the USA are victims of child abuse,10 and it is estimated that 1200–1400 of them are victims of abusive head injury characterized by repeated acceleration–deceleration with or without head impact (Shaken Baby Syndrome, SBS).11 The consequences of this form of child abuse are grave. Up to 30% of victims die and the more than 80% of the survivors will show signs of permanent neurological damage in the form of motor, intellectual and visual deficits, including blindness.11–15 Because external physical manifestations are not always evident, the diagnosis can be missed.16 The ophthalmologist may have a critical role in identifying the victims.17

Clinical presentation

  1. Top of page
  2. A
  3. Introduction
  4. Clinical presentation
  5. Ocular findings
  6. Pathogenesis of ocular findings
  7. Differential diagnosis of ocular findings
  8. Outcome
  9. The role of the ophthalmologist
  10. Future directions
  11. References

There are several important clues in the history of children brought to medical care that should raise the suspicion of abuse: The severity of the clinical signs and symptoms may be incompatible with the history told by the caregiver. Although in some cases the presenting symptoms are vague and non-specific, such as irritability and vomiting,18 severe symptoms like coma and bradycardia can not be explained by histories of a short fall. Less than 70% of perpetrators admit to the abusive act.

The acceleration–deceleration movement of the brain inside a relatively large infant skull, supported by weak cervical musculature, results in tearing of the bridging veins, which causes the subdural haemorrhage found in 90% of cases.19 Autonomic dysregulation or trauma to intradural vessels may also play a role.20 The accumulation of subdural blood is probably not the major cause for the neurological symptoms found in SBS.21 Parenchymal brain injury is caused by hypoxic vascular damage and traumatic axonal injury.22,23 Hypoxia results from a biochemical cascade response to neuronal injury with secondary cerebral oedema and autoinfarction of the major vessels and also from damage to the cervical spine, causing apnoea and bradycardia.24 Another cardinal manifestation seen in up to 55% of the victims are fractures usually in the limbs or ribs.25 More than half of the fractures are multiple, and up to 43% are clinically unsuspected.25,26

Ocular findings

  1. Top of page
  2. A
  3. Introduction
  4. Clinical presentation
  5. Ocular findings
  6. Pathogenesis of ocular findings
  7. Differential diagnosis of ocular findings
  8. Outcome
  9. The role of the ophthalmologist
  10. Future directions
  11. References

Retinal haemorrhages are seen in approximately 85% of victims, with reports ranging from 30% to 100% depending on the population studied. For example, studies that included abusive blunt impact head trauma without repetitive acceleration–deceleration are likely to have lower rates, whereas post-mortem studies are likely to have higher rates.27 Although there is a correlation between the severity of brain injury and severity of the retinal findings, even severe cases of brain trauma may have only few scattered retinal haemorrhages and asymmetry or unilaterality are well recognized.28 In approximately two-thirds of cases, retinal haemorrhages are numerous, located in the subretinal, intraretinal and preretinal space and extend to the ora serrata.19 Intraretinal haemorrhages are the most common and include both superficial nerve fibre layer flame-shaped haemorrhages and deeper dot/blot haemorrhages. White centred haemorrhages may occur but this finding is entirely non-specific and may result from central clearing, fibrin or light reflex from examining instruments and camera.

Another fairly specific ocular sign of abusive injury is retinoschisis. The retina becomes split between layers, most commonly just the internal limiting membrane, forming a cystic cavity that may be partially or completely filled with blood. Recognition of traumatic retinoschisis is aided by the identification of hemorrhagic or hypopigmented circumlinear lines at the edges of the lesion. There may also be pleating of the retina called paramacular folds. The folds may or may not be present at the edge of schisis lesions and can also be observed in the absence of a schisis cavity or remain after a schisis cavity has settled. Schisis-like cavities also can form directly over blood vessels although this is a less specific finding and can result from any cause of bleeding where by blood becomes trapped between the vessels and overlying internal limiting membrane in which the vessel is imbedded. The blood within a retinoschisis cavity may leak into the vitreous hours or days after the initial injury, making careful monitoring and follow up essential.27

Pathogenesis of ocular findings

  1. Top of page
  2. A
  3. Introduction
  4. Clinical presentation
  5. Ocular findings
  6. Pathogenesis of ocular findings
  7. Differential diagnosis of ocular findings
  8. Outcome
  9. The role of the ophthalmologist
  10. Future directions
  11. References

The primary proposed mechanism for retinal haemorrhage in abusive head injury is vitreoretinal traction. The vitreoretinal attachments in babies are extremely firm particularly at the macula, peripheral retina and blood vessels. The repeated acceleration–deceleration movement of the eye induces shearing forces at the vitreoretinal interface and inside the orbit. These mechanical forces may lead to either direct damage to vessels or enough shear to induce disruptions in vascular autoregulation resulting in ‘leaky’ vessels, which may possibly be augmented by damage to the cranial nerves that carry autonomic supply to the retina.29 This hypothesis is supported by post-mortem examinations that shows that victims have significantly more haemorrhages in orbital fat and optic nerve dura than children who died from accidental trauma,29 and by optical coherence tomography studies on SBS victims that demonstrated multiple vitreo-retinal traction sites that may be coupled with intraretinal haemorrhages.30 The frequency of haemorrhage at the retinal periphery is anatomically consistent with the increased vitreoretinal adhesiveness in that area.

An interesting study exploring this theory investigated the ocular anatomy of the woodpecker, a bird that spends its lifetime submitting itself to repeated acceleration–deceleration with head impact.31 It appears that nature had taken multiple measures to protect the woodpecker retina from damage due to this dramatic behaviour: globe movement is restricted due to tight fit within the orbit and fascial connections between the orbital rim and sclera; the sclera is reinforced with cartilage and bone; the optic nerve lacks redundancy, and the vitreous lacks attachments to the posterior pole retina.31 Although there has been mixed success with shaking of small mammal animal models, more recent work with pigs, using only a single large uniplanar force acceleration–deceleration, has demonstrated retinal haemorrhage only at areas of vitreoretinal attachment.32 Also supporting the mechanism of vitreoretinal traction are studies using finite element analysis computer modelling.33,34

Traumatic macular retinoschisis and perimacular folds are also caused by the repetitive acceleration–deceleration forces inducing vitreous traction on the macula, causing it to split its layers. Histologically, the vitreous can be seen still attached to the schisis cavity surface.35 These traction sites have also been demonstrated by optical coherence tomography.30

Others have proposed a role for elevation of intracranial pressure due to intracranial haemorrhage and brain oedema or increased intrathoracic pressure due to chest compression (e.g. causing rib fracture) causing impairment of venous return out of the eye. In the face of unrestricted arterial supply this could result in rupture of retinal capillaries and venules, with the development of retinal haemorrhage. This theory is supported by the existence of retinal haemorrhages in Terson syndrome, which involves intracranial bleeding with raised intracranial pressure associated with intraocular haemorrhage. Many observations, however, contradict this theory. In a study of 75 victims, no correlation was found between raised intracranial, intrathoracic pressure or the side of the brain injury with the presence or severity of retinal haemorrhages.19 Another study demonstrated that in paediatric non-abusive head trauma, retinal haemorrhages are rare and occur at most in fewer than 8% of children with intracranial bleeding.36 Furthermore, children with abusive head trauma usually lack the retinal findings consistent with central retinal vein occlusion37 or papilloedema, which is indicative of increased intracranial pressure.19 Likewise, Purtscher hemorrhagic retinopathy, which occurs in adults following chest compression, is rarely reported in abusive head injury victims.19,38

Although there is little evidence to suggest that increased intracranial pressure or increased intrathoracic pressure play a major role in retinal haemorrhage causation, especially with regards to severe hemorrhagic retinopathy, they may have a role, along with other factors such as disturbances of sodium chemistry, hypoxia, anaemia and brain injury induced coagulopathy, in modulating the appearance of haemorrhages. Other potential factors such as vitamin C levels and thrombophilia remain under study.

Differential diagnosis of ocular findings

  1. Top of page
  2. A
  3. Introduction
  4. Clinical presentation
  5. Ocular findings
  6. Pathogenesis of ocular findings
  7. Differential diagnosis of ocular findings
  8. Outcome
  9. The role of the ophthalmologist
  10. Future directions
  11. References

There are many causes of retinal haemorrhages in children (Table 1). Most causes, like coagulopathies, leukaemia, hyper/hyponatremia or anaemia are easily diagnosed by history, laboratory, eye examination or systemic physical examination and, with the exception of leukaemia, rarely cause more than a few haemorrhages in the posterior pole, usually intraretinal and preretinal. In leukemic patients, haemorrhages, usually intraretinal, were reported in up to 49% of cases, usually in the posterior pole, but some also documented in the periphery.39 These haemorrhages are often associated with obvious retinal leukemic infiltration.

Table 1.  Disorders associated with retinal haemorrhage
  • Incomplete list. These diagnoses are almost all readily diagnosed by history, laboratory, eye examination.

Coagulopathiest
Leukaemia
Hyper/hyponatremia
Anaemia
Carbon monoxide poisoning
Extracorporeal membrane oxygenation
Increased intracranial pressure
Glutaric aciduria type 1
Malaria
Meningitis
Vasculitis
Osteogenesis imperfecta
Accidental head injury
Endocarditis

Type I glutaric aciduria (GA1), a disorder of organic acid metabolism caused by mutations in the glutaryl-CoA dehydrogenase gene, is a known imitator of child abuse. It may cause subdural haemorrhage together with retinal haemorrhage following minor head trauma.40,41 Diagnosis is established by the specific neurologic and neuroragiological findings, which differ from abusive head injury, together with appropriate systemic metabolic testing.41 The haemorrhages are almost always few and confined to the posterior pole.

Perhaps the most common cause of paediatric retinal haemorrhage is normal birth, which can result in an extensive hemorrhagic retinopathy. Up to 50% of normal babies at term examined in the first 24 h of life will have retinal haemorrhages.42 They occur most frequently following vacuum extraction (75%) followed by spontaneous vaginal delivery (33%) and Cesarean section (6.7%).43 Flame-shaped haemorrhages resolve within 7 days after birth, and intraretinal dot/blot haemorrhages are gone usually by 4 weeks.42 Recently, it was reported that large or deep intraretinal haemorrhage, particularly in the fovea, may last to 58 days.44 Although hemorrhagic retinopathy of normal birth may be difficult to distinguish from the retina of abusive head injury before 4 weeks of age, normal babies do not demonstrate traumatic retinoschisis.

Peripapillary flame haemorrhages may be associated with papilloedema, a non-specific marker for increased intracranial pressure. Victims of abusive head injury characterized by repeated acceleration–deceleration with or without head impact rarely have papilloedema even when increased intracranial pressure is present.19,37 When present, they tend to be few in number, intraretinal or preretinal, and confined to the posterior pole, in particular the peripapillary area.45

Many child abuse victims undergo cardiopulmonary resuscitation with chest compression during their treatment. Retinal haemorrhage due to this intervention is rare and the haemorrhages, if possible, are very limited in number and confined to the posterior pole.27,46,47 Purtscher retinopathy, which would be the expected finding in chest crush injury, has never been observed. Increased intrathoracic pressure is also created by the Valsalva manoeuver during cough or excessive vomiting and can cause distinctive preretinal haemorrhage in the posterior pole of adults,48 but studies show that it is extremely rare in children.49,50

The presence of severe retinal haemorrhages following a short fall, during regular child activity, was suggested in one paper that suffered from many flaws including a lack of formal ophthalmology consultation.51 Although the rate of retinal haemorrhage after severe accidents such as motor vehicle accidents is higher, the medical literature continues to confirm the rarity (<3%) of hemorrhagic retinopathy after other forms of minor accidental trauma.52,53 When it does occur, the haemorrhages are usually few or at most modest in number and rarely extend beyond the posterior pole. In this context, the following statement made by The Royal College of Ophthalmologists Working Party for Child Abuse seems appropriate: ‘it is highly unlikely that the forces required to produce retinal haemorrhage in a child less than 2 years of age would be generated by a reasonable person during the course of (even rough) play or an attempt to arouse a sleeping or apparently unconscious child’, and ‘in a child with retinal haemorrhages and subdural haemorrhages who has not sustained a high velocity injury and in whom other recognized causes of such haemorrhages have been excluded, child abuse is much the most likely explanation’.54

Recently, lesions similar to the traumatic retinoschisis of abusive head injury have been described in infants who sustained severe fatal head crush injury.55–57 Similar findings were also described in a series of children who died in motor vehicle accidents.58

A paper examining a series of paediatric head crush victims did not find such lesions.59 Fortunately, such circumstances should be readily distinguished by history or the presence of characteristic head crush injuries such as orbital fracture, multiple skull fracture and cranial nerve injury.

Outcome

  1. Top of page
  2. A
  3. Introduction
  4. Clinical presentation
  5. Ocular findings
  6. Pathogenesis of ocular findings
  7. Differential diagnosis of ocular findings
  8. Outcome
  9. The role of the ophthalmologist
  10. Future directions
  11. References

Neurological outcome of abusive head injury can be grave.12,13 The cause of vision loss is mainly cortical damage,60–64 but also optic atrophy,27 which may be related to direct injury to the nerve caused by the effect of repeated acceleration–deceleration movements on orbital tissues or by direct blunt trauma.65,66 Retinal haemorrhages usually clear without damage to the eye although macular fibrosis and pigmentary changes may rarely result from retinoschsis.62 Large vitreous or preretinal haemorrhages obscuring the fovea will reduce vision as long as they are present and if asymmetric between the two eyes may lead to amblyopia.67 For this reason, young children with haemorrhage in or over the fovea must be followed after injury until one can be certain that visual development has been re-established equally in both eyes. Even in the absence of retinal haemorrhage, these brain-injured children are at risk for strabismus, amblyopia, optic atrophy and cortical visual loss. If there is no eye injury at all, a follow-up visit in no more than 4–6 months to screen for such sequelae is indicated.

The role of the ophthalmologist

  1. Top of page
  2. A
  3. Introduction
  4. Clinical presentation
  5. Ocular findings
  6. Pathogenesis of ocular findings
  7. Differential diagnosis of ocular findings
  8. Outcome
  9. The role of the ophthalmologist
  10. Future directions
  11. References

Visual acuity is not easily tested in babies and even babies with low vision usually act normally. For these reasons all children who are suspected of abusive head injury should be examined by an ophthalmologist as early as possible, preferably within the first 24 h after presentation, even if the visual behaviour seems normal. Although fundus examination by non-ophthalmologist can successfully recognize the ocular findings in about 80% of cases, some may be missed.37,68 Examination should be done by an ophthalmologist well-versed in this subject area is therefore required. Pharmacologic pupil dilation is optimal although the comatose child may already have fixed and dilated pupils. Examinations done by trainees, non-ophthalmologists or examinations with inadequate pupillary dilation should be described as ‘preliminary examination’.

The ocular findings should be described in detail. A labelled drawing of the fundus picture is usually helpful but of course may underestimate the number of haemorrhages seen. Photodocumentation with a fundus camera is useful when available. Retinal photography can not replace the need for a live examination by an ophthalmologist.

The establishment of a child abuse team is advisable in any medical centre that provides paediatric care. This team may include an ophthalmologist. Every child who is suspected of being abused should be evaluated by the team. Reporting to appropriate child protection agencies should ensue if the team feels that there is sufficient evidence to warrant a suspicion of abuse. Abuse need not be proven. In most jurisdictions of the developed world, ophthalmology consultation is mandatory in these situations. Even in the absence of a team, the ophthalmologist must honour the obligation to report a suspicion of abuse.

Future directions

  1. Top of page
  2. A
  3. Introduction
  4. Clinical presentation
  5. Ocular findings
  6. Pathogenesis of ocular findings
  7. Differential diagnosis of ocular findings
  8. Outcome
  9. The role of the ophthalmologist
  10. Future directions
  11. References

Animal models may have particular utility although they do raise some ethical concerns. Biomechanics research using human surrogates such as test dummies, and computer simulations may help us in better understanding the nature and mechanisms of child abuse injury. For example, Cory and Jones69 sought to reconstruct the original shaking experiments conducted by Duhaime et al. in 1987.70 The 1987 study suggested that shaking alone could not cause fatal head injuries. Cory and Jones demonstrated that more accurate design of certain parameters, such as neck joint, torso and mass distribution of the surrogate, produced angular head accelerations with shaking that exceeded those derived in the Duhaime study and also exceeded concussion thresholds with impact occurring on the chest and upper back by the head, a phenomenon not recognized in the 1987 model. Wolfson et al. used multi-body computer modelling and showed similar outcomes.71 Prange utilized finite element modelling to predict axonal head injury in a 1-month-old infant exposed to minor falls and abusive shaking.72,73 The model showed that 1.5-m fall on a soft mattress would not likely cause axonal injury similar to that found in abused infants. Animal models can be also investigated using computer-assisted measurements as shown by Levchakov et al.,74 which demonstrated that the smaller size and stiffer tissue of the rat infant brain makes it more susceptible to traumatic brain injury.

Another promising future direction may involve newer and more sophisticated tools for documentation of injury. It has been suggested that telemedicine consultation using these images can also be helpful in remote medical centres.75 Hand-held ocular coherence tomography devices, which are now commercially available, can now be used to demonstrate the vitroretinal traction induced retinoschisis lesions.76 Specific signs in ocular coherence tomography imaging that may assist us in differentiating retinal haemorrhages caused by shaking from haemorrhages from other causes. Lastly, uniform methods for describing hemorrhagic retinopathy, and perhaps scoring those findings, are being developed. Other areas of research will continue to look at potential differential diagnoses as well as the role of such factors as increased intracranial pressure, hypoxia, thrombophilia, minor coagulopathies and anaemia although there is copious evidence that they are not primarily causative of severe retinal haemorrhages.

Abusive head injury is still a major cause for childhood mortality and morbidity around the world. The ophthalmologist has a critical role in the evaluation and management of these children. Although some of the ocular manifestations of child abuse could be caused by other conditions, the classic picture of too numerous to count multilayered retinal haemorrhages extending to the periphery is highly suggestive of child abuse in the absence of other clear explanations and should therefore prompt appropriate reporting to child protective services to ensure the safety of the child.

References

  1. Top of page
  2. A
  3. Introduction
  4. Clinical presentation
  5. Ocular findings
  6. Pathogenesis of ocular findings
  7. Differential diagnosis of ocular findings
  8. Outcome
  9. The role of the ophthalmologist
  10. Future directions
  11. References