METHODS

We have a database of 90 children under the age of 2 years who were admitted to hospital in South Wales and South West England between 1992 and 1998 where a subdural haemorrhage or effusion was diagnosed by computed tomography (CT), magnetic resonance imaging (MRI), or at postmortem examination. Cases were notified from inpatient data, paediatric neurology and neurosurgery units, and the Welsh Paediatric Surveillance System (run along the same lines as the British Paediatric Surveillance System¹⁷). From these data we have used the inclusion criteria of Geddes et al to identify 65 children with SDH from NAHI^11,13:

1. Head injury where there was a confession by the perpetrator (n = 19).

2. Cases where NAHI was established as a result of criminal conviction in the criminal court where there were unexplained extracranial injuries (n = 10).

3. Cases where there were unexplained injuries elsewhere in the body, other than head injury, but no conviction (all diagnosed at case conference except two who died) (n = 15).

4. Cases where the carer was convicted of injuring the child but in which there was no extra cranial injury (n = 0).

5. Cases where there was major discrepancy between the explanation given by the carer and significant injury, such as a skull fracture, or if the history was developmentally incompatible (NAHI diagnosed at case conference in all except one who died) (n = 21).

Of those excluded, 16 had witnessed accidental or established medical causes and became a small comparison group. Nine did not meet the inclusion criteria.

The clinical research officer extracted clinical details from hospital notes, observation charts, and community case notes. We used the King’s Outcome Scale for Head Injury (KOSCHI) to categorise outcome¹⁸ (1 dead, 2 vegetative, 3 severe disability, 4 moderate disability, 5 good recovery). Child protection records, police files, and legal case records were also examined.

We analysed the first cranial CT/MRI scans and follow up neuroimaging undertaken within the first two weeks of diagnosis for evidence of intracerebral damage. The Bender grading scheme was used to classify symptoms of severity on presentation¹⁹: 1 mildly symptomatic, 2 drowsy variable neurological deficit, 3 stuporous, 4 comatose (GCS 3–5).

We identified 31 cases from the Geddes et al studies^11,13 of infants who died from NAHI and had SDH, and 28 infants and young children with shaken baby syndrome from the study of Johnson and colleagues,¹⁶ and compared them to our case series.

In our analysis we used standard χ² with appropriate degrees of freedom, and Fisher’s exact probability test for 2×2 contingency tables when sample sizes are small. The study was approved for epidemiological analysis by MREC S Wales.

RESULTS

Of the 65 cases, the age at head injury ranged from 19 days to 23 months (mean 5.2 months). There were 57 infants, 48 of whom were 6 months or under. Three children were dead on arrival at hospital, 15 were comatose, eight were stuporous with fluctuating levels of consciousness, 32 were moderately drowsy with fits or neurological deficit, and seven had mild symptoms or general malaise.

Table 1 details the Bender score for presenting symptoms with respect to the KOSCHI outcome score for the 59 children where the outcome is known. There is a significant correlation between the severity of symptoms at presentation to hospital and poor outcome (χ² = 29.07 on 9 df, p < 0.001) (calculations exclude the three children who were dead on arrival).

Macroscopic findings of extensive bleeding around and damage to the cervical spinal cord or brain stem were evident on four of the 14 postmortem examinations. No micropathology findings were available.

Twenty two (34%) children had documented apnoea (table 1), nine had a history of apnoea before admission (one was dead on arrival and three had impaired levels of consciousness), and 13 were recorded as apnoeic at admission (five had documented respiratory arrest). Fourteen of these children required ventilation. Apnoea at presentation was strongly associated with death or severe disability (χ² = 13.3 on 3 df, p < 0.005).

Overall 85% of children had further injuries. These were characteristically multiple. Thirty one children had more than 83 fractures between them (10 had a single fracture, 21 had fractures at multiple sites); 16 children had rib, nine skull, eight long bone, and eight metaphyseal fractures. Eight infants were reported as having recent fractures (four had concurrent old fractures). In 14 the fractures were old (in four reports there was no comment about the timing of the fractures; five cases only had skull fractures that cannot be aged). Forty children were recorded to have bruises; in 28 these were multiple (average four bruises per child, one child had 21 recorded). Two children had adult bites and three burns.

Forming 2×2 contingency tables, the data of table 2 showed that there was no significant difference between the degree of associated injury in children with apnoea and those without. Although the sample size is small, the data indicate a significantly higher number of children with skull fractures in children who presented with apnoea.

SDH was diagnosed on an initial CT scan in 61 cases, on MRI in two, and at postmortem examination only in two cases; 28 children had follow up MRI scans (18 in week 1, seven in week 2, three long term follow up). In 53 cases the investigations were undertaken or reported by a neuroradiologist with a specific interest in paediatric neuroimaging in the tertiary centre. Of the 28 children who were ventilated all scans were undertaken on the day of admission. Table 2 details the intracerebral damage evident on neuroimaging. Of 21 apnoeic children, 10 had cerebral swelling or hypoxic ischaemia on the initial scan compared with eight of 42 without apnoea. Fisher’s test indicated a significant difference between the two groups with p = 0.02.

Table 1 shows a highly significant association between diffuse brain swelling/hypoxic ischaemic damage seen on neuroimaging and poor clinical outcome (χ² = 19.56 on 3 df, p < 0.0003). In a group of 21 cases who had no reported apnoea or intracerebral damage of any kind, only one child died (massive SDH with disseminated intravascular coagulation). There was a significant correlation with a good outcome (χ² = 9.34 on 3 df, p = 0.025).

Of the 16 cases that sustained SDH or effusion from a recognised medical or witnessed accident, only one had apnoea at presentation. Two of the children with severe trauma had diffuse brain swelling. This group had an older age profile range, 85 days to 21 months (mean 8 months). Three children died (two road accident victims, one major trauma). Four had a KOSCHI score of 3, six had a KOSCHI score of 4, and three had a KOSCHI score of 5). The poor outcome was likely to be related to the underlying medical condition in nine cases (meningitis, haemorrhagic disease of the newborn, post-neurosurgery, complex perinatal problems relate to prematurity).

We compared our data with that of other studies (table 3). Although inclusion criteria and definitions vary between studies, the associations between apnoea, other associated injuries, and hypoxic ischaemia are remarkably similar.

DISCUSSION

We have confirmed that SDH from NAHI is particularly prevalent in very young babies who present to hospital with a wide range of symptoms. A significant proportion of these children had apnoeic episodes during the acute phase of their illness. Apnoea is associated with radiological evidence of generalised brain swelling, an early indicator of hypoxic brain damage.^20,21 Coma at presentation, apnoea, and diffuse brain swelling/hypoxic ischaemic damage are associated with a poor prognosis.

We did not see a high incidence of radiological DAI (white matter shearing injury). We acknowledge that we may underestimate DAI on CT scan. It can be more confidently excluded on MRI,^22,23 but is ultimately a neuropathological diagnosis. Previous neuropathology literature reported DAI in NAHI in infants^24–26; this lead to the theory that shaking impact forces frequently cause shearing injury within the brain with consequent poor long term outcome. In the light of current knowledge and more up to date histopathological techniques, Geddes and colleagues^11,13 dispute the validity and proposed pathogenesis of these findings. Recent studies argue that DAI is less commonly seen than previously thought.^11,13,16,27 Our radiological findings support the conclusions of Geddes et al and Johnson and colleagues¹⁶ who advocate that hypoxic-ischaemic injury is of greater importance in terms of both symptoms and signs at presentation and of long term outcome. Diffuse brain swelling, evident on neuroimaging, is known to be associated with a high mortality rate in children with severe head injury,^21,28 more specifically in NAHI.²⁹

Our findings are based on observations recorded in notes and radiological reports drawn from many centres. Our case series includes survivors of NAHI. Nevertheless comparison with a similar case series of Johnson and colleagues¹⁶ and Geddes and colleagues’ subgroup of fatal cases¹¹ are remarkably consistent. Our findings of four children who died and had evidence of macroscopic damage to the cervical spinal cord lend some support to the suggestion that hyperextension/flexion injury to the craniocervical junction may contribute to apnoea and secondary hypoxic ischaemia and diffuse brain swelling. In light of the growing number of reports^8,30 of cervical cord damage in these cases, we would recommend that neuroimaging is extended to include the spinal column.

Most infants and young children with NAHI have associated, serious injuries that would in themselves be sufficient to make a clinical diagnosis of physical child abuse. There is evidence that these infants have been subject to a considerable degree of violence at or around the time of NAHI. In the absence of a high incidence of DAI, Geddes et al conclude that “it may not be necessary to shake an infant very violently to produce stretch injury to its neuraxis” and that “it is possible that the severe acceleration-deceleration injury does not occur in shaken baby syndrome”. These are biomechanical hypotheses proposed by the authors, who, themselves identify 71% of infants with SDH who have significant extracranial injury or skull fracture¹¹ and 85% of children with impact head injury at postmortem examination.¹³ This is indicative of a significant level of force in the majority of their case series. We are concerned that these statements have been widely interpreted in the media and used by defence lawyers¹² to suggest that minimal shaking forces alone may cause “shaken baby syndrome”, when there is no evidence currently to support this.

The majority of SDH seen in NAHI are very shallow and often do not exert significant mass effect on the underlying brain. This may be why the true significance of these collections is sometimes not appreciated when the initial neuroimaging investigations are performed. The SDH itself is often the diagnostic marker of a mechanism of injury and a collection of symptoms and signs that are typically seen in “shaken baby syndrome”. The SDH is rarely the prime cause of the presenting symptoms or responsible for the severe clinical outcome which are more likely to be related to the degree of associated hypoxic-ischaemic damage to the brain.

The factors associated with shaking are multiple and the forces elicited will vary according to the mechanism of injury, be it shaking or shaking impact, the strength and intent of the perpetrator, the size and muscle tone of the baby, and where the baby is held. Small babies have relatively poorly developed respiratory centres and are susceptible to apnoeic episodes. Damage to the cervical cord or brain stem,¹¹ squeezing of the chest, and concussion,³¹ will all impair respiration. Extreme shaking forces may well cause shearing and axonal injury within the brain.⁴ Associated impact injury will contribute to focal brain haemorrhage, contusion, and skull fractures. Together with secondary cerebral hypoperfusion,³² hypoxic ischaemia, and refractory seizures the brain will sustain a combination of diffuse and focal damage.³³

Decisions on forces and mechanisms of injury in this field are clearly complex. The current evidence base is insufficient to make any accurate comment about the degree of force that would be necessary to cause intracranial damage. It is important that multiagency collaborative research to pool biomechanical, clinical, neuropathology, radiology, and sociolegal findings continues to build up this resource. This issue has recently been highlighted by the President of the Family Division, Dame Elizabeth Butler-Sloss, who has called for “further research on the mechanism of subdural haematomas and the degree of force required to cause them in young children and babies, emphasising that this would be ‘highly desirable’ and very helpful for the medical profession faced with the results of injury in hospital, for the child protection teams and the judges and magistrates who try such cases”.³⁴

Although here is evidence of significant associated violence in the majority of infants who suffer from NAHI, at this point in time we cannot quantify the minimum forces required to cause brain damage when a baby is shaken. However, this condition does not arise from normal childcare or play activities. Implicit in this paper and the research literature is that it is never acceptable to shake a baby or child. Where shaking is clinically evident and the care given to the child is deemed “not being what it would reasonable to expect a parent to give”,³⁵ then the child is in need of protection from further harm.