Section 2 -

Shaken Baby Syndrome - Evidence For and Against Henry F. Krous Children's Hospital-San Diego University of California, San Diego School of Medicine San Diego SIDS/SUDC Research Project

Introduction Despite this abundance of observational and experimental evidence about shaken baby syndrome (SBS), unresolved controversies, both in the scientific literature as well as in the prosecution of alleged perpetrators, persist and have been the subject of several reviews. [8, 9, 10, 11, 12] Caffey originated the term "whiplash shaken baby syndrome" to describe a constellation of findings in infants that included subdural and subarachnoid hemorrhages, metaphsyeal fractures, and retinal hemorrhages; further he proposed that consequences to survivors might include cerebral palsy, developmental delay, and epilepsy. [1, 2] Based on research of Ommaya and colleagues, [3, 4, 5, 6] Guthkelch suggested that repeated acceleration and deceleration rather than direct impact was the cause of the intracranial hemorrhages. [7] To date, greater than 280 citations about SBS appear in PubMed searches. Controversies addressed herein are: Is SBS better referred to as inflicted traumatic head injury (ITHI) or abusive head trauma (AHT)? Is SBS a diagnosable entity? Can violent shaking without impact cause the pathology associated with SBS? Is SBS Better Identified As Inflicted Traumatic Head Injury or Abusive Head Trauma? There is increasingly widespread agreement that SBS is better referred to as "inflicted traumatic head injury" (ITHI) or "abusive head trauma" (AHT) since it moves the focus towards the cause and manner of death, and away from controversies, that although scientifically relevant, obfuscate criminal prosecutions. [11] Paradigms supporting this approach can facilitate appropriate analyses of individual cases. [13] Presently, there is widespread consensus that the following injuries are associated with rotational acceleration and deceleration: concussion, tearing of bridging veins with subdural and subarachnoid hemorrhage, interhemispheric subdural hemorrhage, gliding contusions and lacerations at the gray-white interface, traumatic axonal injury, corpus callosum and cerebellar peduncle white matter tearing, craniocervical injury, and diffuse retinal hemorrhages. Hypoxic-ischemia and reperfusion produces secondary cerebral edema progressing to herniation, hypotension, and seizures. Is SBS A Diagnosable Entity? Similar to Caffey's original description, [1, 2] SBS continues to be generally recognized by the presence of intracranial and retinal hemorrhages and acute encephalopathy that are not explained by the history. [14] Other injuries commonly associated with SBS, including to the neck, spinal cord, skeleton, and soft tissues, may also be seen. Infants are the most common victims of SBS. Given the repetition of the injuries and supportive data, the answer is yes. Can Violent Shaking Alone Cause The Pathology Associated With SBS? Clinical Evidence Confessions by perpetrators are the first line of evidence suggesting that shaking without impact can cause the intracranial injuries associated with SBS. [10, 15, 16] Skull or scalp injuries were identified in only 12% (4/32) of cases with perpetrators admitting to only shaking. [16] Symptoms appeared immediately after the abuse in 91% of the cases. Minns reported a 4-month-old infant who presented with clinical features of SBS. [12] Shortly after admission, the perpetrator admitted shaking the infant angrily "in the air". MRI imaging studies of infants with SBS provide evidence that shaking only can produce SDH, cerebral contusion, lacerations, and gray-white interface petechiae. [17] The second line of evidence rests upon the head and neck anatomy unique to the infant. The large head accounts for 10% of infant body weight compared to 2% in the adult. The weak neck muscles give the infant little control over its head movement thereby allowing it to whiplash with each shake. The large extracerebral space is up to 1 cm in depth perhaps predisposing the bridging veins to tearing and subsequent SDH. The laxity of the falx and tentorium of the infant suggests less tethering of the brain allowing it greater movement within the skull. And, the differences in the specific gravity of the gray and white are larger as a result of less myelin, more water, and a cortex fully populated with neurons. Thus greater differences between inertia and tangential accelerations at different radial positions in the gray and white matter predispose to shearing injuries. Experimental Evidence The adult primate experiments of Ommaya et al [5, 18] and Gennarelli and Thibault [19] documented that rotational acceleration/deceleration alone can cause concussion, and brain and upper cord hemorrhage and contusions. Raghupathi, et al subjected 3-5-day-old piglet to rapid, inertial (nonimpact) rotation of the head about its axial plane sustained immediate coma, and postmortem findings of SAH and traumatic axonal injury in central and peripheral white matter tracts in the frontal and temporal lobes and in the midbrain. [20] Subsequently, Raghupathi et al demonstrated graded traumatic axonal injury responses of the brain of 3-5-day-old piglets subjected to a single or double, rapid, non-impact, axial head rotations. [21] Using the biomechanical model of a one-month old baby designed and tested by Duhaime and co-workers in 1987, Cory et al found that combining changes in certain parameters that would lead to increased angular head acceleration with maximal physical shaking could cause angular head acceleration spanning two scaled tolerance limits for concussion. [22] These changes exceeded the original 1987 results suggesting those earlier measured tolerance limits may not be reliable; they therefore concluded "there must now be sufficient doubt in the reliability of the Duhaime et al. (1987) biomechanical study to warrant the exclusion of such testimony in cases of suspected shaken baby syndrome. [22, 23] In Gennarelli and Thibault's study, [19] single acceleration/deceleration pulses were applied to securely-fitted Rhesus monkey heads which rotated through a 600 arc for times varying from 5 to 25 msec with G forces ranging between 100 and 3000. Bilateral acute subdural hemorrhage from torn parasaggital bridging veins caused death in 37 of 128 animals. In his PhD thesis, Morison, the first to use a three dimensional model that accurately represented CSF (protective against translation brain acceleration but lubricates rotation), demonstrated that the combined effect of buoyancy and acceleration resulted in a reduction in the relative translational brain acceleration to only 0.22% of that applied to the skull, [24] (cited by Minns [12]) thereby accounting for the low likelihood of severe brain injury following translational and inertial acceleration impacts. The rotational component of shaking accounts for approximately 93% of the bridging vein strain. This model also demonstrated that the maximum bridging vein stretch ratio is very sensitive to shaking frequency, especially at frequencies between 2-5 Hz; small increases in shaking [20]frequency will result in a disproportionate increase in this ratio increasing the likelihood of tearing and SDH. The ultimate stretch ratio of the bridging veins is 1.5 although some veins may tear at ratios as little as 1.15. Since shaking at a frequency of 4 Hz and amplitude of ± 600 can produce a stretch ratio of approximately 1.26, this model shows that manual shaking places an infant at high risk for SDH. [6, 25, 26] Evidence Against SBS In his report of 54 cases in which someone admitted to have shaken an injured infant, Leestma concluded that valid statistical analyses were not possible and many of the commonly stated aspects of SBS could not be supported. [27] However, it should be noted that his manner of case selection artificially limited the sample size thereby limiting the power for statistics. [28] Detailed case studies are generally published early after recognition of a new disease or pattern of injury in contrast to subsequent papers that present case series, with analysis of case characteristics. Therefore, by restricting his review to published case histories, Leestma eliminated from consideration two published studies in which perpetrators admitted that they inflicted head trauma. [15, 16] In the more recent of these two articles, [16] 69 perpetrators gave enough information to discern reported mechanism of injury; 32 admitted shaking alone. [16] Of these 32 cases, 28 (88%) showed neither skull fracture nor scalp injury. These 28 cases would have markedly increased the statistical power of Leestma's sample, and led to a very different conclusion. Importantly, among the cases which Leestma did review, 18 were fatalities with presentation of both clinical and pathological findings. Analysis of these 18 cases in which data was provided, abnormal mental status (17/17), seizures (6/7), SDH (16/16), retinal hemorrhages (14/14), subarachnoid hemorrhage (9/9), cerebral edema (7/7), and respiratory status (8/8) were reported. [28] Thus, his series actually supports "many of the commonly stated aspects" of SBS. Bandak compared results of head rotational velocity and acceleration derived from his biomechanical experiments on the structural failure limits of the cervical spines of human neonatal cadavers and several animals with those reported in the SBS literature. [29] In contrast to levels of head velocity and acceleration reported in SBS, he calculated that 1. The cervical spine of an infant would experience forces well beyond its structural failure limits, 2. Shaking should cause injury to the cervical spine at considerably lower levels, and 3. The magnitude of his calculated forces are incompatible with the reported rarity of cervical spine injury in SBS. [29] Margulies and Prange subsequently repeated his calculations and found that Bandak's results for neck forces for every single value in his Tables 3 and 4 were actually more than 10 times lower than stated; therefore, they concluded that severe shaking can cause neck injury. [30] References Caffey J. Multiple fractures in the long bones of infants suffering from chronic subdural hematoma. AJR. 1946;56:163-173. Caffey J. On the theory and practice of shaking infants. Its potential residual effects of permanent brain damage and mental retardation. Am J Dis Child. 1972;124(2):161-169. Ommaya AK, Faas F, Yarnell P. Whiplash injury and brain damage: an experimental study. JAMA. 1968;204(4):285-289. Ommaya AK, Yarnell P. Subdural haematoma after whiplash injury. Lancet. 1969;2(614):237-239. Ommaya AK, Hirsch AE. Tolerances for cerebral concussion from head impact and whiplash in primates. J Biomech. 1971;4(1):13-21. Ommaya AK, Gennarelli TA. Cerebral concussion and traumatic unconsciousness. Correlation of experimental and clinical observations of blunt head injuries. Brain. 1974;97(4):633-654. Guthkelch AN. Infantile subdural haematoma and its relationship to whiplash injuries. Br Med J. 1971;2(759):430-431. American Academy of Pediatrics Committee on Child Abuse and Neglect: Shaken baby syndrome: inflicted cerebral trauma. Pediatrics. 1993;92(6):872-875. Case ME, Graham MA, Handy TC, Jentzen JM, Monteleone JA. Position paper on fatal abusive head injuries in infants and young children. Am J Forensic Med Pathol. 2001;22(2):112-122. Krous HF, Byard RW. Shaken infant syndrome: selected controversies. Pediatr Dev Pathol. 1999;2(6):497-498. Krous HF, Byard RW. Controversies in Pediatric Forensic Pathology. Forensic Science, Medicine, and Pathology. 2005;1(1):9-18. Minns RA. 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Cerebral concussion in the monkey: an experimental model. Science. 1966;153(732):211-212. Gennarelli TA, Thibault LE. Biomechanics of acute subdural hematoma. J Trauma. 1982;22(8):680-686. Raghupathi R, Margulies SS. Traumatic axonal injury after closed head injury in the neonatal pig. J Neurotrauma. 2002;19(7):843-853. Raghupathi R, Mehr MF, Helfaer MA, Margulies SS. Traumatic axonal injury is exacerbated following repetitive closed head injury in the neonatal pig. J Neurotrauma. 2004;21(3):307-316. Duhaime AC, Gennarelli TA, Thibault LE, Bruce DA, Margulies SS, Wiser R. The shaken baby syndrome. A clinical, pathological, and biomechanical study. J Neurosurg. 1987;66(3):409-415. Cory CZ, Jones BM. Can shaking alone cause fatal brain injury? A biomechanical assessment of the Duhaime shaken baby syndrome model. Med Sci Law. 2003;43(4):317-333. Morison CN. The dynamics of shaken baby syndrome. Birmingham, UK, Birmingham University; 2002. Holbourne AHS. Mechanics of head injury. 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