Shaken Baby Syndrome

Introduction

The diagnosis “shaken baby syndrome” (SBS) hasbeen widely accepted for over 30 years, but recentevidence from biomechanical and clinical observa-tional studies questions the validity of the syndrome.

Definition

The diagnosis of SBS is based on the clinical triadof encephalopathy, retinal hemorrhage (RH), andsubdural hemorrhage (SDH) in infants, usually undersix months of age, who may die unexpectedly orsurvive with greater or lesser degrees of neurolog-ical damage [1]. The term non-accidental head injury(NAHI) has been preferred as it has no implicationsfor mechanism of injury. Other features often associ-ated include a sole carer at the time of collapse anda clinical history that is incompatible with the sever-ity of the injuries. The diagnosis of inflicted injurybecomes less problematic if there is objective evi-dence of violence, such as bruises, fractures, or burns,but objective evidence of trauma has not always beennecessary in making the diagnosis.

Central to the assessment of these cases is whetherthe triad of findings can be regarded as diagnosticof abuse with any degree of certainty. This reviewexamines the evidence base for each element ofthe triad and the current biomechanical evidenceregarding mechanisms of infant head injury and itspathological investigation.

History

SDH has been associated with child abuse since themid-19th century [2]. Kempe described SDH withmultiple skeletal injuries and bruises as the bat-tered child syndrome and Caffey described long bonefractures and SDH [3–5], but it is Guthkelch [6]who developed the hypothesis that the whiplash–likemovements during shaking cause the characteristicbilateral thin film SDH of the syndrome. He basedhis hypothesis, that shaking causes tearing of thecerebral bridging veins leading to SDH, on the biome-chanical studies of Ommaya [7] who was researching

adult head injury in road traffic accidents. FollowingGuthkelch’s paper, the “shaken baby syndrome” hasbecome widely accepted as a form of child abuse [1].

The Triad of Injuries

The three elements of the triad are encephalopathy,RH, and SDH.

Retinal Hemorrhages (RHs)

RHs have been regarded as an important indicatorof inflicted injury, but many other causes of reti-nal bleeding are recognized in infants, for exampleafter normal birth, raised intracranial pressure, blooddyscrasias, hemoglobinopathies, extracorporeal mem-brane oxygenation, cataract surgery, and accidentaltrauma [8]. Postmortem indirect ophthalmoscopy hasshown RHs to be more common after natural dis-ease and accidental injury than after inflicted injury[9]. These authors also noted that infants suspectedto have been abused were more likely to have oph-thalmological examination in life than infants withaccidental injuries or natural diseases. This bias read-ily distorts the true incidence of RH in non-accidentalinjury. Indeed Vinchon [10] noted in his study ofinfant head injury that “In the construct of our studywe could not obviate the circularity bias, and the eval-uation of the incidence of RH in child abuse remains aself-fulfilling prophecy”. These authors did, however,suggest that the extent and nature of retinal bleedsmay be more important as indicators of inflicted headinjury than their existence per se [10].

The main hypotheses for genesis of RH are thatit is the result of venous obstruction, which in turnmay result from compression of the optic nerveby raised intracranial or intravascular pressure, eventransiently, or that the tissues of the retina are tornduring the act of shaking. This latter hypothesis doesnot withstand biomechanical scrutiny [11].

Encephalopathy

This term may be widely interpreted to include arange of clinical manifestations from feeding dif-ficulties, vomiting, and sleepiness to seizures andfulminating cerebral edema.

The specific neuropathological features of trau-matic brain injury are contusions and traumatic

2 Shaken Baby Syndrome

(a) (b)

Figure 1 (a) Acute axonal injury. Bands of BAPP expression in an infarcted area of brain in acute hypoxic-ischemicinjury. (b) Axonal swellings expressing BAPP restricted to the pontine cortico-spinal tracts, considered to indicate traumaticdamage

axonal injury. Hypoxic-ischemic injury and brainswelling are frequently seen but are not specific fortrauma. Contusions are very uncommon in infantbrain trauma in the absence of skull fractures. Identifi-cation of axonal injury now depends on the immuno-cytochemical demonstration of beta amyloid precur-sor protein (BAPP). This is a very sensitive marker ofinterruption of normal axonal flow but may be upreg-ulated after hypoxic–ischemic injury and metabolicdisruption as well as trauma (Figure 1). Distinctionof traumatic axonal expression of BAPP from othercauses is fraught with difficulty, and depends in parton its distribution [12], [13], [14]. Neuropathologicalstudies have shown that in babies who die followingNAHI, the underlying brain pathology is widespreadhypoxic-ischemic injury and not diffuse traumaticaxonal injury as previously believed [12, 13]. In thisseries axonal injury was seen in a limited distribu-tion in the lower brainstem and in only a minorityof cases. Radiological studies have confirmed thesepathological observations [15].

This observation is important as traumatic axonalinjury will lead to immediate loss of function causingclinical symptoms from the time of trauma. Incontrast, hypoxic-ischemic injury and ensuing brainswelling take variable periods of time to developand a baby so damaged may not show immediatesymptoms. Even fatal brain trauma may present witha lucid interval between injury and clinical collapse[16, 17]. Lucid intervals are more frequently seenin infants less than two years of age [18], reflectingthe very different responses of the infant brain to

injury due to the specific intracranial pathophysiologybefore the skull bones fuse [19].

Damage to the cervical nerve roots has beendocumented as part of the pathology of shaking injury[14]. It has not been established that this is the resultof shaking, as cervical cord displacement resultingfrom brain swelling may also cause traction on nerveroots in the region. Autopsy studies in man andprimates have shown that the spinal cord is displacedduring extension and flexion of the neck [20, 21]and it remains a possibility that hyperextension andflexion could cause traction damage to nerve rootsthroughout the length of the spinal cord, but this hasnot been documented in living infants.

Subdural Hemorrhage (SDH)

SDH is perhaps the most important and consistentcomponent of the triad. In the acutely sick infant, itis frequently the first clinical sign, identified on brainscan, to raise the question of abuse. There are nospecific imaging patterns that can distinguish inflictedfrom accidental intracranial injury [22, 23].

Autopsy and imaging studies show that infantSDH is usually a thin bilateral film and not a thick,unilateral space occupying clot as seen in traumaticSDH in older children and adults [12, 13, 24]. Thisraises the question of whether the two forms have thesame etiology and anatomical source.

Causes of Subdural Hemorrhage. The common-est cause of SDH in infants is said to be trauma[25] although a recent study has shown a significant

Shaken Baby Syndrome 3

incidence (26%) of birth-related SDH [26]. Othercauses in infants include benign enlargement ofthe extracerebral spaces (BEECS), clotting disorders,hemorrhagic disease of the newborn, rare metabolicdiseases, vascular malformations, and neurosurgicalprocedures [25, 27].

Traumatic SDH

Proposed traumatic causes of infant SDH are inflictedinjury such as shaking and/or impact and accidentalinjuries such as falls. Impact includes blunt impact ofan object on the head and that resulting from a fallor striking the moving head on a rigid surface. Thebiomechanical aspects of these injuries are discussedbelow. The vast majority of cases described as SBShave evidence of impact [28]. While the pathologistmay be able to determine features indicative ofimpact, it is not, of course, possible to distinguishaccidental from non-accidental injuries by pathology.

Low-Level Falls

Low-level falls have the potential, albeit only rarely,to cause SDH in infants and young children. Absoluteheight is not as important a criterion for injury asthe exact nature of the fall for a particular infant,in a particular circumstance [29]. The effects oftwisting, rotation, or crushing of the structures of theneck are crucial in terms of outcome. Biomechanicalstudies show that falls even from low levels of3–4 ft can generate far greater forces in the headthan shaking [11]. There are a number of case seriesdemonstrating that infants and children may suffer

intracranial damage including retinal and intracranialhemorrhage after falls from levels as low as 3 ft [10,17, 30–33]. While most babies may suffer little froman apparently trivial fall, this is clearly not alwaysthe case.

Birth-Related SDH

Three studies, using magnetic resonance imaging(MRI), have shown a surprisingly high incidenceof SDH after birth in asymptomatic infants. Whitbyidentified SDH in the first two days of life in 9%[32], while SDH was seen in up to 46% of otherwisenormal neonates using higher resolution MRI scan-ning [26, 34]. With regard to method of delivery,ventouse or instrumental deliveries have been asso-ciated with a higher incidence of intracranial injury[35, 36]. Towner [37] found an increased incidenceof intracranial hemorrhage after instrumental deliverywith ventouse or forceps and emergency caesareansection, but the incidence was lower after caesareansection before labor had begun. However, it shouldbe noted that all of Looney’s cases followed normalvaginal delivery [26].

While neonates with SDH may be asymptomatic[26, 35] they may also have signs in the neonatalperiod including unexplained apnoea, dusky episodes,hypotonia, seizures, and lethargy [38].

Sources of SDH. Traditional belief is that in SBSthe SDH results from tearing of the superficial bridg-ing veins as they cross from the brain to the duralsinuses [6] (Figure 2). This has never been proved.

Figure 2 Infant bridging veins may be visualized by opening the skull very carefully, but they are readily torn in normalautopsy procedures. (Picture courtesy of Dr P. Lantz)

4 Shaken Baby Syndrome

Indeed it is very difficult to find documented evidenceof torn bridging veins at surgery or at autopsy. Cush-ing, who operated on neonates with SDH and sub-sequently performed the autopsies wrote “In two ofthe cases I have examined I have satisfied myself thatsuch ruptures were present. A positive statement, how-ever, cannot be given even for these cases, since thedissection and exposure, difficult enough under anycircumstances, owing to the delicacy of the vessels isthe more so when they are obscured by extravasatedblood” [39]. More recently Maxeiner [40] addressedthe problem by injecting radio-opaque dye into theveins at autopsy to assess their integrity after remov-ing the top of the head in one piece, hard-boiled eggstyle. This approach is not widely used as it destroysmuch of the brain and injection pressures need to becarefully monitored if the veins are not to be rupturedartifactually.

Volpe [41] said that SDH was by no meansalways traumatic and suggested that in neonateswithout tentorial tears the bleeding may arise fromthe tributary veins of the dural sinuses. Autopsystudies from the older literature show bridging veinrupture is uncommon, Craig described 62 neonatalSDH, of which only 3 had torn bridging veins,all of those with overriding sutures [42]. Larrochedescribed 700 autopsies 18% with SDH. [43] Shenoted an association with hypoxic-ischemic injury(Figure 3). She did not identify torn veins.

If SDH does not arise from torn bridging veins,what other sources may there be? Two obvious

alternative sites of origin exist, the dura itself andthe old subdural membranes (Figure 4).

Dural Hemorrhage

The dura is composed of two leaflets, the periostealand the meningeal dura, separated by a thin vascularchannel, which widens to form the large dural sinuses[44]. There are particularly extensive venous sinusesin the posterior falx, [45] a frequent site of high signalon brain scans in asphyxiated infants. Bleeding intothe falx is well recognized in asphyxiated infants[46]. It has long been acknowledged that opticnerve sheath hemorrhage arises from the dura [47]and more recently the dura was proposed as thesource of intracranial SDH in infants [48] (Figure 5).Careful microscopic examination of the dura confirmsthat intradural bleeding is common in asphyxiatedinfants, particularly in the dural folds of the falx andtentorium close to the large venous sinuses [49]. Insome cases intradural bleeding leaks out on to thesubdural surface leading to macroscopically evidentsubdural haematoma [50].

Healing Subdural Membranes

Healing of SDH is by formation of a thin, vascu-lar membrane consisting of fibroblasts, macrophages,which often contain altered blood products, and widethin-walled capillaries with a potential to rebleed[51] (Figure 6). It is uncommon in infants to see adouble layered membrane around a localized massof resolving clot, as seen in the elderly, probablybecause the infant SDH usually forms as a thin film

Figure 3 Fresh subdural blood seen after birth asphyxia. (Picture courtesy of Dr I. Scheimberg)

Shaken Baby Syndrome 5

Superior sagittal sinusArachnoidgranulation

Intradural fluid channel

Lateral lacuna ofsagittal sinus

Inner dural plexus

Arachnoid barriermembrane Falx

Corticaldraining vein

Subarachnoidspace

Dura

Figure 4 Diagram representing a coronal slice through the brain and dura indicating the intradural sinuses and theirrelationship to cortical surface veins, arachnoid granulations, and intradural fluid channels

(a) (b)

Figure 5 (a) The dura is thickened and congested and there is patchy subarachnoid and subdural blood. Autopsy 44 hafter collapse following choking episode. (Courtesy of Dr I. Sheimberg.) (b) H & E stained section of falx showing it tobe destroyed by massive acute bleeding

rather than as a mass lesion. Contrast injection isrequired to identify the membranes radiologically[52]. In some cases, acute SDH leads to accumu-lation of fluid in the subdural space. The reasonsfor this are unknown. Fluid collections may resultfrom immaturity of the arachnoid granulations andimpaired cerebrospinal fluid (CSF) absorption [22],

and be influenced by the method of treatment ofthe acute hematoma. Surgical evacuation or tap-ping may prevent later reaccumulation of fluid [53,54]. The period of time for redevelopment of sub-dural fluid collections may be long, between 15and 111 days [55]. It is likely that an importantcontribution to chronic subdural fluid accumulation is

6 Shaken Baby Syndrome

(c)

(b)(a)

Figure 6 (a) Dural surface showing a very thin yellow-brown membrane, which has partly lifted during removal of thebrain. Head injury four weeks prior to death. (b) H & E stained section of acute bleed overlying a chronic membrane, whichconsists of some six layers of fibroblasts between which are macrophages and new capillaries (three days after collapsewith acute SDH) (c) Same section stained with CD34 to show endothelial cells. Note capillaries growing into the fresh clot

repeated rebleeding and oozing from a chronic sub-dural membrane [56, 57].

There is little information regarding the potentialfor birth-related SDH to evolve into chronic fluidcollections. Whitby followed nine cases with a repeatscan at one month; none had developed a chroniccollection [35]. Rooks followed 18 cases for up to 3months, one developed a further subdural bleed [34].However these studies could not identify membranesas contrast was not used. Chronic membranes havebeen seen at autopsy in up to 31% of infants dyingunexpectedly without previous clinical evidence ofchronic SDH [58]. In view of the potential for acuteaccidental SDH to evolve into a chronic collectionseveral months later [55], it would appear likely thatthe same pattern would follow birth-related SDH. Atthis time, we simply have insufficient information.

Distribution. In the first few days after bleeding,subdural blood sediments under the influence ofgravity and undergoes secondary redistribution to themost dependent part, the posterior falx and tentorium[59]. Radiological studies show that subdural bloodtracks down around the spinal cord [60] and, if thespine of babies with intracranial SDH is examined atautopsy, blood is regularly seen in the subdural spaceand around sacral nerve roots in the most dependentparts of the dural sac (Figure 7).

Differential Diagnosis of SBS

The most common causes of the triad are impact,birth-related SDH, BEECS, coagulopathies, apnoea,asphyxia and choking, acute life-threatening events

Shaken Baby Syndrome 7

(a) (b)

Figure 7 (a) A collection of fresh subdural blood at the dorsal aspect of the sacral spinal cord. Baby died within hoursof inflicted abdominal injury with acute and chronic subdural hemorrhage. (b) Microscope section showing an ellipticalcollection of fresh blood dorsal to the spinal cord. The blood is within a chronic subdural membrane indicated by the ironpigment, stained here by Perl’s stain. Baby died three weeks after traumatic subdural hemorrhage

(ALTEs), osteogenesis imperfecta, osteopenia ofprematurity, and metabolic diseases [14, 28, 61,62, 63].

Choking/Asphyxia

In a considerable number of cases, vomiting and/orreflux are described at the time of collapse, andin some there is a history of feeding difficulties,gastroesophageal reflux, and choking or apnoeicepisodes [14, 62]. SBS is commonly diagnosed in thefirst three months of life, the age of peak incidence ofsudden infant death syndrome. Inhalation of feed orvomit may play a part in sudden infant death [64] andawake apnoea is associated with gastroesophagealreflux [65]. The physiological response to aspirationmay be dramatic; foreign material on the larynxcauses laryngospasm, which is associated with startle,cessation of respiration, hypoxaemia, bradycardia,and a doubling of blood flow to the brain [66].These circumstances, with or even without vigorousresuscitation, may cause reperfusion injury and a pre-existing healing subdural membrane may bleed. Thedura itself may become hemorrhagic and ooze bloodinto the subdural space (Figure 8). As long ago as1905, Cushing suggested that coughing, choking, andvenous congestion may explain some forms of infantSDH [39], a hypothesis recently revived by Geddes,[48, 67].

Biomechanics

Biomechanics is the application of principles ofphysics to biological systems and has been the main-stay of research into motor vehicle safety for sixdecades. It was just such research into noncontacthead injury from rear-end shunts that stimulatedGuthkelch to formulate his hypothesis for SBS in1971 [6]. Ommaya [7] had caused concussion, SDH,and white matter shearing injury (diffuse axonalinjury) in primates by whiplash. Guthkelch suggestedthat the rotational forces of shaking would causetearing of bridging veins and bilateral subdural bleed-ing, although Ommaya himself warned that “It isimprobable that the high speed and severity of thesingle whiplash produced in our animal model couldbe achieved by a single manual shake or even a shortseries of manual shaking of an infant in one episode”.

More recent studies using “crash test dummies”indicate that impact generates far more force thanshaking (Figure 9) and that impact is required toproduce SDH [68]. Cory and Jones [69] generatedforces that exceeded the injury threshold for concus-sion, but not for SDH or axonal injury. Their adultshaker volunteers fatigued after 10 seconds. Whilethey concluded that “It cannot be categorically stated,from a biomechanical perspective, that pure shak-ing cannot cause fatal head injuries in an infant”,they noted that in their experiments there were chinand occipital contacts at the extremes of the shaking

8 Shaken Baby Syndrome

(a) (b)

Figure 8 (a) Cortical vein thrombosis. Infant died 10 days after collapse following two choking episodes. Several surfaceveins are thrombosed (arrows). (b) Section of thrombosed vein shows a network of new capillaries growing into theperiphery of the thrombus (CD31)

125

100

75

50

25

0

Peak head acceleration (g)

Free fall impacts ontocarpeted stairs

(fall heights noted)

25.4

cm

50.8

cm

76.2

cm

Fro

m a

dult

mal

e’s

arm

sInflicted slammingstyle impacts onto

surfaces noted

Leat

her

sofa

Bed

– m

attr

ess

Figure 9 Comparative forces generated by dropping or shaking and slamming a dummy representing a six-month-oldinfant (C Van Ee, personal communication 2007)

motion that could have caused impact. These authorsexpressed their concerns regarding the difficulties inextrapolating to human infants the findings in bothdummy and animal models. Biomechanical studieshave shown that falls and impact to the head pro-duce significant rotational forces when the impactingforces are not aligned through the center of gravityof the head, due to hinging of the head on theneck. Shaking is not necessary to cause rotationalacceleration.

Neck injuries may be underreported in babiesdying after severe abuse [70]. In Ommaya’s study,11 of 19 primates had neck injuries; these were adultanimals with mature neck structure and musculature.

It is likely that the forces required to cause intracra-nial injury will also damage the weak infant neck[71]. In road traffic accidents, infants who suffer sin-gle severe hyperextension forces have cervical frac-tures, dislocations, spinal cord injury, and torn nerveroots, not SDH [72–74].

Investigation of Shaken Baby Syndrome

SBS or NAHI is most likely to occur in an infantdying suddenly under the age of six months. Autopsyshould be performed with careful consideration ofthis diagnosis and appropriate steps taken to supportor exclude it. The records of pregnancy and delivery

Shaken Baby Syndrome 9

must be carefully studied to look for any evidence ofcomplications that could mimic NAHI. These includepregnancy disorders such as oligohydramnios, fetalhypokinesia, and prematurity, which lead to osteope-nia and predispose to fractures. The birth history andmethod of delivery are important as SDH may ariseat this time while being entirely asymptomatic inthe neonatal period. Head circumference charts areimportant; head circumference measurements taken atbirth and in the subsequent weeks may reflect abnor-mal head growth, which can indicate an accumulatingsubdural fluid collection and a propensity to rebleed.

The clinical history may give clues to other prob-lems in the early weeks of life. Vomiting, feedingproblems, and apnoeic episodes and ALTEs mayindicate difficulties with coordination of breathing,sucking and swallowing, and vulnerability to chok-ing. Any event that threatens life may also potentiallyend it.

The history of the baby’s terminal collapse mustalso be carefully examined. Parents may describeevents that reveal a cause for collapse. In any otherfield of medicine, the clinical history is regarded asthe cornerstone of diagnosis and it should not bedisregarded without serious critical evaluation.

The autopsy can reveal evidence of trauma suchas deep bruises and fractures not seen in clinicalexamination. The examination of the intracranialcontents is paramount. The scalp and skull requirecareful examination for evidence of bruising andfractures. Suture separation due to raised intracranialpressure and wormian bones can be mistaken forfractures. When the cranium is opened, the presenceof any intracranial bleeding must be noted. Unclottedblood may escape from the subdural space as theskull is opened and be mistaken for bleeding from thedural sinuses. It is important to note the volume andnature of blood and the presence of xanthochromia,indicating older bleeding. As the cranium is opened,the bridging veins should be visualized and theirintegrity assessed. If there is a question of bridgingvein rupture, histological examination may assist inestablishing this. The dural sinuses and draining veinsshould be examined for evidence of thrombosis.

The dura must be carefully examined for evidenceof older bleeding. A chronic subdural membrane maybe thin and patchy and represented only by patchesof light brown discoloration. Multiple samples shouldbe taken from the dura, including the falx andtentorium, for histological examination to look for

evidence of intradural bleeding and rupture ontothe subdural surface. This may be the source ofsignificant subdural blood.

The brain must be fixed for detailed histologicalexamination.

In all of these cases, the time between collapseand death may play a significant part in the finalpathology. A baby who has collapsed and becomesapnoeic with subsequent cardiopulmonary rescusci-tation (CPR) and ventilation will be shocked andsuffer multiorgan failure with altered clotting, lossof integrity of vessels and membranes, oozing ofblood into intracranial compartments, including thesubarachnoid and subdural spaces, and developmentof the “respirator brain”.

Review of the brain imaging in life is essentialin assessing, as far as possible, just how muchhemorrhage occurred at the time of collapse and howmuch may be the result of subsequent secondarychanges. It is recognized that SDH may continue tobleed after initial onset [75] especially if a baby isvery sick. Finding a large clot at autopsy may suggesttraumatic rupture of a large vessel, but comparisonwith early brain scans may indicate that the bleed wasonly minor at the outset, indicating a slower oozingprocess with different implications for causation. Itis becoming increasingly obvious that not all SDHarises from traumatic rupture of blood vessels.

Acknowledgment

I would like to thank Dr Irene Scheimberg and Dr Pat Lantzfor providing pictures and Dr Chris Van Ee for valuablediscussion and for preparing Figure 8.

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