Pediatr Radiol (2003) 33: 868871 DOI 10.

1007/s00247-003-1025-3

CASE REPORT

Paul M. Parizel Berten Ceulemans Annick Laridon Ozkan Ozsarlak Johan W. Van Goethem Philippe G. Jorens

Cortical hypoxic-ischemic brain damage in shaken-baby (shaken impact) syndrome: value of diffusion-weighted MRI

Received: 5 February 2003 Revised: 30 May 2003 Accepted: 22 June 2003 Published online: 16 September 2003 Springer-Verlag 2003 P.M. Parizel (&) O. Ozsarlak J.W. Van Goethem Department of Radiology, University of Antwerp, Wilrijkstraat 10, 2650 Edegem, Belgium E-mail: parizelp@uia.ua.ac.be Tel.: +32-3-8213732 Fax: +32-3-8252026 B. Ceulemans A. Laridon Department of Pediatric Neurology, University of Antwerp, Wilrijkstraat 10, 2650 Edegem, Belgium P.G. Jorens Department of Pediatric Intensive Care Medicine, University of Antwerp, Wilrijkstraat 10, 2650 Edegem, Belgium

Abstract Shaken-baby syndrome (SBS) is a type of child abuse caused by violent shaking of an infant, with or without impact, and characterized by subdural hematomas, retinal hemorrhages, and occult bone fractures. Parenchymal brain lesions in SBS may be missed or underestimated on CT scans, but can be detected at an earlier stage with diusion-weighted MRI (DW-MRI) as areas of restricted diusion. We demonstrate the value of DW-MRI in a 2-month-old baby boy with suspected SBS. The pattern of diffusion abnormalities indicates that the neuropathology of parenchymal lesions in SBS is due to hypoxicischemic brain injuries, and not to diuse axonal injury.

Keywords Shaken baby syndrome Magnetic resonance imaging Diusion Brain injury Subdural hemorrhage

Introduction
Nonaccidental trauma accounts for a high percentage of craniocerebral injuries in infants less than 1 year of age [1, 2]. Shaken-baby syndrome (SBS) is the most common cause of death or serious neurological or visual impairment in this age group [3]. The syndrome occurs when the infants brain is subjected to rapid acceleration, deceleration or rotational forces, by shaking the head, with or without impact [4]. There is growing evidence that impact to the head is an essential component of the injury complex [5]. Therefore many authors prefer the terminology shaken impact syndrome (SIS) [5, 6, 7]; however, SBS and SIS are often used interchangeably or in combination [8, 9]. SBS is characterized by a combination of intracranial injury (e.g., subdural hematoma,

subarachnoid hemorrhage, parenchymal brain lesions), ocular lesions (retinal hemorrhages), and skeletal manifestations (occult bone fractures) [1, 10, 11]. The clinical diagnosis of SBS is dicult to make and remains controversial [12, 13]. Imaging techniques play a major part in establishing the diagnosis of SBS [2]. The purpose of this paper is to demonstrate that magnetic resonance imaging (MRI), and especially diusion-weighted magnetic resonance imaging (DW-MRI), is the most sensitive and specic method of conrming the hypoxicischemic brain injuries associated with a shaking injury.

Case report
A 2-month-old baby boy was brought to the emergency room with a history of somnolence, frequent crying, diarrhea, and

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Fig. 1 Axial noncontrast CT scan obtained on the day of admission from a 2-month-old baby boy with suspected shaken baby syndrome (SBS). Thin, hypodense extra-axial eusions are seen over both frontal lobes. Multiple hypodense areas are observed in the frontal, temporal, and occipital lobes uncontrolled movements of the upper and lower limbs. Physical examination was unremarkable. The fontanel was normal. There was no fever. Hematologic laboratory data and blood chemical values were normal. No skin lesions or occult bone fractures were found. Both parents denied a history of craniocerebral trauma. Shortly after admission, the boys clinical condition deteriorated rapidly. He developed repetitive generalized tonic-clonic seizures and severe respiratory depression, requiring urgent intubation. The child was ventilated, and given phenytoin. A noncontrast CT scan of the brain (Fig. 1) showed multiple areas of decreased attenuation in both cerebral hemispheres. There were thin, hypodense subdural collections over both frontal lobes. The low-density appearance of these collections could point to Fig. 2 MRI examination, obtained 2 h after admission. a, b Axial turbo FLAIR images reveal bilateral subdural hematomas, extending into the interhemispheric ssure. c, d Axial diusionweighted MR images (DW-MRI), obtained with a b value of 1,000 mm2/s, show conuent hyperintensities involving the cortical gray matter and subcortical white matter in the frontal and temporal and occipital lobes. The lesions were hypointense on the apparent diusion-coecient (ADC) maps, indicating areas of restricted diusion. This nding is consistent with diuse hypoxicischemic brain injury

subacute or chronic subdural hematomas, or acute traumatic hygromas. The diagnosis of shaken-baby syndrome was suspected. Fundoscopic examination revealed widespread bilateral retinal hemorrhages, but no papillary edema. Plain radiographs of the chest, axial skeleton, and extremities showed no abnormalities. Emergency MRI of the brain was performed on the same day (Fig. 2) using the following pulse sequences: axial turbo uidattenuated inversion recovery (FLAIR) images, axial inversion recovery T1-weighted images, axial echo-planar DW-MRI scans with b values of 0, 500, and 1,000 mm2/s (trace images and ADC maps), coronal HASTE T2-weighted scans, and MR angiography (MRA) with 3D time-of-ight technique and maximum intensity projection reconstructions. The MRI examination conrmed bilateral subdural hematomas, extending into the interhemispheric ssure (Fig. 2a, b). The DW-MRI scans revealed gyriform areas of restricted diusion involving the edematous cortical gray matter of both hemispheres (Fig. 2c, d). These areas were hypointense on the corresponding ADC maps. This indicates cytotoxic edema, presumably due to widespread cortical hypoxic-ischemic brain damage. The parenchymal abnormalities were not well seen on the FLAIR images, though it must be remembered that FLAIR images in infants are relatively insensitive in comparison with those of older children and adults. MRA showed normal intracranial arteries. There was no evidence of venous sinus occlusion. When confronted with the imaging ndings, the father admitted to vigorous shaking of the baby. The subdural hematomas were removed neurosurgically, and a ventricular catheter was placed. During the rst postoperative day, rapid increase in intracranial pressure was observed. Despite maximal antiedematous and anticonvulsive treatment, including administration of pentobarbital, the elevation of intracranial pressure persisted. Follow-up CT scans on days 2 and 6 after admission demonstrated a dramatic increase of the cerebral parenchymal ischemic areas and the appearance of intracerebral hemorrhage (Fig. 3). Over the next few days, the patients clinical condition gradually improved. The boy was extubated on day 9 and discharged from the ICU to a pediatric ward in hemodynamically and respiratory stable condition, but with no evidence of higher cortical functions. The child survived and was last seen at the age of 9 months. There was eye contact and motor development was scored at approximately 4 months. Clinical examination revealed acquired microcephaly, a convergent squint, and spastic quadriplegia.

Discussion
The diagnosis of SBS remains a formidable clinical challenge. The consequences of this diagnosis are grave,

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Fig. 3 Follow-up noncontrast CT scan (day 6 after admission) shows a dramatic increase of the cerebral parenchymal abnormalities, which are seen as hypodense regions (suggestive of edema) and hyperdense areas (indicating intraparenchymal hemorrhage). The density in the left frontal horn is a shunt catheter. There is a small amount of blood in the occipital horn on the right

both for the baby and his/her parents or caregivers. Missing the diagnosis of SBS in an acutely ill infant can lead to permanent neurological damage or even death [14]. On the other hand, when a false-positive diagnosis of SBS is made, parents or caregivers may be falsely accused of assault. By clinical examination one cannot dierentiate with certainty between accidental and inicted injury, especially in the absence of external signs of violence [12, 15]. Retinal hemorrhages in an infant are a cardinal feature of SBS. Traditionally, retinal hemorrhages were believed to be caused by an abrupt rise of intracranial pressure (shaking plus strangulation or suocation mechanism); however, recent evidence suggests that the retinal hemorrhages could be the result of mechanical shaking forces [11]. Whatever the etiology, the nding of retinal hemorrhages is not specic, nor does their absence rule out the possibility of nonaccidental trauma. Increasingly, therefore, the diagnosis of SBS relies on radiologic evidence of intracranial damage. CT has revolutionized the assessment and management of suspected SBS, and remains the principal imaging modality in the acute setting [2, 10]. CT scans of the brain nearly always demonstrate subdural hematomas, which are the most common manifestations of SBS. Subdural hematomas of varying ages, or located in the interhemispheric ssure are considered to be highly suggestive of shaking injury [1]. It is believed that the acceleration/deceleration forces which occur during violent shaking are sucient to cause rupture of the vulnerable bridging veins, which, in young babies, can easily be torn [2]. Infants tend to have relatively large volumes of cerebrospinal uid around the brain, which allows for greater movement within the cranial vault [11]. Moreover, the neck muscles

of babies are not strong enough to support the range of motion of their relatively large heads. The presence of subdural hemorrhages can also be explained by a combination of severe hypoxia, brain swelling, and raised central venous pressure, which causes blood to leak from intracranial veins into the subdural space [16]. It must be remembered, however, that not all subdural hematomas are due to child abuse. MRI has increased the sensitivity for diagnosing SBS in detecting and characterizing small extra-axial hemorrhages in infants with equivocal CT ndings [2, 10]. On CT, subdural collections are often of a nonspecic character (e.g., subacute or chronic sudural hematomas that are of low density or isodense), as shown in our patient. MRI has a 50% greater rate of detection of subdural hematomas than CT [17]. Moreover, MRI is more accurate in dating subdural hematomas and allows dierentiation of a recent subdural hemorrhage from one superimposed on a pre-existing one [18]. Even more importantly, MRI reveals the presence of nonhemorrhagic parenchymal brain damage not shown or underestimated on the acutely performed cerebral CT scan, such as diuse axonal trauma or hypoxic-ischemic encephalopathy [2, 3, 15, 19]. DW-MRI is a technique that is sensitive to restricted diusion, reecting cytotoxic edema, which occurs in acute hypoxic-ischemic brain damage. In our patient, we found widespread, gyriform regions of decreased diusion in the cortical gray matter. This pattern suggests that the neurophysiopathology of the severe encephalopathy in SBS is hypoxic-ischemic brain damage, and NOT diuse traumatic axonal injury. Neuropathological studies by Geddes et al. have conrmed that global severe hypoxic damage is by far the most common histological nding in inicted head injury in children, and that widespread axonal damage is much less frequent [20, 21]. The diffusion abnormalities observed in our patient were predominantly found in cortical gray matter, which appeared thickened and edematous. Other investigators have shown diusion abnormalities in the subcortical brain tissue, consistent with watershed infarctions, especially in the posterior brain regions [15]. Magnetic resonance spectroscopy ndings conrm that the pathophysiology of nonaccidental head trauma is due to hypoxic-ischemic injury, by showing the metabolic changes occurring in the infant brain after a shaking injury [22]. Hypoxic injury to the brain results in loss of N-acetyl aspartate and accumulation of lactate, although the mechanism in SBS appears to be somewhat dierent from hypoxic injury alone [22]. In summary, in our patient with SBS, DW-MRI showed a dramatically greater lesion extent than was seen on conventional MR images or on CT scans. DWMRI may represent the most sensitive and specic technique in the evaluation of cerebral damage in shaken babies. The use of DW-MRI may help to guide clinical

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management of these patients, to identify children at high risk for poor outcome, and to provide an estimate regarding the timing of the alleged assault. Thus, the time-dependent signal intensity changes on DW-MRI may be of great importance in forensic medicine. The areas of restricted diusion indicate cytotoxic edema and conrm the neuropathological observations that the

parenchymal brain damage in SBS is predominantly due to diuse hypoxic-ischemic encephalopathy, and not to diuse axonal injury [21].
Acknowledgements We are grateful to V. De Groot, MD, for providing fundoscopic evidence of retinal hemorrhages. We also thank G. Van Hoorde for photographic assistance.

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