This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow E-mail this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My File Cabinet
Right arrow Download to citation manager
Right arrowRequest Permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via CrossRef
Right arrow Citing Articles via Web of Science (19)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Bonnier, C.
Right arrow Articles by Sébire, G.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Bonnier, C.
Right arrow Articles by Sébire, G.
Related Collections
Right arrow Office Practice
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us   Add to Digg   Add to Facebook   Add to Reddit   Add to Technorati   Add to Twitter  
What's this?
PEDIATRICS Vol. 112 No. 4 October 2003, pp. 808-814

Neuroimaging of Intraparenchymal Lesions Predicts Outcome in Shaken Baby Syndrome

Christine Bonnier, MD*, Marie-Cécile Nassogne, MD, PhD*, Christine Saint-Martin, MD{ddagger}, Bettina Mesples, MD§, Hazim Kadhim, MD, PhD*,|| and Guillaume Sébire, MD, PhD*

* Service de Neurologie Pédiatrique
{ddagger} Département de Radiologie, Cliniques Universitaires Saint-Luc, Université Catholique de Louvain, Brussels, Belgium
§ Service de Pédiatrie Générale, Hopital Robert-Debré, Faculté Xavier-Bichat, Université Paris VII, Paris, France
|| Service de Neuropathologie, CHU Brugmann, ULB, Brussels, Belgium


   ABSTRACT
TOP
 ABSTRACT
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Objective. Studies of long-term outcome on nonaccidental head injury (NAHI) in young children have shown severe neurodevelopmental sequelae in most cases. For improving the knowledge of outcome and for identifying prognostic factors, additional clinical and cerebral imaging data are needed. The aim of this study was to describe clinical and imaging features over time and to consider their value for predicting neurodevelopmental outcome.

Methods. A retrospective medical record review was conducted of 23 children with confirmed NAHI, for whom an extended follow-up of 2.5 to 13 years (mean: 6 years) was contemplated. Glasgow Coma Scale scores, severity of retinal hemorrhages, presence of skull fractures, cranial growth deceleration, and sequential neuroimaging data (computed tomography and/or magnetic resonance imaging) were compared with patterns of clinical evolution assessed by the Glasgow Outcome Scale.

Results. Clinical outcome showed that 14 (61%) children had severe disabilities, 8 (35%) had moderate disabilities, and 1 (4%) was normal. A low initial Glasgow Coma Scale score, severe retinal hemorrhages, presence of skull fracture, and cranial growth deceleration were significantly associated with poor developmental outcome. Eighteen of the 23 patients had abnormal magnetic resonance imaging scans. This examination disclosed atrophy when performed beyond 15 days of injury. Atrophy seemingly resulted from various brain lesions, namely, contusions, infarcts, and other lesions within the white matter. Presence of intraparenchymal brain lesions within the first 3 months was significantly associated with neurodevelopmental impairment. Severity of motor and cognitive dysfunctions was related to the extent of intraparenchymal lesions.

Conclusions. Early clinical and radiologic findings in NAHI are of prognostic value for neurodevelopmental outcome.

Key Words: nonaccidental head injury • traumatic brain injury • child abuse • shaken-infant syndrome • neuroimaging • outcome

Abbreviations: NAHI, nonaccidental head injury • SBS, shaken-baby syndrome • CT, computed tomography • MRI, magnetic resonance imaging • GCS, Glasgow Coma Scale • GOS, Glasgow Outcome Scale • GR, good recovery • MD, moderate disability • SD, severe disability • PVS, persistent vegetative state

Nonaccidental head injury (NAHI) includes 1 or more of the following: shaking injury, lesions as a result of direct impact, compression, and penetrating injuries.1 The most frequent form of NAHI, the so-called shaken baby syndrome (SBS), occurs during the first year of life.2 Death occurs in 10% to 40% of patients, and most survivors have poor neurologic outcome.3–10 Neurologic sequelae include cognitive and behavioral disturbances, cerebral palsy, blindness, and epilepsy.11–14 Factors of adverse prognostic significance identified to date include ophthalmologic symptoms,7,15–17 seizures early after injury,18 high intracranial pressure,19 cranial growth impairment,11,12 and major neuroradiologic abnormalities such as the "big black brain," indicating severe edema on computed tomography (CT) scans.20 Recent prospective studies established a correlation between neuroimaging and short-term outcome.21,22 To our knowledge, there are no studies correlating the long-term neurodevelopmental outcome with intraparenchymal lesions investigated by combined CT and magnetic resonance imaging (MRI) of the brain. Thus, the aim of this study was to correlate both early (see "Patients and Methods") clinical and radiologic findings during the first 3 months after injury, with long-term neurodevelopmental outcome in children with a history of NAHI.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Study Population
The medical charts of all patients who were admitted between 1985 and 1998 (n = 25) to Cliniques Universitaires Saint-Luc in Brussels, Belgium, with a diagnosis of NAHI were reviewed retrospectively. The "Child Protection Team" in our hospital established the diagnosis in each patient according to Duhaime criteria.4 These include acute encephalopathy with subdural hemorrhages, cerebral edema, retinal hemorrhages, and fractures, in the context of an inappropriate or inconsistent history, commonly with additional evidence of other malicious injuries. Two infants died during the acute period. Brain imaging was not available for 1 of them; these 2 patients were not included in our study because the goal was to correlate imaging with long-term developmental evolution. The remaining 23 patients underwent the full follow-up procedure described in "Outcome Assessment." Table 1 summarizes the clinical and radiologic findings at the acute phase and the long-term outcome in the 23 patients. Mean age at injury was 4.2 months (range: 3 weeks to 13 months). The male-to-female ratio was 3:1. To improve the sensitivity of our study for detecting long-term sequelae, we included only patients who were 3 years of age or older at the last evaluation. Mean follow-up duration was 6 years (range: 2.5–13 years). The severity of injury was determined using the Glasgow Coma Scale (GCS)23 and the duration of impaired consciousness, adapted for infants by Ewing-Cobbs.21,22,24 When 2 different GCS scores were available during the first 24 hours, the lowest one was considered. The initial GCS was always performed in nonsedated patients. In alignment with other studies of brain injury in young children,24 we separated our patients into 2 groups: 1) patients with GCS 9 to 15 with consciousness impairment for <24 hours and 2) patients with GCS 3 to 8 for at least 6 hours or consciousness impairment for >24 hours. All children underwent skeletal radiographs and optic funduscopy within the first 3 days after admission.


View this table:
[in this window]
[in a new window]
  		TABLE 1. Comparison Between "Initial" Clinical and Radiologic Data With Long-Term Outcome

 
Neuroradiologic Assessment
All children had "initial" (ie, within 2 days after admission) clinical and paraclinical investigations. These included at least 1 CT scan. "Early" and "late" imaging (CT and MRI) studies were defined as studies done before and after 3 months, respectively. Early MRI of the brain (T1- and T2-weighted axial, T1- or T2-weighted coronal and sagittal sections) was done in 12 patients, and late MRI in was done 20 patients. Six of 7 infants (patients 3, 5, 7, 13, 15, 19, and 23) each had 1 MRI during the first 15 days; in patient 15, MRI was repeated (days 2 and 4). One MRI was performed in each of the 9 children (patients 3, 4, 7, 9, 16, 17, 19, 21, and 23) between days 15 and 90. All images were reviewed by an independent investigator who was unaware of clinical outcome. "Diffuse" lesions were defined as extensive lesions on both sides of the brain affecting at least 3 lobes. We described as "infarcts" lesions presenting the following criteria: 1) MRI showing brain parenchymal signal abnormalities corresponding to ischemic lesions and 2) a topography strictly localized to an arterial territory.25

Outcome Assessment
The Glasgow Outcome Scale (GOS),26 adapted for infants by Ewing-Cobbs, was used to assess the overall developmental outcome at last evaluation.21,22 In this score, good recovery (GR) refers to a return to age-appropriate or preinjury levels of functioning; moderate disability (MD) is assigned if the child 1) has a significant reduction in cognitive functioning from estimated premorbid levels, 2) has motor deficits including hemiparesis interfering with daily living activities, or 3) is referred for outpatient rehabilitation therapies. Severe disability (SD) is assigned when 1) cognitive scores are in the deficient range; 2) severe motor deficits are present, such as lack of appropriate postural control or ambulation; or 3) the child is referred for inpatient rehabilitation. Persistent vegetative state (PVS) is defined as total dependence.21,22 The Wechsler Preschool and Primary Scale of Intelligence27 and the Kaufman Assessment Battery for Children28 developmental scales were used in children aged 3 to 6 years at the time of evaluation, and the Wechsler Intelligence Scale for Children-Revised29 and the Kaufman Assessment Battery for Children scales were used in older children.

Statistical Analysis
Student’s t tests for unequal variances were used to compare the means of GOS scores (the 4 GOS categories, namely, GR, MD, SD, and PVS, were scored 80, 60, 40, and 20, respectively).


   RESULTS
TOP
 ABSTRACT
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Correlations Between Initial Clinical Findings and Outcome
Fourteen (61%) of the 23 patients evaluated at a minimum age of 3 years had a poor neurodevelopmental outcome (SD, PVS), 8 (35%) had MD, and 1 (4%) was normal (GR). Thirteen (78%) of the 18 children with low initial GCS scores (<9) had SD or PVS, as compared with only 1 of 5 children with higher initial GCS scores (P =0.04). Of the 20 children (20 of 23 [87%]) who had bilateral retinal hemorrhage initially, 12 had retinal detachment or vitreous hemorrhage; 9 of these 12 had poor outcome (SD or PVS), as compared with 5 of the 11 patients with less severe or no ocular damage (P = .04). Of the 7 children with skull fractures, 6 had SD or PVS, and outcome was significantly worse among the children with skull fractures (P = .01). Twelve of the 14 children with a slowing in head circumference growth (>2 standard deviations) had SD or PVS, and there was a significant difference in outcome between children with head growth slowing and those with unaffected head growth (P = .003; Tables 1 and 2).


View this table:
[in this window]
[in a new window]
  		TABLE 2. Comparison Between Clinical and Radiologic Features and Outcome

 
Correlations Between "Early" (Within the First 3 Months After Injury) Neuroradiologic Findings and Outcome
The initial CT scan showed subdural or subarachnoidal hemorrhage in all but 1 of the children (22 [96%] of 23). The hemorrhages were bilateral in 17 children, unilateral in 5, and interhemispheric in 4. Sixteen of the 23 patients had parenchymal edema; the edema was confined to 1 lobe in 1 patient (patient 1), to a vascular territory in 1 patient (patient 16), and to 1 hemisphere in 4 children (patients 7, 11, 12, and 21); the 10 remaining patients had bilateral parenchymal edema. Two of the 16 patients had intraparenchymal hematoma (patients 15 and 18). MRI was performed between day 1 and day 15 (mean: day 4) in 7 patients (patients 3, 5, 7, 13, 15, 19, and 23). MRI provided no additional information as compared with CT during the first 15 days, except in patient 19, who had lesions on the MRI (performed at day 1) that were not detected by the initial CT scan on day 0. These lesions consisted of a subdural hematoma in the posterior fossa and a focal lesion in the corpus callosum. In contrast, in all 9 patients who had an MRI between day 15 and day 90 (mean: day 33), this investigation provided additional information on intraparenchymal lesions as compared with the initial CT scans. Three types of intraparenchymal lesions were seen on MRI done during this period: 1) lobar atrophy of the gray and white matter suggesting residual postcontusion damage (patient 4); 2) arterial infarcts (n = 4) either at a single site (anterior cerebral artery, patient 19) or at multiple sites (posterior cerebral arteries, patient 16; carotid artery, patients 7 and 21); and 3) white matter lesions suggesting gliotic scars (n = 7), with predominant involvement of 1 hemisphere in 2 patients (patients 7 and 21) and bilateral involvement in 5 patients (patients 9, 16, 17, 19, and 23). The atrophic areas and white matter scars exactly matched the sites of edema seen on the initial CT scans (Tables 1 and 2). Comparison of patients with and without intraparenchymal lesions (Table 2) showed that detection of such lesions by MRI and/or CT during the first 3 months was significantly associated with severe developmental outcome (P = .04), particularly when the lesions were diffuse (P = .025).

Correlation Between "Late" (>3 Months After Injury) Neuroradiologic Findings and Outcome
Twenty-one children had neuroimaging studies (MRI in 20 patients and CT in 1) >3 months after injury (range: 3 months to 13 years; mean: 5.6 years). Chronic subdural hygroma was found in 4 of these children (patients 9, 15, 17, and 21). Sixteen of the 21 patients displayed parenchymal lesions that were also detectable on the initial CT scans or early MRI. The remaining 5 children (patients 3, 5, 8, 10, and 13) had normal initial and late cerebral imaging. Ten children (patients 3, 5, 7, 9, 13, 15, 16, 19, 21, and 23) had both early (before 3 months) and late (after 3 months) MRI. Comparison of these 2 time points showed that the 3 types of intraparenchymal lesions detected on early MRI scans persisted on late MRI and consisted of the following: 1) atrophy involving temporal and parieto-occipital lobes (patients 4 and 12) indicating residual damage after contusion by direct impact or "contre-coup" injury; 2) arterial infarcts detected in 9 patients, either at a single site (middle and anterior cerebral arteries in patients 11 and 19, respectively) or at multiple sites (anterior cerebral arteries, patient 18; posterior cerebral arteries, patient 16; carotid artery, patients 7 and 21; other multifocal patterns, patients 20, 22, and 23); and 3) subcortical gliotic scars in the cerebral white matter detected in 14 patients, usually in both hemispheres (13 of 14 patients), with no preferential distribution pattern. Eleven patients had focal (n = 3) or diffuse (n = 8) lesions of the corpus callosum; 4 of these patients (patients 16, 20, 22, and 23) also had lesions in the cerebellar hemispheric white matter. Finally, comparison of patients with and without intraparenchymal lesions visualized on MRI performed >3 months after injury showed that the presence of such lesions was significantly associated with a poor neurodevelopmental outcome (P = .02).

Recovery seemed to be related to the extent of lesions seen by late MRI (Tables 2 and 3). Patients (n = 10) with diffuse lesions had more severe motor and intellectual impairments and were more likely to have blindness and epilepsy than patients with focal (n = 4) or hemispheric (n = 4) lesions. Seven of the 9 patients (Table 3) who had epilepsy belong to the subgroup of "diffuse lesions." Of these 7 patients with epilepsy, 2 had West syndrome and 5 had polymorphic seizures. In these patients, epilepsy started immediately after injury in 3 patients and within the first 2 years in 4. Seizures were refractory to treatment in 6 of the 7 patients. Among the patients who had no visible lesions on imaging studies (n = 5), 4 had residual disabilities, namely, hemiparesis and mental deficiency (patient 10), visual sensory defect (patient 13), or visuospatial impairment and attention deficit (patients 3 and 8).


View this table:
[in this window]
[in a new window]
  		TABLE 3. Comparison Between Outcome and the Type of Parenchymal Lesions (MRI) in Our Study Group

 

   DISCUSSION
TOP
 ABSTRACT
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Results from our series of patients with NAHI underline the prognostic value of bilateral retinal and vitreous hemorrhages, initial low GCS score, presence of skull fractures, cranial growth deceleration, and intraparenchymal brain abnormalities detected by neuroimaging during the first 3 months. These clinical and radiologic findings were significantly associated with poor long-term neurodevelopmental outcome.

After 3 years, 96% of our patients had disabilities, which were severe (61%) or moderate (35%). This is in agreement with the main reported series13,14,24 in which 45% to 69% of children had poor outcome. Bilateral retinal and vitreous hemorrhage were associated in our series with poor neurodevelopmental outcome as that reported in earlier studies.7,16,17 The depth and duration of coma have been shown to predict the outcome of brain injury in older children.30 This was also the case in our younger patients. This point is also in agreement with a recent study showing that neurologic outcome at 3 and 12 months was correlated with initial GCS and duration of impaired consciousness.22 The presence of skull fractures, which indicates shaken impact syndrome, was also associated with poor neurodevelopmental outcome. Shaking without head impact has been reported to cause brain lesions in infants.6,8–10,31,32 The presence of skull fractures seems to be associated with a worse neurodevelopmental outcome. This was inferred from our results and was pointed out in the literature.2 Cranial growth deceleration was another sign of adverse prognostic significance in our study. This is in keeping with earlier data.11,12 It is noteworthy that in the series studied by Barlow, severe initial seizures and presence of intracranial hypertension predicted poor neurodevelopmental outcome.18,19 Our results are in agreement with this findings.

MRI is recognized as the most sensitive tool for detecting brain lesions in NAHI.33–37 Previous prospective studies showed a correlation between intraparenchymal lesions visualized on brain imaging and short-term outcome.21,22 Our retrospective study is in line with these results. Our results show, in addition, that the reported poor neurodevelopmental outcome in NAHI persists in the long-term. To our knowledge, our study is the first to link early and late MRI findings to long-term neurodevelopmental outcome. Our results showed that MRI done 15 days or more after injury disclosed evidence of 3 etiopathogenic mechanisms leading to atrophy, namely, contusions, infarcts/stroke, and white matter scars (Fig 1). Infarcts were detected in 50% of our patients. In another series, similar lesions (called "infarcts/edema") were reported in one third of 15 patients with NAHI.22 The pathophysiologic mechanisms underlying stroke in NAHI remain unclear. Strangulation has been suggested as a possible cause of infarction in the distribution of the carotid artery.38,39 However, arterial wall dissection, which was long underrecognized in children, is now known to be among the leading causes of arterial ischemic stroke in the pediatric age group.25,40 Injuries such as direct cervical blow or stretching of the neck may be responsible for most cases of arterial dissection. These mechanisms may be implicated in NAHI. Another plausible mechanism for stroke may be fat embolism, a classic complication of long-bone fractures. Such fractures were present in 5 of our patients (patients 11, 18, 20, 22, and 23). Direct intracranial damage (tearing, thrombosis) to the arterial wall could also be another underlying mechanism. Additional neuroradiologic studies, for instance, using MR angiography, may provide more insights into the mechanism of infarcts/stroke in NAHI.


Figure 1
View larger version (132K):
[in this window]
[in a new window]
  		Fig 1. MRI illustrating the radiologic evolution in 2 patients. A and B, Head injury occurred in patient 18 when he was 1.5 months of age. MRI performed 5 years after trauma: T1-weighted sagittal (A) and T2-coronal (B) sections, showing a necrotic lesion in the anterior cerebral artery territory and an extreme thinning of corpus callosum (A). C, Patient 17 was injured at the age of 6 months. MRI (T1-weighted axial section) performed 1 month later showed enlargement of the lateral ventricles, diffuse cortico-subcortical gliotic scars (arrows), and bilateral subdural collections.

 
Subcortical gliotic scars were the most common intraparenchymal lesions in our series. We suggest that these lesions result from the shearing and tearing injuries described in association with acceleration-deceleration effects in both children and adults41–49 and/or from hypoxic axonal damage as suggested by recent neuropathologic studies targeted on patients who presented a very rapid fatal evolution.50,51 In our series, scarring was diffuse; it involved the white matter subjacent to the neocortex in all affected patients and the corpus callosum in the majority. Most of our patients had grade 2 axonal injury as defined by Adams et al,52 which is associated with a high likelihood of poor outcome. Our results are consistent with those of the radiologic work by Levin et al,53 in which the corpus callosum was shown to be particularly vulnerable to mechanical injury, especially in young children.

Another goal of our study was to determine in which time frame neuroimaging provides the best information in NAHI. Between days 1 and 14, when edema is predominant, both MRI and CT scan detected intraparenchymal lesions; MRI provided additional data on the distribution of the lesions and disclosed a small pericerebral hematoma and a focal lesion in the corpus callosum in 1 patient. Thus, as compared with CT scan, very early MRI (between days 1 and 14) did not provide additional data of crucial importance for evaluating the prognosis. In contrast, when performed between 0.5 and 3 months after injury, MRI yielded important information on the distribution and mechanisms of the lesions in all patients. These findings further confirm that changes on brain imaging evolve over time36 and that early brain imaging (especially before day 15) does not unravel the full extent of damages. The anomalies that we detected by MRI between 0.5 and 3 months were correlated with neurodevelopmental outcome. For instance, stroke was associated with a poor outcome in 78% of children and white matter injuries in 82%. When done beyond the first 3 months after injury, MRI did not provide additional significant information and did not modify the prognostic conclusions drawn from earlier imaging data. Some limitations of the prognostic value of MRI could come from the retrospective method that we used. However, we do not think that such limitations would influence our results in an important way, because the timing and number of neuroradiologic examinations were relatively homogeneous in our population. In fact, timing and number of MRI in our patients were not different in the clinically well-appearing patients as compared with the others. Thus, patients who looked well clinically did not undergo fewer examinations, and consequently focal lesions would not have been missed.

Finally, in our series, the severity of sequelae was shown to be related to the extent of brain lesions. However, we found no correlation between the topography of lesions and outcome. This point requires additional exploration involving detailed neuropsychologic assessments in larger series of NAHI patients, preferably using prospective studies.


   FOOTNOTES
 
Received for publication Mar 29, 2002; Accepted Feb 12, 2003.

Reprint requests to (C.B.) Service de Neurologie Pédiatrique, Cliniques Universitaires Saint Luc, Université Catholique de Louvain, Avenue Hippocrate 10/1067, B-1200 Brussels, Belgium. E-mail: Bonnier{at}nepe.ucl.ac.be


   REFERENCES
TOP
 ABSTRACT
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Barlow KM, Minns RA. Annual incidence of shaken impact syndrome in young children. Lancet.2000; 356 :1571 –1572[CrossRef][Web of Science][Medline]
  2. Duhaime AC, Christian CW, Rorke LB, Zimmerman RA. Nonaccidental head injury in infants—the shaken-baby syndrome. N Engl J Med.1999; 338 :1822 –1829
  3. Collins KA, Nichols CA. A decade of pediatric homicide: a retrospective study at the Medical University of South Carolina. Am J Forensic Med Pathol.1999; 20 :169 –172[CrossRef][Web of Science][Medline]
  4. Duhaime AC, Gennarelli TA, Thibault LE, Bruce DA, Margulies SS, Wiser S. The shaken baby syndrome: a clinical, pathological and biomechanical study. J Neurosurg.1987; 66 :409 –415[Web of Science][Medline]
  5. Ludwig S, Warman M. Shaken baby syndrome: a review of 20 cases. Ann Emerg Med.1984; 13 :104 –107[Web of Science][Medline]
  6. Sinal SH, Ball MR. Head trauma due to child abuse: serial computerized tomography in diagnosis and management. South Med J.1987; 80 :1505 –1512[Web of Science][Medline]
  7. Wilkinson WS, Han DP, Rappley MD, Owings CL. Retinal hemorrhage predicts neurologic injury in the shaken baby syndrome. Arch Ophthalmol.1989; 107 :1472 –1474[Abstract/Free Full Text]
  8. Frank Y, Zimmerman R, Leeds NMD. Neurological manifestations in abused children who have been shaken. Dev Med Child Neurol.1985; 27 :312 –316[Web of Science][Medline]
  9. Brenner SL, Mann-Gray S. Race and the shaken baby syndrome: experience at one hospital. J Natl Med Assoc.1989; 81 :183 –184[Medline]
  10. Zepp F, Brühl K, Zimmer B, Schumacher S. Battered child syndrome: cerebral ultrasound and CT findings after vigorous shaking. Neuropediatrics.1992; 23 :188 –219[Web of Science][Medline]
  11. Oliver JE. Microcephaly following baby battering and shaking. BMJ.1975; 2 :262 –264
  12. Bonnier C, Nassogne MC, Evrard P. Outcome and prognosis of whiplash shaken infant syndrome: late consequences after a symptom-free interval. Dev Med Child Neurol.1995; 37 :943 –956[Web of Science][Medline]
  13. Duhaime AC, Christian CW, Moss E, Seidl T. Long-term outcome in infants with the shaking impact syndrome. Pediatr Neurosurg.1996; 24 :292 –298[Web of Science][Medline]
  14. Haviland J, Ross Russell RI. Outcome after severe non-accidental head injury. Arch Dis Child.1997; 77 :504 –507[Abstract/Free Full Text]
  15. Giangiacomo J, Khan JA, Levine C, Thompson VM. Sequential cranial computed tomography in infants with retinal hemorrhages. Ophthalmology.1988; 95 :295 –299[Web of Science][Medline]
  16. Matthews GP, Das A. Dense vitreous hemorrhages predict poor visual and neurological prognosis in infants with shaken baby syndrome. J Ophthalmol Strabismus.1996; 33 :260 –265
  17. Mills M. Funduscopic lesions associated with mortality in shaken baby syndrome. J Am Assoc Pediatr Ophthalmol Strabismus.1998; 68 :117 –132
  18. Barlow KM, Spowart JJ, Minns RA. Early posttraumatic seizures in non-accidental head injury: relation to outcome. Dev Med Child Neurol.2000; 42 :591 –594[CrossRef][Web of Science][Medline]
  19. Barlow KM, Minns RA. The relation between intracranial pressure and outcome in non-accidental head injury. Dev Med Child Neurol.1999; 41 :220 –225[CrossRef][Web of Science][Medline]
  20. Han BK, Towbin RB, De Courten-Myers G, McLaurin RL, Ball WS. Reversal sign on CT: effect of anoxic/ischemic cerebral injury in children. AJR Am J Roentgenol.1990; 154 :361 –368[Abstract/Free Full Text]
  21. Ewing-Cobbs L, Prasad M, Kramer L, Landry S. Inflicted traumatic brain injury: relationship of developmental outcome to severity of injury. Pediatr Neurosurg.1999; 31 :251 –258[CrossRef][Web of Science][Medline]
  22. Prasad M, Ewing-Cobbs L, Swank PR, Kramer L. Predictors of outcome following traumatic brain injury in young children. Pediatr Neurosurg.2002; 36 :64 –74[CrossRef][Web of Science][Medline]
  23. Teasdale G, Jennett B. Assessment of coma and impaired consciousness: a practical scale. Lancet.1974; 2 :81 –84[CrossRef][Web of Science][Medline]
  24. Ewing-Cobbs L, Kramer L, Prasad M, et al. Neuroimaging, physical, and developmental findings after inflicted and non-inflicted traumatic brain injury in young children. Pediatrics.1998; 102 :300 –337[Abstract/Free Full Text]
  25. Husson B, Rodesch G, Lasjaunias P, Tardieu M, Sébire G. Magnetic resonance angiography in childhood arterial brain infarcts: a comparative study with contrast angiography. Stroke.2002; 33 :1280 –1285[Abstract/Free Full Text]
  26. Jennet B, Bond M. Assessment of outcome after severe brain damage: a practical scale. Lancet.1975; 1 :480 –484[Web of Science][Medline]
  27. Wechsler D. Manual for the Wechsler Preschool and Primary Scale of Intelligence-Revised. New York, NY: The Psychological Corporation; 1974
  28. Kaufman AS, Kaufman NL. K-ABC: The Kaufman Assessment Battery for Children. Circle Pines, MN: American Guidance Service; 1983
  29. Wechsler D. Manual for the Wechsler Intelligence Scale for Children-Revised. New York, NY: The Psychological Corporation; 1974
  30. Brink J, Imbus C, Woo-Sam J. Physical recovery after severe closed head trauma in children and adolescents. J Pediatr.1980; 97 :721 –727[CrossRef][Web of Science][Medline]
  31. Conway EE. Nonaccidental head injury in infants: "the shaken baby syndrome revisited." Pediatr Ann.1998; 27 :677 –690[Web of Science][Medline]
  32. Alexander RC, Sato Y, Smith W, Bennet T. Incidence of impact trauma with cranial injuries ascribed to shaking. Am J Dis Child.1990; 144 :724 –726[Abstract/Free Full Text]
  33. Brown JK, Minns RA. Non-accidental head injury, with particular reference to whiplash shaking injury and medico-legal aspects. Dev Med Child Neurol.1993; 35 :849 –869[Web of Science][Medline]
  34. Alexander RC, Schor DP, Smith WL. Magnetic resonance imaging in intracranial injuries from child abuse. J Pediatr.1986; 109 :975 –979[CrossRef][Web of Science][Medline]
  35. Ball WS. Nonaccidental craniocerebral trauma (child abuse): MR imaging. Radiology.1989; 173 :609 –610[Free Full Text]
  36. Dias MS, Backstrom J, Falk M, Li V. Serial radiography in the infant shaken impact syndrome. Pediatr Neurosurg.1998; 29 :77 –85[CrossRef][Web of Science][Medline]
  37. Chabrol B, Decarie JC, Fortin G. The role of cranial MRI in identifying patients suffering from child abuse and presenting with unexplained neurological findings. Child Abuse Negl.1999; 23 :217 –228[CrossRef][Web of Science][Medline]
  38. Bird R, MacMahan JR, Gilles FH, Senac MO, Apthorp JS. Strangulation in child abuse: CT diagnosis. Radiology.1987; 163 :373 –375[Abstract/Free Full Text]
  39. Feldman KW, Simms RJ. Strangulation in childhood: epidemiology and clinical course. Pediatrics.1980; 65 :1079 –1085[Abstract/Free Full Text]
  40. Fullerton HJ, Johnston SC, Smith WS. Arterial dissection and stroke in children. Neurology.2001; 57 :1155 –1160[Abstract/Free Full Text]
  41. Jaspan T, Narborough G, Punt JAG, Lowe J. Cerebral contusional tears as marker of child abuse: detection by cranial sonography. Pediatr Radiol.1992; 22 :237 –245[CrossRef][Web of Science][Medline]
  42. Adams JH, Graham DI, Murray LS, Scott G. Diffuse axonal injury due to non-missile head injury in humans: an analysis of 45 cases. Ann Neurol.1982; 12 :557 –563[CrossRef][Web of Science][Medline]
  43. Graham DI, Clark JC, Adams JH, Genarelli TA. Diffuse axonal injury caused by assault. J Clin Pathol.1992; 45 :840 –841[Abstract/Free Full Text]
  44. Crooks DA. The pathological concept of diffuse axonal injury; its pathogenesis and the assessment of severity. J Pathol.1991; 165 :5 –10[CrossRef][Web of Science][Medline]
  45. Parizel PM, Ozsarlak O, Van Goethem JW, et al. Imaging findings in diffuse axonal injury after closed head trauma. Eur Radiol.1998; 8 :960 –965[CrossRef][Web of Science][Medline]
  46. Graham DI, Ford I, Adams JH, et al. Fatal head injury in children. J Clin Pathol.1989; 42 :18 –22[Abstract/Free Full Text]
  47. Lindenberg R, Freytag E. Morphology of brain lesions from blunt trauma in early infancy. Arch Pathol.1967; 87 :298 –305
  48. Calder JM, Hill I, Scholtz CL. Primary brain trauma in non-accidental injury. J Clin Pathol.1984; 37 :1095 –1100[Abstract/Free Full Text]
  49. Vowles GH, Scholtz CL, Cameron JM. Diffuse axonal injury in early infancy. J Clin Pathol.1987; 40 :185 –189[Abstract/Free Full Text]
  50. Geddes GF, Hackshaw AK, Vowles GH, et al. Neuropathology of inflicted head injury in children. I. Patterns of brain damage. Brain.2001; 124 :1290 –1298[Abstract/Free Full Text]
  51. Geddes GF, Vowles GH, Hackshaw AK, et al. Neuropathology of inflicted head injury in children. II. Microscopic brain injury in infants. Brain.2001; 124 :1299 –1306[Abstract/Free Full Text]
  52. Adams JH, Doyle D, Ford I, et al. Diffuse axonal injury: definition, diagnosis and grading. Histopathology.1989; 15 :49 –59[Web of Science][Medline]
  53. Levin HS, Benavidez DA, Verger-Maestre K, et al. Reduction of corpus callosum growth after severe traumatic brain injury in children. Neurology.2000; 54 :647 –653[Abstract/Free Full Text]
  54. Bayley N. Bayley Scales of Infant Development. 3rd ed. San Antonio, TX: The Psychological Corporation; 1993
PEDIATRICS (ISSN 1098-4275). ©2003 by the American Academy of Pediatrics

Add to CiteULike CiteULike   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us   Add to Digg Digg   Add to Facebook Facebook   Add to Reddit Reddit   Add to Technorati Technorati   Add to Twitter Twitter    What's this?


This article has been cited by other articles:


Home page
 Arch. Dis. Child.Home page
P Koumellis, N S McConachie, and T Jaspan
Spinal subdural haematomas in children with non-accidental head injury
Arch. Dis. Child., March 1, 2009; 94(3): 216 - 219.
[Abstract] [Full Text] [PDF]

Home page
 radtechHome page
A. REYNOLDS
Shaken Baby Syndrome: Diagnosis and Treatment
Radiol. Technol., November 1, 2008; 80(2): 151 - 170.
[Abstract] [Full Text] [PDF]

Home page
 J Child NeurolHome page
C. Bonnier, P. Marique, A. Van Hout, and D. Potelle
Neurodevelopmental Outcome After Severe Traumatic Brain Injury in Very Young Children: Role for Subcortical Lesions
J Child Neurol, May 1, 2007; 22(5): 519 - 529.
[Abstract] [PDF]

Home page
 PediatricsHome page
K. P. Hymel, K. L. Makoroff, A. L. Laskey, M. R. Conaway, and J. A. Blackman
Mechanisms, Clinical Presentations, Injuries, and Outcomes From Inflicted Versus Noninflicted Head Trauma During Infancy: Results of a Prospective, Multicentered, Comparative Study
Pediatrics, May 1, 2007; 119(5): 922 - 929.
[Abstract] [Full Text] [PDF]

Home page
 PediatricsHome page
K. M. Barlow, E. Thomson, D. Johnson, and R. A. Minns
Late Neurologic and Cognitive Sequelae of Inflicted Traumatic Brain Injury in Infancy
Pediatrics, August 1, 2005; 116(2): e174 - e185.
[Abstract] [Full Text] [PDF]

Home page
 JWatch PediatricsHome page
Predicting Outcomes in Shaken Baby Syndrome
Journal Watch Pediatrics and Adolescent Medicine, January 16, 2004; 2004(116): 9 - 9.
[Full Text]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow E-mail this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My File Cabinet
Right arrow Download to citation manager
Right arrowRequest Permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via CrossRef
Right arrow Citing Articles via Web of Science (19)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Bonnier, C.
Right arrow Articles by Sébire, G.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Bonnier, C.
Right arrow Articles by Sébire, G.
Related Collections
Right arrow Office Practice
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us   Add to Digg   Add to Facebook   Add to Reddit   Add to Technorati   Add to Twitter  
What's this?