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Intracranial Hemorrhage in Children Younger Than 3 Years
Prediction of Intent
Robert G. Wells, MD;
Christine Vetter, MD;
Prakash Laud, PhD
Arch Pediatr Adolesc Med. 2002;156:252-257.
ABSTRACT
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Objective To determine whether certain computed tomographic imaging patterns in
infants and young children with intracranial hemorrhage help predict intentional
compared with unintentional injuries.
Design Retrospective consecutive case series over a 10-year period.
Patients Two hundred ninety-three children younger than 3 years with intracranial
hemorrhage.
Main Outcome Measures The sensitivity and specificity of computed tomographic imaging patterns
for intentional head injury.
Setting Regional pediatric medical center.
Results Four variables used in the multiple logistic regression analysis for
predicting intentional head injury were statistically significant (P<.05): subdural hematoma located over the cerebral convexities,
hematoma within the interhemispheric subdural space, hygroma (nonhemic subdural
fluid) with intracranial hemorrhage, and absence of a skull fracture with
intracranial hemorrhage. The prediction model for the diagnosis of intentional
head trauma using combinations of these 4 variables and a .45 probability
cutoff point indicated a sensitivity of 84% (95% confidence interval, 78%-90%)
and a specificity of 83% (95% confidence interval, 74%-89%).
Conclusion Computed tomographic imaging patterns of intracranial hemorrhage in
children younger than 3 years help predict whether the injury was intentional.
INTRODUCTION
THE DIFFERENTIATION between intentional and unintentional causes of
head trauma in infants and young children is a common medical and legal dilemma.
Most head trauma is caused by falls that rarely result in a significant intracranial
pathologic condition; however, intentional injury is the most common cause
of severe traumatic brain injury in infants.1-2
Billmire and Myers3 reported that 64% of infant
head injuries of sufficient severity to warrant hospital admission (excluding
uncomplicated skull fractures) and 95% of serious intracranial injuries are
the result of child abuse. Accurate correlation of the computed tomographic
(CT) findings with the reported mechanism of injury is an essential component
of the care of the infant or young child with head trauma.
Results of studies based on surgical, radiological, and autopsy data
suggest that different types of brain injuries tend to occur with intentional
vs unintentional trauma. Most investigators believe this is caused by a predominance
of inertial forces with intentional brain injury, resulting in movement of
the brain to yield concussion, edema, subdural hematoma, and diffuse axonal
injury. Unintentional head trauma more often involves contact forces, which
tend to produce focal injuries such as laceration, fracture, contusion, and
epidural hematoma.4-6
We retrospectively reviewed all intracranial hemorrhages detected with
CT in children younger than 3 years at our institution over a 10-year period.
The main objective was to determine which CT imaging patterns help predict
whether the injury was intentional.
PATIENTS AND METHODS
PATIENT SELECTION AND CLINICAL DIAGNOSIS
We reviewed the diagnostic imaging reports for all patients younger
than 3 years who underwent cranial CT examinations at Children's Hospital
of Wisconsin, Milwaukee, between February 1, 1991, and May 31, 2001. We selected
all patients with radiological studies that demonstrated intracranial hemorrhage.
We reviewed (blinded to the CT findings) the medical records of these children
and recorded the patient's age and sex, the reported circumstances of the
injury, the presence or absence of concurrent injuries, and the results of
official child abuse investigations. We excluded children with hemorrhage
because of prematurity, birth trauma, medical conditions, or intracranial
surgical procedures. Each of the remaining patients was assigned to 1 of 3
mutually exclusive causative categories as follows: intentional injury, unintentional
injury, and intent uncertain. We considered an injury to be unintentional
if it was witnessed by someone other than the caretaker or there were no discrepancies
between the described mechanism and the physical findings. We additionally
categorized the unintentional injury group according to whether the injury
was caused by a fall, motor vehicle collision, a fall in an infant walker,
or by being struck by an object. We considered an injury to be intentional
if there was a confession of abuse, the injuries were incompatible with the
stated mechanism of injury, or the caretaker offered no explanation for the
injuries. Those patients who could not clearly be assigned to the intentional
or unintentional injury categories were assigned to the intent uncertain group.
CT IMAGE ANALYSIS
We reviewed (blinded to the clinical findings) the CT images of the
study subjects and recorded the location of intracranial hemorrhage according
to the following anatomical categories: epidural, subdural, subarachnoid,
intraventricular, and parenchymal. We recorded additional details of the intracranial
hemorrhage according to the following subcategories: subdural hematoma located
over the cerebral convexities, subdural hematoma located within the interhemispheric
fissure, subdural hematoma in other locations, petechial parenchymal hemorrhage,
and parenchymal hematoma. All study patients had at least one of these findings.
In addition, the presence of subdural hygroma, brain edema, and skull fracture
was recorded. For the purposes of categorization, we considered any subdural
fluid collection with CT attenuation values less than those of the brain to
be a hygroma. The only exceptions were hyperacute subdural hematomas (a mixture
of clotted and unclotted blood), which were categorized as subdural hematomas
only. Chronic subdural hematomas were included in the hygroma category. The
CT imaging categories were not mutually exclusive.
PREDICTION RULE
We selected the following variables to test for an association with
intentional trauma as the cause of intracranial hemorrhage: lack of an epidural
hematoma, interhemispheric subdural hematoma, convexity subdural hematoma,
lack of subarachnoid hemorrhage, intraventricular hemorrhage, lack of petechial
hemorrhage, parenchymal hematoma, hygroma, edema, lack of a fracture, male
sex, and patient age. We treated age as a continuous variable and all others
as binary (yes/no) variables. Logistic regression was used to create a prediction
rule; variables were studied individually and simultaneously. Our final prediction
model included variables that, in the same model, had P values less than .05. We used this model to estimate probabilities
of intentional injury based on combinations of these variables. The sensitivity
and specificity for the diagnosis of intentional trauma were calculated. We
then applied the model to the patients in the intent uncertain category. All
calculations were performed using the LogXact software package (CYTEL Software
Corp, Cambridge, Mass), which uses exact permutational distributions as opposed
to the more commonly available asymptotic likelihood methods.
RESULTS
PATIENT CHARACTERISTICS
The patient characteristics are summarized in Table 1. The study population consisted of 293 individuals, 177
male (60.4%) and 116 female (39.6%) patients. The mechanism of injury was
intentional trauma in 148 patients (50.5%), unintentional trauma in 109 (37.2%),
and intent uncertain in 36 (12.3%). Comparing the children having intentional
vs unintentional injuries, the former tended to be younger (mean age, 8.0
months vs 11.7 months, respectively) and were more frequently male (60.8%
vs 55.0%, respectively).
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Table 1. Patient Characteristics and Causes of Intracranial Hemorrhage
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CT IMAGING PATTERNS AND CAUSES
Four hundred sixty-nine intracranial hemorrhages classified by location
were identified in the 293 study subjects. The imaging findings are correlated
with the causes and are listed in Table
2. The most common site of hemorrhage was in the subdural spaces,
identified in 184 patients (63%) (Figure 1). The most common type of subdural hemorrhage was in the interhemispheric
region, which occurred in 143 children (49%). Most (105 patients [73%]) of
these children had intentional injuries. Unintentional trauma was responsible
for 21 (15%) of the interhemispheric subdural hematomas; all were injuries
associated with relatively high force—3 falls of more than 2 m, 12 motor
vehicle collisions, 4 falls while in an infant walker, and 2 blows to the
head.
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Table 2. Computed Tomographic Imaging Findings Correlated to the Causative
Categories of Injury*
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Figure 1. Common computed tomographic (CT)
findings with intentional trauma. An 18-month-old boy was shaken and thrown
to the floor by his mother's boyfriend 3 hours prior to the CT examination.
Subsequent CT imaging (not shown) demonstrated worsening edema over the next
few days. The child died 5 days later. A, Note the acute convexity subdural
hemorrhage adjacent to the right frontal lobe and along the tentorium (arrows).
B, A more superior CT image shows a right posterior interhemispheric subdural
hematoma (arrow).
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Hemorrhage over the cerebral convexities was almost as common as interhemispheric
hemorrhage, occurring in 137 children (47%). Convexity and interhemispheric
subdural hematomas occurred simultaneously in 96 (52%) of the 184 patients
with subdural hematoma. Intentional injury was the most common cause of convexity
subdural hematoma, occurring in 99 patients (72%). Unintentional injuries
accounted for only 14 (10%) of the convexity subdural hematomas; most were
caused by severe injuries, such as motor vehicle collisions, falls from more
than 2 m, or infant walker–stair injuries. Only 3 patients with this
pattern of hemorrhage fell less than 2 m.
Acute intracranial hemorrhage with coexistent low attenuation subdural
hygromas occurred in 43 patients (15% of the study population). Associated
hemorrhages included 1 epidural hemorrhage, 29 interhemispheric subdural hematomas,
37 convexity subdural hematomas, 1 subarachnoid hemorrhage, 1 petechial hemorrhage,
and 1 intraventricular hemorrhage. All patients with hygromas were in the
intentional injury or intent uncertain categories.
Epidural hematomas occurred in 80 patients (27%). Epidural hematomas
were most frequently associated with unintentional injuries (62 patients [78%])
and were uncommon with intentional injury (14 patients [18%]). Thirty-nine
epidural hematomas (63%) related to unintentional injury were caused by a
fall. Most of the epidural hematomas were small, and not associated with other
injuries; 69 (86%) were less than 1 cm thick and were isolated (Figure 2).
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Figure 2. Common computed tomographic (CT)
appearance of unintentional head trauma. A small (probably venous) epidural
hematoma is present on the right side (arrow) in a 16-day-old boy who had
fallen from his mother's arms onto a concrete floor. Bone windows (not shown)
demonstrated a skull fracture. This hematoma resolved without surgical evacuation,
and the child made a complete clinical recovery.
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Subarachnoid hemorrhage occurred in 36 patients (12%); a coexisting
intracranial injury (edema or other area of hemorrhage) was identified in
27 (75%) of these 36 patients. Unintentional injuries were more common than
intentional injuries in patients with subarachnoid hemorrhage (61% vs 33%).
Nine (41%) of the 22 patients with subarachnoid hemorrhage who had unintentional
injuries had fallen; 10 (45%) were involved in motor vehicle collisions.
Petechial parenchymal hemorrhage was identified in 45 (15%) of the 293
patients. Twenty-seven patients (60%) with petechial hemorrhage had unintentional
trauma and 15 (33%) had intentional trauma. Thirty-two patients (71%) with
petechial hemorrhage had a skull fracture.
Edema accompanied intracranial hemorrhage in 85 patients (29%). In 80
patients (94%) the edema occurred in conjunction with an interhemispheric
subdural hematoma or a convexity subdural hematoma. Sixty-six patients (78%)
with edema were classified in the intentional injury category.
A skull fracture was identified in 140 patients (48%). Seventy-nine
(99%) of the 80 patients with an epidural hematoma had a skull fracture. Forty-three
(29%) of the 148 patients having a diagnosis of intentional trauma had a skull
fracture.
PREDICTION RULE
The logistic regression analysis results are given in Table 3. Evaluation of the variables individually showed P values less than .05 for all variables except intraventricular hemorrhage,
parenchymal hematoma, and male sex. However, in multiple regression, only
4 variables were statistically significant: convexity subdural hematoma, interhemispheric
subdural hematoma, lack of a skull fracture, and hygroma. The final model
is summarized in Table 4. Note
that the hygroma and no fracture variables include the requirement for coexistent
acute intracranial hemorrhage. The model is based on the imaging findings
at the time of clinical presentation; therefore, patients with intracranial
hemorrhage who subsequently develop hygromas should not be considered to have
a hygroma when applying the prediction rule.
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Table 3. Logistic Regression Analysis of Variables Studied Individually
for a Diagnosis of Intentional Trauma
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Table 4. Multiple Logistic Regression Analysis for a Diagnosis of Intentional
Trauma
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The model-based estimates of the probabilities of intentional trauma
according to combinations of the 4 selected variables are listed in Table 5. To maximize both sensitivity and
specificity, we classified patients as having intentional injuries when their
predicted probability of intentional injury in the logistic model was greater
than .45. Using this cutoff point, the sensitivity of the prediction model
for the diagnosis of intentional trauma is 84% (95% confidence interval, 78%-90%)
and the specificity is 83% (95% confidence interval, 74%-89%). The cutoff
point was selected to provide a reasonable balance between the sensitivity
and specificity. Application of the prediction rule to the patients in the
intent uncertain category estimates that 25 (69%) of the 36 patients had intentional
trauma.
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Table 5. Model-Based Estimates of Probabilities of Intentional Trauma*
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COMMENT
We propose a prediction rule for the diagnosis of intentional trauma
in children younger than 3 years with intracranial hemorrhage. The model requires
the exclusion on clinical grounds of patients with hemorrhage due to prematurity,
birth trauma, surgery, or nontraumatic medical causes. No other clinical information
is assumed. We thus attempted to reproduce the common clinical scenario at
the time of presentation of the infant or young child with head trauma, when
the available objective clinical information is incomplete and the reported
history of the injury may be viewed with some skepticism.
The 4 variables that exhibited statistical significance in multiple
logistic regression are compatible with the work of other investigators and
theoretical considerations. The common occurrence of subdural hemorrhages
and lack of skull fractures support the concept that acceleration-deceleration
forces predominate with intentional head injuries. Unintentional injuries
more often involve translational forces, thereby favoring skull fractures
and epidural hematomas. The association of hygroma with the diagnosis of intentional
trauma supports the medical dictum that acute intracranial hemorrhage in combination
with nonhemic subdural fluid (eg, acute and chronic subdural hematomas) indicates
that at least 2 significant episodes of trauma have occurred, unless there
is a clear history of a preexisting medical condition that resulted in a subdural
effusion or hygroma.
To our knowledge, this article reports the largest case series in the
medical literature to investigate the correlation between CT imaging findings
and causes of intracranial hemorrhage in infants and young children. There
are, however, several limitations of this study. A validation sample to test
the predication rule is lacking. The outcome event, intentional trauma, is
subject to variations in medical, legal, and societal definitions. The creation
of the prediction rule assumes that the predictive findings were defined properly
and accurately assessed, that is, the CT images were properly interpreted.
Clinical usefulness of the model requires others using the prediction rule
to use the same definitions of the significant variables.
The separation of the assessment of outcome and clinical prediction
is imperfect in this study. We were blinded to the CT imaging findings while
reviewing the medical records and assigning a diagnosis (the outcome). However,
the clinicians and social service professionals who investigated the circumstances
of the injuries were aware of, and likely influenced by, the CT imaging findings.
This potential error is mitigated by the use of objective factors to assure
a correct diagnosis of intentional injury, such as a confession by the perpetrator,
or the presence of suspicious skeletal injuries, retinal hemorrhages, or soft
tissue injuries. Other limitations are (1) the lack of uniformity in the veracity
of investigation among the subjects in this retrospective study, and (2) the
potential influence of the CT findings on the clinical decision regarding
initiation of a formal child abuse investigation.
Specific confirmatory information in the medical literature for our
findings is lacking; we could find no reports proposing a prediction rule
for neuroimaging findings in the diagnosis of intentional injury. Several
studies evaluating head trauma in abused children have shown a high incidence
of subdural hematoma.7-9
Zimmerman et al9 first reported the important
correlation between child abuse and subdural hemorrhage in the interhemispheric
space; this has been confirmed by other investigators.10
There is wide variation in the reported incidence of chronic nonhemic subdural
fluid collections with intentional head trauma, although the correlation is
widely accepted.11-13
There are a few series in the medical literature that compare head injuries
in children having intentional vs unintentional trauma that include statistical
analysis of the results. Ewing-Cobbs et al14
evaluated 60 patients between 0 and 6 years of age who had brain injuries
and found significantly (P<.05) more subdural
hematomas and hygromas in the patients with intentional injuries than in those
with unintentional injuries. Duhaime et al15
studied 100 children 24 months of age and younger who were admitted to the
hospital with head trauma and found a statistically significant (P<.001) relationship between intentional injury and the presence
of intradural (subdural, subarachnoid, contusion) hemorrhage. Hymel et al10 found interhemispheric hemorrhage, subdural hemorrhage,
"large (nonacute) extra-axial fluid," and basal ganglia edema to occur significantly
more frequently (P .05) in 39 children having
a diagnosis of intentional trauma than in the control group of 39 patients
with unintentional injuries. Reece and Sege16
evaluated 195 children younger than 3 years who had head trauma and found
that hemorrhage in the subdural and subarachnoid spaces occurred with a significantly
(P = .001) higher incidence in patients with intentional
injuries.
Application of the prediction rule to the study patients in the intent
uncertain group estimates that 69% of these children had had intentional injuries.
This is in keeping with the findings of other investigators that child abuse
is significantly underdiagnosed.17
CONCLUSIONS
Intentional trauma is the most common cause of intracranial hemorrhage
in children younger than 3 years. The subdural space is the most common location
of intracranial hemorrhage in children of this age group. Although all severe
head injuries in infants and young children must be viewed with a high index
of suspicion for intentional trauma, the CT imaging findings that are most
useful in differentiating intentional from unintentional causes in those children
with intracranial hemorrhage are convexity subdural hematoma, interhemispheric
subdural hematoma, nonhemic subdural fluid (hygroma), and lack of a skull
fracture.
| What This Study Adds
The neuroimaging findings for infants and young children with traumatic
intracranial hemorrhage provide important clues to the mechanism of the injury.
Several studies of children having intentional trauma have shown a high incidence
of subdural hematoma; however, the sensitivity and specificity of this and
other specific patterns of intracranial injury for the diagnosis of intentional
trauma is unknown. In this study, we evaluated the CT imaging findings in
293 children younger than 3 years who had intracranial hemorrhage. We propose
a prediction model for the diagnosis of intentional trauma based on 4 CT imaging
patterns.
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AUTHOR INFORMATION
Accepted for publication October 22, 2001.
Corresponding author and reprints: Robert G. Wells, MD, Radiology
Department, MS 721, Children's Hospital of Wisconsin, 9000 W Wisconsin Ave,
PO Box 1997, Milwaukee, WI 53201 (e-mail: rwells{at}chw.org).
From the Radiology Department, Children's Hospital of Wisconsin, Milwaukee
(Dr Wells); and the Division of Biostatistics, Medical College of Wisconsin,
Milwaukee (Dr Laud). Dr Vetter is in private practice in Singapore.
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