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Childs Nerv Syst (2010) 26:755–762

DOI 10.1007/s00381-009-1047-8

ORIGINAL PAPER

Natural history of traumatic meningeal bleeding in infants:


semiquantitative analysis of serial CT scans
in corroborated cases
Matthieu Vinchon & Marie Desurmont &
Gustavo Soto-Ares & Sabine De Foort-Dhellemmes

Received: 30 October 2009 Published online: 28 November 2009


# Springer-Verlag 2009

Abstract the falx and sagittal sinus, and then along the tentorium.
Background The natural history of posttraumatic meningeal Decrease and disappearance of blood was variable accord-
bleeding in infants is poorly documented, and the differ- ing to the site and the initial quantity of blood. We found no
ences between inflicted head injury (IHI) and accidental difference between IHI and AT.
trauma (AT) are debated. Autopsy findings have suggested Conclusion Our findings suggest that the primary site of
that anoxia also plays a role in bleeding; however, these meningeal bleeding in infantile head trauma is the convex-
findings may not reflect what occurs in live trauma patients. ity of the brain; blood cells then migrate toward the midline
Purpose We studied the natural history of traumatic following the flow of cerebrospinal fluid circulation and
meningeal bleeding in infants using serial computed inferiorly following gravity. The pattern of bleeding in
tomography (CT) scans in corroborated IHI and AT. traumatic cases appears similar in IHI and AT but different
Materials and methods From our prospective series, we from anoxic lesions.
selected corroborated cases (confessed IHI or AT having
occurred in public), who underwent at least three CT scans Keywords Traumatic head injury . Infant .
in the acute phase. We performed a semiquantitative Shaken baby syndrome . Accidental head trauma .
analysis of meningeal bleeding using a four-tier scale CT scanner . Subdural hematoma . Pathophysiology
(absent, faint, frank, and thick) derived from the Fisher
grading for aneurysmal bleeding in four regions of interest
(convexity, falx cerebri, sagittal sinus, and tentorium Introduction
cerebelli).
Results We studied 20 cases: ten IHI and ten AT. Bleeding Subdural hematomas (SDH) are common traumatic lesions
was maximal at the convexity initially, then increased along in infants not only in inflicted head injury (IHI) but also in
accidental trauma (AT). Computed tomography (CT)
M. Vinchon (*) scanner is the most widely used imaging modality for the
Department of Pediatric Neurosurgery, Lille University Hospital, initial diagnosis and subsequent follow-up of meningeal
59 037 Lille Cedex, France
bleeding in infants [1, 7]. However, the natural history of
e-mail: m-vinchon@chru-lille.fr
meningeal bleeding in infants is poorly documented
M. Desurmont because cases with undisputable trauma, precise dating,
Department of Legal Medicine, Lille University Hospital, and serial imaging are uncommon. Cases of confessed IHI
Lille, France
are difficult to collect, and cases of corroborated AT
G. Soto-Ares (having occurred in public) are rare.
Department of Neuroradiology, Lille University Hospital, As a result, the radiological description of meningeal
Lille, France bleeding in infants has always been mostly qualitative, and
differential diagnosis between IHI and AT has been based
S. De Foort-Dhellemmes
Department of Neuroophthalmology, Lille University Hospital, on such features as thickening of the falx [16, 31],
Lille, France subtemporal hematoma [2, 26], and mixed-density hemato-
756 Childs Nerv Syst (2010) 26:755–762

mas suggesting repeated trauma [15, 16]. These depictions performed during the acute phase were available for
have often been arbitrary and tainted by circular reasoning review. The time of AT was noted from the admission
(description of findings in categories based on the same report; regarding IHI, we chose the time of clinical
findings). Other studies have found that features often onset of symptoms reported on admission as an
considered as indicative of IHI are in fact common in approximation for the time of abuse because several
infants, whatever the cause of trauma [33, 35, 36]. The reports have established that symptoms of IHI generally
temporal evolution of meningeal blood is also poorly occur immediately after abuse [3, 29, 30].
documented; however, knowledge of time-related altera- The first CT scan was often performed in other centers
tions might be useful in forensic investigations for the before referral, following different protocols, including
dating of trauma and the diagnosis of repeated assault. In a axial views without contrast. Control CT scans were all
previous study, we found that dating of trauma could be performed in our institution following a standard proto-
based on the pattern of blood in CT and magnetic resonance col (typically 120 kV, 215 mA, total irradiation dose
imaging (MRI) scans [34]. 458 mGy cm). The indication for and timing of control
Another question is the origin and pathophysiology CT scans were dictated by the need for the medical and
of meningeal bleeding. The classical hypothesis is surgical management of the patient.
tearing of the corticodural bridging veins caused by Each CT scan was reviewed, and data were collected on
shaking [14, 21–23], but this theory has been challenged the date of the CT, volume, and distribution of bleeding and
by recent advances in anatomy [19] and pathology [12, 27, thickness of the SDH. In order to study the extent of
28]. Several authors now consider that the bleeding bleeding on CT scan, we devised a hemorrhage score
originates from the dural venous plexus close to the derived from the Fisher grading widely used to evaluate
sagittal sinus and could be caused by reflux from the aneurysmal rupture [9]; this semiquantitative grading rates
sagittal sinus. However, these data gathered from meningeal bleeding as 0—absence of blood, 1—faint, 2—
autopsy cases in traumatic as well as nontraumatic frank, and 3—blood in thick layers or hematoma. We
cases may not reflect the pathophysiology in live defined four regions of interest (ROI) for the grading of
subjects with traumatic meningeal bleeding. In addition, meningeal bleeding: the convexity of the brain (under the
autopsy data give no indication on the kinetics of calvaria, at some distance from the midline), the superior
meningeal bleeding. Squier and Mack concluded that sagittal sinus (under the calvaria close to the midline), the
“there is a real need for detailed observational studies of falx cerebri (midline meninges at a distance from the
the natural history of infant SDH” [28]. calvaria); and the tentorium cerebelli. The grading in these
In order to study the natural history of traumatic different ROI is illustrated in Fig. 1. In addition, the
meningeal bleeding in infants, we selected cases of infant thickness of the subdural collection as noted on preopera-
victims of corroborated IHI or AT who had serial CT scans. tive CT scans was defined as its maximal depth, measured
The CT scans were studied using a semiquantitative scale perpendicular to the cortex on axial views.
derived from the grading designed by Fisher for aneurysmal These data were plotted in Figs. 2, 3, 4, 5, and 6 with the
bleeding [9]. delay from trauma to CT as the abscissa and the

Materials and methods

Our database was started in April 2001, following previ-


ously published methodology [35], and had since included
prospectively 469 cases of head injuries in children
under the age of 2 years. Among these, 84 were
corroborated cases of IHI or AT. We selected cases of
corroborated IHI, defined as abuse confessed by the
perpetrator, the data being provided by the judiciary to
legal physicians during expertise processes, and cases of
AT independently witnessed accidents having occurred
in public. We did not include cases of birth injury,
which represent a different group with regard to age and
pathophysiology. Corroborated cases of IHI and AT are
the subject of a companion paper. Among these, we
selected cases for which at least three CT scans Fig. 1 Grading of bleeding in the different regions of interest (ROI)
Childs Nerv Syst (2010) 26:755–762 757

Fig. 2 Time evolution of meningeal blood at the convexity of the Fig. 4 Time evolution of meningeal blood at the level of the falx
brain in AT and IHI. Each line represents an individual observation. cerebri in AT and IHI. Each line represents an individual observation.
As a general rule, the score was maximal on the first CT scanner and As a general rule, the score increased initially and then decreased after
then decreased after a variable delay, depending on the initial a variable delay. The delay to peak was generally shorter, and the
importance of bleeding. Note that blood at the convexity can delay to decrease was longer, when the initial bleeding was more
disappear completely within a few days after trauma severe. Note that blood can disappear completely within less than a
week after trauma

hemorrhage score or SDH thickness score as the ordinate. Results


In order to provide a graphic representation of the evolution
of lesions with time for each individual, each observation We selected 20 cases of children under 24 month,
was presented as a three-point plus line. All the observa- victims of confessed IHI or witnessed AT, who had at
tions in the different ROI were plotted together in the least three CT scanners during the acute phase. The
corresponding diagrams. In order to assess the kinetics of mechanism of IHI was shaking in seven cases and
meningeal bleeding between the different ROI, we studied beating in three cases. AT were due to traffic accident
the mean delay to the peak of hemorrhage score in the in eight cases and falls from windows in two cases. The
different ROI; the delay to the peak was the time elapsed clinical and radiological features, comparing IHI and AT,
between the trauma and the earliest CT scan showing the are summarized in Table 1.
highest value attained by the hemorrhage score (Fig. 7). In The temporal variations of the hemorrhage score in
order to compare the natural history of meningeal bleeding the different ROI for each individual observation are
in IHI and AT, we noted the presence of blood in the shown in Figs. 2, 3, 4, and 5. The hemorrhage score at the
different ROI on the first, second, and third CT scanners in convexity of the brain was maximal on the first CT in all
the two groups; these data, along with clinical data on cases; the score decreased at a variable speed, which
admission and at last control, are summarized in Table 1. appeared faster if the initial score was low and slower if
Means were compared using Student’s t test, using the initial score was maximal (Fig. 2). The hemorrhage
commercially available software. score at the falx and sagittal sinus was generally not

Fig. 5 Time evolution of meningeal blood at the level of the


Fig. 3 Time evolution of meningeal blood at the level of the superior tentorium cerebri in AT and IHI. Each line represents an individual
sagittal sinus in AT and IHI. Each line represents an individual observation. As a general rule, the score increased initially, more
observation. As a general rule, the score increased initially and then slowly than for the superior sagittal sinus or the falx cerebri, and then
decreased after a variable delay. The delay to peak was generally decreased after a variable delay. The delay to peak was also generally
shorter, and the delay to decrease was longer, when the initial bleeding shorter, and the delay to decrease was longer, when the initial bleeding
was more severe. Note that blood did not disappear completely along was more severe. Note that blood tends to disappear completely within
the sagittal sinus during the period of the study a few weeks after trauma
758 Childs Nerv Syst (2010) 26:755–762

quence, the cases of AT in the present study group may not


be representative of the whole group; this does not diminish
the finding that the natural history of meningeal bleeding
shows little difference between IHI and AT.
AT are easily datable when these accidents occur in public
and are witnessed. Regarding IHI, precise timing is more
problematic because the perpetrator’s confession may be
absent, imprecise, or even deliberately misleading. However,
several reports have established that symptoms of IHI
generally occur immediately after abuse [3, 29, 30]; our
choice to use the time of clinical onset as an approximation
Fig. 6 Time evolution of subdural collections in AT and IHI. Each
for the time of abuse was dictated by the fact that the police
line represents an individual observation, before drainage. The
increase in thickness was highly variable, and spontaneous regression investigation data at our disposal often lacked precision on
was witnessed in some occasions; in the majority, however, the timing. In a companion paper to the present study, we found
collections regressed only after surgical drainage that the delay to admission was longer for IHI than for AT,
without reaching statistical significance; however, the delay
to the first CT was significantly longer in IHI likely because
maximal from the beginning, increased with some delay, then of the misleading initial presentation. In the present study,
decreased; when the initial rate was high, the slope of the with a more limited number of patients, the delay from
increase was steeper, and the decrease was slower; the opposite trauma to first CT was also shorter in AT; however, only the
was found when the initial score was low (Figs. 3 and 4). The delay to the second CT showed a statistically significant
evolution of the hemorrhage score at the tentorium was difference. These differences may account for some of the
similar to findings at the falx and sagittal sinus but with more discrepancies between the patterns of meningeal blood in IHI
delay (Fig. 5). In general, the blood at the convexity and AT as shown in Table 1.
disappeared completely within a few days after trauma, In our study, the initial imaging was often made in different
whereas the decrease occurred much later in the other ROI. hospitals, following similar protocols of standard use for head
The mean delay to peak of the hemorrhage score for the injuries in infants (plain CT, axial view, brain window). We do
different ROI is shown in Fig. 7. The delay to the peak was not think the technique of the CT scan impacted much on our
longer for the sagittal sinus and falx, compared with the analysis of the extent of meningeal bleeding. Further CT scans
convexity, although the difference was not statistically were made on request, according to the need for medical
significant. The delay to the peak for the tentorium was, management of the child; these variations in timing imposed
however, significantly longer compared with the three other on us the diagram presentation in Figs. 2, 3, 4, 5, and 6.
sites.
The evolution of the thickness of subdural collection in
the different observations is presented in Fig. 6.

Discussion

Analysis of biases

Our study is based on a limited subset of patients because


of restrictive inclusion criteria, which introduces a selection
bias. Most patients in our prospective register were not
included because either their trauma lacked corroboration Fig. 7 Mean delay between the trauma and the peak of meningeal
or they underwent less than three CT scans. Inclusion in the blood in the different ROI. For the convexity of the brain, this delay to
the peak corresponded to the delay to the first CT scanner. The
present series therefore implies a prolonged history with a
difference between delay to the peak at the convexity and along the
longer hospital stay and often an evolution toward a SDH sagittal sinus and the falx did not reach statistical significance;
requiring drainage. Furthermore, both the mildest cases however, the delay to peak at the tentorium was statistically longer.
(who did not require control imaging) and the most severe Our interpretation is that the meninges at the convexity of the brain are
the site of original bleeding, after which part of the blood migrates to
(who died quickly) were not included. The vast majority of
the midline following the circulation and absorption of CSF (falx and
AT occurred at home (not corroborated) or had simple sagittal sinus), while another part sediments following gravity to the
impact lesions not requiring repeated imaging. In conse- recumbent regions of the skull (tentorium)
Childs Nerv Syst (2010) 26:755–762 759

Role of CT Table 1 (continued)

Abuse Accident p value


Since its introduction, CT scanning has been little exploited
as a source of information on head injuries in infants Mean duration of stay
probably because MRI soon emerged as a superior tool for Under sedation (days) 4.9 1.3 0.02
the study of brain lesions, dating of trauma, and diagnosis In ICU (days) 7.2 2.6 0.02
of repeated assault [7, 26]. However, CT scanning has In hospital (days) 21.0 12.4 0.004
Outcome at last control
Table 1 Comparison of clinical and radiological data in AT and IHI Age (months) 26.1 25.7 NS
Sequels 4 1
Abuse Accident p value
Mortality 1 0
Patients
Only means were compared, using Student’s t test; no chi-square test
N 10 10
could be performed because the theoretical values were all under 5. In
M/F 6/4 6/4 this table, only the presence or absence of blood in the different ROI is
Mean age (months) 4.1 7.4 NS reported, with no attempt at quantifying it. This table shows that AT
Signs and symptoms at presentation tended to have more often signs of impact and/or skull fracture than
IHI and that meningeal blood tended to be more widespread in the IHI
Signs of impact 3 10 group, correlated with a more severe clinical presentation and
Coma 3 3 outcome. However, the time-related pattern of blood distribution
Epilepsy 9 3 between the different ROI appeared to depend more on the delay after
trauma than on its cause. For example, the absence of blood along the
Status epilepticus 3 0
tentorium on the second CT scanner in several cases of AT may be
Raised ICP 10 4 related to the significantly shorter delay to second CT scanner in this
First CT group. In summary, the patterns of AT and IHI differed by the
Mean delay (hours) 17.7 8.7 NS presence or absence of signs of impact and the extent of meningeal
bleeding; however, the natural history of meningeal hemorrhage in the
Blood two groups did not appear different
Convexity 10 7
Sagittal sinus 9 9
Falx 10 8
remained of value because of its availability, repeatability,
Tentorium 5 4
and accuracy to diagnose small amounts of fresh blood that
Subdural
would be undetected by MRI [26, 31]. The ease with which
Thickness (mm) 4.2 2.7 NS
CT scan can be repeated allows observations on the kinetics
Second CT
of the lesions [7]. However, no systematic study on the
Mean delay (days) 2.7 1.5 0.04
natural history of meningeal bleeding with imaging has
Blood
been performed probably because of the scarcity of accurate
Convexity 8 6 data, of the difficulty to establish clinicoradiological
Sagittal sinus 10 10 correlates, and of the lack of grading system. In an earlier
Falx 9 9 study, we noted that meningeal blood clots appeared to
Tentorium 10 4 change location between one study and the next [34]. We
Subdural decided to focus on this unreported phenomenon because it
Thickness (mm) 4.9 2.9 NS appeared to illustrate and complement pathological find-
Third CT ings, such as thickening of the falx [16, 36], infiltration of
Mean delay (days) 7.1 12.5 NS the dural channels by red blood cells, and absence of
Blood tearing of the corticodural veins [12, 28]. For our present
Convexity 7 5 study, we selected precisely dated trauma, in order to have a
Sagittal sinus 8 9 reliable starting point, and repeated observations with
Falx 9 7 imaging. For these reasons, we restricted our dataset to
Tentorium 9 9 corroborated IHI or AT, with at least three CT scans.
Subdural
Thickness (mm) 6.1 2.2 0.008 CT evaluation
Raised ICP
Mean delay (days) 1.9 6.1 0.016 We did not find in the literature a scale that quantita-
Puncture 8 6 tively evaluated meningeal bleeding in infantile traumatic
Drainage 6 3 injuries with the aim of studying its natural history. We
760 Childs Nerv Syst (2010) 26:755–762

chose to adapt Fisher’s grading [9] because it has been forceful, abusive shaking, as attested by the delay to
validated and accepted for a long time, its four-tier scale referral, the absence of spontaneous confession, the
has proved both informative and reliable, and it has context of neglect and familial dysfunction, and confirmed
spawned a number of variant evaluation scales. We by confession from the perpetrators [3, 18, 29, 30]. We
defined the different ROI based on our previous experi- also found that the pattern of lesions showed little
ence and on the focus of the literature on the sagittal sinus dissimilarity between IHI and AT but that the pathophys-
[10, 19, 27] and falx cerebri [7, 16, 36]. Considering the iology appeared quite similar in both groups. This
results in our study, we propose that this scale system suggests that the natural history of meningeal bleeding is
could be used for the evaluation of the natural history of related to age rather than to the cause of trauma. One may
traumatic head injuries in infants. wonder whether the autopsy findings described in case of
traumatic as well as nontraumatic death [28] are identical
Pathophysiology to our findings in corroborated trauma cases or are the
result of other, nonspecific, per-mortem processes. Post-
The origin of meningeal bleeding in IHI has long been mortem imaging before autopsy may become necessary to
thought to be the tearing of corticodural bridging veins answer these questions [15].
along the sagittal sinus [16, 21, 23, 36]. However, The evolution of traumatic lesions with time gives
autopsy demonstrated an absence of tearing of these veins indications for the dating of trauma in legal cases. Most
in many cases [12, 19, 28]. Tearing of the bridging veins publications have focused on the modifications of blood
can sometimes be found during craniotomy for massive, density or MRI signal (which can be misleading);
clotted SDH; however, it appears to be a marginal cause of however, several authors have also reported redistribu-
meningeal bleeding in infants. In addition, the energy tion of blood from the convexity to the falx [7, 17, 34] or
required to tear the veins is considered higher than that sedimentation to the tentorium and the spinal axis [5, 8,
resulting from abusive shaking [23, 25]. The origin of 28]. Unlike autopsy, imaging, especially CT scan, can be
meningeal bleeding is now seen by several authors in the repeated at several stages of the disease, allowing the
dura mater itself [5, 19, 28]. In sophisticated micro- follow-up of time-related alterations [7]. In the absence of
anatomical studies, several authors have described venous drainage, the spontaneous evolution toward chronic SDH,
plexuses, as well as dural “holes” in the vicinity of the sagittal with thickening of fibrous membranes and rebleeding, is a
sinus, which are likely involved in the absorption of classical outcome in adults and also occurs in some infants
cerebrospinal fluid (CSF) in infants whose arachnoid villi with brain atrophy [11]. In most infants, however, the
are immature [10, 19, 27]. Pointing out the characteristic SDH evolves quite differently, the accumulation of CSF
thickening of the falx and paramedian location of blood in playing a major role in its pathophysiology [32]. Our
infantile SDH, several authors postulated that the meningeal hypothesis is that after the initial bleeding, blood cells
bleeding could be the result of oozing from these plexuses migrate, following the gradient of circulation of CSF
[5, 19, 28]. Our data appear in accordance with the hypothesis toward its absorption sites, likely the dural “holes”
of bleeding from the dura mater but suggest instead that the described by Squier et al. [27]. Histologically, red blood
initial bleeding occurs at some distance from the midline and cells have been assimilated to “natural tracers of CSF
that the thickening of the falx is a secondary feature. absorption” [38]. We think this is no coincidence that
The traumatic nature of meningeal bleeding in blood accumulates in the meningeal sites that are
infantile SDH has been challenged in recent years. The responsible for the absorption of CSF, at the same time
emphasis was put on “alternative source of bleeding in CSF accumulates in the subdural space. More research is
nontraumatic condition” [19] and on hypoxic mechanisms needed to confirm this hypothesis.
causing brain damage as well as meningeal bleeding [13], Spontaneous disappearance of acute SDH has also been
spurring heated controversy considering the legal impli- reported [6, 17, 20]. The delay to disappearance of subdural
cations [4]. Squier and Mack formulated the hypothesis of blood in neonates has been established at less than 4 weeks
a reflux from the venous sinus to the dural venous [24, 37]; these findings have important medicolegal
plexuses close to the superior sagittal sinus [19, 28]. This implications since birth injury is sometimes presented as a
hypothesis was based on the autopsy finding of dural cause of unexplained SDH diagnosed later in life. In our
bleeding in the paramedian regions, in patients without study, the time to disappearance of meningeal blood varied
evidence of impact, and even in patients who died of following the site and the initial importance of bleeding but
nontraumatic causes. Whatever the origin of bleeding and could be as quick as a few days at the convexity. This
brain damage, we think that the traumatic nature of the emphasizes the importance of careful evaluation of CT
lesions in our series is beyond doubt. In cases of IHI, we scanners for the presence of residual bleeding in sites like
believe that the primum mobile of lesions remains the midline and posterior fossa [7].
Childs Nerv Syst (2010) 26:755–762 761

Conclusion 13. Geddes JF, Tasker RC, Hackshaw AK, Nickols CD, Adams GGW,
Whitwell HL, Scheimberg I (2003) Dural hemorrhage in non-
traumatic infant death: does it explain the bleeding in ‘shaken
In the present study, we studied CT scanner following a baby syndrome’? Neuropathol Appl Neurobiol 29:14–22
semiquantitative method for the study of meningeal 14. Guthkelch AN (1971) Infantile subdural haematoma and its
bleeding in different ROI. Using this method on a selected relationship to whiplash injuries. BMJ 2:430–431
15. Hart BL, Dudley MH, Zumvalt RE (1996) Postmortem cranial
group of patients with known time of trauma, this method
MRI and autopsy correlation in suspected child abuse. Am J
allowed us to approach the natural history of meningeal Forensic Med Pathol 17:217–224
bleeding. We found that blood was maximal from the 16. Harwood-Nash DC (1992) Abuse to the pediatric central nervous
beginning at the convexity and increased with delay on the system. Am J Neuroradiol 13:569–575
17. Kuroiwa T, Tanabe H, Takatsuka H, Arai M, Sakai N, Nagasawa
midline sites, then along the tentorium cerebelli. These S, Ohta T (1993) Rapid spontaneous resolution of acute extradural
findings lead us to formulate hypotheses on the site of and subdural hematomas. Case report. J Neurosurg 78:126–128
initial bleeding and the relation between meningeal bleed- 18. Leestma JE (2006) “Shaken baby syndrome”: do confessions by
ing and clogging of the CSF absorption pathways leading alleged perpetrators validate the concept? J Am Phys Surg 11:14–16
19. Mack J, Squier W, Eastman JT (2009) Anatomy and development
to CSF accumulation in the subdural space. Knowledge of
of the meninges: implications for subdural collections and CSF
these time-related modifications may be of interest for the circulation. Pediatr Radiol 39:200–210
timing of traumatic lesions and the diagnosis of repeated 20. Modic MT, Kaufman B, Bonstelie CT, Tomsick TA, Weinstein
trauma in legal cases. These findings need to be confirmed MA (1981) Megalocephaly and hypodense extracerebral fluid
collections. Radiology 141:93–100
and validated with more cases.
21. Papasian NC, Frim DM (2000) A theoretical model of benign
external hydrocephalus that predicts a predisposition toward extra-
axial hemorrhage after minor head trauma. Pediatr Neurosurg
33:188–193
References 22. Prange MT, Coats B, Duhaime AC, Margulies SS (2003)
Anthropomorphic simulations of falls, shakes, and inflicted
1. Barkovich AJ (2000) Brain and spine injuries in infancy and impacts in infants. J Neurosurg 99:143–150
childhood. In: Barkovich AJ (ed) Pediatric neuroradiology, 3rd 23. Raul JS, Roth S, Ludes B, Willinger R (2008) Influence of the
edn. Lippincott Williams and Wilkins, Philadelphia, pp 157–249 benign enlargement of the subarachnoid space on the bridging
2. Barlow KM, Gibson RJ, McPhillips M, Minns RA (1999) veins strain during a shaking event: a finite element study. Int J
Magnetic resonance imaging in acute non-accidental head injury. Legal Med 122:327–340
Acta Paediatr 88:734–740 24. Rooks VJ, Eaton JP, Ruess L, Petermann GW, Keck-Wherley J,
3. Biron D, Shelton D (2005) Perpetrator accounts in infant abusive Pedersen RC (2008) Prevalence and evolution of intracranial
head trauma brought about by a shaking event. Child Abuse hemorrhage in asymptomatic term infants. Am J Neuroradiol
Neglect 29:1347–1358 29:1082–1089
4. Byard RW, Blumbergs P, Rutty G, Spehake J, Banner J, Krous HF 25. Roth S, Raul JS, Ludes B, Willinger R (2007) Finite element
(2007) Lack of evidence for a causal relationship between analysis of impact and shaking inflicted to a child. Int J Legal
hypoxic–ischemic encephalopathy and subdural hemorrhage in Med 121:223–228
fetal life, infancy, and early childhood. Ped Developmental 26. Sato Y, Yuh WTC, Smith WL, Alexander RC, Kao SCS,
Neuropathol 10:348–350 Ellerbroek CJ (1989) Head injury in child abuse: evaluation with
5. Case ME (2008) Inflicted traumatic injury in infants and young MR imaging. Radiology 173:653–657
children. Brain Pathol 18:571–582 27. Squier W, Lindberg E, Mack J, Darby S (2009) Demonstration of
6. Duhaime AC, Christian C, Armonda R, Hunter J, Hertle R (1996) fluid channels in human dura and their relationship to age and
Disappearing subdural hematomas in children. Pediatr Neurosurg intradural bleeding. Child’s Nerv Syst 25:925–931
25:116–122 28. Squier W, Mack J (2009) The neuropathology of infant subdural
7. Feldman KW, Brewer DK, Shaw DW (1995) Evolution of the haemorrhage. Forensic Sci Int 187:6–13
cranial computed tomography scan in child abuse. Child Abuse & 29. Starling SP, Holden JR, Jenny C (1995) Abusive head trauma:
Neglect 19:307–314 the relationship of perpetrators to their victims. Pediatrics
8. Feldman KW, Weinberger E, Milstein JM, Fligner CL (1997) 95:259–262
Cervical spine MRI in abused infants. Child abuse Neglect 30. Starling SP, Patel S, Burke BL, Sirotnak AP, Stronks S, Rosquist
21:199–205 P (2004) Analysis of perpetrator admissions to inflicted traumatic
9. Fisher CM, Kistler JP, Davis JM (1980) Relation of cerebral brain injury in children. Arch Pediatr Adolesc Med 158:454–458
vasospasm to subarachnoid hemorrhage visualized by computer- 31. Stoodley N (2002) Non-accidental head injury in children:
ized tomographic scanning. Neurosurgery 6:1–9 gathering the evidence. Lancet 360:271–272
10. Fox RJ, Walji AH, Mielke B, Petruk K, Aronyk KE (1996) 32. Vinchon M, Noulé N, Soto-Ares G, Dhellemmes P (2001)
Anatomic details of intradural channels in the parasagittal dura: a Subduroperitoneal drainage for subdural hematomas in infants:
possible pathway for flow of cerebrospinal fluid. Neurosurgery results in 244 cases. J Neurosurg 95:249–255
39:84–91 33. Vinchon M, Noizet O, Defoort-Dhellemmes S, Soto-Ares G,
11. Friede RL (1989) Subdural hematomas, hygromas, and effusions. Dhellemmes P (2002) Infantile subdural hematomas due to traffic
In: Friede RL (ed) Developmental neuropathology. Springer, accidents. Pediatr Neurosurg 37:245–253
Berlin, pp 198–208 34. Vinchon M, Noulé N, Tchofo PJ, Soto-Ares G, Fourier C,
12. Geddes JF, Hackshaw AK, Vowles GH, Whitwell HL (2001) Dhellemmes P (2004) Imaging of head injuries in infants:
Neuropathology of inflicted head injury in children. I. Patterns of temporal correlates and implications for the diagnosis of child
brain damage. Brain 124:1290–1298 abuse. J Neurosurg 101(1 Suppl):44–52
762 Childs Nerv Syst (2010) 26:755–762

35. Vinchon M, Defoort-Dhellemmes S, Desurmont M, Dhellemmes 37. Whitby EH, Griffiths PD, Rutter S, Smith MF, Sprigg A, Ohadike
P (2005) Accidental and nonaccidental head injuries in infants: a P, Davies NP, Rigby S, Paley MN (2004) Frequency and natural
prospective study. J Neurosurg (Pediatrics 4) 102:380–384 history of subdural haemorrhages in babies and relation to
36. Wells RG, Vetter C, Laud P (2002) Intracranial hemorrhage in obstetric factors. Lancet 363:846–851
children younger than 3 years: prediction of intent. Arch Pediatr 38. Yamashima T (1986) Ultrastructural study of the final cerebrospinal
Adolesc Med 156:252–257 fluid pathway in human arachnoid villi. Brain Res 384:68–76

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