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Journal of Forensic and Legal Medicine 52 (2017) 62e69

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Journal of Forensic and Legal Medicine


j o u r n a l h o m e p a g e : w w w . e l s e v i e r . c o m / l o c a t e / j fl m

Traumatic brain injury: Comparison between autopsy and ante-


mortem CT
Stephanie Panzer a, b, *, Lidia Covaliov c, Peter Augat b, Oliver Peschel c
a
Department of Radiology, Trauma Center Murnau, Prof.-Küntscher-Straße 8, D-82418 Murnau, Germany
b
Institute of Biomechanics, Trauma Center Murnau and Paracelsus Medical University Salzburg, Prof.-Küntscher-Straße 8, D-82418 Murnau, Germany
c
Institute of Legal Medicine, Ludwig-Maximilians University, Munich, Nussbaumstraße 26, D-80336 Munich, Germany

a r t i c l e i n f o a b s t r a c t

Article history: Purpose: The aim of this study was to compare pathological findings after traumatic brain injury be-
Received 9 September 2016 tween autopsy and ante-mortem computed tomography (CT). A second aim was to identify changes in
Received in revised form these findings between the primary posttraumatic CT and the last follow-up CT before death.
27 May 2017
Methods: Through the collaboration between clinical radiology and forensic medicine, 45 patients with
Accepted 23 August 2017
Available online 26 August 2017
traumatic brain injury were investigated. These patients had undergone ante-mortem CT as well as
autopsy. During autopsy, the brain was cut in fronto-parallel slices directly after removal without
additional fixation or subsequent histology. Typical findings of traumatic brain injury were compared
Keywords:
Autopsy
between autopsy and radiology. Additionally, these findings were compared between the primary CT and
Virtual autopsy the last follow-up CT before death.
Computed tomography Results: The comparison between autopsy and radiology revealed a high specificity (80%) in most of the
Ante-mortem computed tomography findings. Sensitivity and positive predictive value were high (80%) in almost half of the findings. Sixteen
Traumatic brain injury patients had undergone craniotomy with subsequent follow-up CT. Thirteen conservatively treated pa-
tients had undergone a follow-up CT. Comparison between the primary CT and the last ante-mortem CT
revealed marked changes in the presence and absence of findings, especially in patients with severe
traumatic brain injury requiring decompression craniotomy.
Conclusion: The main pathological findings of traumatic brain injury were comparable between clinical
ante-mortem CT examinations and autopsy. Comparison between the primary CT after trauma and the
last ante-mortem CT revealed marked changes in the findings, especially in patients with severe trau-
matic brain injury. Hence, clinically routine ante-mortem CT should be included in the process of autopsy
interpretation.
© 2017 Elsevier Ltd and Faculty of Forensic and Legal Medicine. All rights reserved.

1. Introduction strength of CT is the cross-sectional technique, with its high spatial


resolution, and the possibility of creating various kinds of re-
Forensic radiology is defined as radiological applications for the constructions in all desired planes.2,3 Furthermore, digital data can
forensic sciences.1 Virtual autopsy, sometimes called “virtopsy”, be easily stored, and cases can be re-examined decades later, even
combines post-mortem radiological imaging, such as computed after burial of the body and liberation of the crime scene.5 Post-
tomography (CT) and magnetic resonance imaging, with autopsy.2,3 mortem CT has been determined to be superior to autopsy in the
There has been more than a ten-fold increase in publications detection of gas accumulation and metallic foreign bodies, and it
related to forensic and post-mortem radiology since 2003 as it provides valuable information for the establishment of trauma
developed from an obscure topic to a relevant field in the forensic patterns and accident reconstruction.2,6e9
sciences.4 However, clinical radiology and post-mortem imaging are not
CT is extensively used to investigate traumatic injury.4 The main the same, and radiologists are at risk of misinterpreting findings if
they rigorously apply the rules of clinical radiological analysis to
post-mortem analysis.9,10 Post-mortem imaging is usually
* Corresponding author. Department of Radiology, Trauma Center Murnau, Prof.- restricted to forensic institutions that collaborate with adjacent
Küntscher-Straße 8, D-82418 Murnau, Germany. radiological departments.2,7
E-mail address: stephanie.panzer@bgu-murnau.de (S. Panzer).

http://dx.doi.org/10.1016/j.jflm.2017.08.007
1752-928X/© 2017 Elsevier Ltd and Faculty of Forensic and Legal Medicine. All rights reserved.

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S. Panzer et al. / Journal of Forensic and Legal Medicine 52 (2017) 62e69 63

Ante-mortem CT is also considered in forensic radiology. It can evaluation.17,18 Thus, at least one of these findings had to be present
provide additional information regarding the clinical situation. in autopsy and/or radiology. The following pathological findings
Furthermore, it is applied in combination with post-mortem CT to were considered:
compare findings and to improve the understanding of post-
mortem features.7,11e13 The number of CT examinations continues - epidural hematoma,
to increase in clinical settings. For example, in severely injured - subdural hematoma,
patients, whole-body CT is increasingly becoming the standard - subarachnoid hemorrhage,
diagnostic technique.14e16 In addition to the above-mentioned - intraventricular hemorrhage,
strengths of CT, ante-mortem CT is widely used in the clinical - diffuse axonal injury,
setting and radiologists are familiar with the analysis. Therefore, - cortical contusions,
these CT examinations may provide additional or complementary - intracerebral hematoma,
information for forensic cases without creating new costs. - brain edema,
The first aim of this study was to compare the assessment of - midline shift,
pathological findings occurring in traumatic brain imaging be- - infarction/necrosis,
tween autopsy and ante-mortem CT in the clinical setting. The - intracranial gas,
second aim was to identify changes in these findings between the - rupture of bridging vein.
first posttraumatic CT and the last follow-up CT before death. An
ulterior motive was to increase the collaboration between radi- If findings were present at more than one site, they were
ology and forensic medicine, not only in scientific studies but also assessed multifocally and termed by additional Arabic numerals.
in the clinical routine. Thereby, ante-mortem CT could provide For collection of autopsy data, the autopsy reports were reviewed
additional information for the interpretation of autopsy findings in for the presence or absence of the above-mentioned findings. For
the clinical situation. radiological data collection, CT examinations were re-evaluated by
the first author (who is a senior radiologist with 18 years of expe-
2. Material and methods rience, including trauma imaging) for the presence or absence of the
findings. In patients with follow-up CT examinations, the primary CT
2.1. Material and the last follow-up CT examination before death were evaluated.

Between June 2005 and November 2014, a total of 475 patients 2.2.2. Comparison between autopsy and radiology
died in the Trauma Center Murnau, Germany, and underwent au- For comparison between autopsy and radiology, data from the
topsy at the Institute of Legal Medicine of the Ludwig-Maximilians- autopsy reports were compared with the findings of the last ante-
University, Munich, Germany. Out of these patients, a collective was mortem CT examination. The number of positive and negative
chosen, including patients with traumatic brain injury (see 2.2.1. for findings was counted for each case. Sensitivity (number of positive
pathological findings indicating traumatic brain injury). The findings in the autopsy that were detected on CT images), speci-
included patients were required to have undergone a recent (day of ficity (number of the negative findings in the autopsy that are also
the trauma or within the following two days) primary unenhanced negative on CT images), and the positive predictive value (number
CT examination prior to any operational treatment in terms of a of the radiologically detected findings that are also positive in the
combined CT of the head and cervical spine as part of a multiple autopsy) were calculated, whereupon the autopsy was determined
trauma CT or a CT of the head. Additionally, patients treated neu- as the gold standard.
rosurgically after the primary CT examinations were required to
have undergone a postoperative CT examination of the head. 2.2.3. Changes in radiological findings on follow-up CTs
CT examinations were performed on one of the following de- The presence and absence of findings was compared between
vices: 64-detector multislice CT (LightSpeed VCT, General Electrics, the primary CT and the last ante-mortem CT. This was done sepa-
Milwaukee, Wisconsin, USA) or 128-detector multislice CT rately for the group of patients that underwent neurosurgical
(SOMATOM Definition ASþ, Siemens, Erlangen, Germany). Follow- treatment by craniotomy and evacuation of hematomas and the
up CTs of the head were performed on these scanners or on a 4- group of patients that were treated conservatively.
detector multislice CT (LightSpeed Plus, General Electrics, Mil- Additionally, measurements were collected for the main he-
waukee, Wisconsin, USA). Cranial CTs as part of a multiple trauma matomas that were surgically evacuated as well as for the degree
or a combined head and neck examination were performed in he- and side of midline shift.
lical mode with slice thickness of 0.625 mm or 0.75 mm, and
120 kV. Isolated cranial CTs were performed in helical or single- 3. Results
slice mode, with slice thickness ranging from 2.5 to 5 mm and
120 kV. 3.1. Demographics and time intervals
During the autopsy procedure, the brain was cut in approxi-
mately 1-cm-thick fronto-parallel slices directly after removal The final population consisted of 45 patients, 31 males and 14
without additional fixation. In cases of necrotic and softened brain females. The mean age at death was 66 years, ranging from 12 to 91
parenchyma, the slice thickness was larger, depending on the brain years. In autopsy reports, the cause of death was reported as a ce-
consistency. rebral cause in 34 cases, a cardiac cause in 3 cases, pneumonia in 3
Autopsy reports were written by at least two independent se- cases, a thoracic cause in 2 cases, and shock and multi-organ failure
nior forensic pathologists without further sub-specialisation. in 1 case. In 1 case, the cause of death was unclear.
The initial CT examination was a multiple trauma CT in 22 cases,
2.2. Methods a combined CT examination of the head and cervical spine in 18
cases and an isolated CT examination of the head in 5 cases. The
2.2.1. Data classification and collection primary CT was performed at the day of trauma in 34 cases, on the
The presence of traumatic brain injury was based on pathologies following day (day 1) in 9 cases, and on day 2 in 2 cases, the mean
assessed during routine autopsy and daily radiological was calculated as 0.3 days. The time interval from the trauma to the

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64 S. Panzer et al. / Journal of Forensic and Legal Medicine 52 (2017) 62e69

last CT had a mean of 2.5 days, ranging from 0 to 24 days. The time injury was diagnosed exclusively on CT images in 3 cases. Intra-
interval from the last CT to death had a mean of 5.3 days, ranging cranial gas was detected exclusively on CT images in 18 cases.
from 0 to 52. Autopsy was performed between days 0 and 5 after Rupture of a bridging vein was reported in 1 autopsy.
death, with a mean of 2.2 days.
Sixteen patients underwent craniotomy with subsequent
3.3. Changes in radiological findings on follow-up CTs
follow-up CTs. Trepanation was performed on the same day of the
trauma in 12 patients, and on day 3, days 2e4, day 7 and day 12 in
In the group of 16 patients with neurosurgical treatment by
one case, respectively. In 13 conservatively treated patients, a
craniotomy, discrepancies were found for most of the assessed
follow-up CT was available. The time interval between the primary
pathological entities between the primary CT and the last post-
CT and the last follow-up CT before death had a mean of 4.2 days,
operative CT before death (Fig. 2a). Findings that were present in the
ranging from 0 to 24 days.
primary CT and were no longer detectable in the last postoperative
CT (“lost findings”) consisted especially of epidural hematomas,
subarachnoid hematomas and midline shift. Findings that devel-
3.2. Comparison between autopsy and radiology
oped between the primary CT and the last postoperative CT before
death (“new findings”) consisted of 8 cases with intracranial gas
The comparison between findings in autopsy protocols and the
accumulation due to the craniotomy as well as of 9 cases with
last ante-mortem CT examinations in the 45 studied cases revealed
infarction/necrosis. New midline shift arose in 6 cases, and different
a high specificity (80%) in most of the findings. Sensitivity and
kinds of haematomas developed in up to 3 cases (Figs. 3e6).
positive predictive value were high (80%) in almost half of the
The group of 13 conservatively treated patients who underwent
assessed pathological findings (Table 1). In general, the presence of
follow-up CT examinations revealed less discrepancies in the
the particular findings was low. The most frequent findings in both
assessed pathological findings between the primary CT and the last
methods were brain edema and subarachnoid hemorrhage, fol-
follow-up CT before death (Fig. 2b). Findings that were present in the
lowed by subdural hematoma, intraventricular hemorrhage and
primary CT and were no longer detectable in the last follow-up CT
cortical contusions (Fig. 1).
(“lost findings”) consisted of subarachnoid and intraventricular
Epidural hematomas all occurred unifocally and had a high
hemorrhage in 2 cases, respectively, and of midline shift and intra-
agreement. Subdural hematomas were predominantly found to be
cranial gas accumulation in 1 case, respectively. Findings that
unifocal in up to 34 cases. In a few cases, they were detected in up to
developed between the primary CT and the last follow-up CT before
three locations. Altogether, these had a high agreement. Subarach-
death (“new findings”) were most frequently brain edema, followed
noid hemorrhage was recorded to be predominantly located in one
by infarction/necrosis, intraventricular hemorrhage and midline shift.
region in up to 38 cases, multifocal appearance was found in about
The rating into the presence and absence of findings in this
half of these cases. CT images clearly revealed more cases with
study did not express their extension. To give an idea of sizes and
subarachnoid hemorrhage than autopsy. Intraventricular hemor-
extensions, some measurements performed predominantly on
rhage was found more frequently on CT images, with presence in 27
primary CT examinations are given as follows: Evacuated epidural
cases. Cortical contusions were predominantly found unifocally in
hematomas had a maximum extension of 58 mm. Evacuated sub-
up to 26 cases and in two different regions in up to 7 cases. They
dural hematomas had a maximum width of 24 mm. Cortical con-
were recorded more frequently in autopsy. Intracerebral hematoma
tusions had a maximum diameter of 73 mm. The maximum change
was detected in 15 cases in one region, and in a few cases, they were
in midline shift within the ante-mortem course was 27 mm.
detected in up to four different parts of the brain, with an overall
high agreement between autopsy and radiology. Brain edema was
recorded slightly more frequently in autopsies, with presence in 39 4. Discussion
cases. Midline shift was predominantly recorded from CT images,
with presence in 23 cases. Infarction/necrosis were found predom- In this study, the typical features of traumatic brain injury were
inantly unifocally in up to 14 cases, and in two different regions in 2 compared between autopsy and ante-mortem CT examinations as
cases, with high agreement between both methods. Diffuse axonal well as between CT examinations in the temporal course.

Table 1
Comparison of presence and absence of pathological findings between autopsy and radiology in the 45 studied cases. Values  80% are highlighted. Diffuse axonal injury and
intracranial gas was not listed as these findings were assessable only on CT. Rupture of bridging vein was not listed as this finding was only assessable in autopsy.

Findings Sensitivity (%) Specificity (%) Positive predictive value (%)

Epidural hematoma 100 97 86


Subdural hematoma 1 83 60 88
Subdural hematoma 2 64 84 64
Subdural hematoma 3 75 93 50
Subarachnoid hemorrhage 1 94 36 76
Subarachnoid hemorrhage 2 85 81 65
Intraventricular hemorrhage 89 58 61
Cortical contusion 1 77 89 91
Cortical contusion 2 43 95 60
Intracerebral hematoma 1 80 90 80
Intracerebral hematoma 2 75 98 75
Intracerebral hematoma 3 0 100 e
Intracerebral hematoma 4 e 98 0
Brain edema 82 67 94
Midline shift 100 55 22
Infarction/necrosis 1 75 85 64
Infarction/necrosis 2 100 100 100

“-“ indicates that the finding was not present in any of the autopsies or CT examinations.

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S. Panzer et al. / Journal of Forensic and Legal Medicine 52 (2017) 62e69 65

Fig. 1. Illustration of the frequencies of findings in autopsy and radiology in the 45 studied cases.
EDH epidural hematoma, SDH subdural hematoma, SAH subarachnoid hemorrhage, IVH intraventricular hemorrhage, DAI diffuse axonal injury, CC cortical contusion, ICH intra-
cerebral hematoma, BE brain edema, MLS midline shift, I/N infraction/necrosis, GAS intracranial gas, RBV rupture of bridging vein.

Despite the different approaches between autopsy, which aims at several locations in many cases. The assessment of diffuse axonal
to clarify the cause of death, and radiology, which aims to make a injury turned out to be limited to CT examinations, because in au-
diagnosis as a basis for therapeutic decisions, the main pathological topsy, it is practicable exclusively in histological examinations.
findings of traumatic brain injury were found to be comparable Diffuse axonal injury indicates extensive injury to the white matter
between both methods. Discrepancies might be partially explained and occurs in about half of all severe head trauma cases. However,
as follows. only a minority of diffuse axonal injury lesions are associated with
In this study, autopsy was determined as the gold standard for hemorrhage and identifiable on CT images.17,20,21 Intraventricular
the statistical evaluation. The autopsy protocols were performed hemorrhage on initial CT has been reported as a marker of diffuse
for the whole body without special focus on the brain. Assessment axonal injury after traumatic brain injury.20 In this study, intraven-
of the findings for this study by using only the present written tricular hemorrhage was assessed frequently, especially on CT ex-
autopsy report was not always possible. Furthermore, clearly aminations indicating diffuse axonal imaging on more than the 3
detectable findings on CT images that were supposed to be present directly diagnosed cases. Brain edema, as the most frequent finding
in autopsy could not be found in some cases. They might have been in this study, had a high agreement between modalities. The diag-
undetectable on thicker slices in necrotic brains, or they were nosis is based on the combination of several features in the autopsy
possibly not documented in the autopsy report. In contrast, CT and on CT images, which are known to have variations. Additionally,
examinations were re-evaluated to check the desired findings, with different populations, and especially different age groups, lead to
a focus on the traumatic brain injury. different brain morphology.22,23 However, in this study, the high
Assessment of extra-axial hematomas and hemorrhages could be agreement is supposed to result from the distinct occurrence of the
performed relatively clearly for both modalities. However, on CT brain edema in the ante-mortem course, which can be clearly
examinations, the assessment of cortical contusions and intracere- diagnosed in both modalities. Assessment of the midline shift
bral hematomas was difficult, especially in cases with severe trau- appeared to have more significance in CT evaluation. Intracranial gas
matic brain injuries, as they were present in several locations and was assessed only on CT examinations. Assessment of pathological
sometimes with a confluent characteristic. The correspondent au- gas collections on ante- and post-mortem CT examinations is known
topsies also revealed partially unclear descriptions. Difficulties in the to be superior to autopsy.6,7,9,10,24 The rupture of a bridging vein was
diagnosis of brain contusions on CT examinations are known from included in this study as a finding, although it was reported exclu-
the literature, with marked variation between even the most expe- sively in 1 autopsy. Ruptures of bridging veins are the major cause of
rienced readers.19 In our study, cortical contusions and intracerebral the development of subdural hematomas.17 On non-enhanced CT
hematomas were assessed not as single lesions but rather as entities examinations, they are not detectable.

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66 S. Panzer et al. / Journal of Forensic and Legal Medicine 52 (2017) 62e69

Fig. 2. a Illustration of lost and new findings between the primary CT and the last follow-up CT before death in the 16 patients with craniotomy. b Illustration of lost and new
findings between the primary CT and the last follow-up CT before death in the 13 patients without craniotomy.
EDH epidural hematoma, SDH subdural hematoma, SAH subarachnoid hemorrhage, IVH intraventricular hemorrhage, DAI diffuse axonal injury, CC cortical contusion, ICH intra-
cerebral hematoma, BE brain edema, MLS midline shift, I/N infraction/necrosis, GAS intracranial gas, RBV rupture of bridging vein.

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Fig. 3. 73-year-old female patient with severe traumatic brain injury. a Primary CT
examination (multiplanar paraaxial reconstruction) illustrating a large epidural he-
matoma on the left side. The hypodense structures within the hematoma represent the
“whirlpool sign”, indicating active bleeding. Note moderate to severe brain edema. b
Follow-up CT examination (paraaxial single slice) 6.5 h after decompression crani-
otomy on the left side and evacuation of the epidural hematoma. Massive brain edema
with herniation of the brain through the osseous defect is shown. Note the develop-
ment of subdural hematoma surrounding the right hemisphere and extension along
the interhemispheric fissure.

Fig. 4. 66-year-old male patient with severe traumatic brain injury. a Primary CT ex-
In addition to the preceding discussion, ante-mortem, peri- amination (multiplanar paraaxial reconstruction) illustrating a large subdural hema-
toma on the left side with “whirlpool sign”. Marked mass effect with midline shift to
mortem and post-mortem changes between the last ante-mortem
the right side is recognisable. Note the fracture of the cranial vault on the right side
CT and the autopsy must be considered as a possible cause for with hematoma of the galea and gas inclusion. b Follow-up CT examination (multi-
differences. planar paraaxial reconstruction) 4 h after decompression craniotomy on the left side,
Comparison between the primary CT after trauma and the last evacuation of the hematoma and insertion of two drainages. Slight remains of the
ante-mortem CT revealed marked changes in the presence and subdural hematoma, moderate brain edema and relocation of the midline are visible.
Note the development of intracerebral hematoma bilaterally in the frontal lobes as well
absence of findings, especially in patients with severe traumatic
as around the third ventricle, with surrounding edema, and slight traumatic sub-
brain injury requiring decompression craniotomy. This indicates arachnoid hemorrhage frontally.
that the diagnoses of the primary CT are often not the same as those
in the last ante-mortem CT or the following autopsy. In these cases,
the primary CT can be used to assist in the forensic reconstruction evacuation of epi- and subdural hematomas and cortical contu-
of the peritraumatic events, whereas the last ante-mortem CT can sions, which were among the main reasons for craniotomy in these
be used to assist in the analysis of the cause of death. cases. Subarachnoid and intraventricular hemorrhage got lost in
Loss of findings was predominantly due to neurosurgical few cases, probably by dilution by liquor or by resorption.

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68 S. Panzer et al. / Journal of Forensic and Legal Medicine 52 (2017) 62e69

Fig. 5. 42-year-old patient with severe traumatic brain injury. a Primary CT exami- Fig. 6. 55-year-old patient with traumatic brain injury. a Primary CT examination
nation (paraaxial single slice) illustrating a large cerebral contusion in the right frontal (multiplanar paraaxial reconstruction) illustrating a large cortical contusion in the
lobe with distinct mass effect, a thin subdural hematoma on the right side and a thin right frontal lobe, slight intraventricular hemorrhage and a hematoma of the galea on
epidural hematoma with gas inclusion on the left side parietally. b Follow-up CT ex- the left side. b Follow-up CT examination (paraaxial single slice) 4 days after decom-
amination (paraaxial single slice) 24 h after decompression craniotomy on the right pression craniotomy on the right side and evacuation of the hematoma. Remains of the
side and evacuation of the hematoma. Slight remains of the cortical contusion are cortical contusions are visible, the intraventricular hemorrhage had increased and
visible, and the midline shift had decreased. Intraventricular hemorrhage is detectable moderate brain edema is present. Note the development of hypodense areals in the
as well as a thin subdural hematoma on the left side frontally. The epidural hematoma posterior aspect of the brain, indicating infarction, and around the cortical contusion
on the left side slightly increased. extending into the corpus callosum indicating edema and resumable infarction.

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S. Panzer et al. / Journal of Forensic and Legal Medicine 52 (2017) 62e69 69

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