Post-mortem forensic neuroimaging: Correlation of MSCT and MRI findings with autopsy results

15
Post-mortem forensic neuroimaging: Correlation of MSCT and MRI findings with autopsy results § Kathrin Yen a,b, * , Karl-Olof Lo ¨vblad c , Eva Scheurer a , Christoph Ozdoba d , Michael J. Thali a , Emin Aghayev a , Christian Jackowski a , Javier Anon a,d , Nathalie Frickey e , Karin Zwygart f , Joachim Weis g , Richard Dirnhofer a a Institute of Forensic Medicine, University of Bern, 3012 Bern, Switzerland b Forensic Radiology Department, Center of Clinical-Theoretical Medicine, Medical University of Graz, Austria c Department of Neuroradiology, University of Geneva, Switzerland d Department of Radiology, Insel Hospitel Bern, Switzerland e Department of Anesthesiology and Intensive Care, University Hospital of Vienna, Austria f Department of Clinical Research, Magnetic Resonance Spectroscopy and Methodology, University of Bern, Switzerland g Institute of Neuropathology, RWTH University, Aachen, Germany Received 28 August 2006; received in revised form 15 December 2006; accepted 21 January 2007 Available online 28 February 2007 Abstract Multislice-computed tomography (MSCT) and magnetic resonance imaging (MRI) are increasingly used for forensic purposes. Based on broad experience in clinical neuroimaging, post-mortem MSCT and MRI were performed in 57 forensic cases with the goal to evaluate the radiological methods concerning their usability for forensic head and brain examination. An experienced clinical radiologist evaluated the imaging data. The results were compared to the autopsy findings that served as the gold standard with regard to common forensic neurotrauma findings such as skull fractures, soft tissue lesions of the scalp, various forms of intracranial hemorrhage or signs of increased brain pressure. The sensitivity of the imaging methods ranged from 100% (e.g., heat-induced alterations, intracranial gas) to zero (e.g., mediobasal impression marks as a sign of increased brain pressure, plaques jaunes). The agreement between MRI and CT was 69%. The radiological methods prevalently failed in the detection of lesions smaller than 3 mm of size, whereas they were generally satisfactory concerning the evaluation of intracranial hemorrhage. Due to its advanced 2D and 3D post-processing possibilities, CT in particular possessed certain advantages in comparison with autopsy with regard to forensic reconstruction. MRI showed forensically relevant findings not seen during autopsy in several cases. The partly limited sensitivity of imaging that was observed in this retrospective study was based on several factors: besides general technical limitations it became apparent that clinical radiologists require a sound basic forensic background in order to detect specific signs. Focused teaching sessions will be essential to improve the outcome in future examinations. On the other hand, the autopsy protocols should be further standardized to allow an exact comparison of imaging and autopsy data. In consideration of these facts, MRI and CT have the power to play an important role in future forensic neuropathological examination. # 2007 Elsevier Ireland Ltd. All rights reserved. Keywords: CT; MRI; Forensic imaging; Virtopsy; Post-mortem neuroradiology 1. Introduction Neurotraumatology and neuropathology play an important role in forensic medicine. This is reflected in the statistics that show traumatic head and brain injury to be the cause of death or severe disablement in thousands of persons each year. According to available European statistics, traumatic head and brain injury has an incidence rate ranging between 150/ 100,000 p.a. and 836/100,000 p.a., with serious and fatal cases www.elsevier.com/locate/forsciint Forensic Science International 173 (2007) 21–35 § Supported by grants from the Gebert-Ruef-Foundation, Basel, Switzerland, and from the Government of Vorarlberg, Bregenz, Austria. * Corresponding author at: Forensic Radiology Department, Center of Clinical-Theoretical Medicine, Medical University of Graz, Harrachgasse 21, A-8010 Graz, Austria. Tel.: +43 316 380 7586. E-mail address: [email protected] (K. Yen). 0379-0738/$ – see front matter # 2007 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.forsciint.2007.01.027

Transcript of Post-mortem forensic neuroimaging: Correlation of MSCT and MRI findings with autopsy results

Post-mortem forensic neuroimaging: Correlation of MSCT

and MRI findings with autopsy results§

Kathrin Yen a,b,*, Karl-Olof Lovblad c, Eva Scheurer a, Christoph Ozdoba d,Michael J. Thali a, Emin Aghayev a, Christian Jackowski a, Javier Anon a,d,

Nathalie Frickey e, Karin Zwygart f, Joachim Weis g, Richard Dirnhofer a

a Institute of Forensic Medicine, University of Bern, 3012 Bern, Switzerlandb Forensic Radiology Department, Center of Clinical-Theoretical Medicine, Medical University of Graz, Austria

c Department of Neuroradiology, University of Geneva, Switzerlandd Department of Radiology, Insel Hospitel Bern, Switzerland

e Department of Anesthesiology and Intensive Care, University Hospital of Vienna, Austriaf Department of Clinical Research, Magnetic Resonance Spectroscopy and Methodology, University of Bern, Switzerland

g Institute of Neuropathology, RWTH University, Aachen, Germany

Received 28 August 2006; received in revised form 15 December 2006; accepted 21 January 2007

Available online 28 February 2007

www.elsevier.com/locate/forsciint

Forensic Science International 173 (2007) 21–35

Abstract

Multislice-computed tomography (MSCT) and magnetic resonance imaging (MRI) are increasingly used for forensic purposes. Based on broad

experience in clinical neuroimaging, post-mortem MSCT and MRI were performed in 57 forensic cases with the goal to evaluate the radiological

methods concerning their usability for forensic head and brain examination. An experienced clinical radiologist evaluated the imaging data. The

results were compared to the autopsy findings that served as the gold standard with regard to common forensic neurotrauma findings such as skull

fractures, soft tissue lesions of the scalp, various forms of intracranial hemorrhage or signs of increased brain pressure. The sensitivity of the

imaging methods ranged from 100% (e.g., heat-induced alterations, intracranial gas) to zero (e.g., mediobasal impression marks as a sign of

increased brain pressure, plaques jaunes). The agreement between MRI and CT was 69%. The radiological methods prevalently failed in the

detection of lesions smaller than 3 mm of size, whereas they were generally satisfactory concerning the evaluation of intracranial hemorrhage. Due

to its advanced 2D and 3D post-processing possibilities, CT in particular possessed certain advantages in comparison with autopsy with regard to

forensic reconstruction. MRI showed forensically relevant findings not seen during autopsy in several cases. The partly limited sensitivity of

imaging that was observed in this retrospective study was based on several factors: besides general technical limitations it became apparent that

clinical radiologists require a sound basic forensic background in order to detect specific signs. Focused teaching sessions will be essential to

improve the outcome in future examinations. On the other hand, the autopsy protocols should be further standardized to allow an exact comparison

of imaging and autopsy data. In consideration of these facts, MRI and CT have the power to play an important role in future forensic

neuropathological examination.

# 2007 Elsevier Ireland Ltd. All rights reserved.

Keywords: CT; MRI; Forensic imaging; Virtopsy; Post-mortem neuroradiology

§ Supported by grants from the Gebert-Ruef-Foundation, Basel, Switzerland,

and from the Government of Vorarlberg, Bregenz, Austria.

* Corresponding author at: Forensic Radiology Department, Center of

Clinical-Theoretical Medicine, Medical University of Graz, Harrachgasse 21,

A-8010 Graz, Austria. Tel.: +43 316 380 7586.

E-mail address: [email protected] (K. Yen).

0379-0738/$ – see front matter # 2007 Elsevier Ireland Ltd. All rights reserved.

doi:10.1016/j.forsciint.2007.01.027

1. Introduction

Neurotraumatology and neuropathology play an important

role in forensic medicine. This is reflected in the statistics that

show traumatic head and brain injury to be the cause of death or

severe disablement in thousands of persons each year.

According to available European statistics, traumatic head

and brain injury has an incidence rate ranging between 150/

100,000 p.a. and 836/100,000 p.a., with serious and fatal cases

K. Yen et al. / Forensic Science International 173 (2007) 21–3522

ranging from 9/100,000 p.a. to 22/100,000 p.a. [1–4]. In one

German study, 68.4% of those with severe head injuries died

before hospital admission [3]. Traumatic head and brain

injuries are especially common in young children and the

elderly, and in Europe and Canada are primarily the result of

motor vehicle accidents, work or sport accidents, and falls in

the elderly. In the United States, most head and brain injuries

occur in young adults and are caused by firearms [5–8]. There is

a need for exact and reliable investigation methods in the

forensic examination of these manifold cases.

The gold standard for the post-mortem forensic assessment

of neurotraumatologic and neuropathological findings is the

forensic autopsy including histological examination. Primary

advantages of this method include direct information by

inspection and palpation and the possibility of taking tissue

specimens. One limitation of autopsy is that it is subjective and

observer-dependent, and cannot be used to provide a second

opinion in court due to the fact that the body tissues are cut and

cannot be stored for a longer time except for selected parts or

small specimens for histological examination. Radiological

imaging methods such as MRI and CT are increasingly entering

the field of forensic medicine, offering a non-invasive

investigation approach, thereby allowing an unlimited storage

of the imaging data and facilitating second opinions in the

course of legal proceedings [9–13]. Considering that CT and

MRI might play an ever-increasing role in post-mortem

forensic neurotraumatology, the principal advantages and

limitations of these imaging methods will have to be evaluated

concerning the possibility of the detection, interpretation and

visualization of forensically relevant findings in comparison

with standard forensic autopsy.

The goal of this study was to evaluate the value of CT and

MR imaging as diagnostic tools for their use in routine forensic

examination of the head, and to investigate the potential

benefits and limitations of the imaging methods in comparison

with autopsy.

2. Methods

2.1. Subjects

The responsible justice department and the local ethics committee approved

the present retrospective study which was part of the ‘‘Virtopsy’’ project [13].

Fifty-seven bodies representing a continuous sample of ‘‘routine’’ forensic

cases were studied using post-mortem pre-autopsy imaging (39 male, 18

female, mean age 42.3 years, range 22 weeks to 87 years).

Table 1

Typical MR imaging parameters

Sequence Coil TRa (ms) TEa (ms) Matrixa,b (mm)

PD/T2 Head 4000 15/85 256 � 192

GRASS Head 300 8–20 256 � 224

T1 Head 400 10–20 256 � 192

T2 Head 4000 85–105 512 � 256

a Slightly deviant parameters in early cases.b Depending on slice direction and volume.c The number of slices exceeded up to 88 when the neck was scanned within thd depending on slice thickness and sequence.

Forty-five of the deceased had suffered head trauma (motor vehicle acci-

dents, n = 22; gunshot injuries, n = 7; falls, n = 6; airplane crashes, n = 4; blunt

force trauma and beating, n = 4; shaken baby syndrome, n = 1, birth trauma,

n = 1), two were natural deaths due to heart failure. The remaining incidents

were hanging, n = 2; throttling, n = 3; drowning, n = 1; mechanical trauma to

regions other than the head (suicidal stabbing), n = 1, medical malpractice,

n = 1, abortion, n = 1, and one was a diving incident. In addition to these, the

MR data of one decomposed body that underwent MR-spectroscopy were

compared to the autopsy findings.

2.2. Post-mortem MSCT and MR imaging

Except for the MR-spectroscopy case, all bodies underwent post-mortem

MSCT and MRI with the scans being performed in clinical units. For imaging,

the bodies were wrapped in two body bags to prevent contamination of the

scanners with blood or other materials and to guarantee the anonymity of the

deceased. A local undertaker transported the corpses to the MSCT and MRI

units. The mean delay between the declaration of death and imaging was

approximately 20 h.

MSCT (GE Lightspeed QX/i unit, General Electric Systems, Milwaukee,

WI) of the head and neck was performed with a collimation of

4 mm � 1.25 mm and a slice thickness of 1.5 mm. All MR examinations were

performed on a 1.5-T system (GE 1.5 T Signa Echospeed Horizon, version 5.8,

General Electric Systems). T1 and T2 weighted sequences, and Gradient

Recalled Acquisition in the Steady State (GRASS) and proton density weighted

sequences were run; the parameters from a typical protocol that was used are

listed in Table 1. All sequences were run in an axial slice orientation. The T2-

sequence was in all cases performed in two different slice orientations (axial and

coronal), and in cases with specific questions (e.g., unclear cause of death,

special reconstruction issues) in a third one. The other sequences were run in

additional coronal or sagittal slice orientations for specifying ambiguous

findings from the axial images. The PD/T2 sequence served as an axial clinical

overview.

The total MR head examination duration was between 40 and 75 min.

MSCT and MR imaging data were transferred to a Siemens (Leonardo, Siemens

medical systems, Erlangen, Germany) or a GE Advantage Windows work-

station respectively (version 9.1, General Electric Medical Systems, Milwau-

kee, WI, USA). Using software provided with the workstations, 2D and 3D

reformations were generated from the MSCT data.

2.3. Forensic autopsy

All bodies were examined externally prior to scanning and the subsequent

autopsy was done by forensic pathologists (K.Y., C.J., E.A., E.S., M.J.T., R.D.).

Standard autopsy was performed with an average delay of 12 h after imaging; in

all corpses, accurate dissection of the cranium was carried out, including

histological analysis in selected cases or bone maceration when a fracture

was present. Forensic reconstruction based on the radiological data was

performed in selected cases (e.g., motor vehicle accidents, gunshot incidents).

According to the autopsy protocols, in 40 of the investigated cases the brain was

considered as the primary ‘‘atrium mortis’’; among these, 24 had suffered

mechanical trauma of the head. Sixteen persons died from central respiratory

arrest due to other reasons (e.g., brain hypoxia following strangulation), and in

FOVb (cm) Slice thicknessa

(mm)

Spacingb

(mm)

Slicesb,c Nexd

24 4 1 56–88 2

24 4 1 18–24 4

24 4 1 22–44 2

24 4 1 56–88 2

e same series.

Fig. 1. MSCT image of the upper head of a man who had fallen from a roof. The

subcutaneous tissue shows swelling and hemorrhage in the left occipito-parietal

region; the location of impact is characterized by contusion bleeding of the

tissue layers under the skin (arrow). Note the hyperdense areas inside the

cranium, which correspond to subarachnoidal hemorrhage.

K. Yen et al. / Forensic Science International 173 (2007) 21–35 23

17 cases the primary atrium mortis was not the brain. As usual in forensic

casework, the main autopsy findings that served as the basis for the definition of

the cause of death were documented in a summary report.

2.4. Radiological evaluation and data analysis

A radiologist from the clinical unit reviewed the MSCTand MRI data during

imaging and suggested preliminary diagnoses. A board-certified radiologist

from a separate radiology unit (K.O.L.) with many years of experience in

diagnostic neuroradiology was responsible for the detailed radiological evalua-

tion on the GE Advantage Windows workstation. The radiologist did the

evaluation blinded to the preliminary evaluation as well as to the autopsy

findings and the photographic documentation. The analysis of the radiological

data was performed with regard to neurotraumatological findings as mentioned

below, which took an average of 30 min per case. As the specific forensic

findings had partially been unknown to the evaluating radiologist, a short

teaching session was held before the evaluation. During this procedure, a

photographic autopsy documentation of the teaching cases (which were not

included in the study) was shown to the radiologist.

A forensic pathologist (K.Y., E.A., C.J., M.J.T.) participated at the MSCT

and MRI scans and the reading sessions (K.Y.). The evaluating radiologist did

not attend the autopsy. In few selected cases where the radiological evaluation

had failed to show a specific autopsy finding, a second look was taken at the

imaging data (K.O.L., C.O.) in knowledge of the autopsy results. The results of

these targeted follow-up examinations have not been included in the statistical

analysis.

Finally, a comparison of radiological and neuropathological findings was

carried out, with the findings documented in the autopsy protocols used as the

gold standard. Sensitivity and specificity of the imaging methods were calcu-

lated for each diagnostic criterion. The following findings were specifically

evaluated in each case: soft tissue injuries of the skin, subcutaneous fatty tissue

and galea; post-mortem alterations (e.g., heat induced injuries, signs of decom-

position); temporal muscles injuries; fractures of the skull and skull base, the

facial bones and cervical vertebrae 1 and 2; intracranial, extra- and intraaxial

hemorrhage, brain contusions and lacerations; plaques jaunes; injuries of the

cerebellum and brain stem; lacerations of the dura mater and tentorium;

pneumencephalon and intracranial foreign bodies; signs of brain edema and

increased brain pressure (e.g., flattened gyri, herniation of the cerebellar tonsils,

midline shifting); vascular embolization, infarction, and pathological disorders

such as atrophy, tumor and congenital malformations. The list of forensically

relevant findings that the radiologist was asked to consider included 122

keywords. Evaluation of the findings was performed in view of a finding being

present in a case or not; exact anatomical or size correlation was not performed

in this study due to the large number of potential findings in each case. This was

also the reason why the radiologist did not search extensively for very discrete

or rare lesions. This procedure was thought to represent a realistic approach of

what could be achieved with a reasonable effort in a routine forensic-radi-

ological examination. In addition, the main findings that were reported in the

autopsy summary report as being the relevant basis for the definition of the

cause of death were compared to the results of the radiological evaluation. The

goal of this procedure was to determine whether the imaging methods are suited

for the detection of the most essential findings concerning the definition of the

cause of death. For forensic reconstruction, the impact axis and the sequence of

events were analyzed as usual in forensic practise in selected cases. These data

were compared to the imaging results regarding the presence, visibility and

presentation of the relevant findings for the reconstruction.

3. Results

3.1. Extracranial findings: skin, galea and temporal

muscles (Table 2a and b; Fig. 1)

Findings that were regularly present were abrasions,

contusions and lacerations of the scalp, which were detected

by MRI rather than CT; however and not surprisingly,

concerning all forms of scalp injury, autopsy was far superior

to the imaging methods. Abrasions were found only in 1 of 18

cases using MRI or CT (sensitivity 6%). MRI and CT showed a

sensitivity of 100% in the evaluation of entrance gunshot

wounds (n = 6) and heat-induced alterations of the skin and

galea (n = 3). Hemorrhage of the temporal muscles was present

in 20 autopsy cases and diagnosed by imaging in 15 (MRI) and

13 (CT), respectively. Overall specificity for the skin, galea and

temporal muscle findings was 97% for CT and 98% for MRI.

3.2. Extracranial findings: skull, skull base and cervical

vertebrae 1 and 2 (Table 2c and d; Figs. 2 and 3)

Twenty-four skull fractures and 20 fractures of the skull base

were found at autopsy, and in 3 cases post-mortem heat-induced

fractures were present that were each detected by both MRI and

CT. Unsurprisingly, CT was better suited to the evaluation of

osseous lesions which were detected at rates of 75% (fractures

of the skull, n = 24) to 100% (mandible fractures, n = 3). CT

revealed seven maxilla and three mandible fractures that were

not mentioned in the autopsy protocols. Imaging failed in the

differentiation of the various fracture forms (e.g., burst fracture,

impression fracture), which was most probably due to the

radiologist being unfamiliar with these forensic classifications.

In our cases, two fractures of the first vertebra remained

undetected by imaging whereas CT revealed two of four

vertebra 2 fractures. In all missed vertebral fractures extensive

osseous injuries of the posterior cranial fossa and upper cervical

spine region were present. Concerning the osseous findings, the

specificity was 96% for CT and 98% for MRI.

Table 2

Correlation of MSCT and MRI with the autopsy findings

K. Yen et al. / Forensic Science International 173 (2007) 21–3524

Table 2 (Continued )

K. Yen et al. / Forensic Science International 173 (2007) 21–35 25

Table 2 (Continued )

1a, c, e, g, i, k, m (left side) display the sensitivity of CT and MRI, and b, d, f, h, j, l, n show the absolute numbers of true positive findings in comparison with autopsy.2The numbers refer to the cases with each finding.

K. Yen et al. / Forensic Science International 173 (2007) 21–3526

3.3. Intracranial, extra-axial hemorrhage: epidural

hematoma, heat-induced epidural hematoma, subdural and

subarachnoid hemorrhage (Table 2e and f; Figs. 3–6)

CT and MRI were almost equivalent in the evaluation of

extra-axial hemorrhage that overall was found in a satisfactory

correlation with the autopsy. The sensitivity ranged between

100% for CT and MRI for the detection of heat-induced

epidural hematoma (n = 3) and 73% (MRI) or 68%, respec-

tively (CT), for the recognition of subdural hemorrhage

(n = 22). In the cases where CT and MRI missed subdural

Fig. 2. Death on site in a motor vehicle accident (driver). The person was

expelled and subsequently overrun by a car. The 3D bone volume-rendered

MSCT scan excellently shows the flexion (and bursting) fracture system on the

left side of the head where a nut from the undercarriage of the car had primary

contact with the skull.

hemorrhage the finding corresponded to a blood layer less than

3 mm in thickness. In the evaluation of extra-axial hematoma,

both imaging techniques showed false positive findings,

particularly of subarachnoid hemorrhage (CT: 11 false positive,

MRI: 9). A young woman who had been manually strangled

presented with distinct subdural hemorrhage at autopsy that

was not visible in CT or MRI even in retrospective analysis,

providing evidence that the hemorrhage might have emerged

post-mortem after the imaging (Fig. 6).

Fig. 3. 3D bone and soft tissue volume-rendered MSCT data demonstrating

heat-induced fracture in a man who died in an airplane crash. Note the typical

‘‘desquamation’’ of the skull bone (white arrows). In the regions where the bone

is missing the dura mater can be seen with parts of epidural hematoma (yellow

arrows).

Fig. 4. Epidural hematoma in a burnt body. (A) In this axial MSCT image epidural hematoma that occurred due to heat is seen in the frontal region; note the inclusion

of air in the hematoma. The covering bones are partially destroyed. (B) Corresponding autopsy finding showing a good correlation to the imaging result.

K. Yen et al. / Forensic Science International 173 (2007) 21–35 27

3.4. Intracranial, intra-axial findings: contusions,

intracerebral hemorrhage, lacerations, brainstem injuries,

decerebration, pneumencephalon; dura mater and

tentorium lesions (Table 2g–l; Fig. 7)

Fifty-three percent of the gray matter contusions were seen

at CT, and MRI detected 41% of those; the radiological

methods were sufficient in the evaluation of findings that had

been termed as ‘‘coup’’ or ‘‘contre-coup’’ lesions during

autopsy. It became obvious that especially findings smaller than

3 mm regularly escaped the radiologist’s analysis. MR and CT

imaging showed a sensitivity of 63% in the detection of

hemorrhages in the white matter and were superior to the

autopsy concerning the evaluation of ventricular hemorrhage as

well as pneumencephalon. As the autopsy was used as the gold

standard in our examination and both findings were rarely

Fig. 5. Eighty-year-old man who died hours after a fall in a tramway. (A) Subdura

components and massive swelling of the brain with compression of the ventricles and

autopsy findings show a good correlation to the imaging data in this case. Due to tech

CT scanning plane. Therefore, the hemorrhagic lesions in the right temporo-occip

mentioned in the autopsy protocols, this was reflected by a high

number of false positive findings. CT revealed ventricular

hemorrhage that had not been described in the autopsy

protocols in 19 cases (MRI: 16) and the finding of a

pneumencephalon in 22 cases (MRI: 17), respectively. The

finding of ‘‘plaques jaunes’’ (n = 2) escaped the radiological

evaluation. MRI was superior to CT concerning the identifica-

tion of lacerations in the brain tissue and brainstem injuries.

The majority of dura mater ruptures were not seen using

imaging methods (sensitivity 31% for MRI, 25% for CT;

specificity 100% for both imaging methods).

Overall specificity for intra- and extra-axial findings was

94% for both CT and MRI. The lowest specificity of each 70%

was found for subarachnoid hemorrhage, ventricular hemor-

rhage and pneumencephalon, the latter being findings that were

rarely mentioned in the autopsy protocols.

l hematoma (yellow arrows) on the right side showing separation of the blood

midline shifting (orange arrows) are easily detected in this MSCT slice. (B) The

nical reasons the plane of the Flechsig cut is hardly ever exactly the same as the

ital region are not displayed in the CT slice shown in (A).

Fig. 6. Twenty-one-year-old female who had been manually strangled. No signs of head trauma. (A) Axial MSCT showing no signs of intracranial hemorrhage.

Diffuse swelling of the brain with levelling of the sulci is however present, and the gray/white matter distinction is markedly reduced. (B) The same case at the

autopsy. Here, the examination revealed distinct subdural hemorrhage that was interpreted to have occurred post-mortem after the imaging, possibly as a

transportation effect. According to clinical experience, subdural hemorrhage of this extent should be seen without difficulties using imaging methods.

K. Yen et al. / Forensic Science International 173 (2007) 21–3528

3.5. Edema, increased brain pressure (Table 2m and n;

Fig. 5)

CT revealed edema of the brain tissue in 85% of the cases

and was slightly superior to MRI (76%) concerning this

common finding. However, the ‘‘classical’’ forensic signs of

increased brain pressure (e.g., flattened gyri, protrusion of

Fig. 7. Intracerebral hemorrhage in a man who died hours after a fall. (A) This axial g

extensive secondary hemorrhage in the right temporo-occipital region of the brain (

arrows). (B) In the formalin-fixed autopsy specimen the finding is also observed. Not

to smearing of blood when cutting the brain tissue.

the cerebellar tonsils) mostly escaped the radiologist’s

evaluation. The overall specificity for edema and increased

brain pressure was 89% for CT and 93% for MRI; among all

findings in this group, the specificity was especially low

concerning generalized brain edema without signs of

increased brain pressure (n = 25; specificity 33% for CT,

52% for MRI, respectively).

radient echo-weighted MR image (TR 300, TE 8.0) well illustrates the finding of

yellow arrows). Furthermore, subdural hemorrhage is seen on this slice (orange

e that the extent of the hemorrhage would easily be overestimated at autopsy due

Fig. 8. MRI findings in a far decomposed body. (A) A hyperintense region in the frontal brain that is consistent with intracerebral hemorrhage is clearly depicted in

this T2 weighted MR image (TR 6000, TE 105). In the right back, a small part of epidural hematoma can be observed in this slice (arrow). MR shows a good imaging

quality despite the brain being in a far decomposed state. (B) At autopsy, the finding of intracerebral hemorrhage is seen well only before the brain is extracted from

the intracranial cavity. Note that the extent of the hematoma seems to be larger than at MRI due to the blood having been smeared at the autopsy. After the first cut,

further dissection is difficult due to the tissue being relatively liquid.

Fig. 9. Suicidal gunshot to the mouth. In this 3D air structure reconstruction

using the MSCT data, air filling of the transverse sinuses is well represented.

The ruptured transverse sinuses were considered as being the portal of air entry

(arrows) that caused air embolism of the heart. The finding was verified by

means of radiology and autopsy.

K. Yen et al. / Forensic Science International 173 (2007) 21–35 29

3.6. Other forensically relevant findings (Figs. 8 and 9)

In a case of a downstairs fall, a large infarction area was seen

at MRI that had been underestimated at autopsy. Beginning

signs of intravital autolysis were present in four cases; all of

them remained undetected at both CT and MRI. On the other

hand, advanced decomposition was detected correctly in all

three cases. In one of these, imaging showed marked epidural

and intracerebral hemorrhage that was more difficult to detect

at autopsy due to the advanced decomposition of the brain

tissue (Fig. 8). Gaseous embolism was shown in two cases by

CT imaging and in one of them by MRI (Fig. 9).

3.7. Evaluation of the cause of death

The main findings for the definition of the cause of death were

detected correctly by imaging in 19 of the 24 (79.2%) head

trauma cases with the brain as the primary atrium mortis. In three

cases (12.5%), the relevant findings that had been noted in the

autopsy summary reports were found to a large part, with one

exception each (i.e., laceration at the base of the brain,

subcortical contusion at the base of the brain, increased brain

pressure). In two cases (8.3%), the main findings were not

detected correctly using imaging methods. Of the 17 cases that

died from extracranial lesions, 10 (58.8%) did not show any

relevant intracranial findings except for small subarachnoid

hemorrhage or slightly increased brain pressure. In the other

seven bodies (41.2%), findings such as intracerebral hemorrhage

or signs of a significant increase of brain pressure were observed.

However, due to the thorax and abdomen being not evaluated in

this study, the assessment of the relevance of intracranial findings

in view of the cause of death was not performed.

3.8. Forensic reconstruction

Due to the advanced possibilities of 2D and 3D

reconstruction of the digital data, especially when based

Fig. 10. Five-month-old baby which was examined because of suspected shaken baby syndrome. (A) 3D volume-rendered MSCT showing the venous sinuses from

behind (t, sinus transversus; ss, sinus sagittalis superior). An extravasation of blood is seen in the frontal cranial vault region (arrows). However, this tiny blood layer

was detected only in a second look examination and in knowledge of the autopsy findings. (B) Corresponding autopsy specimen depicting a small subdural blood layer

(arrows). The finding is not revealed in both axial CT (C) and axial MRI (T1 weighted MR sequence, TR 400, TE 14.0) (D).

K. Yen et al. / Forensic Science International 173 (2007) 21–3530

on CT (Fig. 2), imaging-based reconstruction of the

impact axis or the sequence of events was generally superior

to autopsy especially in view of its feasibility and

the visibility of the traumatic findings. CT and MRI

revealed case-relevant information without the need of

performing time-consuming bone maceration techniques

and provided an excellent two- or three-dimensional over-

view. It took about 30 s to generate a 3D skull recon-

struction, and up to about 10 min when special cuts were

applied.

3.9. Agreement between CT and MRI

Concerning all findings that were evaluated in this

study, the overall agreement between CT and MRI was

69%.

3.10. ‘‘Second-look’’ examination (in knowledge of the

autopsy findings; Fig. 10)

In an exemplary second-look examination of the skull base

with the focus only on orbital roof fractures, seven of eight

fractures were correctly detected; one was not visible even

retrospectively and with knowledge of the autopsy findings.

The diagnosis of specific skull fracture types such as burst or

impression fractures became possible especially when using 3D

reconstructed CT data and after giving the radiologist more

profound forensic background concerning these findings

(Fig. 2). Another forensically relevant issue that was almost

unknown to clinical radiologists was the differentiation of

hematoma caused by direct traumatic impact versus ‘‘indirect’’

fracture hematoma. In the second look examination, this

differentiation was feasible when based on the MR imaging

Fig. 11. Suicidal gunshot to the right temple demonstrating grossly altered anatomy. (A) This sagittal T2-weighted MR image (TR 5000, TE 105) shows massive

destruction of the brain and skull fractures. The brain is sunken back and the frontal region filled with air. (B) Corresponding T1-weighted axial MR slice (TR 480, TE

14) displaying the grossly altered anatomy and partial decerebration.

K. Yen et al. / Forensic Science International 173 (2007) 21–35 31

data, as fracture hematoma of the galea was not accompanied

by subcutaneous fatty tissue hemorrhage of the covering

tissues.

In a case of a motor vehicle accident as well as in one

gunshot injury case, the injury leading to the entrance of air in

the cranial cavity, thus being the origin of gaseous embolism of

the heart, was detected using CT. Missing parts of the brain

could be defined in cases with partial decerebration; however,

in these cases diagnosis was complicated due to the grossly

altered anatomy (Fig. 11). Some lesions of the dura mater were

not seen even in knowledge of the autopsy findings especially

when they were localized near the skull base. In one case of

shaken baby syndrome, CT was found to be negative but

retrospectively revealed the finding of a slight subdural blood

layer (Fig. 10).

4. Discussion

Post-mortem plain radiography of the head has been

routinely used in forensic medicine mainly for the evaluation

of gunshot injuries and for identification purposes [14, and

references therein]. Cranial CT imaging is increasingly being

performed in forensic examinations [9–11,13,15–24], whereas

most reports that exist on post-mortem MRI of the head and in

situ brain [12,13,19,23–31] are based on small case samples. In

a post-mortem MRI study of six cases Ros et al. [32] concluded

that MRI was well suited for the detection of air and fluids in the

body spaces; however, the autopsy correlation concerning

intracranial findings was poor. Hart et al. [33] found a good

correlation between MRI and autopsy in the post-mortem

examination of 11 cases of suspected child abuse, especially for

subdural hematoma and diffuse edema; on the other hand,

subarachnoid hemorrhage and small subdural hematoma

escaped the radiological evaluation. Forensically relevant CT

or MRI examinations of the formalin-fixed brain have been

performed by several authors [34–38]. Further post-mortem CT

and MRI studies that are of forensic interest to some extent

comprise fetal necropsy [39–45] and imaging of archeological

specimens, as recently performed on the Tutankhamun mummy

(unpublished data).

In clinical forensic medicine, imaging offers the only

possibility to obtain a non-invasive insight into the cranium.

The forensic examiner is thus occasionally confronted with

plain radiographs or CT and MRI data when it comes to

investigate neurotraumatological findings in cases of living

persons. Neuroradiological evaluation in forensic medicine is

based on numerous clinical imaging studies, which have been

performed on living patients over many years; the listing of all

the relevant literature would go far beyond the scope of this

study. In accordance with recent studies, the extensive clinical

experience with CT and MR imaging can be transferred to post-

mortem situations and serve as a basis for post-mortem

diagnostics, as there is no relevant difference between the

radiological appearances of most findings in ante- or post-

mortem brains in the first days after death [12–14,31,32,34].

The sound clinical experience in the field of head and brain

radiology is useful for post-mortem examinations as the clinical

neuroradiologists are familiar with many of the findings

expected. However, our results show that this was not the case

when it came to evaluating several specific forensic aspects

such as particular fracture forms, or cases with massive

destruction of anatomical structures. In the latter group, the

image reader regularly had major difficulties in orientation and

therefore interpretation of the findings (Fig. 11). The problem is

well known from autopsy when destruction of the skull and

brain is so extensive that the structures cannot be anatomically

allocated anymore, but for the forensically inexperienced

radiologist this turned out to be especially problematic.

K. Yen et al. / Forensic Science International 173 (2007) 21–3532

To cover the whole forensic neurotrauma spectrum we

included the evaluation of extracranial findings that are visible

at the external examination of a body (e.g., abrasions or

lacerations of the skin, gunshot wounds) in our study, despite

knowing that the role of imaging for these regions is and

probably will continue to be of little forensic value. The minor

relevance of imaging externally visible findings was reflected

by the poor outcome in this group of findings, which was

probably aggravated by the lack of experience of the radiologist

concerning the evaluation of these findings that are clinically

irrelevant. Furthermore, especially when using MRI data,

radiological analysis was generally difficult in peripheral

regions that were surrounded by air due to artefacts.

Reflecting the results of this study, CT and MR imaging

seem to have a realistic potential to become useful adjuncts to

forensic autopsy in future neurotraumatologic examinations.

The forensic potential of MRI and CT became obvious when it

came to the evaluation of findings such as gunshot-induced

injuries or complex skull fracture systems, where forensic

reconstruction benefited from the excellent image processing

possibilities offered primarily by CT imaging. Compared to

autopsy, imaging was also superior concerning the detection of

pneumencephalon or ventricular hemorrhage. These findings

were rarely mentioned in the autopsy protocols, but appeared

obvious not only to the radiologist, but also to the forensic

examiner in the imaging data. Furthermore, imaging revealed

maxilla and mandible fractures which had not been documen-

ted in the autopsy protocols. Not surprisingly, the finding of

intracranial gas is hardly detected at autopsy even if clearly

present radiologically. As the facial tissues are not cut in the

routine autopsy process due to ethical reasons, facial bone

fractures can easily escape the autopsy evaluation especially if

they are not accompanied by externally visible deformation or

obvious crepitation. For the findings mentioned above,

radiology might represent the new ‘‘golden standard’’, rather

than the autopsy. Follow-up studies will figure out the forensic

value of CT and MRI concerning these findings.

Although there were only three burnt bodies among our

cases, epidural hematoma (Figs. 3 and 4) was seen by means of

radiology in all of them, as were osseous fractures due to heat

(Fig. 3). In a very decomposed body that underwent MR

spectroscopy, the findings of epidural and intracerebral

hemorrhage were accurately diagnosed (Fig. 8); at autopsy,

the location and extent of the findings were harder to evaluate

due to the advanced decomposition and liquefaction of the

brain. This demonstrates that MRI can be of diagnostic value

even in cases with a longer post-mortem interval, and that the

quality of the imaging seems not to be significantly diminished

even by longer post-mortem periods. Another situation in

which MRI was notably advantageous compared to autopsy

was a case of occipital brain infarction due to a massive

increased brain pressure; here, MRI revealed the extent of the

infarction area more distinctly than autopsy.

In the case of a child with suspected shaken baby syndrome,

no craniocerebral abnormalities were found by imaging.

Following autopsy that depicted a thin subdural blood layer,

a second retrospective evaluation including reformatting of the

CT data revealed a tiny subdural hemorrhage (Fig. 10). In

contrast, one manual strangulation case showed distinct

subdural hemorrhage at autopsy to an extent that is normally

detected by both CT and MRI without difficulties. As the

radiological examinations were both negative even when

performed retrospectively, it was concluded that the finding

might have occurred post-mortem after the imaging (Fig. 6).

Concerning the cause of death, CT and MRI showed an

overall good correlation with autopsy. The main findings that

were reported in the summary autopsy reports were detected

correctly in the majority of cases.

Despite the aforementioned, in the present study both MRI

and CT were to a varying extent inferior to autopsy in view of

the detection of several craniocerebral findings. For example,

due to technical limitations (limited resolution), lesions smaller

than 3 mm regularly escaped the radiological analysis. Injuries

that were localized in the base of the brain were also generally

difficult to detect.

4.1. Standardization of the imaging protocols

In some cases no gradient echo sequences had been

performed despite their being especially suited for the detection

of hemorrhagic lesions, and some of the MRI protocols used

were not fully optimized for post-mortem situations, thus

limiting the study’s outcome. Future studies should provide a

standardization of the MRI and CT protocols for post-mortem

craniocerebral imaging as this will be an essential basis for

future forensic neuroimaging, allowing an optimized evaluation

of the traumatological findings and making the results

comparable.

4.2. Technical improvements

As mentioned already, a general problem of using imaging

methods for forensic purposes is the still restricted resolution of

the images that can be obtained. This limited resolution

explains that alterations smaller than about 3 mm in size mostly

escaped imaging, both by CT and MRI. The quality of the

radiological examination was further reduced by diagnostic

difficulties based on imaging artefacts (e.g., susceptibility

artefacts at the scalp/hair and surrounding air barrier

complicating the evaluation of the skin and subcutaneous

tissue). Future technology (e.g., 3 T or more MRI, special post-

mortem sequences) might overcome these problems that are

also relevant in clinical medicine and therefore the topic of

extensive studies in ongoing clinical research. Minimally

invasive imaging techniques (post-mortem angiography [37],

post-mortem biopsy) are currently being developed to increase

the diagnostic range that can be obtained based on imaging

data. Additionally, some specific MRI applications such as

diffusion weighted and diffusion tensor imaging have a

potential value in forensic diagnostics. Diffusion-weighted

MRI is routinely used in clinical medicine for the detection of

acute ischemic lesions [46]. There, it has shown specific

advantages by offering an early and exact demarcation of the

ischemic region, and by allowing a differentiation between

K. Yen et al. / Forensic Science International 173 (2007) 21–35 33

vasogenic and cytotoxic edema through unequal values of the

apparent diffusion coefficient ADC. In other brain lesions such

as hematomas, the utility of diffusion weighted imaging has

been shown to be limited due to the presence of susceptibility-

related artifacts when using echo-planar imaging, but it can,

however, probably help to differentiate between perihemorra-

gic edema and ischemia [47]. Diffusion tensor imaging, on the

other hand, will be very useful in assessing the presence of

small intracerebral lesions that might disrupt normal tissue

integrity, and has a great forensic potential of directly

displaying traumatic disruption of nerve fiber structures [48].

4.3. Forensic training of the radiologists

The present study showed a partially unsatisfactory

correlation between radiological and autopsy findings espe-

cially when it came to evaluate special forensic findings such as

soft tissue injuries of the scalp, various fracture forms, or

specific forensic signs of increased brain pressure. As all these

findings were not familiar to the clinical radiologist and

therefore hardly diagnosed, to our opinion future evaluations

could be improved with a previous training of the involved

radiologists, giving them a sound basis for what findings they

will have to expect and which of these are essential for the

forensic expert. The somewhat unsatisfying concordance of CT

and MR imaging with autopsy concerning a few specific

forensic issues demonstrates the limited outcome when the

forensic-radiological evaluation is done from a radiologist’s

point of view without sufficient forensic training. This is also

reflected by a comment that the reader had ‘‘not especially

searched for orbital roof fractures when the whole skull was

vastly burst’’; in his eyes, this finding was of no relevance

facing the extent of traumatic injury. In a second look, when he

had been asked to look only for orbital fractures, he detected

seven of eight correctly and without problems. Similarly, facing

the extent of accompanying posterior fossa and upper cervical

spine fractures in some neck injury cases, the radiologist did not

focus specifically on vertebral fractures and thus did not

mention them. Concerning the forensically important fracture

forms, the examiner could define various fracture patterns after

having received more profound teaching about the morphology

of these findings. In conclusion, one basic inference that can be

drawn from this study is that the quality of future forensic

expertises that are based upon radiological data will depend

largely on the previous forensic training of the involved

radiological experts.

4.4. Standardization of the autopsy protocols

Besides illustrating the need for forensic training for the

radiologists, the study also demonstrates that the autopsy

protocols need to be further standardized. Since the autopsy

was used as the gold standard, false positive findings occurred

in the radiological examinations; this was due to the fact that

the lesions were indeed present but had not been mentioned in

the autopsy protocols. For example, the finding of a

pneumencephalon had not been noted in the autopsy protocols

even if the head had been partially destroyed, and the autopsy

protocols were generally characterized by a high inter-observer

variance concerning, among others, the description of signs of

increased brain pressure. It appeared that the diagnosis of some

findings such as brain swelling is based on different criteria in

radiological and autopsy evaluation. Midline shifting along

with compression of the liquor spaces is the main sign

indicating increased brain pressure at the radiological evalua-

tion. For the forensic pathologist, swelling of the gyri and

leveling of the sulci, swelling of the cerebellar tonsils, and other

signs such as pressure induced gray matter hemorrhage or the

presence of mediobasal pressure lines are of equal or even

higher diagnostic value concerning the detection of increased

brain pressure at autopsy. These often slight signs are not well

known to the clinical radiologists, which is expressed by low

CT and MRI sensitivity values when comparing the two

methods.

5. Conclusions

The present study has shown some promising results

concerning the diagnostic abilities of CT and MRI in forensic

neuropathology, but it has also demonstrated that further

improvements are needed in order to increase the sensitivity of

forensic-radiological analysis. Allowing the radiological

examiners to gain knowledge about forensically relevant

findings and using standardized autopsy and imaging protocols

as a basis for the comparison of autopsy and radiology will help

to bring the two specialized disciplines closer to each other and

open the door for a prolific interdisciplinary knowledge

transfer. Future forensic-radiological studies are expected to

broaden the basis of the challenging field of forensic

neuroimaging.

Acknowledgments

Special thanks goes to Roland Dorn, Urs Koenigsdorfer and

Therese Perinat (Institute of Forensic Medicine Bern) for

excellent technical assistance and to Verena Beutler, Elke

Spielvogel, Carolina Dobrowolska and Christoph Laeser from

the Insel Hospital Bern for their unremitting help with late-

night data acquisition. Also, many thanks to Christina

Jacobsen, University of Copenhagen, Denmark, for reviewing

the manuscript.

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