- Email: [email protected]
PMCT findings of intervertebral separation
Journal of Forensic Radiology and Imaging 2 (2014) 182–187
Contents lists available at ScienceDirect
Journal of Forensic Radiology and Imaging journal homepage: www.elsevier.com/locate/jofri
PMCT findings of intervertebral separation Yusuke Kawasumi a,n, Akihito Usui b,1, Yoshiyuki Hosokai b,2, Miho Sato a,1, Yoshie Hayashizaki c,3, Haruo Saito b,4, Tadashi Ishibashi a,5, Masato Funayama c,2 a
Tohoku University Graduate School of Medicine, Department of Clinical Imaging, 2-1 Seiryo-machi, Aoba-ku, Sendai, Miyagi 980-8575, Japan Tohoku University Graduate School of Medicine, Department of Diagnostic Image Analysis, 2-1 Seiryo-machi, Aoba-ku, Sendai, Miyagi 980-8575, Japan c Tohoku University Graduate School of Medicine, Department of Forensic Medicine, 2-1 Seiryo-machi, Aoba-ku, Sendai, Miyagi 980-8575, Japan b
art ic l e i nf o
a b s t r a c t
Article history: Received 31 May 2013 Received in revised form 16 December 2013 Accepted 2 September 2014 Available online 10 September 2014
Objectives: To evaluate the post-mortem computed tomography (PMCT) findings of intervertebral separation. Methods: 10 subjects who had undergone PMCT and forensic autopsy were evaluated. The median age was 69 years (range, 25–89 years), and all subjects were men. 19 intervertebral separations were identified at autopsy. 2 radiologists reviewed the CT findings such as misalignment of the spine, intervertebral space widening, gas in the intervertebral space, and haemorrhage in the tissues surrounding the spine before and after autopsy using a 3D DICOM workstation. Results: The observers detected 6 of 19 (32%) intervertebral separations before autopsy. After autopsy, they reviewed the CT considering the autopsy results and detected 13 of 19 (68%) intervertebral separations; misalignment (n¼ 7; 37%), widening (n¼5; 26%), gas (n¼2; 11%), and haemorrhage (n¼7; 37%). No finding indicating intervertebral separation was detected in 6 intervertebral separations. Conclusion: Re-evaluation with autopsy results improved the detectability of intervertebral separation on PMCT. Adequate experience and training regarding the interpretation are required. & 2014 Elsevier Ltd. All rights reserved.
Keywords: Forensic autopsy Post-mortem CT Cervical spine Hyperextension (over-extension)
1. Introduction The use of post-mortem radiological imaging is increasing in forensic medicine [1,2] and has proven useful. Post-mortem radiology may even become established as a new sub-specialty. Post-mortem radiological imaging diagnosis is often difficult because there are many differences between post-mortem and clinical imaging findings. To validate the radiological findings in forensic medicine, direct comparison of the images and autopsy results is necessary. Vertebral injury, especially to the cervical spine, can cause death in major trauma cases. Vertebral injuries include fractures and
n
Corresponding author. Tel.: þ 81 22 717 7936; fax: þ 81 22 717 7944. E-mail addresses: [email protected] (Y. Kawasumi), [email protected] (A. Usui), [email protected] (Y. Hosokai), [email protected] (M. Sato), [email protected] (Y. Hayashizaki), [email protected] (H. Saito), [email protected] (T. Ishibashi), [email protected] (M. Funayama). 1 Tel.: þ81 22 717 8683; fax: þ 81 22 717 7944. 2 Tel.: þ81 22 717 7936; fax: þ 81 22 717 7944. 3 Tel./fax: þ 81 22 717 8110. 4 Tel.: þ81 22 717 7938; fax: þ 81 22 717 7944. 5 Tel.: þ81 22 717 7481; fax: þ81 22 717 7944. http://dx.doi.org/10.1016/j.jofri.2014.09.001 2212-4780/& 2014 Elsevier Ltd. All rights reserved.
ligament injuries. Vertebral fracture is often associated with spinal cord injury, and even vertebral ligamentous injury without fracture occasionally results in spinal cord injury [3–6], and can cause death. Consequently, vertebral ligament injury should not be overlooked. Vertebral fractures are usually identified not only at autopsy but also on computed tomography (CT) because the fracture line or vertebral collapse is clearly visualised in almost all cases on CT [3,7– 11]. Ligament injuries can be detected easily by autopsy, because one can recognize a clear haemorrhage around the lesions. However these injuries are often difficult to visualise directly on CT images. Several clinical studies have demonstrated CT is inadequate for screening of ligamentous injuries [3,9–15]. Since May 2009, post-mortem computed tomography (PMCT) before forensic autopsy has been performed at our institution. Approximately 200 cases have been subjected to CT, and vertebral ligamentous injuries were found to frequently involve “intervertebral separation” at autopsy. Such intervertebral separation is caused by forcible over-extension of the head. The sequence of these injuries are tearing of the anterior longitudinal ligament, avulsion or separation of the intervertebral disc (which may tear a small fragment off the vertebral body near the tear), tearing of the posterior longitudinal ligament, and fracture and dislocation of the articular facets [16]. If intervertebral separation can be specified on CT images, CT may be able to predict vertebral ligamentous injury
Y. Kawasumi et al. / Journal of Forensic Radiology and Imaging 2 (2014) 182–187
indirectly, and ultimately, spinal cord injury. In the present study, the correlation between the PMCT findings and autopsy results of intervertebral separation were evaluated retrospectively.
2. Materials and methods The present retrospective study, which involved review of previously obtained image data, was approved by the ethics board of our institution, and informed consent was not required. 2.1. Study cases In the present study, 10 consecutive cases with 19 intervertebral separations were detected at autopsy at forensic autopsy from August 2009 to September 2010. The median age was 69 years (range, 25–89 years). All the subjects were men. The elapsed time from death to CT examination was within 2 days except for 1 case. The exception case was caused by a delay in uncovering the dead body. At autopsy, 7 deaths were attributed to vertebral injury with bleeding due to intervertebral separation (5 injuries from falls, 2 injuries from traffic accidents); 2 died of drowning; 1 died of brain stem injury caused by a fall. Spinal cord injury was histopathologically verified in 7 subjects. Some cases included a small fragment of the vertebral body above the tear. There was no subject excluded in this study. The details of the cases are shown in Table 1.
183
with 2 scans. First, the head was subject to conventional CT; the tube voltage was 120 kVp, and the tube current was arbitrarily changed by the installed mode. The rotation time was 1.5 s/ rotation. Field of view was S-size, and matrix size was 512 512 pixels. The collimation was 4.0 and 8.0 mm. Reconstruction filter was FC27, and reconstruction interval was 0. The second scan was from the head to the pelvis using the helical mode; the tube voltage was 120 kVp, and the tube current was arbitrarily changed by the installed mode. The rotation time was 0.75 s per rotation. Field of view was S-size, and matrix size was 512 512 pixels. The table speed was 14 mm per rotation, and the helical beam pitch was 0.875. Reconstruction filter was FC10, and reconstruction interval was 0. The reconstructed slice thickness of the images was 2.0 mm. The CT techniques are shown in Table 2. All cases underwent an autopsy shortly after the forensic CT. When the neck structure including the tongue was removed en bloc, the anterior aspect of the cervical vertebrae is disclosed. When there was a clear haemorrhage on the anterior surface of cervical vertebrae, the presence or absence of spine injury Table 2 CT techniques. Head (conventional scan) Head-pelvis (helical scan) Tube voltage (kVp) Tube current (mA) Rotation time (s) Field of view Matrix size (pixels) Collimation (mm) Beam pitch Table speed (mm/rot) Reconstruction filter Reconstruction interval
2.2. CT scan and autopsy An 8-channel multi-detector CT (MDCT) scanner (Aquilion 8; Toshiba Medical Systems, Japan) was used for all examinations. All subjects were scanned in the body bag while fully unclothed. No contrast material was administered. In all cases, CT was performed
120 arbitrarily 1.5 S-size 512 512 4.0, 8.0 (4-stacks) Non-helical Non-helical FC27 0
120 arbitrarily 0.75 LL-size 512 512 2 0.875 14 FC10 0
Table 1 Cases of intervertebral separation. CT Findings (After second interpretation) Case Age Sex Cause of death
Time since death
Position of intervertebral separation
Spinal cord injury
Results of First interpretation
Misalignment Widening Gas Haemorrhage
1
67
M
Drowning
1–2 days
C3/4 C4/5 Th9/10 Th10/11
Not detected Not detected Detected Detected
þ þ
2
71
M
Vertebral injury from a fall
Half-1 day
C3/4
þ
Detected
þ
þ
3
76
M
Vertebral injury from a fall
Half-1 day
C4/5
þ
Not detected
þ
4
64
M
Brain stem injury from a fall
Several days -1 week
Th3/4
Not detected
þ
5
89
M
Vertebral injury from a traffic accident
Not analysed
C3/4 C6/7
þ
Detected Not detected
þ
þ
6
71
M
Vertebral injury from a traffic accident
Not analysed
C4/5
þ
Not detected
þ
þ
7
64
M
Vertebral injury from a fall
2-3 days
C6/7 C5/6
Detected Not detected
þ
þ
8
83
M
Drowning
Half-1 day
C3/4 C6/7
þ
Not detected Not detected
þ þ
þ þ
9
62
M
Vertebral injury from a fall
1-2 days
C5/6
þ
Detected
þ
þ
10
25
M
Vertebral injury from a fall
Half-1 day
C3/4 C4/5 C6/7 C7/Th1
þ
Not Not Not Not
þ
þ
detected detected detected detected
184
Y. Kawasumi et al. / Journal of Forensic Radiology and Imaging 2 (2014) 182–187
including intervertebral separations was checked. All the autopsies were performed by a professor of forensic medicine with more than 25 years of experience in forensic autopsy. 2.3. Image interpretation All CT image data were sent to a DICOM server (POP-Net Server; ImageONE, Tokyo, Japan). Two radiologists read the images in consensus. The radiologists had from 9 to more than 25 years of experience in general radiology as well as 1 or 2 subspecialties in gastrointestinal, thoracic, or cardiovascular radiology. Additionally, the radiologists had approximately 2 years of experience in interpretation
of PMCT. The radiologists observed axial images with a 2-dimensional DICOM viewer (POP-Net Essential; ImageONE, Tokyo, Japan), and reviewed volume-rendering and multi-planar reconstruction images with a 3-dimensional DICOM workstation (Ziostation ver. 2.0.0.1; Ziosoft, Tokyo, Japan). The radiologists interpreted the CT images before autopsy (the first interpretation). After receiving the autopsy reports from forensic doctors, the CT images were reviewed, and the correlations between CT findings and autopsy results regarding intervertebral separation were discussed (the second interpretation). The major imaging findings that the radiologists reviewed were misalignment of the spine, intervertebral space widening, gas in the intervertebral space, and haemorrhage in the tissues surrounding the
Fig. 1. A 71-year-old man fell down a small roadside hill. (a) Front view of cervical spine at autopsy. Marked intervertebral separation is visible at the C3/4 level (arrowhead), (b) the muscles around the cervical spine are swollen and have a high-density (arrow) and (c) C3 posterior subluxation on C4 (arrow). C3/4 facet joint were also dislocated.
Fig. 2. A sailor discovered a 67-year-old man floating in the sea. (a) Left front view of cervical spine at autopsy. Minor intervertebral separation at Th10/11 (arrowhead). (b) A high-density formation around the thoracic aorta (arrow). This formation indicates haemorrhage due to intervertebral separation. (c) Abnormal finding of spine is unclear.
Y. Kawasumi et al. / Journal of Forensic Radiology and Imaging 2 (2014) 182–187
spine. In this study, finding of dislocation of vertebral body was defined as ‘misalignment’, and finding of a intervertebral space more dilated than other spaces was defined as ‘intervertebral space widening’. In Table 1, ‘Misalignment’, ‘Widening’, ‘Gas’, ‘Haemorrhage’ are misalignment of the spine, intervertebral space widening, gas in the intervertebral space, and haemorrhage in the tissues surrounding the spine, respectively.
3. Results Intervertebral separation was detected in 10 cases at autopsy. The total number of intervertebral separations was 19; 16 of the injuries were found in the cervical spine, and 3 were in the thoracic spine. All injuries caused varying degrees of haemorrhage in the tissues
185
surrounding the spine, indicating that all the intervertebral separations occurred before death. At the first interpretation, the observers could detect only 6 of 19 (32%) intervertebral separations. They found misalignment of the spine in 2 separations (11%), intervertebral space widening in 2 separations (11%), gas in the intervertebral space in 2 separations (11%) and haemorrhage in the tissues surrounding the spine in 3 separations (16%). At the second interpretation, abnormal findings in varying degrees were retrospectively detected on CT images in 13 out of 19 (68%) intervertebral separations. The details about detected CT findings were as follows; misalignment of the spine (n¼7; 37%), intervertebral space widening (n¼5; 26%), gas in the intervertebral space (n¼ 2; 11%), and haemorrhage in the tissues surrounding the spine (n¼7; 37%) (Table 1). Representative cases are shown in the figures (Figs. 1–7). 6 intervertebral separations showed no abnormal CT findings.
Fig. 3. A 64-year-old man was found under a bridge and was assumed to have fallen from the bridge. (a) Front view of cervical spine at autopsy. Intervertebral separation is evident at the Th3/4 level (arrowheads). (b) Minimal misalignment in a horizontal direction at the Th3/4 level only on the reconstructed coronal images (arrow). (c) The facet joints are also dislocated (arrowheads).
Fig. 4. A 64-year-old man was found dead in the prone position between his garden shed and a neighbour's wall under the suspicion he had fallen from a tree while pruning. (a) Left lateral view of cervical spine with intervertebral separation at the C6/7 and C5/6 at autopsy (arrowheads). (b) Distension of the intervertebral space and gas in the intervertebral space at the C6/7 level (arrows). Gas in the intervertebral space without distension of the intervertebral space at C5/6 (arrowhead). These finding would suggest intervertebral separation.
186
Y. Kawasumi et al. / Journal of Forensic Radiology and Imaging 2 (2014) 182–187
Fig. 5. A 62-year-old man was found lying at the bottom of the stairs and was suspected to have fallen down the stairs. (a) Front view of cervical spine at autopsy with intervertebral separation at the C5/6 level (arrowhead). (b) A small amount of widening of the anterior intervertebral space and a small amount of gas in the space at the C5/ 6 level (arrow).
Fig. 6. A 76-year-old man was found lying in the street with no apparent serious injury. (a) Front view of cervical spine at autopsy with intervertebral separation at the C4/5 level (arrowhead). At autopsy, the anterior longitudinal ligament was torn, but the posterior longitudinal ligament was intact. (b) The muscles appear to be slightly swollen (arrows). (c) Abnormal finding of spine is unclear.
4. Discussion Although detecting intervertebral separation in CT is difficult, careful interpretation can reveal minor abnormal findings associated with intervertebral separation in some cases. Vertebral ligament injury with or without vertebral fracture occasionally involves spinal cord injury and can be a cause of death [3–6]. Although evaluation of ligament injury is important for determining the cause of death, evaluation of ligaments on CT images is relatively difficult [3,9–15]. Since 2009, the authors have conducted a CT examination immediately before every forensic autopsy. Detection of intervertebral separation may help toward assessment of spinal cord injury and the cause of death. One of the
problems for the Japanese public health is the low rate of autopsies. This may result in not only the overlooking of criminal cases, but also poor statistics for causes of death. It is difficult to abruptly increase the rate of autopsies, and the government has recently recommended the use of PMCT for cadavers as a supplementary approach to diagnosing the cause of death without autopsy. Therefore, the presentations of intervertebral separations on forensic PMCT were retrospectively examined. Misalignment of the spine is comparatively visible on reconstructed coronal and sagittal CT images [9,11,17–20]. However, it was difficult to detect misalignment in some cases with definite separation detected at autopsy because of minimal misalignment, such as that in Case 4 (Fig. 3). Consequently, detection of even slightly irregular lines is necessary for observation of PMCT. On the other hand, it is necessary to carefully distinguish an intervertebral separation from degenerative spondylosis. 2 out of the 5 separations with intervertebral space widening showed gas in the intervertebral space (Figs. 4 and 5). No case without intervertebral space widening showed gas. The presence of gas may be an index of intervertebral separation because the gas presumably flows into the intervertebral space from outside. Unfortunately, there were insufficient cases with gas to reach a definitive conclusion. A degenerative intervertebral disc occasionally contains gas. Additionally, the amount of gas is probably influenced by the progress of decay. Therefore, careful diagnosis of this finding is necessary. Haemorrhage around the spine due to intervertebral separation is frequently found at autopsy. In the present study, all intervertebral separations caused varying degrees of haemorrhage in the tissues surrounding the spine. Therefore, none of the lesions were artefacts, and all were caused at the time of death. On clinical CT images, haemorrhage is usually found as a high-density formation or swelling of the surrounding tissues (e.g., muscle) [10,11]. In the present study, haemorrhage was recognized in 7 out of 19 intervertebral separations, but most of the findings were faint (Fig. 6) and would probably have been missed if not observed retrospectively. At the first interpretation, the observers detected only 6 of 19 (32%) intervertebral separations. The diagnostic performance resulted in one-half of that in the second interpretation. The reasons for this would likely be that their experiences in PMCT interpretation were insufficient and some of the changes that indicated the intervertebral separations were minimal. A certain level of training is needed for diagnosis of intervertebral separation on PMCT images. Christe et al. reported that 6 out of 13 spine fractures were missed at autopsy, and suggested that PMCT instead of autopsy should be the gold standard for spine fractures [21]. In our study,
Y. Kawasumi et al. / Journal of Forensic Radiology and Imaging 2 (2014) 182–187
187
Fig. 7. A 25-year-old man was found lying in a roadside ditch with a bicycle near him. (a) Front view of cervical spine at autopsy with intervertebral separation at the C3/4, C4/5, C6/7, and C7/Th1 levels (arrowheads). At autopsy, the anterior longitudinal ligament was torn on 4 lesions respectively, and the posterior longitudinal ligament of C4/5 level was also torn. There were no autopsy records of the posterior longitudinal ligament of the C3/4, C6/7, and C7/Th1 level. (b) Slight misalignment in the anteroposterior direction at the C4/5 level was found (arrow). The step-off at the spinolaminar line at C4-C5, narrowing of the spinal canal at C4-C5, and the fracture at C4 posterior element. However, no findings indicative of vertebral ligamentous injury were detected at the C3/4, C6/7, or C7/Th1 level.
6 out of 19 intervertebral separations had no abnormal CT finding even at the second interpretation. Therefore, PMCT should not be the gold standard for intervertebral separation. In the present study, the case series was small. The authors intend to increase the number of cases and obtain more definitive evidence of the indicators of intervertebral separation and thus ligament injury on CT. Additionally, this study could have selection bias because the case series were selected only from the victims who had undergone autopsy. We could not position the subjects optimally because of post-mortem rigidity, which might have made the detection of intervertebral separation more difficult. The observers in this study were only 2 radiologists and they did not perform independent readings, therefore this study lacked reproducibility testing for CT readings. 5. Conclusion PMCT findings of intervertebral separation are misalignment of spine, intervertebral space widening, gas in the intervertebral space, and haemorrhage in the tissues surrounding the spine. These findings are sometimes minimal, but evaluation with autopsy results improves the detectability of the findings. Therefore considerable caution is advisable in their interpretation, and adequate experience and training regarding the interpretation are also required. References [1] R. Dirnhofer, C. Jackowski, P. Vock, et al., VIRTOPSY: minimally invasive, imaging-guided virtual autopsy, Radiographics, 26, 20061305–1333. [2] S.A. Bolliger, M.J. Thali, S. Ross, et al., Virtual autopsy using imaging: bridging radiologic and forensic sciences. A review of the Virtopsy and similar projects, Eur. Radiol. 18 (2007) 273–282. [3] J.J. Diaz Jr., J.M. Aulino, B. Collier, et al., The early work-up for isolated ligamentous injury of the cervical spine: does computed tomography scan have a role? J. Trauma 59 (2005) 897–904. [4] G.J. Hogan, S.E. Mirvis, K. Shanmuganathan, T.M. Scalea, Exclusion of unstable cervical spine injury in obtunded patients with blunt trauma: is MR imaging needed when multi-detector row CT findings are normal? Radiology 237 (2005) 106–113. [5] T.J. Harris, C.C. Blackmore, S.K. Mirza, G.J. Jurkovich, Clearing the cervical spine in obtunded patients, Spine 33 (2008) 1547–1553.
[6] T. Okuda, S. Shiotani, H. Hayakawa, et al., A case of fatal cervical discoligamentous hyperextension injury without fracture: correlation of postmortem imaging and autopsy findings, Forensic Sci. Int. 225 (1–3) (2013) 71–74. [7] S.C. Gale, V.H. Gracias, P.M. Reilly, et al., The inefficiency of plain radiography to evaluate the cervical spine after blunt trauma, J. Trauma 59 (2005) 1121–1125. [8] M.M. Griffen, E.R. Frykberg, A.J. Kerwin, Radiographic clearance of blunt cervical spine injury: plain radiograph or computed tomography scan, J. Trauma 55 (2003) 222–227. [9] J.F. Holmes, S.E. Mirvis, E.A. Panacek, et al., Variability in computed tomography and magnetic resonance imaging in patients with cervical spine injuries, J. Trauma 53 (2002) 524–530. [10] M.A. Levitt, A.E. Flanders, Diagnostic capabilities of magnetic resonance imaging and computed tomography in acute cervical spinal column injury, Am. J. Emerg. Med. 9 (1991) 131–135. [11] J.R. Crim, K. Moore, D. Brodke, Clearance of the cervical spine in multitrauma patients: the role of advances imaging, Semin. Ultrasound, CT, MRI 22 (2001) 283–305. [12] G.B. Kasimatis, E. Panagiotopoulos, P. Megas, et al., The adult spinal cord injury without radiographic abnormalities syndrome: magnetic resonance imaging and clinical findings in adults with spinal cord injuries having normal radiographs and computed tomography studies, J. Trauma 65 (2008) 86–93. [13] P. Kothari, B. Freeman, M. Grevitt, et al., Injury to the spinal cord without radiological abnormality (SCIWORA) in adults, J. Bone Joint Surg. [Br.] 82 (B) (2000) 1034–1037. [14] M.K. Tewari, D.S. Gifti, P. Singh, et al., Diagnosis and prognostication of adult spinal cord injury without radiographic abnormality using magnetic resonance imaging: analysis of 40 patients, Surg. Neurol. 63 (2005) 204–209. [15] A.J. Schoenfeld, C.M. Bono, K.J. McGuire, et al., Computed tomography alone versus computed tomography and magnetic resonance imaging in the identification of occult injuries to the cervical spine: a meta-analysis, J. Trauma 68 (2010) 109–114. [16] M.J. Shkrum, D.A. Ramsay, Forensic Pathology of Trauma, Humana press, Totowa, New Jersey, USA (2007) 574–577. [17] K. Brohi, M. Healy, T. Fotheringham, et al., Helical computed tomographic scanning for the evaluation of the cervical spine in the unconscious, intubated trauma patient, J. Trauma 58 (2005) 897–901. [18] K.E. Radcliff, P. Ben-Galim, N. Dreiangel, et al., Comprehensive computed tomography assessment of the upper cervical anatomy: what is normal? Spine J. 10 (2010) 219–229. [19] N. Dreiangel, P. Ben-Galim, R. Lador, et al., Occipitocervical dissociative injuries: common in blunt trauma fatalities and better detected with objective computed tomography-based measurements, Spine J. 10 (2010) 704–707. [20] P.J. Schenarts, J. Diaz, C. Kaiser, et al., Prospective comparison of admission computed tomographic scan and plain films of the upper cervical spine in trauma patients with altered mental status, J. Trauma 51 (2001) 663–669. [21] A. Christe, S. Ross, L. Oesterhelweg, et al., Abdominal trauma – sensitivity and specificity of postmortem noncontrast imaging findings compared with autopsy findings, J. Trauma 66 (5) (2009) 1302–1307.
Contents lists available at ScienceDirect
Journal of Forensic Radiology and Imaging journal homepage: www.elsevier.com/locate/jofri
PMCT findings of intervertebral separation Yusuke Kawasumi a,n, Akihito Usui b,1, Yoshiyuki Hosokai b,2, Miho Sato a,1, Yoshie Hayashizaki c,3, Haruo Saito b,4, Tadashi Ishibashi a,5, Masato Funayama c,2 a
Tohoku University Graduate School of Medicine, Department of Clinical Imaging, 2-1 Seiryo-machi, Aoba-ku, Sendai, Miyagi 980-8575, Japan Tohoku University Graduate School of Medicine, Department of Diagnostic Image Analysis, 2-1 Seiryo-machi, Aoba-ku, Sendai, Miyagi 980-8575, Japan c Tohoku University Graduate School of Medicine, Department of Forensic Medicine, 2-1 Seiryo-machi, Aoba-ku, Sendai, Miyagi 980-8575, Japan b
art ic l e i nf o
a b s t r a c t
Article history: Received 31 May 2013 Received in revised form 16 December 2013 Accepted 2 September 2014 Available online 10 September 2014
Objectives: To evaluate the post-mortem computed tomography (PMCT) findings of intervertebral separation. Methods: 10 subjects who had undergone PMCT and forensic autopsy were evaluated. The median age was 69 years (range, 25–89 years), and all subjects were men. 19 intervertebral separations were identified at autopsy. 2 radiologists reviewed the CT findings such as misalignment of the spine, intervertebral space widening, gas in the intervertebral space, and haemorrhage in the tissues surrounding the spine before and after autopsy using a 3D DICOM workstation. Results: The observers detected 6 of 19 (32%) intervertebral separations before autopsy. After autopsy, they reviewed the CT considering the autopsy results and detected 13 of 19 (68%) intervertebral separations; misalignment (n¼ 7; 37%), widening (n¼5; 26%), gas (n¼2; 11%), and haemorrhage (n¼7; 37%). No finding indicating intervertebral separation was detected in 6 intervertebral separations. Conclusion: Re-evaluation with autopsy results improved the detectability of intervertebral separation on PMCT. Adequate experience and training regarding the interpretation are required. & 2014 Elsevier Ltd. All rights reserved.
Keywords: Forensic autopsy Post-mortem CT Cervical spine Hyperextension (over-extension)
1. Introduction The use of post-mortem radiological imaging is increasing in forensic medicine [1,2] and has proven useful. Post-mortem radiology may even become established as a new sub-specialty. Post-mortem radiological imaging diagnosis is often difficult because there are many differences between post-mortem and clinical imaging findings. To validate the radiological findings in forensic medicine, direct comparison of the images and autopsy results is necessary. Vertebral injury, especially to the cervical spine, can cause death in major trauma cases. Vertebral injuries include fractures and
n
Corresponding author. Tel.: þ 81 22 717 7936; fax: þ 81 22 717 7944. E-mail addresses: [email protected] (Y. Kawasumi), [email protected] (A. Usui), [email protected] (Y. Hosokai), [email protected] (M. Sato), [email protected] (Y. Hayashizaki), [email protected] (H. Saito), [email protected] (T. Ishibashi), [email protected] (M. Funayama). 1 Tel.: þ81 22 717 8683; fax: þ 81 22 717 7944. 2 Tel.: þ81 22 717 7936; fax: þ 81 22 717 7944. 3 Tel./fax: þ 81 22 717 8110. 4 Tel.: þ81 22 717 7938; fax: þ 81 22 717 7944. 5 Tel.: þ81 22 717 7481; fax: þ81 22 717 7944. http://dx.doi.org/10.1016/j.jofri.2014.09.001 2212-4780/& 2014 Elsevier Ltd. All rights reserved.
ligament injuries. Vertebral fracture is often associated with spinal cord injury, and even vertebral ligamentous injury without fracture occasionally results in spinal cord injury [3–6], and can cause death. Consequently, vertebral ligament injury should not be overlooked. Vertebral fractures are usually identified not only at autopsy but also on computed tomography (CT) because the fracture line or vertebral collapse is clearly visualised in almost all cases on CT [3,7– 11]. Ligament injuries can be detected easily by autopsy, because one can recognize a clear haemorrhage around the lesions. However these injuries are often difficult to visualise directly on CT images. Several clinical studies have demonstrated CT is inadequate for screening of ligamentous injuries [3,9–15]. Since May 2009, post-mortem computed tomography (PMCT) before forensic autopsy has been performed at our institution. Approximately 200 cases have been subjected to CT, and vertebral ligamentous injuries were found to frequently involve “intervertebral separation” at autopsy. Such intervertebral separation is caused by forcible over-extension of the head. The sequence of these injuries are tearing of the anterior longitudinal ligament, avulsion or separation of the intervertebral disc (which may tear a small fragment off the vertebral body near the tear), tearing of the posterior longitudinal ligament, and fracture and dislocation of the articular facets [16]. If intervertebral separation can be specified on CT images, CT may be able to predict vertebral ligamentous injury
Y. Kawasumi et al. / Journal of Forensic Radiology and Imaging 2 (2014) 182–187
indirectly, and ultimately, spinal cord injury. In the present study, the correlation between the PMCT findings and autopsy results of intervertebral separation were evaluated retrospectively.
2. Materials and methods The present retrospective study, which involved review of previously obtained image data, was approved by the ethics board of our institution, and informed consent was not required. 2.1. Study cases In the present study, 10 consecutive cases with 19 intervertebral separations were detected at autopsy at forensic autopsy from August 2009 to September 2010. The median age was 69 years (range, 25–89 years). All the subjects were men. The elapsed time from death to CT examination was within 2 days except for 1 case. The exception case was caused by a delay in uncovering the dead body. At autopsy, 7 deaths were attributed to vertebral injury with bleeding due to intervertebral separation (5 injuries from falls, 2 injuries from traffic accidents); 2 died of drowning; 1 died of brain stem injury caused by a fall. Spinal cord injury was histopathologically verified in 7 subjects. Some cases included a small fragment of the vertebral body above the tear. There was no subject excluded in this study. The details of the cases are shown in Table 1.
183
with 2 scans. First, the head was subject to conventional CT; the tube voltage was 120 kVp, and the tube current was arbitrarily changed by the installed mode. The rotation time was 1.5 s/ rotation. Field of view was S-size, and matrix size was 512 512 pixels. The collimation was 4.0 and 8.0 mm. Reconstruction filter was FC27, and reconstruction interval was 0. The second scan was from the head to the pelvis using the helical mode; the tube voltage was 120 kVp, and the tube current was arbitrarily changed by the installed mode. The rotation time was 0.75 s per rotation. Field of view was S-size, and matrix size was 512 512 pixels. The table speed was 14 mm per rotation, and the helical beam pitch was 0.875. Reconstruction filter was FC10, and reconstruction interval was 0. The reconstructed slice thickness of the images was 2.0 mm. The CT techniques are shown in Table 2. All cases underwent an autopsy shortly after the forensic CT. When the neck structure including the tongue was removed en bloc, the anterior aspect of the cervical vertebrae is disclosed. When there was a clear haemorrhage on the anterior surface of cervical vertebrae, the presence or absence of spine injury Table 2 CT techniques. Head (conventional scan) Head-pelvis (helical scan) Tube voltage (kVp) Tube current (mA) Rotation time (s) Field of view Matrix size (pixels) Collimation (mm) Beam pitch Table speed (mm/rot) Reconstruction filter Reconstruction interval
2.2. CT scan and autopsy An 8-channel multi-detector CT (MDCT) scanner (Aquilion 8; Toshiba Medical Systems, Japan) was used for all examinations. All subjects were scanned in the body bag while fully unclothed. No contrast material was administered. In all cases, CT was performed
120 arbitrarily 1.5 S-size 512 512 4.0, 8.0 (4-stacks) Non-helical Non-helical FC27 0
120 arbitrarily 0.75 LL-size 512 512 2 0.875 14 FC10 0
Table 1 Cases of intervertebral separation. CT Findings (After second interpretation) Case Age Sex Cause of death
Time since death
Position of intervertebral separation
Spinal cord injury
Results of First interpretation
Misalignment Widening Gas Haemorrhage
1
67
M
Drowning
1–2 days
C3/4 C4/5 Th9/10 Th10/11
Not detected Not detected Detected Detected
þ þ
2
71
M
Vertebral injury from a fall
Half-1 day
C3/4
þ
Detected
þ
þ
3
76
M
Vertebral injury from a fall
Half-1 day
C4/5
þ
Not detected
þ
4
64
M
Brain stem injury from a fall
Several days -1 week
Th3/4
Not detected
þ
5
89
M
Vertebral injury from a traffic accident
Not analysed
C3/4 C6/7
þ
Detected Not detected
þ
þ
6
71
M
Vertebral injury from a traffic accident
Not analysed
C4/5
þ
Not detected
þ
þ
7
64
M
Vertebral injury from a fall
2-3 days
C6/7 C5/6
Detected Not detected
þ
þ
8
83
M
Drowning
Half-1 day
C3/4 C6/7
þ
Not detected Not detected
þ þ
þ þ
9
62
M
Vertebral injury from a fall
1-2 days
C5/6
þ
Detected
þ
þ
10
25
M
Vertebral injury from a fall
Half-1 day
C3/4 C4/5 C6/7 C7/Th1
þ
Not Not Not Not
þ
þ
detected detected detected detected
184
Y. Kawasumi et al. / Journal of Forensic Radiology and Imaging 2 (2014) 182–187
including intervertebral separations was checked. All the autopsies were performed by a professor of forensic medicine with more than 25 years of experience in forensic autopsy. 2.3. Image interpretation All CT image data were sent to a DICOM server (POP-Net Server; ImageONE, Tokyo, Japan). Two radiologists read the images in consensus. The radiologists had from 9 to more than 25 years of experience in general radiology as well as 1 or 2 subspecialties in gastrointestinal, thoracic, or cardiovascular radiology. Additionally, the radiologists had approximately 2 years of experience in interpretation
of PMCT. The radiologists observed axial images with a 2-dimensional DICOM viewer (POP-Net Essential; ImageONE, Tokyo, Japan), and reviewed volume-rendering and multi-planar reconstruction images with a 3-dimensional DICOM workstation (Ziostation ver. 2.0.0.1; Ziosoft, Tokyo, Japan). The radiologists interpreted the CT images before autopsy (the first interpretation). After receiving the autopsy reports from forensic doctors, the CT images were reviewed, and the correlations between CT findings and autopsy results regarding intervertebral separation were discussed (the second interpretation). The major imaging findings that the radiologists reviewed were misalignment of the spine, intervertebral space widening, gas in the intervertebral space, and haemorrhage in the tissues surrounding the
Fig. 1. A 71-year-old man fell down a small roadside hill. (a) Front view of cervical spine at autopsy. Marked intervertebral separation is visible at the C3/4 level (arrowhead), (b) the muscles around the cervical spine are swollen and have a high-density (arrow) and (c) C3 posterior subluxation on C4 (arrow). C3/4 facet joint were also dislocated.
Fig. 2. A sailor discovered a 67-year-old man floating in the sea. (a) Left front view of cervical spine at autopsy. Minor intervertebral separation at Th10/11 (arrowhead). (b) A high-density formation around the thoracic aorta (arrow). This formation indicates haemorrhage due to intervertebral separation. (c) Abnormal finding of spine is unclear.
Y. Kawasumi et al. / Journal of Forensic Radiology and Imaging 2 (2014) 182–187
spine. In this study, finding of dislocation of vertebral body was defined as ‘misalignment’, and finding of a intervertebral space more dilated than other spaces was defined as ‘intervertebral space widening’. In Table 1, ‘Misalignment’, ‘Widening’, ‘Gas’, ‘Haemorrhage’ are misalignment of the spine, intervertebral space widening, gas in the intervertebral space, and haemorrhage in the tissues surrounding the spine, respectively.
3. Results Intervertebral separation was detected in 10 cases at autopsy. The total number of intervertebral separations was 19; 16 of the injuries were found in the cervical spine, and 3 were in the thoracic spine. All injuries caused varying degrees of haemorrhage in the tissues
185
surrounding the spine, indicating that all the intervertebral separations occurred before death. At the first interpretation, the observers could detect only 6 of 19 (32%) intervertebral separations. They found misalignment of the spine in 2 separations (11%), intervertebral space widening in 2 separations (11%), gas in the intervertebral space in 2 separations (11%) and haemorrhage in the tissues surrounding the spine in 3 separations (16%). At the second interpretation, abnormal findings in varying degrees were retrospectively detected on CT images in 13 out of 19 (68%) intervertebral separations. The details about detected CT findings were as follows; misalignment of the spine (n¼7; 37%), intervertebral space widening (n¼5; 26%), gas in the intervertebral space (n¼ 2; 11%), and haemorrhage in the tissues surrounding the spine (n¼7; 37%) (Table 1). Representative cases are shown in the figures (Figs. 1–7). 6 intervertebral separations showed no abnormal CT findings.
Fig. 3. A 64-year-old man was found under a bridge and was assumed to have fallen from the bridge. (a) Front view of cervical spine at autopsy. Intervertebral separation is evident at the Th3/4 level (arrowheads). (b) Minimal misalignment in a horizontal direction at the Th3/4 level only on the reconstructed coronal images (arrow). (c) The facet joints are also dislocated (arrowheads).
Fig. 4. A 64-year-old man was found dead in the prone position between his garden shed and a neighbour's wall under the suspicion he had fallen from a tree while pruning. (a) Left lateral view of cervical spine with intervertebral separation at the C6/7 and C5/6 at autopsy (arrowheads). (b) Distension of the intervertebral space and gas in the intervertebral space at the C6/7 level (arrows). Gas in the intervertebral space without distension of the intervertebral space at C5/6 (arrowhead). These finding would suggest intervertebral separation.
186
Y. Kawasumi et al. / Journal of Forensic Radiology and Imaging 2 (2014) 182–187
Fig. 5. A 62-year-old man was found lying at the bottom of the stairs and was suspected to have fallen down the stairs. (a) Front view of cervical spine at autopsy with intervertebral separation at the C5/6 level (arrowhead). (b) A small amount of widening of the anterior intervertebral space and a small amount of gas in the space at the C5/ 6 level (arrow).
Fig. 6. A 76-year-old man was found lying in the street with no apparent serious injury. (a) Front view of cervical spine at autopsy with intervertebral separation at the C4/5 level (arrowhead). At autopsy, the anterior longitudinal ligament was torn, but the posterior longitudinal ligament was intact. (b) The muscles appear to be slightly swollen (arrows). (c) Abnormal finding of spine is unclear.
4. Discussion Although detecting intervertebral separation in CT is difficult, careful interpretation can reveal minor abnormal findings associated with intervertebral separation in some cases. Vertebral ligament injury with or without vertebral fracture occasionally involves spinal cord injury and can be a cause of death [3–6]. Although evaluation of ligament injury is important for determining the cause of death, evaluation of ligaments on CT images is relatively difficult [3,9–15]. Since 2009, the authors have conducted a CT examination immediately before every forensic autopsy. Detection of intervertebral separation may help toward assessment of spinal cord injury and the cause of death. One of the
problems for the Japanese public health is the low rate of autopsies. This may result in not only the overlooking of criminal cases, but also poor statistics for causes of death. It is difficult to abruptly increase the rate of autopsies, and the government has recently recommended the use of PMCT for cadavers as a supplementary approach to diagnosing the cause of death without autopsy. Therefore, the presentations of intervertebral separations on forensic PMCT were retrospectively examined. Misalignment of the spine is comparatively visible on reconstructed coronal and sagittal CT images [9,11,17–20]. However, it was difficult to detect misalignment in some cases with definite separation detected at autopsy because of minimal misalignment, such as that in Case 4 (Fig. 3). Consequently, detection of even slightly irregular lines is necessary for observation of PMCT. On the other hand, it is necessary to carefully distinguish an intervertebral separation from degenerative spondylosis. 2 out of the 5 separations with intervertebral space widening showed gas in the intervertebral space (Figs. 4 and 5). No case without intervertebral space widening showed gas. The presence of gas may be an index of intervertebral separation because the gas presumably flows into the intervertebral space from outside. Unfortunately, there were insufficient cases with gas to reach a definitive conclusion. A degenerative intervertebral disc occasionally contains gas. Additionally, the amount of gas is probably influenced by the progress of decay. Therefore, careful diagnosis of this finding is necessary. Haemorrhage around the spine due to intervertebral separation is frequently found at autopsy. In the present study, all intervertebral separations caused varying degrees of haemorrhage in the tissues surrounding the spine. Therefore, none of the lesions were artefacts, and all were caused at the time of death. On clinical CT images, haemorrhage is usually found as a high-density formation or swelling of the surrounding tissues (e.g., muscle) [10,11]. In the present study, haemorrhage was recognized in 7 out of 19 intervertebral separations, but most of the findings were faint (Fig. 6) and would probably have been missed if not observed retrospectively. At the first interpretation, the observers detected only 6 of 19 (32%) intervertebral separations. The diagnostic performance resulted in one-half of that in the second interpretation. The reasons for this would likely be that their experiences in PMCT interpretation were insufficient and some of the changes that indicated the intervertebral separations were minimal. A certain level of training is needed for diagnosis of intervertebral separation on PMCT images. Christe et al. reported that 6 out of 13 spine fractures were missed at autopsy, and suggested that PMCT instead of autopsy should be the gold standard for spine fractures [21]. In our study,
Y. Kawasumi et al. / Journal of Forensic Radiology and Imaging 2 (2014) 182–187
187
Fig. 7. A 25-year-old man was found lying in a roadside ditch with a bicycle near him. (a) Front view of cervical spine at autopsy with intervertebral separation at the C3/4, C4/5, C6/7, and C7/Th1 levels (arrowheads). At autopsy, the anterior longitudinal ligament was torn on 4 lesions respectively, and the posterior longitudinal ligament of C4/5 level was also torn. There were no autopsy records of the posterior longitudinal ligament of the C3/4, C6/7, and C7/Th1 level. (b) Slight misalignment in the anteroposterior direction at the C4/5 level was found (arrow). The step-off at the spinolaminar line at C4-C5, narrowing of the spinal canal at C4-C5, and the fracture at C4 posterior element. However, no findings indicative of vertebral ligamentous injury were detected at the C3/4, C6/7, or C7/Th1 level.
6 out of 19 intervertebral separations had no abnormal CT finding even at the second interpretation. Therefore, PMCT should not be the gold standard for intervertebral separation. In the present study, the case series was small. The authors intend to increase the number of cases and obtain more definitive evidence of the indicators of intervertebral separation and thus ligament injury on CT. Additionally, this study could have selection bias because the case series were selected only from the victims who had undergone autopsy. We could not position the subjects optimally because of post-mortem rigidity, which might have made the detection of intervertebral separation more difficult. The observers in this study were only 2 radiologists and they did not perform independent readings, therefore this study lacked reproducibility testing for CT readings. 5. Conclusion PMCT findings of intervertebral separation are misalignment of spine, intervertebral space widening, gas in the intervertebral space, and haemorrhage in the tissues surrounding the spine. These findings are sometimes minimal, but evaluation with autopsy results improves the detectability of the findings. Therefore considerable caution is advisable in their interpretation, and adequate experience and training regarding the interpretation are also required. References [1] R. Dirnhofer, C. Jackowski, P. Vock, et al., VIRTOPSY: minimally invasive, imaging-guided virtual autopsy, Radiographics, 26, 20061305–1333. [2] S.A. Bolliger, M.J. Thali, S. Ross, et al., Virtual autopsy using imaging: bridging radiologic and forensic sciences. A review of the Virtopsy and similar projects, Eur. Radiol. 18 (2007) 273–282. [3] J.J. Diaz Jr., J.M. Aulino, B. Collier, et al., The early work-up for isolated ligamentous injury of the cervical spine: does computed tomography scan have a role? J. Trauma 59 (2005) 897–904. [4] G.J. Hogan, S.E. Mirvis, K. Shanmuganathan, T.M. Scalea, Exclusion of unstable cervical spine injury in obtunded patients with blunt trauma: is MR imaging needed when multi-detector row CT findings are normal? Radiology 237 (2005) 106–113. [5] T.J. Harris, C.C. Blackmore, S.K. Mirza, G.J. Jurkovich, Clearing the cervical spine in obtunded patients, Spine 33 (2008) 1547–1553.
[6] T. Okuda, S. Shiotani, H. Hayakawa, et al., A case of fatal cervical discoligamentous hyperextension injury without fracture: correlation of postmortem imaging and autopsy findings, Forensic Sci. Int. 225 (1–3) (2013) 71–74. [7] S.C. Gale, V.H. Gracias, P.M. Reilly, et al., The inefficiency of plain radiography to evaluate the cervical spine after blunt trauma, J. Trauma 59 (2005) 1121–1125. [8] M.M. Griffen, E.R. Frykberg, A.J. Kerwin, Radiographic clearance of blunt cervical spine injury: plain radiograph or computed tomography scan, J. Trauma 55 (2003) 222–227. [9] J.F. Holmes, S.E. Mirvis, E.A. Panacek, et al., Variability in computed tomography and magnetic resonance imaging in patients with cervical spine injuries, J. Trauma 53 (2002) 524–530. [10] M.A. Levitt, A.E. Flanders, Diagnostic capabilities of magnetic resonance imaging and computed tomography in acute cervical spinal column injury, Am. J. Emerg. Med. 9 (1991) 131–135. [11] J.R. Crim, K. Moore, D. Brodke, Clearance of the cervical spine in multitrauma patients: the role of advances imaging, Semin. Ultrasound, CT, MRI 22 (2001) 283–305. [12] G.B. Kasimatis, E. Panagiotopoulos, P. Megas, et al., The adult spinal cord injury without radiographic abnormalities syndrome: magnetic resonance imaging and clinical findings in adults with spinal cord injuries having normal radiographs and computed tomography studies, J. Trauma 65 (2008) 86–93. [13] P. Kothari, B. Freeman, M. Grevitt, et al., Injury to the spinal cord without radiological abnormality (SCIWORA) in adults, J. Bone Joint Surg. [Br.] 82 (B) (2000) 1034–1037. [14] M.K. Tewari, D.S. Gifti, P. Singh, et al., Diagnosis and prognostication of adult spinal cord injury without radiographic abnormality using magnetic resonance imaging: analysis of 40 patients, Surg. Neurol. 63 (2005) 204–209. [15] A.J. Schoenfeld, C.M. Bono, K.J. McGuire, et al., Computed tomography alone versus computed tomography and magnetic resonance imaging in the identification of occult injuries to the cervical spine: a meta-analysis, J. Trauma 68 (2010) 109–114. [16] M.J. Shkrum, D.A. Ramsay, Forensic Pathology of Trauma, Humana press, Totowa, New Jersey, USA (2007) 574–577. [17] K. Brohi, M. Healy, T. Fotheringham, et al., Helical computed tomographic scanning for the evaluation of the cervical spine in the unconscious, intubated trauma patient, J. Trauma 58 (2005) 897–901. [18] K.E. Radcliff, P. Ben-Galim, N. Dreiangel, et al., Comprehensive computed tomography assessment of the upper cervical anatomy: what is normal? Spine J. 10 (2010) 219–229. [19] N. Dreiangel, P. Ben-Galim, R. Lador, et al., Occipitocervical dissociative injuries: common in blunt trauma fatalities and better detected with objective computed tomography-based measurements, Spine J. 10 (2010) 704–707. [20] P.J. Schenarts, J. Diaz, C. Kaiser, et al., Prospective comparison of admission computed tomographic scan and plain films of the upper cervical spine in trauma patients with altered mental status, J. Trauma 51 (2001) 663–669. [21] A. Christe, S. Ross, L. Oesterhelweg, et al., Abdominal trauma – sensitivity and specificity of postmortem noncontrast imaging findings compared with autopsy findings, J. Trauma 66 (5) (2009) 1302–1307.