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Comparison between postmortem computed tomography and autopsy in the detection of traumatic head injuries
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Original Article
Comparison between postmortem computed tomography and autopsy in the detection of traumatic head injuries L. Legrand a,b,c,∗ , T. Delabarde b,d,e , R. Souillard-Scemama a,b , I. Sec b,d,f , I. Plu b,d,g , J-M. Laborie b,d,f , Y. Delannoy b,d,h , L. Hamza b,d,i , M. Taccoen b,d , L. de Jong a,b,c , J. Benzakoun a,b,c , M. Edjlali a,b,c , J-F. Méder a,b,c , C. Oppenheim a,b,c , B. Ludes b,d,e a
Service d’imagerie morphologique et fonctionnelle, centre hospitalier Sainte-Anne, 1 rue Cabanis, 75014 Paris, France Pôle universitaire d’imagerie post-mortem, Université Paris Descartes, 12, rue de l’Ecole de Médecine, 75006 Paris, France c INSERM UMR 1266, Institut de Psychiatrie et Neurosciences de Paris, 102-108 rue de la Santé, 75014 Paris, France d Institut médico-légal de Paris, 2, place Mazas, 75012 Paris, France e CNRS UMR 5288 Institut National de la transfusion sanguine, 6, rue Cabanel, 75015 Paris, France f Unité médico-judiciaire, Hôtel-Dieu, 1, place du Parvis de Notre-Dame, 75004 Paris, France g Sorbonne Université, 91, boulevard de l’Hôpital, 75013 Paris, France h Institut médico-légal de Lille, rue André Verhaeghe, 59000 Lille, France i Service d’accueil des urgences, hôpital Avicenne, 125, rue de Stalingrad, 93000 Bobigny, France b
a r t i c l e
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Article history: Available online xxx Keywords: Postmortem computed tomography Autopsy Traumatic head injuries Hemorrhage Fracture
a b s t r a c t Introduction. – The aim of this study was to assess the agreement between postmortem computed tomography (PMCT) and autopsy in detecting traumatic head injuries. Materials and Methods. – Consecutive cases of death that underwent both unenhanced PMCT and conventional autopsy were collected from our institution database during a period of 3 years and reviewed retrospectively. PMCT images were reviewed for the presence of fractures (cranial vault, skull base, facial bones and atlas/axis) and intracranial hemorrhage. Kappa values were calculated to determine the agreement between PMCT and autopsy reports. Results. – 73 cases were included, of which 44 (60%) had head trauma. Agreement between PMCT and autopsy was almost perfect ( = 0.95) for fractures and substantial ( = 0.75) for intracranial hemorrhage. PMCT was superior to autopsy in detecting facial bone and upper cervical spine fractures, and intraventricular hemorrhage. However, in some cases thin extra-axial blood collections were missed on PMCT. Conclusions. – The agreement between PMCT and autopsy in detecting traumatic head injuries was good. Using a combination of both techniques increases the quality of postmortem evaluation because more lesions are detected. © 2019 Elsevier Masson SAS. All rights reserved.
Introduction CT MRI PMCT
computed tomography magnetic resonance imaging postmortem computed tomography
∗ Corresponding author at: Service d’imagerie morphologique et fonctionnelle, centre hospitalier Sainte-Anne, 1 rue Cabanis, 75014 Paris, France. E-mail address: [email protected] (L. Legrand).
Traumatic head injuries are a leading cause of death [1], responsible for approximatively 50,000 deaths each year in the United States. The main etiologies are accidents (e.g. traffic, sports, work and domestic accidents, falls) and aggressions (e.g. physical abuse of children, injuries from bladed weapons or firearms in young adults) [2]. Autopsy is the gold standard for postmortem evaluation of traumatic head injuries, but it is invasive, operator-dependent and irreversible. Secondary analyses are rarely performed, as they can never be as efficient as the first one. Whereas the number of autopsies has decreased in recent years [3], mainly for budget-related reasons, the use of post-mortem imaging (computed tomography [CT] and magnetic resonance imaging [MRI])
https://doi.org/10.1016/j.neurad.2019.03.008 0150-9861/© 2019 Elsevier Masson SAS. All rights reserved.
Please cite this article in press as: Legrand L, et al. Comparison between postmortem computed tomography and autopsy in the detection of traumatic head injuries. J Neuroradiol (2019), https://doi.org/10.1016/j.neurad.2019.03.008
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has increased [4]. Advantages of post-mortem CT (PMCT) scanning are: • its fast acquisition (< 15 minutes for a full-body scan); • its non-invasive character, preserving the integrity of the corpse and traces of evidence; • the digital data storage allowing easy secondary and remote readings; • the provision of details on lesion location to guide autopsy; • the possibility to produce “non-gruesome evidence” to display in court. Furthermore, besides searching for the cause of death, PMCT can also be used for identification purpose [5], notably in cases of mass disaster. Studies that compared the performance of post-mortem imaging to that of autopsy have mainly focused on the reliability of CT and/or MRI scanning to identify the cause of death [6,7]. When exploring trauma caused by firearms, PMCT can provide valuable additional information on localization of projectiles, entry and exit points, and ballistic trajectory [8]. While some PMCT-autopsy correlation studies have been performed for full-body trauma [9–12], others have focused on the cranial region [2,8,13–15], with PMCT being read by radiologists [2,13,15] or by forensic pathologists [14]. These studies showed that PMCT is superior to autopsy in detecting pneumocephalus, intraventricular hemorrhages and facial skeleton fractures [2], but that the detection of small hemorrhagic injuries [2,13,15] and injuries of the skull base [2,8], especially fractures of the anterior and middle cranial fossa [14], are part of its main limitations. The literature of PMCT-autopsy correlation studies is limited, varies considerably in terms of methodologies, and most studies have a small sample size. The seminal forensic PMCT-autopsy correlation study (n = 57) was based on a 4-detector row scanner [2], which is no longer in use in most institutions. A recent larger study (n = 203) reviewing autopsy and PMCT reports did use up-todate 64- or 256-detector row scanners [15], but the PMCT reading lacked a standardized protocol and therefore may have overlooked more subtle signs of trauma. The aim of this retrospective correlation study was to (re-)examen the benefits and limitations of 64-detector PMCT imaging compared to autopsy. Cranial PMCT was reviewed in a standardized way by a neuroradiologist trained in post-mortem imaging and performance in the detection of traumatic head injuries was compared to that of autopsy. Materials and methods Study population For this study we included all deceased cases who underwent PMCT scanning at Sainte-Anne Hospital and autopsy at the Paris Forensics Institute between May 2014 and January 2017 (n = 105). We excluded cases with only an external examination instead of a complete autopsy (n = 27), cases for which no autopsy report was available (n = 4) and one case with a mummified cranial and cervical region. Our final dataset included 73 cases of which 58 were men and 15 women with a mean age of 34 years (SD 22) [range: 24 days old-86 years old]).
enclosed in body bags for reasons of hygiene and to respect their anonymity. The protocol included anteroposterior and lateral scout views, two main spiral scans (one focused on the head and neck, and another focused on the chest, abdomen, pelvis and limbs), and supplemental spiral scans for the limbs if required. The following parameters were used for the head and neck spiral scan: 120 kV, 250 mA (dose modulation), 0.8 s/rotation, pitch of 0.531, beam collimation 0.625 × 64, slice thickness 1.25 mm, field of view 32 cm. Of note, the first 8 corpses in the series received a single spiral scan from the head to the pelvis, and thus had a larger field of view and lower radiation dose at the level of head compared to the rest of the sample. Data were transferred onto a GE Advantage Windows post-treatment workstation (version 4.6) for multiplanar and 3D Volume Rendering reconstructions. Images were reconstructed with soft tissue and bone algorithms. Autopsy Prior to autopsy, a pre-report of the PMCT was transmitted by the radiologist to the forensic pathologist. Autopsy started with an external examination, performed by one of 12 forensic pathologists. Subsequently, the cranium was opened and the brain was removed. When brain damage was apparent upon macroscopic examination, the brain was not further dissected but placed in a formaldehyde solution for potential future anatomical pathology examination. If no external brain damage was found, one or more sections were performed. Analysis of data PMCT A neuroradiologist with 3 years of experience in post-mortem imaging (LL) and blinded to the autopsy results, reviewed all PMCT scans of the head and neck regions. Following a standardized reading protocol, the presence or absence of fracture(s) (cranial vault, base of the skull, facial skeleton, cervical vertebrae C1/C2), pneumocephalus, projectile(s) and intracranial hemorrhage (extra-axial [epidural and subdural hematomas, subarachnoid and intraventricular hemorrhage] or intraparenchymal [contusions or shear/diffuse axonal injuries]) were reported. The number/type of fractures and hemorrhage size as well as their precise localization were not systematically reported. In complex cases (n < 10), the PMCT was reviewed by two neuroradiologists (LL and JFM). Targeted rereading was carried out whenever an abnormality observed at autopsy had not been detected during the first PMCT reading, in order to understand potential causes for false negative at PMCT. These rereadings were not included in the statistical analyses. Autopsy The autopsy reports were reread by the neuroradiologist using the same reading grid used for PMCT. Also, cause of death was extracted from the autopsy reports. Statistical analyses For each item of the structured report, kappa values were calculated to determine the agreement between the PMCT and autopsy [16]. Results
Technique Population PMCT CT scanning was performed at the request of law enforcement authorities. Corpses were scanned using a 64-detector CT scanner (GE Lightspeed, General Electric Systems, Milwaukee, WI, USA),
Of the total study population (n = 73), 44 (60%) had head trauma. In 37 (84%) head trauma cases, the pathologist considered the head trauma the direct cause of death (24 bullet wounds, 5 falls,
Please cite this article in press as: Legrand L, et al. Comparison between postmortem computed tomography and autopsy in the detection of traumatic head injuries. J Neuroradiol (2019), https://doi.org/10.1016/j.neurad.2019.03.008
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Fig. 1. Suspected physical abuse involving a two-year-old child. At autopsy (a-c): linear fracture to the right side of the occipital bone (a,b), right-sided subdural and subarachnoid hemorrhage (c). PMCT (d-g) displays a discrete subarachnoid and subdural hemorrhage (red arrow) but no fracture. “Second look” reading of PMCT did not highlight the fracture but revealed a thin hematoma of the right occipital subcutaneous soft tissue (white arrow). This false negative PMCT was attributed to spatial resolution limits.
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Table 1 Agreement between autopsy and PMCT in the detection of post traumatic head lesions. Types of lesions Fracture
Hemorrhage
Cranial vault Skull base Facial bones Atlas/axis Epidural hematoma Subdural hematoma Subarachnoid hemorrhage Intraventricular hemorrhage Intra-axial hemorrhage
Detected by autopsy only
Detected by PMCT only
Detected by both techniques
Total
1 0 0 0 3 1 6 0 4
0 0 4 6 0 3 5 25 6
30 27 24 2 0 10 25 1 14
31 27 28 8 3 14 36 26 24
0.97 1 0.88 0.37 0 0.80 0.69 0.05 0.65
0.95
0.75
Fig. 2. 76-year-old man deceased from a deep traumatic maxillofacial hemorrhage caused by a firearm projectile. At PMCT (a), fracture/sinking in of the lateral wall of the right maxillary sinus (white arrow) and low-density projectiles (“Gomm Cogne”, red arrows). The facial skeleton fracture was not found during the autopsy (b) due to the vast hematoma.
3 physical abuses, 2 bladed weapons, 2 collapsed building, one traffic accident). In 7 (16%) head trauma cases, head trauma was not considered the direct cause of death (5 collapsed building, one traffic accident, one fall). The remaining 29 cases (40%) without head trauma were considered controls (21 bullet wounds, 6 natural deaths [all children], one diving accident, one blood loss from a circumcision). The mean (SD) time between the declaration of death and the CT scan was 2.5 (3.0) days [range: 0–13 days]. The time between the CT scan and the autopsy was 1.1 (1.3) day [range: 0–6 days]. Agreement between PMCT and autopsy in the detection of traumatic head injury Table 1 displays the number of cases of fractures and intracranial hemorrhages detected on PMCT and observed at autopsy, and associated kappa values.
Fractures, projectiles and pneumocephalus For fractures, agreement between PMCT and autopsy was almost perfect ( = 0.95). More specifically, for cranial vault fractures ( = 0.97), there was only one case where the fracture was observed at autopsy but not detected on PMCT (Fig. 1). Agreement was perfect for basilar fractures ( = 1.00), almost perfect for fractures of the facial skeleton ( = 0.88) with 4 facial skeleton fractures detected on PMCT but not at autopsy (Fig. 2), and fair for fractures of the upper cervical spine ( = 0.37) (Fig. 3). Agreement was perfect for the 9 projectiles cases (Fig. 4). Pneumocephalus was noted in 47 cases (64%) in the PMCT, but never mentioned in the autopsy reports. It was present in 100% of cases with basilar skull fractures and in 94% of cases with fractures of the cranial vault (Fig. 3).
Intracranial hemorrhage Agreement was substantial in showing intracranial hemorrhage ( = 0.75). Of note, out of the 4 false negative cases, 3 were part of
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Fig. 3. 54-year-old man deceased from a traumatic head injury caused by a firearm. Facial skeleton (white arrows) and cervical spine (red arrows) fractures found at PMCT (a-d), not described in the autopsy report. Compound fracture of the cranial vault with pneumocephalus (white asterisks) and right-sided brain herniation (red asterisk, dilaceration of the brain at autopsy).
the 8 first cases who did not receive a separate dedicated head CT, and agreement was almost perfect ( = 0.82) after exclusion of these 8 PMCT. There was a total lack of agreement for epidural hematomas (Fig. 5), an almost perfect agreement ( = 0.80) for subdural hematomas (Figs. 1,5,6), a substantial agreement ( = 0.69) for subarachnoid hemorrhages (Figs. 1, 4–6), a slight agreement for intraventricular hemorrhages ( = 0.05) with only one case mentioned in the autopsy report against 26 cases at PMCT (Fig. 4), and a substantial agreement ( = 0.65) for contusions and shear injuries (Fig. 5). Discussion Our study confirmed that PMCT is superior to autopsy in the detection of fractures of the facial skeleton and upper cervical spine, intraventricular hemorrhage and pneumocephalus (indiscernible during autopsy). These results are consistent with a recent review on traumatic deaths [11], which concluded that “in cases where
conventional autopsy is performed, PMCT can function as an important adjunct that detects many additional injuries,” and that “in situations where conventional autopsy is rejected or unavailable, PMCT is an adequate alternative that detects most injuries.” Like the authors of this study, we recommend the implementation of PMCT in routine postmortem investigations of trauma victims. For the present study, instead of computing the sensitivity and specificity of PMCT compared to autopsy as the gold standard, we studied the agreement in detecting traumatic head injuries among the two techniques. Autopsy revealed lesions missed on PMCT, and conversely PMCT demonstrated lesions that were not observed during autopsy. Part of the reasons why PMCT detected lesions missed on autopsy was because some anatomical locations are not routinely dissected or specialized manoeuvres are not routinely performed [7,15]. For instance, facial fractures can be overlooked at autopsy (even with resection of the facial mask) but are easily visible at PMCT [11]. While some authors advocate the combination of PMCT/autopsy should serve as the gold standard for determin-
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Fig. 4. . Death from a cranioencephalic wound caused by a firearm projectile. PMCT (a-c) and autopsy (d,e). The 8-mm occipital projectile (f, white arrows) with right-sided supraorbital entry hole (black arrow). PMCT shows a subarachnoid (red arrows) and intraventricular (green arrow) hemorrhage, not confirmed at autopsy since the brain was placed in formaldehyde and the dissection was done later.
ing cause of death [10], others maintain that both methods carry a substantial false positive rate [15]. Strength of our study was the standardized reading of the PMCT by a neuroradiologist experienced in forensic PMCT. Specialized forensic training is recommended for radiologists interpreting PMCT [2]. A dead body exhibits hypostasis and decomposition [17,18]. In the intracranial region, signs of cerebral edema, putrefaction (intravascular/pericerebral air) [19] and hypostasis (vascular hyperdensities, fluid levels in the venous sinuses) are common features. Knowledge of these PMCT signs is important to avoid false positive reporting of injuries. As for antemortem CT, there are well known pitfalls for the diagnosis of subarachnoid hemorrhage on PMCT [20]. Awareness of artifacts related to the method of preservation, such as the “freezing effect” [21] (frozen tissue exhibiting a lower density than non-frozen tissue), is also important. Regarding PMCT acquisition, our findings strongly support the acquisition of a separate skull and neck CT with a smaller field of view and higher mAs compared to the body CT. Using parameters of body CT for scanning the head may lead to false negative findings. Since thin extra-axial hemorrhagic collections are a well documented cause of PMCT false negatives [2,11,13], some studies support the use of high resolution head CT to detect small-sized lesions [2,14]. Also in our dataset we found 3 cases of small epidu-
ral hematomas (few millimeters thickness) detected at autopsy but missed on PMCT. Even though these small hemorrhages are clinically less important, they can be critical in medicolegal investigations [11]. Nevertheless, there is always a possibility that some discrepancies arise from additional trauma while transporting the corps from the CT scan to the autopsy room [2,13]. Our study has limitations. First, its retrospective nature did not allow for the most accurate correlation between PMCT and autopsy (number of fractures, hemorrhage size). Second, autopsies were performed with knowledge of the initial PMCT results, which may have led to extra injuries found at autopsy [11]. Third, the assessment of post-traumatic lesions at autopsies was not performed in a standardized manner. Fourth, when brain damage was found upon macroscopic examination, the brain was not cut but placed in formaldehyde and stored for later anatomical pathology analysis (in all but one case). In those cases, as pathology reports were not available, the lack of agreement – notably for intraventricular hemorrhage – was due to the organization of medicolegal investigations and not to the ability of autopsy to confirm the existence of such an injury. Other potential limitations were that subcutaneous soft tissues were not systematically assessed and 3D Volume Rendering was not systematically obtained. Finally, we mixed paediatric and adult populations, since it reflects real life practice in forensic departments.
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Fig. 5. Man deceased abroad two weeks earlier from head trauma from a bladed weapon who underwent preservation measures (pronounced formolization of the brain). At autopsy (a,b): multiple fractures, layers of extradural hemorrhage (white arrows), diffuse subarachnoid hemorrhage (red arrows), right temporal cortical contusions, cerebral edema with cerebellar herniation. At PMCT (c-e): subarachnoid hemorrhage (red arrows), right temporal contusions (green arrow), cerebral edema with cerebellar herniation (blue arrow); the extradural hemorrhage is not displayed, but a hyperdense subdural hematoma of the tentorium cerebelli (yellow arrows) is clearly visible; pneumocephalus may also be noted, along with deep hypodensities (orange arrows) related to the method of preservation (“freezing effect”).
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Fig. 6. PMCT of a 4-month-old shaken baby showing a subdural hematoma (white arrows) and a subarachnoid hemorrhage (red arrow), confirmed at autopsy.
Conclusion This study showed good agreement of PMCT and autopsy in detecting fractures and intracranial hemorrhage in cases of traumatic head trauma. PMCT detected most injuries found at autopsy, but was superior to autopsy in detecting facial skeleton and upper cervical spine fractures, as well as in detecting intraventricular hemorrhage. We confirm that PMCT is an important adjunct prior to autopsy, that could also serve as an adequate alternative when autopsy is rejected or unavailable. Disclosure of interest The authors declare that they have no competing interest. Acknowledgments We would like to thank the team of forensic pathologists from the Paris Forensics Institute, and the teams of radiographers and radiologists from Sainte-Anne Hospital. References [1] Davanzo JR, Sieg EP, Timmons SD. Management of Traumatic Brain Injury. Surg Clin North Am 2017;97:1237–53. [2] Yen K, Lovblad KO, Scheurer E, Ozdoba C, Thali MJ, Aghayev E, et al. Post-mortem forensic neuroimaging: correlation of MSCT and MRI findings with autopsy results. Forensic Sci Int 2007;173:21–35. [3] Shojania KG, Burton EC. The vanishing nonforensic autopsy. N Engl J Med 2008;358:873–5. [4] Thali MJ, Yen K, Schweitzer W, Vock P, Boesch C, Ozdoba C, et al. Virtopsy, a new imaging horizon in forensic pathology: virtual autopsy by postmortem multislice computed tomography (MSCT) and magnetic resonance imaging (MRI)–a feasibility study. J Forensic Sci 2003;48:386–403. [5] Deloire L, Diallo I, Cadieu R, Auffret M, Alavi Z, Ognard J, et al. Post-mortem Xray computed tomography (PMCT) identification using ante-mortem CT-scan of the sphenoid sinus. J Neuroradiol 2018. [6] Roberts IS, Benamore RE, Benbow EW, Lee SH, Harris JN, Jackson A, et al. Postmortem imaging as an alternative to autopsy in the diagnosis of adult deaths: a validation study. Lancet 2012;379:136–42.
[7] Le Blanc-Louvry I, Thureau S, Duval C, Papin-Lefebvre F, Thiebot J, Dacher JN, et al. Post-mortem computed tomography compared to forensic autopsy findings: a French experience. Eur Radiol 2013;23:1829–35. [8] Oehmichen M, Gehl HB, Meissner C, Petersen D, Hoche W, Gerling I, et al. Forensic pathological aspects of postmortem imaging of gunshot injury to the head: documentation and biometric data. Acta Neuropathol 2003;105:570–80. [9] Lin MJ, Barry N, Akusoba I, Hon HH, Cohen MS, Shukla P, et al. Traditional autopsy versus computed tomography imaging autopsy in trauma: A case of s¨ ynergistic disagreement¨. Surgery 2016;160:211–9. [10] Scholing M, Saltzherr TP, Fung Kon Jin PH, Ponsen KJ, Reitsma JB, Lameris JS, et al. The value of postmortem computed tomography as an alternative for autopsy in trauma victims: a systematic review. Eur Radiol 2009;19:2333–41. [11] Jalalzadeh H, Giannakopoulos GF, Berger FH, Fronczek J, van de Goot FRW, Reijnders UJ, et al. Post-mortem imaging compared with autopsy in trauma victims – a systematic review. Forensic Sci Int 2015;257:29–48. [12] Schmitt-Sody M, Kurz S, Reiser M, Kanz KG, Kirchhoff C, Peschel O, et al. Analysis of death in major trauma: value of prompt post mortem computed tomography (pmCT) in comparison to office hour autopsy. Scand J Trauma Resusc Emerg Med 2016;24:38. [13] Anon J, Remonda L, Spreng A, Scheurer E, Schroth G, Boesch C, et al. Traumatic extra-axial hemorrhage: correlation of postmortem MSCT, MRI, and forensicpathological findings. J Magn Reson Imaging 2008;28:823–36. [14] Jacobsen C, Bech BH, Lynnerup N. A comparative study of cranial, blunt trauma fractures as seen at medicolegal autopsy and by computed tomography. BMC Med Imaging 2009;9:18. [15] Graziani G, Tal S, Adelman A, Kugel C, Bdolah-Abram T, Krispin A. Usefulness of unenhanced post mortem computed tomography – findings in postmortem non-contrast computed tomography of the head, neck and spine compared to traditional medicolegal autopsy. J Forensic Leg Med 2018;55:105–11. [16] Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics 1977;33:159–74. [17] Smith AB, Lattin Jr GE, Berran P, Harcke HT. Common and expected postmortem CT observations involving the brain: mimics of antemortem pathology. AJNR Am J Neuroradiol 2012;33:1387–91. [18] Ishida M, Gonoi W, Okuma H, Shirota G, Shintani Y, Abe H, et al. Common postmortem computed tomography findings following atraumatic death: differentiation between normal postmortem changes and pathologic lesions. Korean J Radiol 2015;16:798–809. [19] Dedouit F, Otal P, Costagliola R, Loubes Lacroix F, Telmon N, Rouge D, et al. Role of modern cross-sectional imaging in thanatology: a pictorial essay. J Radiol 2006;87:619–38. [20] Shirota G, Gonoi W, Ikemura M, Ishida M, Shintani Y, Abe H, et al. The pseudoSAH sign: an imaging pitfall in postmortem computed tomography. Int J Legal Med 2017;131:1647–53. [21] Sugimoto M, Hyodoh H, Rokukawa M, Kanazawa A, Murakami R, Shimizu J, et al. Freezing effect on brain density in postmortem CT. Leg Med (Tokyo) 2016;18:62–5.
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Original Article
Comparison between postmortem computed tomography and autopsy in the detection of traumatic head injuries L. Legrand a,b,c,∗ , T. Delabarde b,d,e , R. Souillard-Scemama a,b , I. Sec b,d,f , I. Plu b,d,g , J-M. Laborie b,d,f , Y. Delannoy b,d,h , L. Hamza b,d,i , M. Taccoen b,d , L. de Jong a,b,c , J. Benzakoun a,b,c , M. Edjlali a,b,c , J-F. Méder a,b,c , C. Oppenheim a,b,c , B. Ludes b,d,e a
Service d’imagerie morphologique et fonctionnelle, centre hospitalier Sainte-Anne, 1 rue Cabanis, 75014 Paris, France Pôle universitaire d’imagerie post-mortem, Université Paris Descartes, 12, rue de l’Ecole de Médecine, 75006 Paris, France c INSERM UMR 1266, Institut de Psychiatrie et Neurosciences de Paris, 102-108 rue de la Santé, 75014 Paris, France d Institut médico-légal de Paris, 2, place Mazas, 75012 Paris, France e CNRS UMR 5288 Institut National de la transfusion sanguine, 6, rue Cabanel, 75015 Paris, France f Unité médico-judiciaire, Hôtel-Dieu, 1, place du Parvis de Notre-Dame, 75004 Paris, France g Sorbonne Université, 91, boulevard de l’Hôpital, 75013 Paris, France h Institut médico-légal de Lille, rue André Verhaeghe, 59000 Lille, France i Service d’accueil des urgences, hôpital Avicenne, 125, rue de Stalingrad, 93000 Bobigny, France b
a r t i c l e
i n f o
Article history: Available online xxx Keywords: Postmortem computed tomography Autopsy Traumatic head injuries Hemorrhage Fracture
a b s t r a c t Introduction. – The aim of this study was to assess the agreement between postmortem computed tomography (PMCT) and autopsy in detecting traumatic head injuries. Materials and Methods. – Consecutive cases of death that underwent both unenhanced PMCT and conventional autopsy were collected from our institution database during a period of 3 years and reviewed retrospectively. PMCT images were reviewed for the presence of fractures (cranial vault, skull base, facial bones and atlas/axis) and intracranial hemorrhage. Kappa values were calculated to determine the agreement between PMCT and autopsy reports. Results. – 73 cases were included, of which 44 (60%) had head trauma. Agreement between PMCT and autopsy was almost perfect ( = 0.95) for fractures and substantial ( = 0.75) for intracranial hemorrhage. PMCT was superior to autopsy in detecting facial bone and upper cervical spine fractures, and intraventricular hemorrhage. However, in some cases thin extra-axial blood collections were missed on PMCT. Conclusions. – The agreement between PMCT and autopsy in detecting traumatic head injuries was good. Using a combination of both techniques increases the quality of postmortem evaluation because more lesions are detected. © 2019 Elsevier Masson SAS. All rights reserved.
Introduction CT MRI PMCT
computed tomography magnetic resonance imaging postmortem computed tomography
∗ Corresponding author at: Service d’imagerie morphologique et fonctionnelle, centre hospitalier Sainte-Anne, 1 rue Cabanis, 75014 Paris, France. E-mail address: [email protected] (L. Legrand).
Traumatic head injuries are a leading cause of death [1], responsible for approximatively 50,000 deaths each year in the United States. The main etiologies are accidents (e.g. traffic, sports, work and domestic accidents, falls) and aggressions (e.g. physical abuse of children, injuries from bladed weapons or firearms in young adults) [2]. Autopsy is the gold standard for postmortem evaluation of traumatic head injuries, but it is invasive, operator-dependent and irreversible. Secondary analyses are rarely performed, as they can never be as efficient as the first one. Whereas the number of autopsies has decreased in recent years [3], mainly for budget-related reasons, the use of post-mortem imaging (computed tomography [CT] and magnetic resonance imaging [MRI])
https://doi.org/10.1016/j.neurad.2019.03.008 0150-9861/© 2019 Elsevier Masson SAS. All rights reserved.
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has increased [4]. Advantages of post-mortem CT (PMCT) scanning are: • its fast acquisition (< 15 minutes for a full-body scan); • its non-invasive character, preserving the integrity of the corpse and traces of evidence; • the digital data storage allowing easy secondary and remote readings; • the provision of details on lesion location to guide autopsy; • the possibility to produce “non-gruesome evidence” to display in court. Furthermore, besides searching for the cause of death, PMCT can also be used for identification purpose [5], notably in cases of mass disaster. Studies that compared the performance of post-mortem imaging to that of autopsy have mainly focused on the reliability of CT and/or MRI scanning to identify the cause of death [6,7]. When exploring trauma caused by firearms, PMCT can provide valuable additional information on localization of projectiles, entry and exit points, and ballistic trajectory [8]. While some PMCT-autopsy correlation studies have been performed for full-body trauma [9–12], others have focused on the cranial region [2,8,13–15], with PMCT being read by radiologists [2,13,15] or by forensic pathologists [14]. These studies showed that PMCT is superior to autopsy in detecting pneumocephalus, intraventricular hemorrhages and facial skeleton fractures [2], but that the detection of small hemorrhagic injuries [2,13,15] and injuries of the skull base [2,8], especially fractures of the anterior and middle cranial fossa [14], are part of its main limitations. The literature of PMCT-autopsy correlation studies is limited, varies considerably in terms of methodologies, and most studies have a small sample size. The seminal forensic PMCT-autopsy correlation study (n = 57) was based on a 4-detector row scanner [2], which is no longer in use in most institutions. A recent larger study (n = 203) reviewing autopsy and PMCT reports did use up-todate 64- or 256-detector row scanners [15], but the PMCT reading lacked a standardized protocol and therefore may have overlooked more subtle signs of trauma. The aim of this retrospective correlation study was to (re-)examen the benefits and limitations of 64-detector PMCT imaging compared to autopsy. Cranial PMCT was reviewed in a standardized way by a neuroradiologist trained in post-mortem imaging and performance in the detection of traumatic head injuries was compared to that of autopsy. Materials and methods Study population For this study we included all deceased cases who underwent PMCT scanning at Sainte-Anne Hospital and autopsy at the Paris Forensics Institute between May 2014 and January 2017 (n = 105). We excluded cases with only an external examination instead of a complete autopsy (n = 27), cases for which no autopsy report was available (n = 4) and one case with a mummified cranial and cervical region. Our final dataset included 73 cases of which 58 were men and 15 women with a mean age of 34 years (SD 22) [range: 24 days old-86 years old]).
enclosed in body bags for reasons of hygiene and to respect their anonymity. The protocol included anteroposterior and lateral scout views, two main spiral scans (one focused on the head and neck, and another focused on the chest, abdomen, pelvis and limbs), and supplemental spiral scans for the limbs if required. The following parameters were used for the head and neck spiral scan: 120 kV, 250 mA (dose modulation), 0.8 s/rotation, pitch of 0.531, beam collimation 0.625 × 64, slice thickness 1.25 mm, field of view 32 cm. Of note, the first 8 corpses in the series received a single spiral scan from the head to the pelvis, and thus had a larger field of view and lower radiation dose at the level of head compared to the rest of the sample. Data were transferred onto a GE Advantage Windows post-treatment workstation (version 4.6) for multiplanar and 3D Volume Rendering reconstructions. Images were reconstructed with soft tissue and bone algorithms. Autopsy Prior to autopsy, a pre-report of the PMCT was transmitted by the radiologist to the forensic pathologist. Autopsy started with an external examination, performed by one of 12 forensic pathologists. Subsequently, the cranium was opened and the brain was removed. When brain damage was apparent upon macroscopic examination, the brain was not further dissected but placed in a formaldehyde solution for potential future anatomical pathology examination. If no external brain damage was found, one or more sections were performed. Analysis of data PMCT A neuroradiologist with 3 years of experience in post-mortem imaging (LL) and blinded to the autopsy results, reviewed all PMCT scans of the head and neck regions. Following a standardized reading protocol, the presence or absence of fracture(s) (cranial vault, base of the skull, facial skeleton, cervical vertebrae C1/C2), pneumocephalus, projectile(s) and intracranial hemorrhage (extra-axial [epidural and subdural hematomas, subarachnoid and intraventricular hemorrhage] or intraparenchymal [contusions or shear/diffuse axonal injuries]) were reported. The number/type of fractures and hemorrhage size as well as their precise localization were not systematically reported. In complex cases (n < 10), the PMCT was reviewed by two neuroradiologists (LL and JFM). Targeted rereading was carried out whenever an abnormality observed at autopsy had not been detected during the first PMCT reading, in order to understand potential causes for false negative at PMCT. These rereadings were not included in the statistical analyses. Autopsy The autopsy reports were reread by the neuroradiologist using the same reading grid used for PMCT. Also, cause of death was extracted from the autopsy reports. Statistical analyses For each item of the structured report, kappa values were calculated to determine the agreement between the PMCT and autopsy [16]. Results
Technique Population PMCT CT scanning was performed at the request of law enforcement authorities. Corpses were scanned using a 64-detector CT scanner (GE Lightspeed, General Electric Systems, Milwaukee, WI, USA),
Of the total study population (n = 73), 44 (60%) had head trauma. In 37 (84%) head trauma cases, the pathologist considered the head trauma the direct cause of death (24 bullet wounds, 5 falls,
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Fig. 1. Suspected physical abuse involving a two-year-old child. At autopsy (a-c): linear fracture to the right side of the occipital bone (a,b), right-sided subdural and subarachnoid hemorrhage (c). PMCT (d-g) displays a discrete subarachnoid and subdural hemorrhage (red arrow) but no fracture. “Second look” reading of PMCT did not highlight the fracture but revealed a thin hematoma of the right occipital subcutaneous soft tissue (white arrow). This false negative PMCT was attributed to spatial resolution limits.
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Table 1 Agreement between autopsy and PMCT in the detection of post traumatic head lesions. Types of lesions Fracture
Hemorrhage
Cranial vault Skull base Facial bones Atlas/axis Epidural hematoma Subdural hematoma Subarachnoid hemorrhage Intraventricular hemorrhage Intra-axial hemorrhage
Detected by autopsy only
Detected by PMCT only
Detected by both techniques
Total
1 0 0 0 3 1 6 0 4
0 0 4 6 0 3 5 25 6
30 27 24 2 0 10 25 1 14
31 27 28 8 3 14 36 26 24
0.97 1 0.88 0.37 0 0.80 0.69 0.05 0.65
0.95
0.75
Fig. 2. 76-year-old man deceased from a deep traumatic maxillofacial hemorrhage caused by a firearm projectile. At PMCT (a), fracture/sinking in of the lateral wall of the right maxillary sinus (white arrow) and low-density projectiles (“Gomm Cogne”, red arrows). The facial skeleton fracture was not found during the autopsy (b) due to the vast hematoma.
3 physical abuses, 2 bladed weapons, 2 collapsed building, one traffic accident). In 7 (16%) head trauma cases, head trauma was not considered the direct cause of death (5 collapsed building, one traffic accident, one fall). The remaining 29 cases (40%) without head trauma were considered controls (21 bullet wounds, 6 natural deaths [all children], one diving accident, one blood loss from a circumcision). The mean (SD) time between the declaration of death and the CT scan was 2.5 (3.0) days [range: 0–13 days]. The time between the CT scan and the autopsy was 1.1 (1.3) day [range: 0–6 days]. Agreement between PMCT and autopsy in the detection of traumatic head injury Table 1 displays the number of cases of fractures and intracranial hemorrhages detected on PMCT and observed at autopsy, and associated kappa values.
Fractures, projectiles and pneumocephalus For fractures, agreement between PMCT and autopsy was almost perfect ( = 0.95). More specifically, for cranial vault fractures ( = 0.97), there was only one case where the fracture was observed at autopsy but not detected on PMCT (Fig. 1). Agreement was perfect for basilar fractures ( = 1.00), almost perfect for fractures of the facial skeleton ( = 0.88) with 4 facial skeleton fractures detected on PMCT but not at autopsy (Fig. 2), and fair for fractures of the upper cervical spine ( = 0.37) (Fig. 3). Agreement was perfect for the 9 projectiles cases (Fig. 4). Pneumocephalus was noted in 47 cases (64%) in the PMCT, but never mentioned in the autopsy reports. It was present in 100% of cases with basilar skull fractures and in 94% of cases with fractures of the cranial vault (Fig. 3).
Intracranial hemorrhage Agreement was substantial in showing intracranial hemorrhage ( = 0.75). Of note, out of the 4 false negative cases, 3 were part of
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Fig. 3. 54-year-old man deceased from a traumatic head injury caused by a firearm. Facial skeleton (white arrows) and cervical spine (red arrows) fractures found at PMCT (a-d), not described in the autopsy report. Compound fracture of the cranial vault with pneumocephalus (white asterisks) and right-sided brain herniation (red asterisk, dilaceration of the brain at autopsy).
the 8 first cases who did not receive a separate dedicated head CT, and agreement was almost perfect ( = 0.82) after exclusion of these 8 PMCT. There was a total lack of agreement for epidural hematomas (Fig. 5), an almost perfect agreement ( = 0.80) for subdural hematomas (Figs. 1,5,6), a substantial agreement ( = 0.69) for subarachnoid hemorrhages (Figs. 1, 4–6), a slight agreement for intraventricular hemorrhages ( = 0.05) with only one case mentioned in the autopsy report against 26 cases at PMCT (Fig. 4), and a substantial agreement ( = 0.65) for contusions and shear injuries (Fig. 5). Discussion Our study confirmed that PMCT is superior to autopsy in the detection of fractures of the facial skeleton and upper cervical spine, intraventricular hemorrhage and pneumocephalus (indiscernible during autopsy). These results are consistent with a recent review on traumatic deaths [11], which concluded that “in cases where
conventional autopsy is performed, PMCT can function as an important adjunct that detects many additional injuries,” and that “in situations where conventional autopsy is rejected or unavailable, PMCT is an adequate alternative that detects most injuries.” Like the authors of this study, we recommend the implementation of PMCT in routine postmortem investigations of trauma victims. For the present study, instead of computing the sensitivity and specificity of PMCT compared to autopsy as the gold standard, we studied the agreement in detecting traumatic head injuries among the two techniques. Autopsy revealed lesions missed on PMCT, and conversely PMCT demonstrated lesions that were not observed during autopsy. Part of the reasons why PMCT detected lesions missed on autopsy was because some anatomical locations are not routinely dissected or specialized manoeuvres are not routinely performed [7,15]. For instance, facial fractures can be overlooked at autopsy (even with resection of the facial mask) but are easily visible at PMCT [11]. While some authors advocate the combination of PMCT/autopsy should serve as the gold standard for determin-
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Fig. 4. . Death from a cranioencephalic wound caused by a firearm projectile. PMCT (a-c) and autopsy (d,e). The 8-mm occipital projectile (f, white arrows) with right-sided supraorbital entry hole (black arrow). PMCT shows a subarachnoid (red arrows) and intraventricular (green arrow) hemorrhage, not confirmed at autopsy since the brain was placed in formaldehyde and the dissection was done later.
ing cause of death [10], others maintain that both methods carry a substantial false positive rate [15]. Strength of our study was the standardized reading of the PMCT by a neuroradiologist experienced in forensic PMCT. Specialized forensic training is recommended for radiologists interpreting PMCT [2]. A dead body exhibits hypostasis and decomposition [17,18]. In the intracranial region, signs of cerebral edema, putrefaction (intravascular/pericerebral air) [19] and hypostasis (vascular hyperdensities, fluid levels in the venous sinuses) are common features. Knowledge of these PMCT signs is important to avoid false positive reporting of injuries. As for antemortem CT, there are well known pitfalls for the diagnosis of subarachnoid hemorrhage on PMCT [20]. Awareness of artifacts related to the method of preservation, such as the “freezing effect” [21] (frozen tissue exhibiting a lower density than non-frozen tissue), is also important. Regarding PMCT acquisition, our findings strongly support the acquisition of a separate skull and neck CT with a smaller field of view and higher mAs compared to the body CT. Using parameters of body CT for scanning the head may lead to false negative findings. Since thin extra-axial hemorrhagic collections are a well documented cause of PMCT false negatives [2,11,13], some studies support the use of high resolution head CT to detect small-sized lesions [2,14]. Also in our dataset we found 3 cases of small epidu-
ral hematomas (few millimeters thickness) detected at autopsy but missed on PMCT. Even though these small hemorrhages are clinically less important, they can be critical in medicolegal investigations [11]. Nevertheless, there is always a possibility that some discrepancies arise from additional trauma while transporting the corps from the CT scan to the autopsy room [2,13]. Our study has limitations. First, its retrospective nature did not allow for the most accurate correlation between PMCT and autopsy (number of fractures, hemorrhage size). Second, autopsies were performed with knowledge of the initial PMCT results, which may have led to extra injuries found at autopsy [11]. Third, the assessment of post-traumatic lesions at autopsies was not performed in a standardized manner. Fourth, when brain damage was found upon macroscopic examination, the brain was not cut but placed in formaldehyde and stored for later anatomical pathology analysis (in all but one case). In those cases, as pathology reports were not available, the lack of agreement – notably for intraventricular hemorrhage – was due to the organization of medicolegal investigations and not to the ability of autopsy to confirm the existence of such an injury. Other potential limitations were that subcutaneous soft tissues were not systematically assessed and 3D Volume Rendering was not systematically obtained. Finally, we mixed paediatric and adult populations, since it reflects real life practice in forensic departments.
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Fig. 5. Man deceased abroad two weeks earlier from head trauma from a bladed weapon who underwent preservation measures (pronounced formolization of the brain). At autopsy (a,b): multiple fractures, layers of extradural hemorrhage (white arrows), diffuse subarachnoid hemorrhage (red arrows), right temporal cortical contusions, cerebral edema with cerebellar herniation. At PMCT (c-e): subarachnoid hemorrhage (red arrows), right temporal contusions (green arrow), cerebral edema with cerebellar herniation (blue arrow); the extradural hemorrhage is not displayed, but a hyperdense subdural hematoma of the tentorium cerebelli (yellow arrows) is clearly visible; pneumocephalus may also be noted, along with deep hypodensities (orange arrows) related to the method of preservation (“freezing effect”).
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Fig. 6. PMCT of a 4-month-old shaken baby showing a subdural hematoma (white arrows) and a subarachnoid hemorrhage (red arrow), confirmed at autopsy.
Conclusion This study showed good agreement of PMCT and autopsy in detecting fractures and intracranial hemorrhage in cases of traumatic head trauma. PMCT detected most injuries found at autopsy, but was superior to autopsy in detecting facial skeleton and upper cervical spine fractures, as well as in detecting intraventricular hemorrhage. We confirm that PMCT is an important adjunct prior to autopsy, that could also serve as an adequate alternative when autopsy is rejected or unavailable. Disclosure of interest The authors declare that they have no competing interest. Acknowledgments We would like to thank the team of forensic pathologists from the Paris Forensics Institute, and the teams of radiographers and radiologists from Sainte-Anne Hospital. References [1] Davanzo JR, Sieg EP, Timmons SD. Management of Traumatic Brain Injury. Surg Clin North Am 2017;97:1237–53. [2] Yen K, Lovblad KO, Scheurer E, Ozdoba C, Thali MJ, Aghayev E, et al. Post-mortem forensic neuroimaging: correlation of MSCT and MRI findings with autopsy results. Forensic Sci Int 2007;173:21–35. [3] Shojania KG, Burton EC. The vanishing nonforensic autopsy. N Engl J Med 2008;358:873–5. [4] Thali MJ, Yen K, Schweitzer W, Vock P, Boesch C, Ozdoba C, et al. Virtopsy, a new imaging horizon in forensic pathology: virtual autopsy by postmortem multislice computed tomography (MSCT) and magnetic resonance imaging (MRI)–a feasibility study. J Forensic Sci 2003;48:386–403. [5] Deloire L, Diallo I, Cadieu R, Auffret M, Alavi Z, Ognard J, et al. Post-mortem Xray computed tomography (PMCT) identification using ante-mortem CT-scan of the sphenoid sinus. J Neuroradiol 2018. [6] Roberts IS, Benamore RE, Benbow EW, Lee SH, Harris JN, Jackson A, et al. Postmortem imaging as an alternative to autopsy in the diagnosis of adult deaths: a validation study. Lancet 2012;379:136–42.
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Please cite this article in press as: Legrand L, et al. Comparison between postmortem computed tomography and autopsy in the detection of traumatic head injuries. J Neuroradiol (2019), https://doi.org/10.1016/j.neurad.2019.03.008