European Journal of Radiology

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1 European Journal of Radiology 82 (2013) Contents lists available at SciVerse ScienceDirect European Journal of Radiology jo ur n al hom epage: Hypothermic death: Possibility of diagnosis by post-mortem computed tomography Yusuke Kawasumi a,, Naoki Onozuka a,1, Ayana Kakizaki a,1, Akihito Usui c,2, Yoshiyuki Hosokai c,1, Miho Sato a,2, Haruo Saito c,3, Tadashi Ishibashi a,4, Yoshie Hayashizaki b,5, Masato Funayama b,5 a Tohoku University Graduate School of Medicine, Department of Clinical Imaging, 2-1 Seiryo-machi, Aoba-ku, Sendai, Miyagi, , Japan b Tohoku University Graduate School of Medicine, Department of Forensic Medicine, 2-1 Seiryo-machi, Aoba-ku, Sendai, Miyagi, , Japan c Tohoku University Graduate School of Medicine, Department of Diagnostic Image Analysis, 2-1 Seiryo-machi, Aoba-ku, Sendai, Miyagi, , Japan a r t i c l e i n f o Article history: Received 20 September 2012 Accepted 8 November 2012 Keywords: Tomography Spiral computed Forensic medicine Autopsy Post-mortem changes Hypothermia a b s t r a c t Referring to our experience with post-mortem computed tomography (CT), many hypothermic death cases presented a lack of increase in lung-field concentration, blood clotting in the heart, thoracic aorta or pulmonary artery, and urine retention in the bladder. Thus we evaluated the diagnostic performance of post-mortem CT on hypothermic death based on the above-mentioned three findings. Twenty-four hypothermic death subjects and 53 non-hypothermic death subjects were examined. Two radiologists assessed the presence or lack of an increase in lung-field concentration, blood clotting in the heart, thoracic aorta or pulmonary artery, and measured urine volume in the bladder. Pearson s chi-square test and Mann Whitney U-test were used to assess the relationship between the three findings and hypothermic death. The sensitivity, specificity, accuracy, positive predictive value (PPV) and negative predictive value (NPV) of the diagnosis were also calculated. Lack of an increase in lung-field concentration and blood clotting in the heart, thoracic aorta or pulmonary artery were significantly associated with hypothermic death (p = , p < , respectively). The hypothermic death cases had significantly more urine in the bladder than the non-hypothermic death cases (p = ). Regarding the diagnostic performance with all three findings, the sensitivity was 29.2% but the specificity was 100%. These three findings were more common in hypothermic death cases. Although the sensitivity was low, these findings will assist forensic physicians in diagnosing hypothermic death since the specificity was high Elsevier Ireland Ltd. All rights reserved. 1. Introduction When a body is found on land in a cold environment, one of the most important forensic views is whether the cause of victim s death is hypothermia or not. Some autopsy findings have been noticed with increased regularity among hypothermia victims Abbreviations: CT, computed tomography; DICOM, digital imaging and communication in medicine; MDCT, multi-detector computed tomography; NPV, negative predictive value; PPV, positive predictive value. Corresponding author. Tel.: ; fax: addresses: ssu@rad.med.tohoku.ac.jp (Y. Kawasumi), t7402r0506@med.tohoku.ac.jp (A. Usui), hosokai@med.tohoku.ac.jp (Y. Hosokai), meifan58@m.tains.tohoku.ac.jp (M. Sato), hsaito@med.tohoku.ac.jp (H. Saito), tisibasi@med.tohoku.ac.jp (T. Ishibashi), yoshie@forensic.med.tohoku.ac.jp (Y. Hayashizaki), funayama@forensic.med.tohoku.ac.jp (M. Funayama). 1 Tel.: ; fax: Tel.: ; fax: Tel.: ; fax: Tel.: ; fax: Tel.: ; fax: and they are haemorrhagic gastric erosions (Wischnewsky spots), cherry red pink of hypostatic lividity, the difference of the colour of the blood from the right and left ventricle [1 3]. However, these findings have been treated not as diagnostic but as just supportive, and the role of autopsy is to rule out other causes of death. The use of post-mortem computed tomography (CT) is becoming increasingly common and has an important role in forensic medicine [3 8]. At our institution, a post-mortem CT before forensic autopsy has been performed since May, Approximately 250 cases have been subjected to post-mortem CT, and nearly 10% of these were hypothermic death. On the post-mortem CT images, detecting the findings described as positive for hypothermic death on autopsy was nearly impossible because they are minimal or microscopic [3]. Conversely, we have observed that a number of hypothermic death cases presented the following three characteristic findings: (1) lack of increase in concentration of lung fields, (2) blood clotting in the heart, thoracic aorta or pulmonary artery, and (3) urine retention in the bladder. The CT s diagnostic performance for hypothermic death was evaluated according to these three findings X/$ see front matter 2012 Elsevier Ireland Ltd. All rights reserved.

2 362 Y. Kawasumi et al. / European Journal of Radiology 82 (2013) Materials and methods This retrospective study was approved by the ethics board of our institution. Informed consent was not required for this study, which involved a review of previously obtained image data Study cases At our institution, 250 subjects had undergone post-mortem CT and a forensic autopsy between May, 2009 and May, Each subject s cause of death was confirmed by autopsy. Twenty-four of the 250 subjects died from hypothermia (12 males and 12 females, average age 63.9 years). As controls, 60 subjects were chosen at random from the remaining 226, and several questionable subjects (e.g., a case with a poorly-defined bladder, and an infant) were excluded. Finally, the control group consisted of 53 subjects (38 males and 15 females, average age 59.6 years). The causes of death in the non-hypothermia cases included drowning (n = 13), trauma (n = 12), cardiovascular failure (n = 6), asphyxia (n = 5), burning including carbon monoxide intoxication (n = 5), ischaemic heart disease (n = 5), chemical addiction (n = 4), and other (n = 3). The interval between death and CT was approximately 2 days Computed tomography and autopsy An eight-channel multi-detector row CT (MDCT) scanner (Aquilion 8; Toshiba Medical Systems, Tokyo, Japan) was used for all examinations. All subjects were scanned unclothed in a body bag. No contrast material was administered. In all cases, two CT scans were performed. First, the head was subjected to conventional CT; the tube voltage was 120 kvp and the tube current was changed arbitrarily based on the installed mode. The rotation time was 1.5 s per rotation. The collimations were 4.0 and 8.0 mm. The images were reconstructed at 4-mm slice thicknesses. The second scan was taken from the head to the pelvis in the helical mode; the tube voltage was 120 kvp and the tube current was changed arbitrarily based on the installed mode. The rotation time was 0.75 s per rotation. The table speed was 14 mm per rotation and the helical beam pitch was The reconstructed slice thickness of the images was 2 mm. In all cases, a conventional autopsy was performed shortly after forensic CT. All autopsies were performed by a forensic pathologist who had more than 30 years of experience in forensic autopsies, and his colleagues. After receiving the autopsy reports from the forensic physicians, we reviewed the CT images and discussed the agreement between the CT findings and autopsy results Image assessment All CT image data were sent to a digital imaging and communication in medicine (DICOM) server (POP-Net Server; ImageONE, Tokyo, Japan), which could be observed with a two-dimensional DICOM viewer (POP-Net Essential; ImageONE, Tokyo, Japan) and a three-dimensional DICOM workstation (Ziostation ver ; Ziosoft, Tokyo, Japan). Two radiologists retrospectively interpreted the CT images. One radiologist had 9 years of experience and the other more than 25 years of experience in general radiology, and an additional 1 2 years of experience in a subspecialty. The radiologists also had approximately 2 years of experience in interpreting postmortem forensic CT. They assessed the presence of an increase in lung-field concentration and blood clot in the heart, thoracic aorta or pulmonary artery. All determinations were arrived at by consensus. In each case, only the bladder was extracted as a threedimensional volume using a three-dimensional DICOM workstation (Ziostation ver ; Ziosoft, Tokyo, Japan). The volume of urine was calculated automatically Statistical analysis Pearson s chi-square test of independence was used to assess the relationship between hypothermic death and lack of increase in lung-field concentration or blood clotting in the heart, thoracic aorta or pulmonary artery. The sensitivity, specificity, accuracy, positive predictive value (PPV) and negative predictive value (NPV) of the diagnosis of hypothermic death were also calculated to evaluate the diagnostic performance of hypothermic death on postmortem CT scans. The difference in the urine volume in the bladder between the hypothermic and the non-hypothermic death cases was evaluated using the Mann Whitney U-test. A cut-off value was determined, and the sensitivity, specificity, accuracy, PPV and NPV of the hypothermic death diagnosis were calculated. Additionally, the sensitivity, specificity, accuracy, PPV and NPV of the hypothermic death diagnosis were calculated in the presence of all three findings. 3. Results 3.1. Lack of an increase in lung field concentration Eleven of 24 hypothermic death cases had no increase in lungfield concentration. In contrast, 5 of 53 non-hypothermic death cases had no increase in lung-field concentration. Pearson s chisquare test demonstrated that a lack of increase in lung-field concentration was significantly associated with hypothermic death (p = ). The sensitivity of the hypothermic death diagnosis was 45.8%, specificity 90.6%, accuracy 76.6%, PPV 68.8%, and NPV 78.7% Blood clotting in the heart, thoracic aorta or pulmonary artery Blood clotting in the heart, thoracic aorta or pulmonary artery was found in 15 of 24 hypothermic death cases, and in 8 of 53 nonhypothermic death cases. Pearson s chi-square test demonstrated that blood clotting was significantly associated with hypothermic death (p < ). The sensitivity of the hypothermic death diagnosis was 62.5%, specificity 84.9%, accuracy 77.9%, PPV 65.2%, and NPV 83.3% Urine retention in the bladder The average amount of urine retention in the bladders of the hypothermic death cases was ml ( ml), while the amount of the non-hypothermic death cases was 92.9 ml ( ml). The Mann Whitney U-test showed that the hypothermic death cases retained significantly more urine in the bladder than the non-hypothermic death cases (p = ). When the cut-off value was set at 67.1 ml, 18 of 24 hypothermic death cases and 12 of 53 non-hypothermic death cases were positive. Subsequently, the sensitivity of the hypothermic death diagnosis was 75.0%, specificity 77.4%, accuracy 77.6%, PPV 60.0%, and NPV 87.2% Diagnostic performance based on all three findings When positivity for hypothermic death was defined as the presence of all three findings, 7 of 24 hypothermic death cases were positive. In contrast, none of the non-hypothermic death cases were

3 Y. Kawasumi et al. / European Journal of Radiology 82 (2013) positive. Under these conditions, the sensitivity of the hypothermic death diagnosis was 29.2%, specificity 100%, accuracy 77.9%, PPV 100%, and NPV 75.7%. 4. Discussion This study showed that the lack of an increase in lung-field concentration, blood clotting in the heart, thoracic aorta or pulmonary artery and urine retention in the bladder were significantly more frequent in hypothermic death cases than in non-hypothermic death cases on post-mortem CT. Generally, the increase in lung-field concentration on postmortem CT was due to post-mortem hypostasis (Fig. 1a), pulmonary oedema (Fig. 1b), drowning, and other causes. In addition, Fig. 2. A case of death due to hypothermia. No increase in lung-field concentration was found. Fig. 1. (a) A typical case of post-mortem CT showing hypostasis in the lungs. The concentration increase was localised to the dorsal portion of the lungs (death was due to cervical trauma). (b) A typical case of post-mortem CT showing pulmonary oedema. Ground-glass opacity and thickened septum were found in the entire lung field (death was due to cardiovascular failure). forensic texts and reports describe that pulmonary oedema is commonly found in hypothermic death [1 3,9]. Clinical practices also report that hypothermia induces pulmonary congestion and oedema [10,11]. However, approximately half of our hypothermic death cases lacked an increased lung-field concentration (Fig. 2), which was rare in the non-hypothermic death cases. At autopsy, these lungs immediately shrank after thoracotomy incision (Fig. 3a), and the lungs and airways were not wet (Fig. 3b). The lack of an increase in lung-field concentration indicates dried lungs, presumably due to hypothermia. Therefore, dried lungs, but not pulmonary oedema, is a characteristic finding of hypothermic death. On post-mortem CT, the blood in the heart, thoracic aorta or pulmonary artery sometimes forms a fluid fluid level and on occasion, clots. The fluid fluid level is not coagulated and is the result of blood cell deposition (Fig. 4: death due to drowning). In forensic fields, it is well-known by experience that the fluidity of the blood maintains after acute deaths, while the clotting is presumed to be the result of a slow death, and clotting ability remaining functional until death. Almost all cases of death due to hypothermia at our institution showed clotted blood (Fig. 5). Hypothermia causes people to die slowly, thus this finding is consistent with hypothermic death. Many hypothermic death cases tend to retain a large amount of urine in the bladder, and in the present study the bladders were firm (Fig. 6). Although the reason for urine retention is not clearly understood, cold diuresis [9 12] has been suggested. Cold diuresis is one of the vital reactions that prevent the fall of body temperature. When a body is exposed to cold, peripheral vasoconstriction occurs to prevent peripheral heat loss. As a result, central blood flow increases, and subsequently, diuresis results. Since hypothermic death requires time, urine retention may occur during hypothermic death. In our experience, other causes of death, such as head trauma and drug addiction, sometimes had comparable quantities of urine in the bladder and will be a subject of a future investigation. In terms of diagnostic performance, the specificity of each finding was higher than the sensitivity. Furthermore, when all three findings were taken into consideration, sensitivity decreased

4 364 Y. Kawasumi et al. / European Journal of Radiology 82 (2013) Fig. 3. Autopsy findings of a case of death due to hypothermia. (a) The lungs shrank and were not wet. (b) The trachea and main bronchus were dry. Fig. 4. A case of death due to drowning. A fluid fluid level is formed in the heart (arrows). further; however, specificity increased to 100%, indicating that a case that has all three findings is likely a hypothermic death. However, the sensitivity was approximately 30%, thus allowing for an increase in the number of false-negative cases. Therefore, additional CT findings are required to improve the diagnosis of hypothermic death. This study included relatively few subjects; thus a larger-scale study is necessary to improve the reliability of the results. Fig. 5. A case of death due to hypothermia. Blood clotting was found in the heart, aorta and pulmonary artery (arrows).

5 Y. Kawasumi et al. / European Journal of Radiology 82 (2013) aid forensic physicians in diagnosing hypothermic death since the specificity was high. Acknowledgement The authors wish to thank Professor Funayama and his colleagues, whose comments and suggestions were valuable throughout this study. References Fig. 6. The bladder of a patient who died from hypothermia. The bladder retained a large quantity of urine and was firm. The English in this document has been checked by at least two professional editors, both native speakers of English. For a certificate, please see: 5. Conclusion On post-mortem CT, the lack of an increase in lung-field concentration, blood clotting in the heart, thoracic aorta or pulmonary artery, and urine retention in the bladder were found more frequently in the hypothermic death cases than the non-hypothermic death cases. Although the sensitivity was low, these findings will [1] Dolinak D, Matshes E, Lew E, editors. Forensic Pathology Principles and Practice. Amsterdam: Elsevier; [2] Tsokos M, editor. Forensic Pathology Reviews Volume 5. New York, USA: Humana Press; [3] Thali MJ, Dirnhofer R, Vock P, editors. The Virtopsy Approach. Boca Raton, USA: CRC Press; [4] Poulsen K, Simonsen J. Computed tomography in connection with medico-legal autopsies. Forensic Science International 2006;171: [5] Dirnhofer R, Fackowski C, Vock P, et al. VIRTOPSY: minimally invasive. Imagingguided virtual autopsy. RadioGraphics 2006;26: [6] Bolliger SA, Thali MJ, Ross S, et al. Virtual autopsy using imaging: bridging radiologic and forensic sciences. A review of the Virtopsy and similar projects. European Radiology 2008;18: [7] Christe A, Flach P, Ross S, et al. Clinical radiology and postmortem imaging (Virtopsy) are not the same: specific and unspecific postmortem signs. Legal Medicine 2010;12: [8] Usui A, Kawasumi Y, Hosokai Y, et al. Usefulness of postmortem computed tomography before forensic autopsy for alerting forensic personnel to tuberculosis infection. Japanese Journal of Radiology 2012, [9] Turk EE. Hypothermia. Forensic Science, Medicine, and Pathology 2010;6: [10] Paton BC. Accidental hypothermia. Pharmacology & Therapeutics 1983;22: [11] Danzl DF, Pozos RS. Accidental hypothermia. New England Journal of Medicine 1994;331(26): [12] Mikami H. Studies on cold diuresis in the Antarctica. Japanese Journal of Biometeorlogy 1997;34:121 9.