Legal Medicine 17 (2015) 198–200

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Case Report

Two forensic autopsy cases of death due to upper gastrointestinal hemorrhage: A comparison of postmortem computed tomography and autopsy findings Hideto Suzuki ⇑, Iwao Hasegawa, Norio Hoshino, Tatsushige Fukunaga Tokyo Medical Examiner’s Office, Tokyo Metropolitan Government, Japan

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Article history: Received 27 November 2014 Received in revised form 21 December 2014 Accepted 24 December 2014 Available online 6 January 2015 Keywords: Gastrointestinal hemorrhage Postmortem computed tomography Forensic autopsy

a b s t r a c t In this report, we describe two autopsy cases of death due to upper gastrointestinal hemorrhage (Case 1: gastric ulcer, Case 2: aortoduodenal fistula). Postmortem computed tomography (CT) images from both cases revealed pooling of gastric fluid, which contained high attenuation areas, although these images also mirrored the different sources of the gastrointestinal hemorrhage. Fluid collection was observed in the small intestine for both cases, although the high attenuation areas were only remarkable in Case 2. The autopsy in Case 1 revealed a peptic ulcer, with small vessels exposed on the surface of the ulcer. Melena was also observed throughout the intestine, although clotting was only observed inside the stomach. The autopsy in Case 2 revealed diffuse massive clotting from the stomach to the upper portion of the ileum, which was due to a primary aortoduodenal fistula. Given our autopsy findings, the extent of the high attenuation areas in the digestive tract during postmortem CT scanning may be correlated with the speed of the gastrointestinal hemorrhage before death. Carefully evaluating the radiodensity of the gastrointestinal contents during postmortem CT scanning may indicate the primary site of the hemorrhage before the autopsy, thereby facilitating the accurate identification of the cause of death during forensic autopsy. Ó 2015 Elsevier Ireland Ltd. All rights reserved.

1. Introduction Acute abdomen remains a significant cause of death in sudden, unexpected deaths among elderly persons [1]. Among the deaths related to various abdominal diseases, gastrointestinal hemorrhage has been frequently reported in forensic autopsy cases [1–9], and various lesions have been reported as the primary site of hemorrhage, including peptic ulcers [1], gastric cancers [2], esophageal varices [3], and aortoenteric fistulae [4–7]. In clinical practice, several reports have suggested that computed tomography (CT) angiography and enterography can potentially be used to identify the source of obscure gastrointestinal bleeding [10,11]. Recently, the role of postmortem CT scanning as an adjunct to conventional autopsy has been well documented [12,13], although only a few reports have been published regard-

⇑ Corresponding author at: Tokyo Medical Examiner’s Office, Tokyo Metropolitan Government, 4-21-18 Otsuka, Bunkyo-ku, Tokyo 112-0012, Japan. Tel.: +81 3 3944 1481; fax: +81 3 3944 7585. E-mail address: [email protected] (H. Suzuki). http://dx.doi.org/10.1016/j.legalmed.2014.12.010 1344-6223/Ó 2015 Elsevier Ireland Ltd. All rights reserved.

ing the usefulness of postmortem CT scanning in cases of fatal gastrointestinal hemorrhage [2,9]. We describe two autopsy cases of death due to upper gastrointestinal hemorrhage, where the postmortem CT images providing a striking contrast between the cases. Based on a comparison of the CT images and autopsy findings, the present cases suggest that carefully evaluating the radiodensity of the bowel contents during postmortem CT scanning may help identify the primary site of gastrointestinal hemorrhage before autopsy. 2. Methods Whole body postmortem CT was performed before autopsy using a sequential scanner (Somatom Definition AS, Siemens AG, München, Germany) and the following parameters: 120 kV; quality reference mAs: 535; thickness: 64  0.6 mm; and field of view: 500 mm. Image data were analyzed by forensic pathologists using syngo.via (Siemens AG). The radiodensity of the bowel contents was calculated as the mean of three measurements in the corresponding areas.

H. Suzuki et al. / Legal Medicine 17 (2015) 198–200

3. Case report

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3.1. Case 1 A man in his 60s, who was living alone, was found dead in his house. According to an acquaintance, he had complained of epigastric pain, loss of appetite, and general fatigue in the month before his death, although he had not consulted a doctor. An external examination was performed approximately 20 h after his death, and did not reveal any open injuries, although extremely weak postmortem livedo was observed on his back. The deceased was 166 cm tall and weighed 55 kg, with a body mass index of 20.0 kg/m2. Unenhanced postmortem CT scanning was performed approximately 22 h after his death. The main findings from the CT images were pooling of gastric fluid containing high attenuation areas (mean: 49.3 HU; Fig. 1a), hypertrophy of the gastric wall (especially on the posterior side), and proximity of the stomach to the pancreas (Fig. 1b). Fluid collection was also observed in the small intestine, although it did not contain any areas of high radiodensity (mean: 25.0 HU; Fig. 1c). Forensic autopsy was performed approximately 23 h after death. The autopsy revealed severe anemia throughout all organs, and only 20 mL of blood was collected from the heart. A giant ulcerative lesion (9  6 cm) was observed on the posterior gastric wall, which was severely adhered to the pancreas (Fig. 2a). Small vessels were exposed on the surface of the ulcer, and the gastric contents (300 mL) included clotted blood. Melena, a black tar-like substance, was observed throughout the small intestine and colon (Fig. 2b), although no clotting was evident. The other major organs did not reveal any additional specific findings. Upon histological examination, distinct layers were observed in the ulcerative lesion, including a surface coat of necrotic debris, fibrinoid necrosis, granulation tissue, and extensive fibrous tissue; these findings were compatible with a chronic peptic ulcer. Proximal tubular necrosis of the kidney was also observed; therefore, the cause of death was determined to be severe anemia due to a hemorrhagic gastric ulcer.

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Fig. 1. Postmortem CT images from Case 1 (a–c) and Case 2 (d–f). Asterisks indicate high attenuation areas. (a, d) Pooling of gastric fluid that contains high attenuation areas. (b) Hypertrophy of the gastric wall is visible, especially on the posterior side. The stomach is currently proximal to the pancreas. (c) Fluid collection is visible in the small intestine, although it does not contain areas of high radiodensity. (e) The duodenum and the small intestine are distended with fluids that contain masses of high radiodensity. (f) The inferior part of the duodenum is proximal to the abdominal aorta, where the aorta is slightly distended (2.1  1.4 cm) compared to the other parts of the aorta.

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Fig. 2. Macroscopic autopsy findings for Case 1. (a) A giant ulcerative lesion (9  6 cm) is visible on the posterior gastric wall, which is severely adhered to the pancreas. (b) Melena (black, tar-like substance) is visible throughout the small intestine, although clotting is not evident.

3.2. Case 2 A man in his 60s was found dead, with hematemesis, at his workplace. He had a history of heavy alcohol consumption, and had consulted a doctor for chronic pancreatitis, diabetes mellitus, and hypertension, although alcoholic liver cirrhosis or gastric ulcer had not been detected. The deceased was 159 cm tall and weighed 40 kg, with a body mass index of 15.8 kg/m2. Unenhanced postmortem CT scanning was performed approximately 28 h after his death, and pooling of gastric fluid, with high radiodensity, was observed on the CT images (mean: 72.3 HU; Fig. 1d). The duodenum and small intestine were distended with fluids that contained masses of high radiodensity (mean: 76.3 HU; Fig. 1e and f). The inferior part of the duodenum was proximal to the abdominal aorta, which was slightly distended (2.1  1.4 cm) compared to the other parts of the abdominal aorta (Fig. 1f). Calcification in the abdominal aorta and pancreas was also observed. Forensic autopsy was subsequently performed approximately 29 h after death. At the autopsy, severe anemia was observed throughout all organs, and only 20 mL of blood was collected from the heart. Adhesion between the inferior part of the duodenum and the abdominal aorta was observed, and dissection of the abdominal aorta revealed a partial aneurysm (3.5  3.0 cm). The aneurysm was located on the anterior wall of the abdominal aorta, approximately 8 cm below the celiac trunk, which had ruptured into the duodenum (Fig. 3a). The gastric contents were bloody (200 mL), and contained a massive clot; massive clotting was also observed in the duodenum and the ileum (Fig. 3b). Additional macroscopic autopsy findings included severe atherosclerosis of the aorta and atrophic pancreas. Microscopic examination revealed that elastic fibers were severely disrupted in the tunica media of the aneurysm wall, and infiltration of lymphocytes was observed in the tunica

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Fig. 3. Macroscopic autopsy findings for Case 2. (a) Dissection of the abdominal aorta reveals a fistula between the anterior wall of the abdominal aorta and the inferior part of the duodenum (arrow). Inset: A magnified image of the ruptured aneurysm. (b) Massive clotting is visible in the duodenum and ileum.

adventitia. Deposition of fibrin was also noted around the internal surface of the aneurysm wall, and mild fat deposition from the hepatocytes and proliferation of fibrous tissue was observed in the pancreas. Based on the autopsy findings, the cause of death was determined to be gastrointestinal hemorrhage due to a primary aortoduodenal fistula.

4. Discussion Postmortem CT revealed high radiodensity areas in the gastric contents for both cases, and in the contents of the duodenum and small intestine for Case 2. A positive correlation and significant association have been established between hemoglobin (hematocrit) levels and the attenuation of blood on unenhanced CT images [14,15]. The increase in attenuation (i.e., radiodensity) is caused by clot retraction, as the process of clot retraction includes the elimination of water, which increases the concentration of red blood cells and hemoglobin [16]. Based on the autopsy findings, the high attenuation areas in the present cases’ digestive tracts corresponded to the location of the clotting. Interestingly, the radiodensity in the duodenum and small intestine on the CT images provided a striking contrast between the two cases. In Case 1, high attenuation areas were observed in the stomach, although they were not observed in the contents of the duodenum and small intestine. Given the deceased’s history, and our autopsy findings, it appears that the hemorrhage had proceeded slowly (over the course of several days) from the small vessels on the surface of the peptic ulcer. Erythrocytes entering the gastrointestinal lumen are typically lysed, producing free hemoglobin that is subsequently converted to free hematin (Fe3+ state) and globin [17]. The attenuation of hemoglobin is largely related to its protein content (i.e., globin), and its iron content contributes to only 7–8% of the total attenuation [18]. The globin is typically digested by pancreatic and intestinal mucosal proteases into peptides and amino acids [18], and therefore degradation and dilution of hemoglobin in the gastrointestinal fluid may have reduced the radiodensity of the contents of the duodenum and small intestine in Case 1. In contrast, the rapid hemorrhage from the ruptured aneurysm into the digestive tract in Case 2 must have exceeded the degradation and dilution capacity of the gastrointestinal fluid. This subsequently resulted in massive clot formation, which created the broad, high attenuation areas on the postmortem CT images. Before performing the autopsy, a diagnosis of aortoduodenal fistula

was not conclusive, as the diameter of the aorta (on the CT images) was not as large as those that have been previously reported (mean diameter of the aorta from a primary aortoenteric fistula: 6.2 cm) [19]. In addition, none of our other findings suggested the presence of an aortoduodenal fistula, which is typically indicated by the presence of gas within the calcified wall of the aneurysm or extraluminal gas in the periaortic region [20]. However, this case highlights the fact that that large vessel involvement should be considered before autopsy when broad, high attenuation areas are observed in the digestive tract during postmortem CT scanning. The postmortem CT images from the present cases mirrored the features of the gastrointestinal hemorrhage from different sources. Although further data is needed, the present cases suggest that the extent of high attenuation areas in the digestive tract during postmortem CT scanning may correlate with the speed of the gastrointestinal hemorrhage. Therefore, high attenuation areas may be limited near the primary site of hemorrhage if the speed of the hemorrhage is low. In such cases, forensic pathologists should be aware of subtle high attenuation areas in the digestive tract, or changes in the thickness of the intestine. In addition, the pathology of the large vessels and en bloc resection of the involved sites should be considered if broad, high attenuation areas are observed in the digestive tract during postmortem CT scanning. References [1] Ng CY, Squires TJ, Busuttil A. Acute abdomen as a cause of death in sudden, unexpected deaths in the elderly. Scott Med J 2007;52:20–3. [2] Yamazaki K, Shiotani S, Ohashi N, Doi M, Kikuchi K, Nagata C, et al. Comparisons between computed tomography (CT) and autopsy findings in cases of abdominal injury and disease. Forensic Sci Int 2006;162:163–6. [3] Tsokos M, Türk EE. Esophageal variceal hemorrhage presenting as sudden death in outpatients. Arch Pathol Lab Med 2002;126:1197–200. [4] Ihama Y, Miyazaki T, Fuke C, Ihama Y, Matayoshi R, Kohatsu H, et al. An autopsy case of a primary aortoenteric fistula: a pitfall of the endoscopic diagnosis. World J Gastroenterol 2008;14:4701–4. [5] Vogel Y, Keilmann O, Jochheim R, Tannapfel A. A rare cause of haematemesis with fatal gastrointestinal bleeding. Internist (Berl) 2010;51:1053–6. article in German. [6] Egan C, Szontagh-Kishazi P, Flavin R. Aortic fistula after neoadjuvant chemoradiotherapy and esophagectomy for esophageal carcinoma: an unusual cause of sudden death. Am J Forensic Med Pathol 2012;33:270–2. [7] Ambepitiya SG, Michiue T, Bessho Y, Kamikodai Y, Ishikawa T, Maeda H. An unusual presentation of thoracic aortic aneurysm rupturing into the esophagus: an autopsy case report. Forensic Sci Med Pathol 2010;6:121–6. [8] Christoffersen RK, Nielsen TS, Vesterby A. Dieulafoy lesion of the esophagus causing massive upper gastrointestinal bleeding and death: a case report. Am J Forensic Med Pathol 2012;33:186–7. [9] Rashid SN, Bouwer H, O’Donnell C. Lethal hemorrhage from a ureteric-arterialenteric fistula diagnosed by postmortem CT angiography. Forensic Sci Med Pathol 2012;8:430–5. [10] Lee SS, Oh TS, Kim HJ, Chung JW, Park SH, Kim AY, et al. Obscure gastrointestinal bleeding: diagnostic performance of multidetector CT enterography. Radiology 2011;259:739–48. [11] Kennedy DW, Laing CJ, Tseng LH, Rosenblum DI, Tamarkin SW. Detection of active gastrointestinal hemorrhage with CT angiography: a 4(1/2)-year retrospective review. J Vasc Interv Radiol 2010;21:848–55. [12] Poulsen K, Simonsen J. Computed tomography as routine in connection with medico-legal autopsies. Forensic Sci Int 2007;171:190–7. [13] Leth PM. Computed tomography used as a routine procedure at postmortem investigations. Am J Forensic Med Pathol 2009;30:219–22. [14] Stein J, Huerta K. When looking at a non-contrast head CT, what actually appears white in an acute hemorrhagic stroke? Cal J Emerg Med 2002;3:70–1. [15] Black DF, Rad AE, Gray LA, Campeau NG, Kallmes DF. Cerebral venous sinus density on noncontrast CT correlates with hematocrit. AJNR Am J Neuroradiol 2011;32:1354–7. [16] Buyck PJ, De Keyzer F, Vanneste D, Wilms G, Thijs V, Demaerel P. CT density measurement and H:H ratio are useful in diagnosing acute cerebral venous sinus thrombosis. AJNR Am J Neuroradiol 2013;34:1568–72. [17] Walker HK, Hall WD, Hurst JW, editors. Clinical methods: the history, physical, and laboratory examinations. Boston: Butterworths; 1990. p. 490. [18] New PF, Aronow S. Attenuation measurements of whole blood and blood fractions in computed tomography. Radiology 1976;121:635–40. [19] Saers SJ, Scheltinga MR. Primary aortoenteric fistula. Br J Surg 2005;92: 143–52. [20] Ranasinghe W, Loa J, Allaf N, Lewis K, Sebastian MG. Primary aortoenteric fistulae: the challenges in diagnosis and review of treatment. Ann Vasc Surg 2011;25:386.e1–5.

Two forensic autopsy cases of death due to upper gastrointestinal hemorrhage: a comparison of postmortem computed tomography and autopsy findings.

In this report, we describe two autopsy cases of death due to upper gastrointestinal hemorrhage (Case 1: gastric ulcer, Case 2: aortoduodenal fistula)...
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