The Journal of TRAUMA威 Injury, Infection, and Critical Care
Intrahepatic Gas at Postmortem Computed Tomography: Forensic Experience as a Potential Guide for In Vivo Trauma Imaging Christian Jackowski, MD, Martin Sonnenschein, MD, Michael J. Thali, MD, Emin Aghayev, MD, Kathrin Yen, MD, Richard Dirnhofer, MD, and Peter Vock, MD Background: Until August 2004 there were 106 forensic cases examined with postmortem multislice computed tomography (MSCT) and magnetic resonance (MR) imaging before traditional autopsy within the Virtopsy project. Intrahepatic gas (IHG) was a frequent finding in postmortem MSCT examinations. The aim of this study was to investigate its cause and significance. Methods: There were 84 virtopsy cases retrospectively investigated concerning the occurrence, location, and volume of IHG in postmortem MSCT imaging (1.25 mm collimation, 1.25 mm thickness). We assessed and noted the occurrence of intestinal distention, putrefaction, and systemic gas embolisms and the cause of death, pos-
sible open trauma, possible artificial respiration, and the postmortem interval. We investigated the relations between the findings using the contingency table (2 test) and the comparison of the postmortem intervals in both groups was performed using the t test in 79 nonputrefied corpses. Results: IHG was found in 47 cases (59.5%). In five of the cases, the IHG was caused or influenced by putrefaction. Gas distribution within the liver of the remaining 42 cases was as follows: hepatic arteries in 21 cases, hepatic veins in 35 cases, and portal vein branches in 13 cases; among which combinations also occurred in 20 cases. The presence of IHG was strongly related to open trauma with sys-
temic gas. Pulmonary barotrauma as occurring under artificial respiration or in drowning also caused IHG. Putrefaction did not seem to influence the occurrence of IHG until macroscopic signs of putrefaction were noticeable. Conclusions: IHG is a frequent finding in traumatic causes of death and requires a systemic gas embolism. Exceptions are putrefied or burned corpses. Common clinical causes such as necrotic bowel diseases appear rarely as a cause of IHG in our forensic case material. Key Words: Forensic radiology, Virtopsy, Postmortem imaging, Intrahepatic gas, Gas embolism. J Trauma. 2007;62:979 –988.
P
ostmortem imaging using multislice computed tomography (MSCT) and magnetic resonance (MR) imaging is being evaluated by several research groups1–7 as a postmortem investigation technique alternative to traditional destructive autopsy in selected cases. Thereby, intrahepatic gas (IHG) was recognized as a frequent finding in postmortem MSCT examinations. It was first described by Yamazaki et al.8 as hepatic portal venous gas. Shiotani et al.9 published the first retrospective study in 190 nontraumatic deaths correlating the occurrence of intrahepatic portal venous gas with gastrointestinal distention. Traumatic causes of IHG were missing in this study as well as postmortem alterations such as putrefaction; all cases were scanned within 2 hours postmortem. Having data of more than 100 forensic cases with full body MSCT and MR scanning we intended to investigate the
Submitted for publication September 12, 2005. Accepted for publication November 18, 2005. Copyright © 2007 by Lippincott Williams & Wilkins, Inc. From the Institute of Forensic Medicine (C.J., M.J.T., E.A., K.Y., R.D.) and the Institute of Diagnostic Radiology, Inselspital, (M.S., P.V.), University of Bern, Switzerland. Address for reprints: Christian Jackowski, MD, University of Bern, Institute of Forensic Medicine, IRM – Buehlstrasse 20, CH-3012 Bern, Switzerland; email:
[email protected]. DOI: 10.1097/01.ta.0000198733.22654.de
Volume 62 • Number 4
occurrence of IHG according to conditions, that are thought to influence the occurrence of IHG such as venous or systemic air embolism,10 artificial respiration, gastrointestinal distention, and putrefaction.11
MATERIALS AND METHODS From 106 virtopsy cases, 18 cases presenting with direct traumatic injury of the liver (e.g. total destruction of the corpse when run over by train or gun shot wound channels through the liver), 1 case of adipocire, 1 case that was found in a glacier that was scanned before defrosting as well as 1 newborn, and 1 fetus were excluded. The remaining 84 cases were investigated using the scanning procedures corresponding to the virtopsy approach as already described in previous publications from 2000 to 2004.1,12,13 The severity of IHG was semiquantitatively assessed by a subjective observer-dependent grading score from 0 (no gas within the liver), 1 (small amounts of gas within the small peripheral intrahepatic vessels predominantly in anterior parts of the liver), 2 (moderate amounts of IHG within major intrahepatic vessels) to 3 (large amounts of IHG, completely filling the major hepatic vessels), demonstrated in Figure 1. This grading was supported by an objective quantification of the IHG volume. A three-dimensional volume-rendering model of the liver was generated after manual tracing of the liver contours on axial images on a workstation. Volume 979
The Journal of TRAUMA威 Injury, Infection, and Critical Care
Fig. 1. Semiquantitative grading of IHG accumulation. (A) Grade 0: no visible gas within the liver vessels; ( B) grade 1: small amounts of gas within the small peripheral intrahepatic vessels, predominantly in anterior parts of the liver; (C) grade 2: moderate amounts of intrahepatic gas within major intrahepatic vessels; ( D) grade 3: large amounts of intrahepatic gas, completely filling the major hepatic vessels.
analysis of the model was performed twice, once before and a second time after exclusion of voxels of less than ⫺500 Hounsfield Units (HU). Subtraction of the volumes left the excluded volume representing the IHG volume. Values between 0 mL and 1 mL were rounded up to 1 mL and all further values were rounded to the next whole milliliter value. The IHG location was assessed using the anatomic intrahepatic course of the gas-filled vessel (CJ, MS). When very small volumes did not allow an assessment of the vessel course the occurrence of extra hepatic gas was used to distinguish between the different liver vessels. Thereby, small gas bubbles within the liver were verified to be within the hepatic veins, when additional gas was found within the right heart or the major systemic veins. A simultaneous occurrence of gas within the extra hepatic course of the portal vein indicated the intrahepatic portal vein as location of the IHG. Similarly, systemic arterial gas helped with the hepatic artery system. This method was used when only the venous or the arterial part of the systemic vessel system or only the portal vein contained gas. As soon as more systemic vessels in980
cluded gas, the IHG was not classified using this method. In several cases, the appendant MR imaging data sets were used to distinguish between the different intrahepatic vessels. The occurrence of gastrointestinal distention was investigated in all 84 cases and semiquantitatively graded from 0 (physiologic amounts of gas within bowel), 1 (slightly increased amounts of gas within bowel), 2 (distinctively increased amounts of gas within bowel) to 3 (severe intestinal distention with ballooning of the abdomen) according to Figure 2. All included cases were investigated for radiologic signs of putrefaction, such as extra luminal intraparenchymateous collection of gas11,14 or signs of putrefaction noted within the autopsy protocols, such as green coloration of the skin in the abdominal region. Putrefaction was found to be positive when at least the radiologic or one autoptical sign was positive. The five definite putrefaction cases were excluded from statistical calculations leaving 79 cases to be further investigated. Furthermore, all cases were checked for the presence of systemic gas embolism. The diagnosis of systemic gas emApril 2007
IHG at Postmortem CT
Fig. 2. Semiquantitative grading of postmortem gastrointestinal distention in an axial cross section and corresponding VR air structure reconstruction. (A) Grade 0: physiologic gas amounts within bowel; ( B) grade 1: slightly increased amounts of gas within bowel; (C) grade 2: distinctively increased amounts of gas within bowel; ( D) grade 3: severe intestinal gaseous distention with ballooning of the abdomen.
bolism was made when gas was visible at MSCT lung window settings within cardiac cavities, major systemic vessels, or both, and no signs of putrefaction were noted within the autopsy protocol or seen at postmortem imaging. Additionally, the cases were checked for open trauma. Trauma was considered to be open when vessel lumina gained access to the ambient air. Artificial respiration was noted in each case that either received extensive resuscitation attempts or died under intensive care conditions. Relations between the findings were analyzed (contingency table, 2, p ⬍ 0.01) and the postmortem intervals (PMI) were compared (t test, two tail).
RESULTS Table 1 displays the occurrence of IHG, its intrahepatic location, the grading of intestinal distention, signs of putrefaction, and the occurrence of systemic gas embolism. Table 1 also displays the cause of death, comments, and the postmortem interval (PMI) in each case. Five cases (6%) showed signs of putrefaction and three of them with a severe destruction of the liver tissue also had extra luminal intraparenchymateous gas (Fig. 3). Volume 62 • Number 4
Within our study, IHG occurred in 42 cases (50%) without definitive signs of putrefaction. Of these, the gas distribution was as follows: hepatic arteries in 21 cases, hepatic veins in 35 cases, and portal vein branches in 13 cases. Combinations occurred in 20 cases. Two cases remained unclassified. In 2 cases, gas was detected exclusively within the hepatic arteries, in 16 cases within the hepatic veins, and in 2 cases within the portal vein branches. Affection of two intrahepatic vessel systems occurred for hepatic arteries and hepatic veins in 9 cases, for hepatic veins and portal vein branches in 1 case, and hepatic artery and portal vein branches in 1 case. We saw involvement of all three intrahepatic vessel systems in nine cases. Intestinal distention was diagnosed in 61 cases (72.6%) (grade 1–38 [45.2%]; grade 2–17 [20.2%]; grade 3– 6 [7.1%]) and 1 of the burned corpses was not diagnosable because of the destruction of the bowel. Systemic gas embolism was diagnosed in 42 cases (50%). Of the systemic gas embolism cases, 39 (92.9%) presented also with IHG. Only three of the nonputrefied IHG cases (7.1%) presented without systemic gas embolism. All three were burned corpses. There was a strong significant 981
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Table 1 Results in All 84 Investigated Forensic Cases Case 1 2 3
Grade Grade Grade Grade Gas 0 1 2 3 Volume
24 25 27 28 30 31 32 33 34 35 36 37 40 43 46 47 50 51 53 54 55 56
66 67 68 69 70 72 73 74 75 76 77 78 79 80 81 83 84 85
982
⫹⫹ ⫹
x x
⫺ ⫺ ⫹⫹ ⫹⫹⫹ ⫹⫹⫹ ⫺ ⫺ ⫹⫹ ⫹ ⫺ ⫹ ⫹⫹ ⫺
0 x x x 0 x x x 0 0 0 x x x
3 mL a. ⫹ v. ⫹ p. 1 mL a. 1 mL v.
⫹⫹ ⫹ ⫹⫹⫹ ⫹⫹⫹ ⫺ ⫹ ⫹ ⫹⫹ ⫹ ⫺ ⫹⫹ ⫺ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹⫹ ⫹ ⫹ ⫹
0 0 0 x 0 x 0 x 0 0 x 0 0 0 0 x 0 0 0 x x 0
1 mL v. ⫹ p. 13 mL a. ⫹ v. ⫹ p.
no bowel ⫹⫹⫹
x
123 mL tis. des. 18 mL a. ⫹ v. ⫹ p. 1 mL a. ⫹ v.
⫹⫹⫹ ⫹⫹⫹ ⫹
x x
6 mL a. ⫹ v. ⫹ p. 16 mL a. ⫹ v.
⫹ ⫺ ⫹ ⫹ ⫹⫹⫹ ⫹ ⫹ ⫹ ⫹⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹⫹ ⫹
7 mL a. ⫹ v. 2 mL v.
x
x x 1 mL a. ⫹ v. 1 mL v.
x x x x x
8 mL v. 3 mL v. 1 mL v.
x x x x x
1 mL v. 9 mL a. ⫹ v. ⫹ p. 4 mL a. ⫹ v.
x x x x x x
81 mL tis. des. 19 mL a. ⫹ v. ⫹ p.
x x x 3 mL a. ⫹ v.
x x x x
71 mL a. ⫹ v. ⫹ p.
x x x x x
1 mL ?
x x x x x x x x
62 63 65
x x
x x x x x x x x x x x
21 mL 189 mL 2 mL 2 mL 3 mL 2 mL 3 mL 6 mL 32 mL 2 mL
p. tis. des. v. v. v. p. a. ⫹ v. a. ⫹ v. v. a. ⫹ v. ⫹ p.
x x
4 mL a. ⫹ v. ⫹ p.
x x x
Systemic Gas Embolism x 0 0
x
58 61
Intestinal Putrefaction Distension‡ Noted ⫹ ⫺ ⫺
x x x
4 5 6 7 8 9 10 11 12 15 16 18 19 21 22 23
Location
1 mL
a. ⫹ v.
x
0 x x
x
x
x
0 x x x x 0 x 0 x x x 0 x x 0 0 0 x 0 0 x
Cause of Death Gunshot to the head* Exsanguination* Exsanguination/fat embolism* Air embolism* Exsanguination/air embolism* Heart failure† Craniocerebral trauma* Craniocerebral trauma* Exsanguination* Strangulation† Gunshot to the head* Gunshot to the head* Craniocerebral trauma* Gunshot to the head* Craniocerebral trauma* Cerebral edema† Gunshot to the head* Gunshot to the head* Craniocerebral trauma/air embolism* SIDS† Heart failure† Craniocerebral trauma* Craniocerebral trauma* Exsanguination* Air embolism* Strangulation† Exsanguination* Drowning† Fat embolism* Exsanguination* Fat embolism* Craniocerebral trauma* Septicemia/heart failure† Cerebral edema* Exsanguination* Manual strangulation† Manual strangulation† Hypothermia† Exsanguination* Multiple organ failure* Carbon monoxide poisoning† Burn shock† Exsanguination/fat embolism* Pneumonia† Exsanguination* Fat embolism/positional asphyxia* Exsanguination* Craniocerebral trauma* Cerebral edema* Cerebral edema* Drowning Air embolism* Gunshot to the head* Craniocerebral trauma* Strangulation Drowning Drowning Exsanguination/drowning* Blood aspiration* Craniocerebral trauma* pneumothorax* Strangulation† Craniocerebral trauma* Heart failure†
Comments
PMI 24 hr 24 hr 24 hr
Burned corpse
24 hr 24 hr
Artificial respiration Artificial respiration
72 hr 48 hr 24 hr 24 hr 24 hr 24 hr 12 hr 24 hr 24 hr 5 hr 24 hr 96 hr 48 hr 24 hr
Artificial respiration
Artificial respiration Artificial respiration
Artificial respiration Artificial respiration Artificial respiration Artificial respiration
Artificial respiration Artificial Artificial Artificial Artificial
respiration respiration respiration respiration
Artificial respiration Artificial respiration Artificial respiration Burned corpse Burned corpse
36 hr 24 hr 2–4 wk 24 hr 12 hr 24 hr 24 hr 24 hr 12 hr 36 hr 60 hr 24 hr 48 hr 48 hr 48 hr 12 hr 36 hr 36 hr 48 hr 12 hr 72 hr 24 hr 24 hr 48 hr 3–4 wk 12 hr 24 hr
Artificial respiration Artificial respiration
Artificial respiration Artificial respiration Burned corpse Burned corpse Artificial respiration Artificial respiration Artificial respiration
24 hr 24 hr 6 hr 24 hr 144 hr 24 hr 12 hr 12 hr 48 hr 48 hr 24 hr 120 hr 48 hr 48 hr 12 hr 12 hr 24 hr 12 hr
April 2007
IHG at Postmortem CT
Table 1 Results in All 84 Investigated Forensic Cases (continued) Case
Grade Grade Grade Grade Gas 0 1 2 3 Volume
Location
Intestinal Putrefaction Distension‡ Noted
Systemic Gas Embolism
p. a. ⫹ p. v.
⫹⫹ ⫹ ⫹ ⫹⫹
x x x 0
v.
x x x x x
⫹ ⫹⫹ ⫹⫹ ⫹ ⫹ ⫹⫹
x 0 0 0 0 0
97 98
x x
⫺ ⫺
0 0
99 100 101 102 103 104
x x
0 0 x x x x
86 87 88 89
x
90 91 92 93 94 96
105 106
x x
3 mL 37 mL 3 mL
x
1 mL
x
x x x x
2 mL 1 mL 1 mL 1 mL
v. ? v. v.
⫹⫹ ⫹ ⫹ ⫹⫹ ⫺ ⫹⫹⫹
x
1 mL
v.
⫺
x
3 mL
a.
⫹⫹
x
x
Cause of Death Intoxication† Strangulation† Pneumothorax* Exsanguination/fat embolism* Heart failure† Manual strangulation† Intoxication† Heart failure† Strangulation† Pneumonia/necrotizing laryngitis† Strangulation† Immaturity (fetus 22 weeks)† Heart failure† Hypothermia† Heart failure† Craniocerebral trauma* Cerebral edema* Exsanguination/fat embolism* Exsanguination/fat embolism* Heart failure†
Comments
PMI
Artificial respiration
24 hr 48 hr 60 hr 48 hr
Artificial respiration
Artificial respiration
Artificial respiration
48 hr 24 hr 24 hr 24 hr 24 hr 24 hr 6 hr 24 hr
Artificial respiration Artificial respiration
24 hr 24 hr 24 hr 24 hr 48 hr 24 hr 48 hr
Artificial respiration
24 hr
Semiquantitative subjective grading of the quantity of the intrahepatic gas from 0 to 3 (according to Fig. 1) and the result of the volumetric computed tomography assessment are seen. The intrahepatic location is noted. When it could not be assessed a question mark was set. The occurrence of intestinal distention is noted (according to Fig. 2). Putrefaction signs as well as the occurrence of systemic gas embolism are displayed. Comments show whether the case underwent artificial respiration or was burned. PMI indicates the time between death and scanning. * Traumatic cause of death. † Nontraumatic cause of death. ‡ ⫺, grade 0; ⫹, grade 1; ⫹⫹, grade 2; ⫹⫹⫹, grade 3. a, hepatic artery; v, hepatic veins; p, portal vein branches; PMI, postmortem interval; tis. des.; tissue destruction.
relation of the finding of IHG and systemic gas as well as a strong significant relation between systemic gas and traumatic cause of death. The intrahepatic measured gas volumes varied from 1 mL to 189 mL. The three highest volumes measured were 81 mL, 123 mL, and 189 mL and occurred in putrefaction cases. The range in all 79 nonputrefaction cases was 1 to 71 mL. Intestinal gas amounts in nonputrefied cases did not differ from normal physiologic vital dimensions (grade 0) in 17 cases (21.5%). Intestinal distention of grade 1 occurred in 38 cases (48.1%), of grade 2 in 17 cases (21.5%), and of grade 3 in 6 cases (7.7%). One case showed a destruction of the intestine because of burning. There was no significant relation between the occurrence of gastrointestinal distention (all gradings) and IHG in our data although in grade 3 gastrointestinal distention five of six cases showed IHG. All of the IHG cases involving the intrahepatic branches of the portal vein showed at least grade 1 distention. Artificial respiration was noticed in 31 (39.2%) of the nonputrefied cases and showed no significant relation to the occurrence of IHG. After exclusion of the five putrefaction cases the mean postmortem interval (PMI) in 42 cases showing IHG was 29.1 hours (standard deviation 14.3 hours) and in 37 cases Volume 62 • Number 4
without IHG 29.3 hours (s 15.8 hours). There was no significant difference in PMIs of both groups. Of the 79 nonputrefied cases, 48 (60.8%) presented with an open trauma as cause of death (Table 1). Of these, 32 (66.7%) also showed IHG. There was a significant relation between open trauma and the occurrence of IHG in our population.
DISCUSSION This study investigated the occurrence and cause of IHG detected in postmortem MSCT investigations. Yamazaki et al.8 and Shiotani et al.9 first described hepatic portal venous gas as a frequent finding in postmortem computed tomography and correlated it to the occurrence of intestinal distention. Their 190 cases were of nontraumatic nature and scanned within 2 hours postmortem. Thereby, the traumatic causes of IHG as well as postmortem alterations such as putrefaction leading to IHG were missing. We noticed within our first 100 virtopsy cases more locations of IHG, such as the hepatic venous system, the hepatic arterial system, and within the tissue. Biliary tract gas, a frequent clinical finding,15 did not occur in our 79 investigated cases. 983
The Journal of TRAUMA威 Injury, Infection, and Critical Care Intrahepatic Venous Gas
Fig. 3. Putrefaction gas. Axial MSCT image of the liver in putrefaction case 70 and corresponding air structure reconstruction in an anteroposterior view. Note the diffuse and more bubble-like distribution of the putrefaction gas within the decomposed dorsal liver tissue in addition to the predominantly anterior intravascular gas.
Wolfel and Brogdon16 comprehensibly considered the gas within the liver seen on plain radiographs to be driven into the biliary tree from the upper gastrointestinal tract at the time of a blunt abdominal injury. Our findings do not support this possible explanation for IHG in cases of abdominal trauma. We did not detect relevant volumes of gas within the biliary tract although biliary gas could not be completely excluded because two cases of IHG could not be classified.
The most frequent location of IHG in this study was the hepatic venous system. Having abundant traumatic cases within our population and noticing the strong relation of systemic gas embolism and intrahepatic venous gas, we assume trauma with gas embolism to be the commonest cause. Mainly craniocerebral trauma and head shot wounds were associated with IHG. Both conditions range among the main causes for venous air embolism according to the literature and our own experiences.10,17–20 We also hypothesize this to be the mechanism for intrahepatic venous gas accumulation. Other traumatic injuries might also cause gas to enter the hepatic venous system such as blunt or open abdominal trauma.21 Thereby, it remains arguable whether a retrograde gas transport into the liver veins occurs passively postmortem when the corpse is stored in supine position because of the ascending force. Alternatively, it might occur vitally in retrograde direction via an increased right ventricular pressure and an insufficiency of the tricuspid valve after gaseous occlusion of the pulmonary artery even against the buoyancy of gas bubbles in fluids (Fig. 4). The second explanation might be supported by the finding of gas within the vessels of dorsal liver parts, which are below the level of the vena cava in supine position.
Intrahepatic Arterial Gas In 21 cases, gas was shown within the arterial system. Gas can enter the arterial system via a patent foramen ovale combined with an increasing right atrial pressure in gaseous pulmonary artery embolism. It may even pass the pulmonary capillary bed22–25 or in direct pulmonary trauma (contusion, laceration) with damage to the alveolar-capillary barrier it may reach the pulmonary veins.26 We also assume alveolar
Fig. 4. Intrahepatic venous gas in upright corpse position. Gas within hepatic veins (arrows) and hepatic arteries (doubled arrow) in a case of a gunshot wound to the head and remaining in upright position. Either an active and vital retrograde gas transportation downwards into the hepatic veins resulting from an increased right ventricular pressure after total gaseous occlusion of the right ventricular outflow tract and pulmonary artery, or a passive gas transport caused by buoyancy from right atrium into the liver veins, when the corpse was stored and scanned in supine position, might have been responsible.
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IHG at Postmortem CT rupture because of emphysema aquosum in cases of drowning or because of pulmonary barotrauma caused by high-inspiratory pressures during artificial respiration to cause systemic arterial gas emboli.27–30 This might explain the 10 cases which showed gas within the liver vessels, but died because of a nontraumatic manner of death. Four of them died of heart failure (cases 85, 90, 101, and 106) under artificial respiration. Because the PMI in these four cases (12– 48 hours) did not increase as compared with the entire population studied, we assume an agonal barotrauma because of artificial respiration as the most likely cause for the intravascular gas. Additionally, the two drowning cases (cases 76 and 77) had alveolar ruptures because of a typical drowning process31 that facilitated the entrance of gas into the vascular system. In strangulation (case 87) the pulmonary trauma caused by the strong breathing attempts against narrowed or occluded airways also facilitated ruptures of the alveolar wall and gas could enter the mediastinum32 or the pulmonary vascular system. The 31 artificial respiration cases included only 14 cases with IHG and thereby had a lower percentage of IHG (45.2%), as compared with the entire population studied (53.2%). In some cases of natural death (cases 85, 90, 101, and 106), resuscitation seems to be the only obvious mechanism allowing gas to enter the vascular system. Other cases with IHG and a traumatic manner of death might have been influenced in their occurrence of intravascular gas by artificial respiration.
Intrahepatic Portal Venous Gas Portal venous gas occurred in 13 cases and exclusively in 2 of them. In clinical radiology portal venous gas is indicative of necrotic bowel disease, e.g. after mesenteric artery occlusion33– 40 or in Crohn disease.41,42 Blunt traumatic injury is rarely considered to cause portal venous gas but an increasing number of case reports describe the finding of portal venous gas without necrotic bowel diseases.21,43– 46 Portal venous gas was also described in child abuse.47 The two cases with exclusively portal venous gas (cases 69 and 86) need a more detailed discussion. Case 69 was based on a person who was hit by a motorcycle and suffered fatal abdominal blunt trauma indicating traumatic damage of the mucosa allowing intestinal gas to enter the portal venous system. Case 86 was based on a person who succumbed to lethal oral intoxication with severe necrosis of the intestinal mucosa and grade 2 distention. In these two cases, we assume a damage to the barrier between the intestinal lumen and the capillary bed of the mesentery to be responsible for the portal venous gas, comparable to the clinical experience in necrotic bowel disease. All additional cases with portal venous gas either already showed putrefaction signs or also presented with gas in further hepatic vessels. Because most of them also had suffered trauma, we assume the mechanism of the gas entry to the portal vein was through the capillary bed of the intestine after Volume 62 • Number 4
arterial gas embolism. This may be supported by the 10 cases that showed a combination of hepatic artery gas embolism and portal venous gas as the mesenterial arteries are branching in anatomic correlation to the celiac trunk. Massive amounts of portal venous gas were also present in strangulation (case 87). Knowing the severe barotrauma caused arterial gas embolism including the mesenterial arteries in this case we postulate a passage of the arterial gas via the mesenteric capillary bed into the portal vein as cause for the massive portal venous gas (Fig. 5). Systemic arterial gas that does not enter the supra-aortic arteries will predominantly accumulate within the celiac trunk and the mesenteric arteries as these are the nondependent branches of the abdominal aorta when death occurs in supine position, such as under intensive care or resuscitation.
Burned Corpses In burned corpses (cases 56, 58, and 79), the gas distribution did not follow the above-mentioned rules. The development of intravascular gas was assumed to be caused by heat in all vessels. Remarkable is the fact that burned corpses were the only exception that showed IHG without systemic gas embolism. The heat affected predominantly the surface of the trunk and the IHG was found in the periphery of the liver.
Putrefaction Putrefaction was only found to be a cause of relevant volumes of IHG in cases that showed radiologic signs of putrefaction or when signs of putrefaction were noticed during autopsy. This was based on the results of Pedal et al.48 who investigated intracardiac gas in 111 autopsy cases chromatographically. They found putrefaction gas in 64 cases, of which only 6 had no note of putrefaction within the autopsy protocol. The lack of chromatographic confirmation of putrefaction gas is a limitation of our retrospective study. The earliest time that putrefaction gas starts developing is considered to be 148 to 2 days49,50 postmortem. Thus, in some cases with a PMI of more than 1 day, the measured gas volumes might have been influenced by beginning putrefaction. However, we assume that this is not a relevant influence on the volume of gas until secure signs of putrefaction are noticed either at autopsy or in postmortem imaging. This can be supported by the mean PMI in the group of cases with IHG (after exclusion of the five secure putrefaction cases) and the group without IHG. The mean PMI did not significantly differ between both groups; therefore, a relevant influence of putrefaction is also statistically improbable. In our study, the cases of IHG even showed a slightly shorter mean PMI. This does not exclude the possibility that particular cases with an increased PMI and probably warm postmortem conditions might have already developed putrefaction gas before any macroscopic or radiologic signs. However, our results do not support the assumption of Oliver et al.,51 who presented four cases of diving fatalities and ascribed small amounts of gas within the intrahepatic circulation as a postmortem alter985
The Journal of TRAUMA威 Injury, Infection, and Critical Care
Fig. 5. Intrahepatic gas without putrefaction. Axial MSCT images (small figures in the middle) and corresponding air structure reconstructions of the abdomen in an anteroposterior view. (A) Case 78: only the hepatic vein system (arrow) is involved in the gas embolism; ( B) case 69: the intrahepatic gas is located exclusively in the portal vein system (dashed arrow); (C) case 87: intrahepatic gas is located predominantly in the intrahepatic portal vein system (dashed arrow) in combination with small amounts within hepatic artery branches (note the doubled course, doubled arrows); (D) case 36: the intrahepatic gas because of venous and arterial air embolism within hepatic vein/inferior vena cava (arrow), hepatic artery/celiac trunk (doubled arrows), and intrahepatic portal branches (dashed arrow).
ation because of putrefaction. They supported their explanation by the presentation of a control scan of a head shot wound case with a PMI of 27 hours, which also showed gas within the liver vessels. As shown in our results, IHG is a very frequent finding in craniocerebral trauma and it is mostly because of venous air embolism. In our opinion, Oliver’s case was not a proof of early postmortem putrefaction gas formation in postmortem imaging. However, decompression in scuba diving accidents has also to be considered as a potential cause of IHG in postmortem computed tomography examination, although the circumstances should normally give enough clues to the cause. Impressive amounts of gas within the liver vessels in scuba diving accidents were shown in postmortem computed tomography by several authors.51,52 Besides putrefaction gas and decompression, an early postmortem nonbacterial CO2 formation50,53 has to be discussed as a possible source of gas bubbles in postmortem MSCT examinations. Within the supravital period, the pro986
duction of CO2 via the aerobic metabolism can last up to 10 to 15 hours postmortem. Additionally, the increase in lactate levels54 because of the supravital glycolysis will cause an increased release of CO2 from the bicarbonate of the blood.50 The protein decomposition furthermore leads to increasing CO2 within the blood.55 In particular cases, the gas volume might be slightly influenced by these reactions but the 37 cases without IHG argue against a relevant systematic postmortem CO2 formation.
Intestinal Distention Investigation of intestinal distention did not reveal any obvious relation to the occurrence of IHG except for grade 3 distention. Intestinal distention of grades 0 to 2 seemed not to have an effect on the finding of IHG because the occurrence of IHG was not increased compared with the cases without distention. In 5 of 6 cases (83.3%) with grade 3 intestinal distention IHG occurred. The small number of cases does not allow for any conclusion. April 2007
IHG at Postmortem CT As seen in Table 1, similar gas volumes were not always subjectively graded within the same group. Especially small volumes (1– 4 mL) were variably graded between grade 1 and 2. We assume this to be caused by a different gas distribution within the liver. The volume distributed within many small vessels may lead to an underestimation and the same volume seen within fewer but major vessels may act conversely. We appraise the objectively measured gas volumes as more valuable when compared with the subjective observer dependant grading. When putrefaction and other processes contributing to postmortem gas development, such as burning or local microbiologic infections (clostridia), can be excluded, distinct volumes of IHG represent a so-called vital sign.1 Although the transport into the liver vessels may also occur passively postmortem, its entrance into the systemic circulation and its distribution within the body needs an ongoing circulation. Especially hepatic arterial gas embolism depends on an antegrade blood flow. Besides all forensic causes of IHG, nonforensic clinical entities have to be taken into consideration, such as gas gangrene within the intestine and abdomen,56 enteritis and colitis,35,57 cholangitis,35 seizure,58 or idiopathic gas.59,60
7.
8.
9.
10.
11.
12.
13.
14.
CONCLUSION
15.
IHG is a frequent finding in postmortem imaging in forensic medicine. The most common cause is of a traumatic nature because of craniocerebral trauma or blunt forces. It is strongly related to the occurrence of systemic gas embolism.
16.
ACKNOWLEDGMENTS We would like to thank the team of MTRA’s (Karin Zwygart, Verena Beutler, Elke Spielvogel, Christoph Laeser, and Carolina Dobrowolska) for their excellent help in acquiring the scans within the virtopsy project as well as Urs Ko¨nigsdorfer and Roland Dorn for their experienced assistance at autopsy and Therese Pe´rinat for the histologic preparations as well as Naseem J. Malik for the support in article preparation.
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