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Serial postmortem abdominal radiographic findings in canine cadavers
Forensic Science International 192 (2009) 43–47
Contents lists available at ScienceDirect
Forensic Science International journal homepage: www.elsevier.com/locate/forsciint
Serial postmortem abdominal radiographic findings in canine cadavers Hock Gan Heng a,b,*, Gayathri Thevi Selvarajah b,c, Hiang Tee Lim b, Jin Seng Ong b, Jiehan Lim b, Jin Tatt Ooi b a
Department of Veterinary Clinical Sciences, Purdue University, 625, Harrison Street, West Lafayette, IN 4790, USA Faculty of Veterinary Medicine, Universiti Putra Malaysia, 43400 Serdang, Selangor, Malaysia c Department of Clinical Sciences of Companion Animals, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 104, 3584 CM, Utrecht, Netherlands b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 19 September 2008 Received in revised form 22 May 2009 Accepted 22 July 2009 Available online 29 August 2009
Postmortem radiographic examinations of animals are often performed in judicial investigation to rule out gunshot and fractures due to cruelty or illegal hunting or poaching activities. Literature describing postmortem changes seen on radiographs of animals is rarely available. Serial abdominal radiography of 6 recently euthanized dogs were performed in an interval of 8 h at a tropical ambient temperature of 22– 33 8C. Severe decomposition of the cadavers prevented the study to be performed beyond 24 h. Gradual increment of gas accumulation in the gastrointestinal tract, liver, spleen, kidney and blood vessels were observed. Increased amount of gas in the gastrointestinal tract was detected as early as 8 h posteuthanasia and continuously increased throughout the study. Gas was seen in the portal vein and caudal vena cava of all cadavers at 16 h post-euthanasia. The presence of gas in the aorta occurred at a later stage. Tubular branching gas pattern in the liver and spleen was first observed and progressed to vesicular gas pattern due to tissue decomposition. This study showed that abdominal radiographic postmortem changes occurred most rapidly between 8 and 16 h post-euthanasia at the ambient temperature of 22–33 8C. ß 2009 Elsevier Ireland Ltd. All rights reserved.
Keywords: Postmortem radiograph Canine cadavers Abdomen
1. Introduction Postmortem radiographic examination as an ancillary investigation prior to traditional necropsy can detect changes which could not easily been seen on traditional necropsy [1–3]. Forensic radiology in animals is often performed in judicial investigation to rule out gunshot and fractures due to cruelty or illegal hunting or poaching activities [2,4]. A whole body skeletal radiological survey is recommended before an autopsy on a suspected fatal case of abused animals and humans as the abused victims were more likely to have multiple fractures [1–3]. Postmortem radiographic examination of a dead cat revealed multiple sites of venous air embolism as a result of air entering the venous system by crossing damaged vascular walls secondary to insufflation of a pharyngeal diverticulum prior to death [5]. Radiological detection of intravascular gas in dead fetuses in dogs with late term pregnancies had been reported [6].
* Corresponding author at: Department of Veterinary Clinical Sciences, Purdue University, 625, Harrison Street, West Lafayette, IN 4790, USA. Tel.: +1 765 494 0821; fax: +1 765 494 7276. E-mail address: [email protected] (H.G. Heng). 0379-0738/$ – see front matter ß 2009 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.forsciint.2009.07.016
The use of computed tomography and magnetic resonance in the postmortem radiographic examination is termed virtual autopsy [7,8]. This helped to detect internal bleeding, bullet paths, brain contusion, gas embolism, blood aspiration to the lung and hidden fracture hard to find in a traditional necropsy [7,9,10]. Various post-processing techniques can be used to provide strong forensic evidence for use in legal proceedings [7]. Virtual autopsy supplement and may be partially replacing the conventional necropsy in human medicine. This is because it is more acceptable as many people are dismayed at the idea of the body of their beloved one being mutilated [7]. Computed tomography guided postmortem tissue sampling in human cadavers had been recommended in cases where conventional necropsy is refused [11]. Investigation of an illegal lynx shooting by plane radiography and three-dimensional multislice computed tomography had been reported [4]. Computed tomography evaluation of postmortem changes of the Hounsfield units of melon, bone, blubber and mandibular fat of bottlenose dolphin was performed. It was found that there were no statistically significant differences of Hounsfield units between the live, recently dead and frozen followed thawing samples of the organs examined [12]. Formation of putrefactive gas in the vascular system, body cavities and soft tissues secondary to decomposition of the cadavers makes interpretation of postmortem radiology of the
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thorax and abdomen in both human and animal more complicated [7,13]. In humans, postmortem CT had identified gas in the hepatic portal veins associated with gastrointestinal distension [14], in the cardiovascular system secondary to cardiopulmonary resuscitation [15] and in the mediastinum and soft tissue in cadavers of hanged persons [16]. A recent study on postmortem abdominal radiographs of feline cadavers performed within 12 h of death revealed the presence of intravascular gas in 27% of the cadavers [13]. The gas was detected in aorta, femoral artery, celiac and cranial mesenteric arteries, and caudal superficial epigastric artery, and also in the parenchyma of liver and spleen [13]. There were very few veterinary literatures on postmortem radiology [4,5,13]. Information such as the production of putrefactive gas in relation to postmortem interval may be helpful in estimating the time of death in animals. In addition to this, knowledge of normal postmortem radiographic findings is needed to interpret the differentiation between antemortem injuries and postmortem artifacts especially in cases involving medicolegal investigation [17]. Therefore, this prospective study was conducted to document the postmortem radiographic changes in relation to postmortem interval in the abdomen of canine cadavers. 2. Materials and methods Six pound dogs consisting of 4 males and 2 females from Kuala Lumpur City Hall, Malaysia, that were scheduled for humane euthanasia were included in this prospective study. General physical examination and basic hematological profiling were carried out on all the 6 dogs. Dogs were observed for defecation and urination as an indication of its state of health. All dogs were fasted for 12 h, however water was provided ad libitum till 2 h prior to humane euthanasia. Euthanasia was carried out using pentobarbitone sodium (6% Sagatal1) at the rate of 60 mg/kg administered intravenously with the application of light muzzle and proper restraining of dogs by well trained personnel. This was performed away from other dogs therefore no fear or unnecessary physiological responses such as vocalization or apparent terminal gasps were observed during or after euthanasia. Left lateral and ventrodorsal abdominal radiographs were performed immediately after euthanasia and an interval of 8 h thereafter. The cadavers were kept at the normal average ambient temperature of 22–33 8C on left lateral recumbency and was only manipulated every 8 hourly for the positioning of radiography. The radiographs were interpreted by a single board-certified radiologist (Heng). Radiographic changes such as the presence of gas and/or fluid in the peritoneal cavity and retroperitoneal space and gas in the blood vessels were observed. The size of the stomach was estimated and the diameter of the small intestines and colon were measured. The width of the small intestines was considered normal when it is less then 1.6 the height of the L5 at its narrowest point. The diameter of the colon was considered normal when it is less then 1.5 the length of L7. A simple in situ necropsy examination was conducted on all cadavers 24 h post-euthanasia.
3. Results 3.1. Physical examination and hematology Generally the dogs were healthy with no apparent abnormalities. They were all adult local dogs of similar body size with a body condition scores between 2 and 3 out of 5. Palpation of the abdomen did not reveal any pain or mass. Diarrhea was not observed in any dogs. Urination was normal in all dogs. The body temperature and pulse were within normal range. Auscultation of the thorax revealed normal lung sound. Abdominal palpation was not performed in 1 dog because it was not approachable due to its fierce temperament. Mild leukocytosis ranging from 19.3 to 25 109/L was observed in 3 of the 6 dogs. Other hematological and biochemistry parameters were unremarkable. All dogs had radiographs taken immediately post-euthanasia, as well as at 8 and 16 h post-euthanasia. All cadavers became stiffened at 8 h post-euthanasia. Bleeding from nose and gross distention of abdomen was present at 16 h post-euthanasia. Radiographs were not made in 3 cadavers at 24 h post-euthanasia due to extremely distended abdomen and excessive serosanguineous discharges from the orifices.
3.2. Radiographic findings The peritoneal cavity and retroperitoneal space were normal immediately after euthanasia. Small amount of peritoneal gas was detected at 8 h post-euthanasia in 1 cadaver. Gas was present in the peritoneal cavity of all and in the retroperitoneal space of 4 cadavers at 16 h post-euthanasia. Abdominal distension due to free gas in the peritoneal cavity in 5 cadavers was evident at this point of time. There was continuous increase of the amount of peritoneal gas and abdominal distention, and development of retroperitoneal gas in 1 cadaver at 24 h post-euthanasia (Fig. 1). Liver was normal in all cadavers immediately after euthanasia. At 8 h post-euthanasia, intrahepatic gas in a manner of tubular branching pattern was present in 2 cadavers. The livers of the remaining 4 cadavers were normal. Intrahepatic gas was present in all cadavers at 16 h post-euthanasia: 1 with tubular branching, 1 with vesicular and 4 with mixed tubular branching and vesicular pattern. The intrahepatic vesicular gas pattern developed following the tubular branching gas pattern in 2 cadavers. At 24 h post-euthanasia, intrahepatic gas was seen in all the 3 cadavers: 2 vesicular patterns which progressed from tubular branching pattern and 1 mixed tubular branching and vesicular pattern. Spleen was normal in all cadavers immediately after euthanasia. Intrasplenic tubular branching gas pattern was present in 1 cadaver at 8 h post-euthanasia. Intrasplenic vesicular gas pattern was present in 3 cadavers at 16 h post-euthanasia. The spleen of 1 cadaver was normal and was not identified in 2 cadavers. Intrasplenic tubular branching gas pattern in 1 cadaver progressed to become vesicular gas pattern in 1 cadaver at 24 h posteuthanasia. The previously seen normal spleen had developed intrasplenic tubular branching gas pattern at this point of time. Spleen in 1 cadaver was not identified. Gas in the portal vein and caudal vena cava was seen at 8 h post-euthanasia in 1 cadaver. Gas in the caudal vena cava was present in all the 6 cadavers at 16 h post-euthanasia. Other blood vessels where gas could be detected during this time were abdominal aorta (2), femoral artery (2), caudal superficial epigastric artery (1), internal iliac artery (2) and portal vein (1). Progressive increment of the amount of gas in the blood vessels was observed at 24 h post-euthanasia and gas in the aorta, caudal vena cava and femoral artery was seen in all the 3 cadavers. Tubular branching gas was present in the right renal parenchyma in 1 cadaver at 16 h and persists at 24 h posteuthanasia (Fig. 1E). Gas in the internal iliac arteries in 1 cadaver was observed. There was slight increase in size of the stomach with gas in 1 cadaver at 8 h post-euthanasia. At 16 h post-euthanasia, stomach of 1 cadaver had become extremely distended with gas; 2 cadavers had slightly distended and 2 cadavers had unchanged size of the stomach. The excessive accumulation of the free peritoneal gas and presumed much stretched stomach wall making the stomach wall difficult to visualized thus the stomach was not identified in the radiographs of 24 h post-euthanasia. The small intestines were normal in size immediately posteuthanasia. There was an increase in the amount of small intestinal gas in all cadavers. The small intestines were doubled in size in 4 cadavers at 8 h post-euthanasia. All the 6 cadavers had gas distended small intestines of 2–3 times the initial width at 16 h post-euthanasia. All of them had very prominent gas filled duodenum. The size of the gas distended small intestines was unchanged in 2 cadavers and slight increase of width in 1 cadaver at 24 h post-euthanasia. The colon was filled with feces and gas with normal size immediately post-euthanasia. At 8 h post-euthanasia, there was an increase in the amount of gas in 3 cadavers with same size. The
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Fig. 1. Serial lateral abdominal radiographs of a male dog. (A) Immediate after euthanasia. There are no abnormalities of the abdomen. (B) 8 h after euthanasia. There is faint tubular gas pattern in the liver. The small intestines and colon are more gas distended. Some loops of the intestines are distended beyond the normal limits (which is now >1.6 the narrowest point of the body of L5). The transverse colon is gas filled and distended beyond the normal limits. (C) 16 h after euthanasia. There is moderate amount of free gas present in the peritoneal and retroperitoneal cavities which leads to slight abdominal distension. There is further gas distension of the small intestines. Most of the intestinal loops are distended beyond normal limits. Tubular and vesicular gas pattern is present in the liver. There is vesicular gas pattern in the spleen. Gas is present in the cranial abdominal aorta, caudal vena cava and femoral arteries. (D) 24 h after euthanasia. There is large amount of free gas in the peritoneal and retroperitoneal cavities causing marked distension of the abdomen. The previously seen tubular gas pattern of the liver is less evident and it is predominantly replaced by vesicular gas pattern. There is still vesicular gas pattern in the spleen. There is a further increased visualization of the gas filled femoral arteries. Subcutaneous emphysema is present and it is more prominent at the cranial abdomen. The previously seen tubular gas pattern in the kidney is unchanged. It is difficult to see the caudal vena cava. (E) Close-up view of the right cranial abdomen of the ventrodorsal radiograph at 16 h post-euthanasia. Tubular gas pattern is present in the right kidney. A gas filled moderately distended duodenum is superimposed over the right kidney.
colon could not be differentiated from the gas filled distended small intestines in 3 cadavers. At 16 h post-euthanasia, it was not possible to differentiate the colon from the gas distended small intestines in 5 cadavers. The colon was slightly more gas distended in 1 cadaver. The colon was unchanged at 24 h posteuthanasia. The size of the urinary bladder was consistent throughout the study in all cadavers. There was no evidence of intraparenchymal gas in the prostate of the cadavers. Severe subcutaneous emphysema developed in 1 cadaver at 16 h post-euthanasia. Additional cadaver developed subcutaneous emphysema at 24 h post-euthanasia.
3.3. In situ gross necropsy findings Three cadavers had severe distension of the abdomen and large amount of serosanguineous discharges from the natural orifices. Grossly, the abdominal organs of all dogs were anatomically normal and there was a high degree of decomposition of all organs. There was gaseous distension of the stomach, small intestines and colon in all dogs. The mucosa of the intestines appeared thin due to distension, but no evidence of perforation or rupture of the intestines causing spillage of its contents into the abdominal cavity was observed. The livers were soft with the presence of gas distended bubbles on the parenchyma. The spleens and pancreas
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were mushy and friable while the kidneys were slimy and discolored. Generally the cadavers were consistent with the advanced stage of postmortem decomposition. 4. Discussion The physical examination performed confirmed that all dogs were healthy without apparent disease prior to euthanasia. The slight leukocytosis observed in 3 dogs could merely be due to the immunological response towards boarding and transportation stress prior to blood collection. Since other parameters tested were within normal limits, we excluded possible causes for infections or septicemia. This is an important exclusion because in septicemia conditions, body decomposition can be accelerated and this could affect the radiographic postmortem changes observed. All cadavers developed rigor mortis (stiffness of the muscles of body after death) within the first 8 h of death. This made the positioning of the cadavers for radiographic procedure difficult. In human cadavers, maximum stiffness of rigor mortis developed within 6–12 h of death [18]. The initial plan for the project was to obtain the abdominal radiographs at 8 h interval post-euthanasia until 48 h. This was not performed due to severe postmortem decomposition of the cadavers. Decomposition is the disintegration of body tissue after death. This followed the arrest of the biochemical processes which preserve the integrity of the cellular and subcellular membranes and organelles. Two parallel processes of decomposition are autolysis (self dissolution by body enzymes released for the disintegrating cells) and putrefaction (decomposition changes produced by the action of microorganisms) [18,19]. The project was terminated 24 h post-euthanasia because all cadavers were severely decomposed and manipulation of the cadavers was difficult. Some organs were not able to be identified on the radiographs at 24 h post-euthanasia due to massive gas accumulation in the small intestines and the peritoneal cavity. The increased amount of gas in the small intestines and colon was detected as early as 8 h post-euthanasia and occurred continuously throughout the study. Although gas was detected in the parenchyma of liver and spleen, peritoneal cavity, retroperitoneal space and blood vessels at 8 h post-euthanasia, it generally developed in the abdomen of the canine cadavers between 8 and 16 h post-euthanasia. Subcutaneous emphysema developed 16 h post-euthanasia. This observation suggests that detection of gas in the abdomen may be used to estimate the time of death within the first 24 h under the prescribed ambient temperature of 22–33 8C. This study agrees with the proposal of intrahepatic gas as a putrefaction process [13] and not due to disease process such as abdominal visceral injury, bowel distension secondary to artificial respiration, acute circulatory dysfunction or open trauma leading to vessel luminal gained access to ambient air [14,15,20,21]. There were no obvious infections or abnormality of the dogs or surgical procedures performed on them prior to euthanasia. Furthermore, the presence of increased amount of gas in the small intestines and colon preceded gas in the other organs’ system. Under average temperature climate, the intestinal bacteria produced large amounts of foul-smelling gas that flows into the blood vessels and tissue 2–3 days after death in human corpses [18]. This could be recognized at postmortem imaging due to massive gas accumulation within the vascular system, body cavities and soft tissues [7]. In this study, putrefaction of the cadavers occurred rapidly within the first 8 h post-euthanasia. The progression of the putrefaction was indicated by the gradual increment of the amount of putrefactive gas detected over 24 h period. The rate of putrefaction is influenced by many factors such as ambient temperature, and prior state of health of the individual such as
sepsis, fever and thickness of insulating layer of body fat [19,22]. High ambient temperature setting in this study may play a major role in the acceleration of the rate of putrefaction. There was no evidence of sickness that could lead to higher body temperature prior to death in the dogs. All dogs were fasted 12 h prior to euthanasia and had very minimal gas in the stomach and the rate of gas accumulation in the stomach was slower than the small intestines. Generally, enzymatic reactions that occur with autolysis and putrefaction are inhibited by low temperatures of refrigerators [22]. Intravascular gas was detected in only 27% of feline cadavers within 12 h of death kept at 4 8C compared to 100% of canine cadavers developed intravascular gas within 16 h posteuthanasia in this study [13]. In the feline cadavers study, the small bowel distension was minimal. Again this was most likely due to the different ambient temperatures in these two studies and the rate of putrefaction was slow in the feline cadavers. Other possible cause for the different rates of putrefaction in humans and dogs is the different amount of normal flora in the small intestines. The small intestines of dogs contain larger number of normal flora compared to humans [23–25] and this may lead to rapid production of putrefactive gas in the dogs. Intraparenchymal gas of liver was detected in postmortem radiology in both humans and animals [7,13]. Postmortem detection of intraparenchymal gas of the spleen and kidney was not reported in humans. Postmortem detection of splenic gas was reported in cats [13]. In this current study, gas was initially present in tubular branching pattern in the liver and spleen. This indicates that the gas was in the hepatic portal veins and also spleen veins. This was mainly due to centrifugal movement of gas in the portal vein. In the later stage, vesicular gas pattern dominated in both liver and spleen [26]. The changes of the gas pattern seen are probably due to escape of gas from the intraparenchymal blood vessels into the parenchyma secondary to autolysis of both organs [22]. The detection of vesicular gas pattern alone indicates the advanced stage of decomposition of the cadavers mainly involving autolysis of the organ parenchyma. In a recent publication, the intrahepatic gas was determined to be in the hepatic arteries, veins and hepatic portal branches [20]. The presence of gas in the hepatic arteries and veins was most likely related to trauma and associated with systemic gas embolism. Although there were no crosssectional images in this study, we are confident to determine that the intrahepatic gas was indeed in the hepatic portal veins due to its progressive nature of gas movement. The presence of tubular branching gas pattern in the liver preceded the gas in the aorta. Tubular branching gas pattern of the kidney was only observed in 1 cadaver at 16 and 24 h post-euthanasia. We speculate that if the study was performed beyond 24 h, the number of cadavers having intraparenchymal gas in the kidney will increase. This is most likely again due to centrifugal movement of gas in the portal vein. The internal organs putrefy at markedly different rates. The intestine and pancreas autolyse within hours of death because the usual intracellular autolysis is abetted by the action of the now uninhibited digestive juices [18,22]. The prostate and uterus may still be recognizable in a partially skeletonized body even a year later [18]. The pancreas was not recognized in the radiograph thus the changes could not be documented. There were no radiographic changes of the prostate and urinary bladder as they decomposed at a slow rate. Postmortem radiology is becoming popular in veterinary medicine. This is due to pets becoming an important part of most families and being humanized by the owners. Postmortem radiology investigation should be offered if the owners refuse a traditional necropsy. This should be performed within a short interval of death if the cadaver is stored at normal ambient temperature due to the rapid decomposition changes. In a forensic investigation, the cadaver should be stored at a lower ambient
H.G. Heng et al. / Forensic Science International 192 (2009) 43–47
temperature to reduce the rate of decomposition prior to radiographic procedure. Acknowledgements This work was supported by a grant from Veterinary Teaching Hospital, Universiti Putra Malaysia. We thank Ms. Sandy Campbell for her assistance in manuscript preparation. References [1] J.E. Cooper, M.E. Cooper, Introduction to Veterinary and Comparative Forensic Medicine, Blackwell Publishing, Oxford Ames, IA, 2007. [2] M.D. Merck, Veterinary Forensics: Animal Cruelty Investigations, Blackwell Publishing, Ames, IA, 2007. [3] P. Saukko, B. Knight, The forensic autopsy, in: P. Saukko, B. Knight (Eds.), Knight’s Forensic Pathology, Arnold, London/New York, 2004, pp. 1–51. [4] M.J. Thali, B.P. Kneubuehl, S.A. Bolliger, A. Christe, U. Koenigsdorfer, C. Ozdoba, E. Spielvogel, R. Dirnhofer, Forensic veterinary radiology: ballistic-radiological 3D computer tomographic reconstruction of an illegal lynx shooting in Switzerland, Forensic Sci. Int. 171 (2007) 63–66. [5] C.P. Ober, T.C. Spotswood, R. Hancock, Fatal venous air embolism in a cat with a retropharyngeal diverticulum, Vet. Radiol. Ultrasound 47 (2006) 153–158. [6] C.S. Farrow, J.P. Morgan, E.C. Story, Late term fetal death in the dog: early radiographic diagnosis, J. Am. Vet. Radiol. Soc. 17 (1976) 7. [7] R. Dirnhofer, C. Jackowski, P. Vock, K. Potter, M.J. Thali, VIRTOPSY: minimally invasive, imaging-guided virtual autopsy, Radiographics 26 (2006) 1305–1333. [8] M.J. Thali, M. Braun, U. Buck, E. Aghayev, C. Jackowski, P. Vock, M. Sonnenschein, R. Dirnhofer, VIRTOPSY—scientific documentation, reconstruction and animation in forensic: individual and real 3D data based geo-metric approach including optical body/object surface and radiological CT/MRI scanning, J. Forensic Sci. 50 (2005) 428–442. [9] E. Aghayev, M. Sonnenschein, C. Jackowski, M. Thali, U. Buck, K. Yen, S. Bolliger, R. Dirnhofer, P. Vock, Postmortem radiology of fatal hemorrhage: measurements of cross-sectional areas of major blood vessels and volumes of aorta and spleen on MDCT and volumes of heart chambers on MRI, Am. J. Roentgenol. 187 (2006) 209– 215. [10] K. Yen, M. Sonnenschein, M.J. Thali, C. Ozdoba, J. Weis, K. Zwygart, E. Aghayev, C. Jackowski, R. Dirnhofer, Postmortem multislice computed tomography and magnetic resonance imaging of odontoid fractures, atlantoaxial distractions and ascending medullary edema, Int. J. Legal Med. 119 (2005) 129–136.
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Contents lists available at ScienceDirect
Forensic Science International journal homepage: www.elsevier.com/locate/forsciint
Serial postmortem abdominal radiographic findings in canine cadavers Hock Gan Heng a,b,*, Gayathri Thevi Selvarajah b,c, Hiang Tee Lim b, Jin Seng Ong b, Jiehan Lim b, Jin Tatt Ooi b a
Department of Veterinary Clinical Sciences, Purdue University, 625, Harrison Street, West Lafayette, IN 4790, USA Faculty of Veterinary Medicine, Universiti Putra Malaysia, 43400 Serdang, Selangor, Malaysia c Department of Clinical Sciences of Companion Animals, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 104, 3584 CM, Utrecht, Netherlands b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 19 September 2008 Received in revised form 22 May 2009 Accepted 22 July 2009 Available online 29 August 2009
Postmortem radiographic examinations of animals are often performed in judicial investigation to rule out gunshot and fractures due to cruelty or illegal hunting or poaching activities. Literature describing postmortem changes seen on radiographs of animals is rarely available. Serial abdominal radiography of 6 recently euthanized dogs were performed in an interval of 8 h at a tropical ambient temperature of 22– 33 8C. Severe decomposition of the cadavers prevented the study to be performed beyond 24 h. Gradual increment of gas accumulation in the gastrointestinal tract, liver, spleen, kidney and blood vessels were observed. Increased amount of gas in the gastrointestinal tract was detected as early as 8 h posteuthanasia and continuously increased throughout the study. Gas was seen in the portal vein and caudal vena cava of all cadavers at 16 h post-euthanasia. The presence of gas in the aorta occurred at a later stage. Tubular branching gas pattern in the liver and spleen was first observed and progressed to vesicular gas pattern due to tissue decomposition. This study showed that abdominal radiographic postmortem changes occurred most rapidly between 8 and 16 h post-euthanasia at the ambient temperature of 22–33 8C. ß 2009 Elsevier Ireland Ltd. All rights reserved.
Keywords: Postmortem radiograph Canine cadavers Abdomen
1. Introduction Postmortem radiographic examination as an ancillary investigation prior to traditional necropsy can detect changes which could not easily been seen on traditional necropsy [1–3]. Forensic radiology in animals is often performed in judicial investigation to rule out gunshot and fractures due to cruelty or illegal hunting or poaching activities [2,4]. A whole body skeletal radiological survey is recommended before an autopsy on a suspected fatal case of abused animals and humans as the abused victims were more likely to have multiple fractures [1–3]. Postmortem radiographic examination of a dead cat revealed multiple sites of venous air embolism as a result of air entering the venous system by crossing damaged vascular walls secondary to insufflation of a pharyngeal diverticulum prior to death [5]. Radiological detection of intravascular gas in dead fetuses in dogs with late term pregnancies had been reported [6].
* Corresponding author at: Department of Veterinary Clinical Sciences, Purdue University, 625, Harrison Street, West Lafayette, IN 4790, USA. Tel.: +1 765 494 0821; fax: +1 765 494 7276. E-mail address: [email protected] (H.G. Heng). 0379-0738/$ – see front matter ß 2009 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.forsciint.2009.07.016
The use of computed tomography and magnetic resonance in the postmortem radiographic examination is termed virtual autopsy [7,8]. This helped to detect internal bleeding, bullet paths, brain contusion, gas embolism, blood aspiration to the lung and hidden fracture hard to find in a traditional necropsy [7,9,10]. Various post-processing techniques can be used to provide strong forensic evidence for use in legal proceedings [7]. Virtual autopsy supplement and may be partially replacing the conventional necropsy in human medicine. This is because it is more acceptable as many people are dismayed at the idea of the body of their beloved one being mutilated [7]. Computed tomography guided postmortem tissue sampling in human cadavers had been recommended in cases where conventional necropsy is refused [11]. Investigation of an illegal lynx shooting by plane radiography and three-dimensional multislice computed tomography had been reported [4]. Computed tomography evaluation of postmortem changes of the Hounsfield units of melon, bone, blubber and mandibular fat of bottlenose dolphin was performed. It was found that there were no statistically significant differences of Hounsfield units between the live, recently dead and frozen followed thawing samples of the organs examined [12]. Formation of putrefactive gas in the vascular system, body cavities and soft tissues secondary to decomposition of the cadavers makes interpretation of postmortem radiology of the
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thorax and abdomen in both human and animal more complicated [7,13]. In humans, postmortem CT had identified gas in the hepatic portal veins associated with gastrointestinal distension [14], in the cardiovascular system secondary to cardiopulmonary resuscitation [15] and in the mediastinum and soft tissue in cadavers of hanged persons [16]. A recent study on postmortem abdominal radiographs of feline cadavers performed within 12 h of death revealed the presence of intravascular gas in 27% of the cadavers [13]. The gas was detected in aorta, femoral artery, celiac and cranial mesenteric arteries, and caudal superficial epigastric artery, and also in the parenchyma of liver and spleen [13]. There were very few veterinary literatures on postmortem radiology [4,5,13]. Information such as the production of putrefactive gas in relation to postmortem interval may be helpful in estimating the time of death in animals. In addition to this, knowledge of normal postmortem radiographic findings is needed to interpret the differentiation between antemortem injuries and postmortem artifacts especially in cases involving medicolegal investigation [17]. Therefore, this prospective study was conducted to document the postmortem radiographic changes in relation to postmortem interval in the abdomen of canine cadavers. 2. Materials and methods Six pound dogs consisting of 4 males and 2 females from Kuala Lumpur City Hall, Malaysia, that were scheduled for humane euthanasia were included in this prospective study. General physical examination and basic hematological profiling were carried out on all the 6 dogs. Dogs were observed for defecation and urination as an indication of its state of health. All dogs were fasted for 12 h, however water was provided ad libitum till 2 h prior to humane euthanasia. Euthanasia was carried out using pentobarbitone sodium (6% Sagatal1) at the rate of 60 mg/kg administered intravenously with the application of light muzzle and proper restraining of dogs by well trained personnel. This was performed away from other dogs therefore no fear or unnecessary physiological responses such as vocalization or apparent terminal gasps were observed during or after euthanasia. Left lateral and ventrodorsal abdominal radiographs were performed immediately after euthanasia and an interval of 8 h thereafter. The cadavers were kept at the normal average ambient temperature of 22–33 8C on left lateral recumbency and was only manipulated every 8 hourly for the positioning of radiography. The radiographs were interpreted by a single board-certified radiologist (Heng). Radiographic changes such as the presence of gas and/or fluid in the peritoneal cavity and retroperitoneal space and gas in the blood vessels were observed. The size of the stomach was estimated and the diameter of the small intestines and colon were measured. The width of the small intestines was considered normal when it is less then 1.6 the height of the L5 at its narrowest point. The diameter of the colon was considered normal when it is less then 1.5 the length of L7. A simple in situ necropsy examination was conducted on all cadavers 24 h post-euthanasia.
3. Results 3.1. Physical examination and hematology Generally the dogs were healthy with no apparent abnormalities. They were all adult local dogs of similar body size with a body condition scores between 2 and 3 out of 5. Palpation of the abdomen did not reveal any pain or mass. Diarrhea was not observed in any dogs. Urination was normal in all dogs. The body temperature and pulse were within normal range. Auscultation of the thorax revealed normal lung sound. Abdominal palpation was not performed in 1 dog because it was not approachable due to its fierce temperament. Mild leukocytosis ranging from 19.3 to 25 109/L was observed in 3 of the 6 dogs. Other hematological and biochemistry parameters were unremarkable. All dogs had radiographs taken immediately post-euthanasia, as well as at 8 and 16 h post-euthanasia. All cadavers became stiffened at 8 h post-euthanasia. Bleeding from nose and gross distention of abdomen was present at 16 h post-euthanasia. Radiographs were not made in 3 cadavers at 24 h post-euthanasia due to extremely distended abdomen and excessive serosanguineous discharges from the orifices.
3.2. Radiographic findings The peritoneal cavity and retroperitoneal space were normal immediately after euthanasia. Small amount of peritoneal gas was detected at 8 h post-euthanasia in 1 cadaver. Gas was present in the peritoneal cavity of all and in the retroperitoneal space of 4 cadavers at 16 h post-euthanasia. Abdominal distension due to free gas in the peritoneal cavity in 5 cadavers was evident at this point of time. There was continuous increase of the amount of peritoneal gas and abdominal distention, and development of retroperitoneal gas in 1 cadaver at 24 h post-euthanasia (Fig. 1). Liver was normal in all cadavers immediately after euthanasia. At 8 h post-euthanasia, intrahepatic gas in a manner of tubular branching pattern was present in 2 cadavers. The livers of the remaining 4 cadavers were normal. Intrahepatic gas was present in all cadavers at 16 h post-euthanasia: 1 with tubular branching, 1 with vesicular and 4 with mixed tubular branching and vesicular pattern. The intrahepatic vesicular gas pattern developed following the tubular branching gas pattern in 2 cadavers. At 24 h post-euthanasia, intrahepatic gas was seen in all the 3 cadavers: 2 vesicular patterns which progressed from tubular branching pattern and 1 mixed tubular branching and vesicular pattern. Spleen was normal in all cadavers immediately after euthanasia. Intrasplenic tubular branching gas pattern was present in 1 cadaver at 8 h post-euthanasia. Intrasplenic vesicular gas pattern was present in 3 cadavers at 16 h post-euthanasia. The spleen of 1 cadaver was normal and was not identified in 2 cadavers. Intrasplenic tubular branching gas pattern in 1 cadaver progressed to become vesicular gas pattern in 1 cadaver at 24 h posteuthanasia. The previously seen normal spleen had developed intrasplenic tubular branching gas pattern at this point of time. Spleen in 1 cadaver was not identified. Gas in the portal vein and caudal vena cava was seen at 8 h post-euthanasia in 1 cadaver. Gas in the caudal vena cava was present in all the 6 cadavers at 16 h post-euthanasia. Other blood vessels where gas could be detected during this time were abdominal aorta (2), femoral artery (2), caudal superficial epigastric artery (1), internal iliac artery (2) and portal vein (1). Progressive increment of the amount of gas in the blood vessels was observed at 24 h post-euthanasia and gas in the aorta, caudal vena cava and femoral artery was seen in all the 3 cadavers. Tubular branching gas was present in the right renal parenchyma in 1 cadaver at 16 h and persists at 24 h posteuthanasia (Fig. 1E). Gas in the internal iliac arteries in 1 cadaver was observed. There was slight increase in size of the stomach with gas in 1 cadaver at 8 h post-euthanasia. At 16 h post-euthanasia, stomach of 1 cadaver had become extremely distended with gas; 2 cadavers had slightly distended and 2 cadavers had unchanged size of the stomach. The excessive accumulation of the free peritoneal gas and presumed much stretched stomach wall making the stomach wall difficult to visualized thus the stomach was not identified in the radiographs of 24 h post-euthanasia. The small intestines were normal in size immediately posteuthanasia. There was an increase in the amount of small intestinal gas in all cadavers. The small intestines were doubled in size in 4 cadavers at 8 h post-euthanasia. All the 6 cadavers had gas distended small intestines of 2–3 times the initial width at 16 h post-euthanasia. All of them had very prominent gas filled duodenum. The size of the gas distended small intestines was unchanged in 2 cadavers and slight increase of width in 1 cadaver at 24 h post-euthanasia. The colon was filled with feces and gas with normal size immediately post-euthanasia. At 8 h post-euthanasia, there was an increase in the amount of gas in 3 cadavers with same size. The
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Fig. 1. Serial lateral abdominal radiographs of a male dog. (A) Immediate after euthanasia. There are no abnormalities of the abdomen. (B) 8 h after euthanasia. There is faint tubular gas pattern in the liver. The small intestines and colon are more gas distended. Some loops of the intestines are distended beyond the normal limits (which is now >1.6 the narrowest point of the body of L5). The transverse colon is gas filled and distended beyond the normal limits. (C) 16 h after euthanasia. There is moderate amount of free gas present in the peritoneal and retroperitoneal cavities which leads to slight abdominal distension. There is further gas distension of the small intestines. Most of the intestinal loops are distended beyond normal limits. Tubular and vesicular gas pattern is present in the liver. There is vesicular gas pattern in the spleen. Gas is present in the cranial abdominal aorta, caudal vena cava and femoral arteries. (D) 24 h after euthanasia. There is large amount of free gas in the peritoneal and retroperitoneal cavities causing marked distension of the abdomen. The previously seen tubular gas pattern of the liver is less evident and it is predominantly replaced by vesicular gas pattern. There is still vesicular gas pattern in the spleen. There is a further increased visualization of the gas filled femoral arteries. Subcutaneous emphysema is present and it is more prominent at the cranial abdomen. The previously seen tubular gas pattern in the kidney is unchanged. It is difficult to see the caudal vena cava. (E) Close-up view of the right cranial abdomen of the ventrodorsal radiograph at 16 h post-euthanasia. Tubular gas pattern is present in the right kidney. A gas filled moderately distended duodenum is superimposed over the right kidney.
colon could not be differentiated from the gas filled distended small intestines in 3 cadavers. At 16 h post-euthanasia, it was not possible to differentiate the colon from the gas distended small intestines in 5 cadavers. The colon was slightly more gas distended in 1 cadaver. The colon was unchanged at 24 h posteuthanasia. The size of the urinary bladder was consistent throughout the study in all cadavers. There was no evidence of intraparenchymal gas in the prostate of the cadavers. Severe subcutaneous emphysema developed in 1 cadaver at 16 h post-euthanasia. Additional cadaver developed subcutaneous emphysema at 24 h post-euthanasia.
3.3. In situ gross necropsy findings Three cadavers had severe distension of the abdomen and large amount of serosanguineous discharges from the natural orifices. Grossly, the abdominal organs of all dogs were anatomically normal and there was a high degree of decomposition of all organs. There was gaseous distension of the stomach, small intestines and colon in all dogs. The mucosa of the intestines appeared thin due to distension, but no evidence of perforation or rupture of the intestines causing spillage of its contents into the abdominal cavity was observed. The livers were soft with the presence of gas distended bubbles on the parenchyma. The spleens and pancreas
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were mushy and friable while the kidneys were slimy and discolored. Generally the cadavers were consistent with the advanced stage of postmortem decomposition. 4. Discussion The physical examination performed confirmed that all dogs were healthy without apparent disease prior to euthanasia. The slight leukocytosis observed in 3 dogs could merely be due to the immunological response towards boarding and transportation stress prior to blood collection. Since other parameters tested were within normal limits, we excluded possible causes for infections or septicemia. This is an important exclusion because in septicemia conditions, body decomposition can be accelerated and this could affect the radiographic postmortem changes observed. All cadavers developed rigor mortis (stiffness of the muscles of body after death) within the first 8 h of death. This made the positioning of the cadavers for radiographic procedure difficult. In human cadavers, maximum stiffness of rigor mortis developed within 6–12 h of death [18]. The initial plan for the project was to obtain the abdominal radiographs at 8 h interval post-euthanasia until 48 h. This was not performed due to severe postmortem decomposition of the cadavers. Decomposition is the disintegration of body tissue after death. This followed the arrest of the biochemical processes which preserve the integrity of the cellular and subcellular membranes and organelles. Two parallel processes of decomposition are autolysis (self dissolution by body enzymes released for the disintegrating cells) and putrefaction (decomposition changes produced by the action of microorganisms) [18,19]. The project was terminated 24 h post-euthanasia because all cadavers were severely decomposed and manipulation of the cadavers was difficult. Some organs were not able to be identified on the radiographs at 24 h post-euthanasia due to massive gas accumulation in the small intestines and the peritoneal cavity. The increased amount of gas in the small intestines and colon was detected as early as 8 h post-euthanasia and occurred continuously throughout the study. Although gas was detected in the parenchyma of liver and spleen, peritoneal cavity, retroperitoneal space and blood vessels at 8 h post-euthanasia, it generally developed in the abdomen of the canine cadavers between 8 and 16 h post-euthanasia. Subcutaneous emphysema developed 16 h post-euthanasia. This observation suggests that detection of gas in the abdomen may be used to estimate the time of death within the first 24 h under the prescribed ambient temperature of 22–33 8C. This study agrees with the proposal of intrahepatic gas as a putrefaction process [13] and not due to disease process such as abdominal visceral injury, bowel distension secondary to artificial respiration, acute circulatory dysfunction or open trauma leading to vessel luminal gained access to ambient air [14,15,20,21]. There were no obvious infections or abnormality of the dogs or surgical procedures performed on them prior to euthanasia. Furthermore, the presence of increased amount of gas in the small intestines and colon preceded gas in the other organs’ system. Under average temperature climate, the intestinal bacteria produced large amounts of foul-smelling gas that flows into the blood vessels and tissue 2–3 days after death in human corpses [18]. This could be recognized at postmortem imaging due to massive gas accumulation within the vascular system, body cavities and soft tissues [7]. In this study, putrefaction of the cadavers occurred rapidly within the first 8 h post-euthanasia. The progression of the putrefaction was indicated by the gradual increment of the amount of putrefactive gas detected over 24 h period. The rate of putrefaction is influenced by many factors such as ambient temperature, and prior state of health of the individual such as
sepsis, fever and thickness of insulating layer of body fat [19,22]. High ambient temperature setting in this study may play a major role in the acceleration of the rate of putrefaction. There was no evidence of sickness that could lead to higher body temperature prior to death in the dogs. All dogs were fasted 12 h prior to euthanasia and had very minimal gas in the stomach and the rate of gas accumulation in the stomach was slower than the small intestines. Generally, enzymatic reactions that occur with autolysis and putrefaction are inhibited by low temperatures of refrigerators [22]. Intravascular gas was detected in only 27% of feline cadavers within 12 h of death kept at 4 8C compared to 100% of canine cadavers developed intravascular gas within 16 h posteuthanasia in this study [13]. In the feline cadavers study, the small bowel distension was minimal. Again this was most likely due to the different ambient temperatures in these two studies and the rate of putrefaction was slow in the feline cadavers. Other possible cause for the different rates of putrefaction in humans and dogs is the different amount of normal flora in the small intestines. The small intestines of dogs contain larger number of normal flora compared to humans [23–25] and this may lead to rapid production of putrefactive gas in the dogs. Intraparenchymal gas of liver was detected in postmortem radiology in both humans and animals [7,13]. Postmortem detection of intraparenchymal gas of the spleen and kidney was not reported in humans. Postmortem detection of splenic gas was reported in cats [13]. In this current study, gas was initially present in tubular branching pattern in the liver and spleen. This indicates that the gas was in the hepatic portal veins and also spleen veins. This was mainly due to centrifugal movement of gas in the portal vein. In the later stage, vesicular gas pattern dominated in both liver and spleen [26]. The changes of the gas pattern seen are probably due to escape of gas from the intraparenchymal blood vessels into the parenchyma secondary to autolysis of both organs [22]. The detection of vesicular gas pattern alone indicates the advanced stage of decomposition of the cadavers mainly involving autolysis of the organ parenchyma. In a recent publication, the intrahepatic gas was determined to be in the hepatic arteries, veins and hepatic portal branches [20]. The presence of gas in the hepatic arteries and veins was most likely related to trauma and associated with systemic gas embolism. Although there were no crosssectional images in this study, we are confident to determine that the intrahepatic gas was indeed in the hepatic portal veins due to its progressive nature of gas movement. The presence of tubular branching gas pattern in the liver preceded the gas in the aorta. Tubular branching gas pattern of the kidney was only observed in 1 cadaver at 16 and 24 h post-euthanasia. We speculate that if the study was performed beyond 24 h, the number of cadavers having intraparenchymal gas in the kidney will increase. This is most likely again due to centrifugal movement of gas in the portal vein. The internal organs putrefy at markedly different rates. The intestine and pancreas autolyse within hours of death because the usual intracellular autolysis is abetted by the action of the now uninhibited digestive juices [18,22]. The prostate and uterus may still be recognizable in a partially skeletonized body even a year later [18]. The pancreas was not recognized in the radiograph thus the changes could not be documented. There were no radiographic changes of the prostate and urinary bladder as they decomposed at a slow rate. Postmortem radiology is becoming popular in veterinary medicine. This is due to pets becoming an important part of most families and being humanized by the owners. Postmortem radiology investigation should be offered if the owners refuse a traditional necropsy. This should be performed within a short interval of death if the cadaver is stored at normal ambient temperature due to the rapid decomposition changes. In a forensic investigation, the cadaver should be stored at a lower ambient
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