Pediatr Radiol (2015) 45:517–526 DOI 10.1007/s00247-014-3258-8
MINISYMPOSIUM: POST MORTEM IMAGING
Normal pediatric postmortem CT appearances Willemijn M. Klein & Dennis G. H. Bosboom & Desiree H. J. L. M. Koopmanschap & Rutger A. J. Nievelstein & Peter G. J. Nikkels & Rick R. van Rijn
Received: 2 September 2014 / Revised: 3 November 2014 / Accepted: 26 November 2014 # Springer-Verlag Berlin Heidelberg 2015
Abstract Postmortem radiology is a rapidly developing specialty that is increasingly used as an adjunct to or substitute for conventional autopsy. The goal is to find patterns of disease and possibly the cause of death. Postmortem CT images bring to light processes of decomposition most radiologists are unfamiliar with. These postmortem changes, such as the formation of gas and edema, should not be mistaken for pathological processes that occur in living persons. In this review we discuss the normal postmortem thoraco-abdominal changes and how these appear on CT images, as well as how to differentiate these findings from those of pathological processes. Keywords Postmortem . Fetus . Child . Whole-body computed tomography . Forensic imaging
Introduction Postmortem imaging techniques are increasingly used to determine the cause of death in adults, children and fetuses. W. M. Klein (*) : D. G. H. Bosboom : D. H. J. L. M. Koopmanschap Department of Radiology and Nuclear Medicine, Radboud University Medical Center, Geert Grooteplein Zuid 10, 6525GA Nijmegen, The Netherlands e-mail:
[email protected] R. A. J. Nievelstein Department of Radiology, University Medical Center Utrecht, Utrecht, The Netherlands P. G. J. Nikkels Department of Pathology, University Medical Center Utrecht, Utrecht, The Netherlands R. R. van Rijn Department of Radiology, Academic Medical Center, Amsterdam, The Netherlands
Postmortem CT is an elegant and fast method of evaluating the body and the cause of death in a noninvasive way, providing visualization of the organs as well as gas and fluid in situ [1, 2]. Conventional autopsy has remained the gold standard, but the number of societal objections to this method is increasing because of its invasiveness and the possibility of unauthorized organ removal [3]. Consequently, noninvasive postmortem imaging techniques are more and more appreciated and preferred by the public. For children, as well as adolescents and adults, postmortem CT is the imaging modality most commonly used for the evaluation of the cause and manner of death. Moreover, postmortem CT can be used in fetuses to focus on the calcified bones [4] and aerated parts. Although it is more time-consuming, MRI can also be very useful in adults and children, especially in fetuses and neonates [3, 5]. In specialist centers postmortem MRI is the preferred visualization method for fetuses and neonates because it can nicely depict congenital malformations of the brain and spinal cord, the intrathoracic and intra-abdominal organs as well as skeletal malformations [6]. A combination of CT or MRI, clinical information, laboratory tests and minimally invasive tissue sampling can maximize diagnostic value [7, 8]. Postmortem radiology interpretation is not the same as for living patients [9]. The radiologist should be aware of normal postmortem changes and avoid misdiagnosing these changes as signs of pathology. Immediately after demise, a series of physical–chemical changes occurs in a fairly orderly way until the body has completely disintegrated. To begin with, the body temperature slowly decreases (algor mortis). The arrest of the heart function causes the circulation to stop, and subsequently sedimentation of the blood cells occurs within the large blood vessels. Then veins and small arteries collapse, and the blood is likely to sag to the small vessels in the dependent parts of the body, which results in color changes to the skin (livor mortis). In the first hour after death the muscles relax (although bowel movements may continue for
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some time). Then the continuing anaerobic chemical processes in the muscles cause adenosine triphosphate (ATP) resources to dry out, resulting in a stiffening of the muscles (rigor mortis). The heart muscle stiffens, as well, and this should not be mistaken for myocardial hypertrophy. This state can last up to 24 h, after which the muscles soften again because of putrefaction [10]. The rate of this decomposition process depends on many factors both inside and outside the body, such as the postmortem interval, the cause of death (nature, trauma, infection), treatment (chemotherapy, resuscitation), clothing, temperature of the body and of the surroundings, air humidity and presence of insects. These features have to be taken into account when interpreting the images of a postmortem CT scan. The interpretation of the postmortem CT images depends on the stage of decomposition. Gas and fluid can be normal findings in the decomposition process; however they must be distinguished from pathological findings that indicate disease and cause of death [11]. We review the normal postmortem changes on thoracoabdominal CT in deceased children. There are only a few cross-sectional studies on postmortem changes, and hardly any prospective information is available on decomposition as it appears on CT images. Also, most studies involve adult rather than pediatric bodies, which is a limitation of this review. Therefore, this article largely represents the expertise of the authors.
Postmortem changes to the body Appearances on postmortem CT, such as gas and fluid, can be normal postmortem findings or they can be a sign of pathology, depending on the peri- and postmortem circumstances of the body and its surroundings. We will discuss this in the following sections. It is important to know the constitution of the body in the perimortem period in order to correctly interpret the postmortem findings and to decide whether these are indicative of disease or normal postmortem changes. For instance, the radiologist needs to know the symptoms and duration of a possible disease, the presence of fever, the started therapies and attempts of resuscitation, and the postmortem interval.
Postmortem interval The constitution of the deceased body changes over time because organ functioning and cellular processes have ceased. The decomposition increases with the postmortem interval (i.e. the time passed since the moment of death). We found no pediatric studies on this subject. One prospective study on adults evaluated the intrahepatic gas on postmortem CT [12]
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but no other prospective data were available about this process and how it appears on CT. The influence of many factors on the rate of decay can be estimated from experience [13, 14]. Visible changes on CT in the body begin with the collapse of the vessels and the sedimentation of blood cells soon after the heart has stopped beating and circulation has ended (Figs. 1 and 2). After the last expiration, the volume of the lungs decreases and fluid becomes visible in the intrapulmonary septa, comparable to an expiration CT in a living person. However, the pulmonary volume loss continues and intraseptal edema and pleural fluid increase over hours [15] (Fig. 3).
Bowel distention Energy (adenosine triphosphate, ATP) and oxygen levels quickly drop within the first few hours after demise, which causes cell and membrane functioning to slowly come to an end [16]. This may be one of the reasons fluid sinks through the capillary membranes into the dependent parts of the body. On CT this looks like edema in the subcutaneous fat and in the muscles and like fluid in the abdominal and thoracic cavities (Fig. 4). In the abdomen, the bowel movements probably stop within a few hours after death. The enteral gas that is produced by enteral bacteria increases for several hours, probably because the bacteria continue to live and produce gas. The bowels distend during the first couple of hours after death, and the abdomen can show distension. A small amount of free abdominal fluid is a normal finding on postmortem CT (Fig. 4).
Vascular gas Another postmortem phenomenon is vascular gas, which is often seen in the mesenteric and hepatic veins (Figs. 5 and 6). It is hypothesized that this is enteric gas that has crossed the bowel wall into the mesenteric veins [12, 17]. However, vascular gas can also be found in many other veins as well as arteries, so this must have an origin other than enteric gasses and could be from dissolved gases coming out of fluid within the blood. One other theory on the origin of hepatic venous gas is that it is caused by traumatic gas embolisms [18, 19]. Indeed, we have seen this more often in pediatric and adult bodies after intravascular therapy, resuscitation attempts or infectious disease (Figs. 5 and 6). The exact origin of the postmortem vascular gas has not been clarified and it probably has multiple sources. In further stages of putrefaction, a small amount of gas can be found in the abdominal cavity, as well as in the organs, heart, mediastinum and subcutaneous fat. The order and rate of appearance of all of these postmortem changes depends on
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Fig. 1 Blood sedimentation on postmortem imaging in a 10-yearold girl with spina bifida and sepsis of unknown cause. Postmortem CT and autopsy showed that the ventriculoperitoneal drain had migrated into the jejunum, causing the fatal septic shock. These CT images show normal postmortem findings. a Axial CT shows sedimentation of blood in the aorta (white arrow); normal smooth surface of the fluid in the trachea (open arrow); normal subcutaneous edema at the back (arrowhead). b Axial CT shows sedimentation of blood in the heart (white arrow). c Coronal volume reconstruction shows the ventriculo-peritoneal drain in the jejunum (arrow)
many factors, so they cannot be used to determine time of death [13, 20].
Body size Age and body size are important factors in the process of postmortem changes. A small body is likely to decompose more quickly than a larger one, as was studied in pigs [21]. However, we have also observed slower decomposition after cooling in the mortuary of a smaller body compared to larger
Fig. 2 Postmortem imaging in a healthy 12-year-old girl who suddenly became unwell and died despite adequate resuscitation attempts. The cause of death was arrhythmia. Axial postmortem CT shows normal sedimentation in the heart (arrow). CT shows changes at both lungs bases that are likely related to resuscitation attempts
bodies. Smaller bodies are probably also influenced more by the surrounding temperature than larger bodies because of their smaller volume in combination with a relatively large body surface. Also, obese patients are known to show early decomposition, probably because of the insulating subcutaneous fat [13].
Fetuses and neonates Neonates and fetuses who die before their first breath do not have air in the alveoli. However, they may have air in the oral and nasal cavity, pharynx, trachea and even main bronchi after gasping in cases of perinatal death (Figs. 7 and 8). Neonates who have breathed have larger amounts of air in the major and
Fig. 3 Postmortem axial chest CT shows normal pulmonary edema in a 5-month-old who was found dead in her bed. No cause of death was found
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Fig. 4 Bowel changes. Postmortem imaging in an 18-month-old boy who was born at 37 weeks’ gestational age, after intrauterine hypoxemia. He had a cardiac abnormality (ventricular septal defect, open Botallian duct). At age 1 year he had cardiopulmonary arrest and successful resuscitation. He also had epilepsy. In the month before his death he was more dyspneic and had more insults. He died after respiratory insufficiency at age 18 months. No resuscitation was attempted and autopsy was refused. Parents consented to postmortem total body CT
and cerebral MRI, which were conducted 4–5 h after death. a Axial chest CT shows bilateral consolidations in the lungs, which we interpreted as bilateral pneumonia and postmortem edema. We further noted normal postmortem bowel distention and a normal small amount of subcutaneous edema. b Coronal reconstruction shows a dissection of the ascending aorta (arrow). c Axial CT at abdominal level shows normal postmortem bowel distention and a normal small amount of subcutaneous edema (arrow)
minor airways. If a fetus or neonate has been dead outside the womb for several days or longer without cooling, decomposition can produce gas in all structures, including the lungs. Major decomposition changes make it hard, if not impossible, to say whether a baby has taken a breath and lived after birth [22, 23]. To diminish the decomposition changes we keep bodies in the cooled room of the mortuary and perform the CT and MRI scan as soon as possible, within 24 h. Fetuses that die in utero and stay in the sterile uterus for several days show maceration consisting of deformation, subcutaneous edema and loss of contrasts in the brain and thoraco-abdominal organs. No gas is found in these fetuses, however, when they are scanned shortly after birth, because they did not gasp, breathe or drink. There may be some air in the mouth after clinical inspection by a physician. The situation of the enteral structures and the amount of enteral gas seems dependent on the feeding pattern. A baby who died before ever drinking has tiny fluidfilled bowels. It is of interest to note that in neonates who have not passed meconium, this meconium has a high density on CT images. There may be a small amount of air in the stomach caused by gasping and
swallowing. Non-fed neonates are thought to have sterile bowels. The postmortem changes of bowels (distension) and mesentery (vascular air) become apparent at a much later stage than in a baby who has been fed. The feeding pattern and probably also the amount and type of gas-producing enteric bacteria influence the bowel distension in children and adults.
Temperature The temperature of the body can increase (fever) or decrease (undertemperature) the rate of decomposition. The cooling of the body slows down but does not stop the process of decomposition [24].
Treatment and cause of death If a patient had medical treatment, the appearance of the body on CT may be influenced by this. Intravascular lines can introduce gas into the vessels at insertion. Amphetamines induce hyperthermia, increasing the decomposition
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Fig. 5 Vascular gas on postmortem CT imaging in an 8-year-old girl. The girl had oculo-cerebro-cutaneous syndrome and had a replacement of her gastrostoma Mickey button. The third day after surgery she was found dead in bed, lying in vomit. Her parents consented in autopsy and postmortem CT (conducted 28 h after death). a Axial CT of the abdomen shows major distention with pathological amounts of free peritoneal air (white arrow) and fluid (open arrow). At autopsy the
fluid turned out to be the enteral feeding. b Axial and (c) sagittal CT images show an abnormally large amount of gas in the peritoneal cavity, hepatic veins, aorta (white arrow) and intraspinal space (open arrows), which can be caused by the open connection through the gastrostoma, as well as the infectious process. The cause of death was peritonitis with enteral feeding after dislocation of the Mickey button
rate [13]. Another example in our experience is chemotherapy, which induces necrosis and is therefore thought to increase the rate of decomposition. Furthermore, the cause of death is very important in the interpretation of the findings. Abscesses and infectious processes, for example, locally produce an abnormal amount of free fluid, edema and gas. Infectious death speeds the process of decomposition, which is seen on CT as excessive vascular gas and peritoneal or pleural fluid and edema [13]. Death by exsanguination causes vessels to collapse more than usual, even the thoracic aorta, and it reduces the heart size (Fig. 9) [25]. A traumatic cause of death is usually combined with open wounds
and therefore abnormal gas distributions are found in the subcutaneous fat, muscles and vascular structures. The open wounds provide a portal of entry for exogenous bacteria. Like traumatic death, attempts at resuscitation have a major influence on the state of the body. Attempted resuscitation can cause rib fractures, lung contusions, and hematothorax and pneumothorax, which in combination with heart massage give an abnormal distribution of vascular gas and free air in the body (Figs. 6 and 10) [26]. In addition, fluid around the liver, spleen and pancreas are sometimes observed, probably a result of local contusions and lacerations caused by the resuscitation maneuvers [27].
Fig. 6 Postmortem vascular gas in a 4-month-old boy with psychomotor retardation who suddenly became unwell. Resuscitation was unsuccessful. Postmortem axial CT showed expected amounts of postmortem venous gas (a) and rib fractures (b), caused by resuscitation attempts. These findings were considered normal postmortem changes. a
Gas in the hepatic (white arrow) and renal veins (open arrow). b Rib fractures (arrows). c Three-dimensional axial CT reconstruction of the thoracic cage from below shows the bilateral anterolateral rib fractures (arrowheads), most likely caused by attempted resuscitation
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Fig. 7 Gas in the trachea on postmortem sagittal CT image in a neonate after the pregnancy was terminated because of several congenital malformations, cardiac anomalies among them. There is gas in the trachea (arrow), fitting with gasping postnatally. There is no air in the lungs or stomach
Resuscitation is usually combined with intravascular and even intraosseous treatment, which further influence the postmortem gas distribution in the body.
Postmortem changes related to surroundings Knowledge of the surroundings of the body is very important for the interpretation of the scan images, in perimortem as well as postmortem situations. Temperature, clothing, humidity, and presence of water and insects are all exogenous factors that influence the process of decomposition and how the body appears on CT. Children who die in a hospital or at home are in an area at room temperature (20°Celsius). They are usually kept in that room for several hours with their parents and relatives before they are moved to the mortuary (4°Celsius). A postmortem CT scan is usually made within 24 h and shows little postmortem changes such as pulmonary edema and bowel distension. If children die outside, the temperature and humidity of the air are of great influence to the decomposition of the body. Higher temperature (heat wave, fire) and higher air humidity (rain) accelerate the decomposition processes. High humidity of the air and surroundings speeds up the decomposition process, while low air humidity dries and mummifies the
Fig. 8 Gas in the trachea and lungs on postmortem CT imaging in a neonate following termination of pregnancy at 23 weeks. The pregnancy was terminated because of arthrogryposis multiplex. The child died shortly after birth. a Axial image shows a small amount of air in the trachea, main bronchi and bronchioles (arrowheads). b Threedimensional coronal CT reconstruction of the intrathoracic air
Fig. 9 Exsanguination in an 18-year-old woman who died in a car accident, with major thoracic blood loss. Permission was given for postmortem CT but not for conventional autopsy. Axial CT image shows a small heart and collapsed thoracic aorta (white arrow), both signs of exsanguination. Also note the sediment in the pleural fluid (open arrows), fitting the diagnosis of hematothorax. There are thorax drains on both sides (arrowheads)
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Fig. 10 Effects of attempted resuscitation and bowel disease in a 4-yearold girl with a 7q35 deletion, psychomotor retardation and epileptic insults. She became unconscious after vomiting. She died after 1 h of unsuccessful resuscitation attempts. The cause of death was unknown and unexpected. An abdominal swelling was felt at physical examination. Parents consented to conventional autopsy as well as postmortem total body CT and cerebral and abdominal MRI (which were conducted 5–6 h after death). a Axial CT of the thorax shows normal postmortem
pulmonary edema (arrow) in combination with resuscitation contusions as well as consolidation, possibly aspiration (arrowhead), and pleural effusion. b Axial CT image shows a whirl sign, recognized as a midgut volvulus (arrow). c Autopsy photo shows the midgut volvulus (arrow) and necrotized ileum. The cause of death was found at CT, MRI and autopsy to be a midgut volvulus. Image c courtesy of the Department of Pathology, Radboud University Medical Center, the Netherlands
body. Furthermore, the surface on which the child is lying is important, whether it is a clean floor or woodland soil, not only because of the humidity and temperature but also because of the presence of insects and rodents that can accelerate the decomposition. Under these circumstances of high temperature, high humidity and presence of insects, the CT images show more edema and vascular gas than are usually expected. This should not be mistaken for pathological processes of, for instance, infectious diseases and sepsis. The presence or absence of clothing can be important in the interpretation of CT appearances, whether there is physiological decomposition or part of the pathological disease and cause of death. Indeed, clothing can protect the body from rapid decomposition [14]. Children who die by drowning usually have large amounts of fluid in their airways, paranasal sinuses and stomach [28–30]. On CT images the lungs show ground-glass opacities and thickened septa. Also centrilobular nodules and consolidations can be visible, as well as emphysema and fibrosis [31]. A longer period underwater does not necessarily lead to a larger amount of water, edema and swelling of the body. Inhalation of salty or chlorinated water into the lungs could lead to more irritation and edema of the pulmonary tissue, and this is visible on CT images as ground-glass opacities. The aspirated dirt of a pond or ditch with bacteria and insects can lead to more consolidations in the lung and accelerate the process of decomposition. These are, however, nonspecific findings and the diagnosis of the cause of death should be in accordance with the circumstances of the finding of the body.
of decay after death, as discussed above. No mistakes should be made in studying these findings, and the possible circumstances of the body should be taken into account in their interpretation. In this section we describe the normal findings, compare these to pathological findings and illustrate with images. Important among these findings is the sedimentation of the blood in the vessels (Fig. 1). When the heart stops beating and the blood pressure drops to very low levels, the blood flow ends. The arterial wall deforms and sags but does not collapse completely, while the blood cells sediment to the dependent side of the artery. This is visible in the larger arteries and the heart (Fig. 2). The sediment in the pulmonary trunk could be mistaken for a saddle embolism. However, sediment has a horizontal lining, whereas a saddle embolism is usually curved into the main pulmonary arteries. Differentiating these observations is sometimes difficult, and secondary signs such as right ventricle dilatation can be helpful. Pre- and postmortem clots can be difficult to distinguish at other locations, as well. Postmortem clots are formed without circulation and thus usually lie on the dependent portion of the artery, i.e. as a result of gravity. Premortem clots, on the other hand, are round and are found at a more central location in the artery. In conventional autopsy the pre- and postmortem blood clots are easily distinguished because postmortem clots are not organized and fall apart, while thrombi formed during life are organized and stick together. When blood pressure drops, veins and small arteries collapse, which is a normal postmortem change. If the central arteries have also collapsed it could be a sign of exsanguination (Fig. 9). The larger part of the blood volume stays in the capillaries, not visible on CT. Soon after death the capillary membranes cease functioning (because of the drop in oxygen and adenosine triphosphate), and the intravascular blood follows the physical forces of gravity and pressure differences. Blood cells cross the capillary membrane and sink into the subcutaneous fat at the dependent side of the body. On the
Normal postmortem findings Several observations on postmortem CT that would indicate pathological findings in living persons may be normal in postmortem situations and caused by the normal processes
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outside of the body this is visible as body staining and on CT as subcutaneous edema (Fig. 1). A similar process is happening in the lung parenchyma. The pressure of both the inhaled air and the vascular system drop after death has occurred, and the fluids spread to the lower-pressure areas. On CT this is visible within hours after death as septal edema and pleural fluid. Note that this is a response to gravity, and therefore the fluid sinks to the dependent parts of the body (Fig. 3). In some cases the appearance of normal postmortem edema is therefore distinguishable from consolidations caused by pneumonia or contusion after trauma or resuscitation, because it gradually increases in density from the ventral to the dorsal side of the lungs (Figs. 4 and 10). In perinatally deceased children gas content can vary from no gas in the airways to the presence of gas in the trachea, bronchi and bronchioli (Figs. 7 and 8). Fluid in the pharynx, trachea and main left and right bronchi can be a normal postmortal finding on CT. This usually concerns a small amount of fluid with a smooth surface (Fig. 1). Large amounts of fluid are found in drowned children (Fig. 11) and in those at a later stage of putrefaction. Aspirated foods can have irregular surfaces, different densities and an alveolar pattern (Fig. 12). Distension of the bowel by fluid and gas is a normal postmortem finding, as explained above (Fig. 4). The increase in enteral fluid after death is probably caused by the leakage of the membranes and the flow to the lower-pressure areas. The normal postmortem distension may be difficult to distinguish from a pathological distension, e.g., bowel disease or sepsis (Figs. 5 and 10). Gas in the mesenteric and hepatic veins can be a normal postmortem finding [18]. It is found on most but not all
Fig. 11 CT imaging after drowning in a 6-year-old mentally retarded girl who escaped to her parents’ attention and was found on the bottom of the swimming pool. After resuscitation she was brought to the hospital. a Axial CT shows fluid levels in the maxillary sinuses (arrows). b Coronal reconstruction of chest CT shows alveolar edema (white arrow) and enteral fluid (open arrow), consistent with the recent submersion. She died 2 days later with severe cerebral damage
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Fig. 12 Food aspiration in a 14-year-old boy with Cornelia de Lange syndrome who had a fever for 3 days when he suddenly got respiratory problems and apnea. Resuscitation was started. Mucus and blood came out of the endotracheal tube. The boy died, and postmortem axial chest CT shows alveolar consolidations suspected for massive aspiration
postmortem CT scans (Figs. 5 and 6) [19]. The gas may be more abundant in cases of infectious diseases and intensive care treatment with intravascular lining. The amounts of gas can be more profound and widespread in cases of resuscitation attempts and trauma with open wounds, such as traffic accidents or penetrating trauma. In those cases, gas can be found about anywhere in abdominal and thoracic veins and arteries, the spleen, kidneys, soft tissues, mediastinum and sometimes even in the intraspinal veins (Fig. 5). Free peritoneal gas is found, as well. This is usually a normal (or expected) postmortem finding in cases of severe trauma, resuscitation attempts, or advanced putrefaction. However, it needs to be distinguished from cases with pathological free peritoneal air, as in cases with bowel perforation. The radiologist must be well-informed about the disease and the peri- and postmortem circumstances of the body and weigh all the influencing factors to decide whether peritoneal gas is pathological or a normal postmortem sign of
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Fig. 13 CT in an 8-month-old was found unconscious in bed. He had an out-of-hospital resuscitation and stayed in intensive care for 3 days before he died. Neither postmortem CT nor autopsy revealed the cause of death. There was diffuse anoxic cerebral damage. The postmortem axial CT image (10 h after death) shows contrast material in the gallbladder related to an intravenous-contrast-enhanced CT performed 3 days earlier (arrow). No gas is visible in the hepatic veins
decomposition. This can be a challenging task and requires considerable experience. A small amount of free peritoneal fluid in the mesentery, paracolic space or pelvis is normally present within several hours after death. Larger amounts of abdominal fluid could be a sign of disease such as hemorrhage, peritonitis and enteritis, or major putrefaction (Figs. 5 and 10). Another normal finding can be density in the gallbladder, which can be the result of hepatic secretion of intravascular contrast medium and should not be mistaken for sludge or calculi (Fig. 13). Subcutaneous and muscle edema are also normal postmortem findings and are usually seen within a few hours of death. The edema can be found in the dependent body parts and increases with the postmortem interval (Fig. 1).
Conclusion After death, the body continues to change in a process of decomposition that can be observed on CT images. Therefore findings such as gas, fluid and edema that are pathological in living patients can be normal findings in the deceased. The radiologist should take notice of peri- and postmortem circumstances of the body and its surroundings, as well as normal postmortem changes of the body in order to correctly interpret images.
Conflicts of interest None
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