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Original Research |
1 Center of Forensic Imaging and Virtopsy, Institute of Forensic Medicine,
University of Bern, Bern, Switzerland.
2 Institute of Forensic Medicine, University of Lausanne, Rue du Bugnon 21,
CH-1005 Lausanne, Switzerland.
3 Department of Cardiovascular Surgery, University of Bern, Inselspital, Bern,
Switzerland.
4 Institute of Diagnostic Radiology, University of Bern, Inselspital, Bern,
Switzerland.
5 Institute of Anatomy, University of Bern, Bern, Switzerland.
Received March 16, 2007;
accepted after revision September 19, 2007.
This study was financially supported by the Virtopsy Foundation. The method
described is patent pending.
Abstract
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MATERIALS AND METHODS. Postmortem perfusion with an oily liquid is established with a circulation machine. An oily contrast agent is introduced as a bolus injection, and radiographic imaging is performed. In this pilot study, the upper or lower extremities of four human cadavers were perfused. In two cases, the vascular system of a lower extremity was visualized with anterograde perfusion of the arteries. In the other two cases, in which the suspected cause of death was drug intoxication, the veins of an upper extremity were visualized with retrograde perfusion of the venous system.
RESULTS. In each case, the vascular system was visualized up to the level of the small supplying and draining vessels. In three of the four cases, vascular abnormalities were found. In one instance, a venous injection mark engendered by the self-administration of drugs was rendered visible by exudation of the contrast agent. In the other two cases, occlusion of the arteries and veins was apparent.
CONCLUSION. The method described is readily applicable to human cadavers. After establishment of postmortem perfusion with paraffin oil and injection of the oily contrast agent, the vascular system can be investigated in detail and vascular abnormalities rendered visible.
Keywords: minimally invasive autopsy • iodized oil • noninvasive autopsy • postmortem angiography • virtual autopsy
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Since the beginning of the 16th century, the importance of postmortem vascular investigation has been evidenced by the regular appearance of publications dealing with this issue [4–13]. But until recently there has existed no practicable method for investigating the entire vascular system in situ. Methods such as vascular casting have been applied only to isolated organs and are not practicable for the entire body [5]. Water-soluble contrast agents rapidly penetrate the surrounding tissue, causing edema and deforming artifacts [5].
In the context of the Virtopsy project, a new technique for postmortem
visualization of the vascular system has been developed. The technique entails
injection of a lipophilic contrast agent after vascular perfusion with diesel
oil [6]. With this two-step
method, high-quality angiograms can be obtained. The initial perfusion with an
oily medium flushes out the postmortem clots and remaining blood. Increasing
the viscosity of the applied oil selectively excludes the capillary system
from the circulation because of the process of microembolization
[6,
14,
15]. The possibility of
inducing this event can be of great advantage in postmortem angiography. With
increasing time after death, the process of extravasation becomes highly
pronounced, especially in the microcirculation. Bolus injection of iodized oil
(Lipiodol Ultra Fluide, Andre Guerbet) renders the vascular system visible.
This highly radiopaque (
2,000 H) substance is transported in diesel oil
through the vascular system in analogy to the delivery of contrast agent by
the circulating blood in clinical angiography.
Having performed our feasibility study with an animal model [6], we undertook testing of the two-step method in humans. Essential modifications included replacement of the diesel oil with odorless paraffin oil and use of a modified heart–lung machine instead of a peristaltic pump. The method was applied to the upper and lower extremities of four human cadavers, and the images revealed various vascular pathologic conditions, such as vessel occlusion and venous injection marks.
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In the first case, the cadaver was that of an elderly man. External
examination revealed no remarkable pathologic changes. The cadaver in case 2
also was that of an elderly man. External examination evinced signs of
peripheral arterial occlusion, such as cyanosis, hair loss, and glabrous shiny
skin, and of venous insufficiency, such as hyperpigmentation of the skin of
the leg). In case 3, the cadaver was that of a 39-year-old man with a history
of drug abuse. External examination revealed a 1.5-cm-diameter hematoma in the
left cubital fossa with a central wound resembling a needle prick. In case 4,
the cadaver was that of a 29-year-old woman with a history of drug abuse.
External examination revealed a large number of injection marks in both
cubital spaces ( 50 marks on each side).
Step 1: Establishment of Postmortem Perfusion
Cases 1 and 2: antegrade arterial perfusion of right lower
extremity—To perfuse the lower extremities (Fig.
1A,
1B,
1C,
1D), partial postmortem
circulation of the vessels was established as described in our feasibility
study performed with animal cadavers
[6]. In each case, the femoral
vessels of one leg were prepared. Cannulas (22-French) were introduced into
the right femoral artery and vein in the cranial to caudal direction. After
the cannulas were affixed, the vessels were ligated on the cranial side of the
insertion site. The cannula introduced into the femoral artery was then
connected to the tube of a pressure-controlled heart–lung machine (HL20,
Fumedica Maquet), which had been modified by removal of the artificial lung
surface and introduction of a software-operated pressure- and
volume-controlled perfusion mode (soon to be marketed as modified HLM 20,
Fumedica Maquet).
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The tubes were deaerated and filled with paraffin oil (Paraffinum Perliquidium, Alliance Chemical), which was diluted with 20% decane (Tetradecane, Fluka) to decrease its viscosity. Slight aeration was effected by filling the tubes with the perfusate before connecting them to the cannulated vessel. The colorless paraffin oil was rendered visible by addition of Sudan red III (0.01%). The viscosity of the final mixture was 24.39 mPa/s at 20°C. A board-certified clinical perfusion scientist performed perfusion with the following parameters: perfusion volume, approximately 800 mL; pressure gradient, approximately 50 mm Hg; flow rate, approximately 200 mL/min; time, 3–5 minutes. Perfusion was successful if the perfusate emerging from the cannulated femoral vein contained postmortem blood clots and remaining blood.
Cases 3 and 4: retrograde venous perfusion of left upper extremity—The cadavers in cases 3 and 4 manifested injection mark wounds in the left cubital space. The suspected cause of death was drug intoxication. In forensic medicine, a toxicologic examination is routinely performed in such cases, the samples of tissue and blood being obtained before and during autopsy. To avoid contamination of the samples, these operations were performed before perfusion was initiated. Because the presence of drug-injection-induced venous lesions was suspected, retrograde venous perfusion was established to suppress arterial filling and to facilitate venous visualization and diagnosis.
The left brachial vein was cannulated with an 18-French catheter in the cranial to caudal direction. Ligation of the vein was distal to the cannula to avoid bidirectional flow of the perfusate. The cannula was then connected to the tube of the modified heart–lung machine as described earlier and with the same perfusate. The perfusion parameters were as follows: perfusion volume, approximately 400 mL; pressure gradient, approximately 30 mm Hg; flow rate, approximately 150 mL/min; time, 3–5 minutes. Perfusion was deemed successful if the superficial veins became accentuated beneath the skin.
Step 2: Angiography
In all cases, MDCT angiography (Somatom Sensation 6 unit, Siemens Medical
Solutions) was performed with the following parameters: collimation, 1.25 mm;
slice width, 1.25 mm; reconstruction increment, 1.0 mm. In cases 1 and 2,
after a perfusion time of 3 minutes, 40 mL of iodized oil was injected as a
bolus into the vascular system through a three-way stopcock inserted into the
tube system of the heart–lung machine. Two MDCT scans of the legs were
obtained within 2 minutes (30 seconds and 2 minutes after injection of the
contrast agent). Perfusion was running during the entire imaging procedure. In
case 3, after 1 minute of perfusion, a bolus of 40 mL of iodized oil was
injected into the running circulation. MDCT scans were obtained 1 minute later
with the aforementioned parameters.
In case 4, angiography was performed as indicated for case 3. After acquisition of the first scan, perfusion was stopped. Inspection with the naked eye revealed macroscopic filling of the veins was possible only up to the level of the elbow. The first CT scan revealed dispersal of the contrast agent was arrested at the same level. For visualization of the veins of the forearm, 20 mL of a 1:4 mixture of contrast agent and perfusate was injected into the cephalic vein with a 30-mL syringe and a 1.1 x 40 mm needle. The perfusate was added to the contrast agent to lower its viscosity. Immediately after this injection, an additional scan of the forearm was obtained with the aforementioned parameters.
Data Evaluation
The angiograms were evaluated by a board-certified radiologist, a
board-certified anatomist, and two board-certified forensic pathologists.
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Case 2
In the cadaver in case 2, which evinced macroscopic signs of peripheral
arterial occlusion (Fig. 2A,
2B,
2C,
2D,
2E), angiograms disclosed a
large number of perfused vessels at the level of the thigh. Below the knee,
few vessels were visible. More distally, in the lower two thirds of the leg,
almost no perfused vessels were seen (Figs.
2A and
2B). This nonperfused area
corresponded to the cyanotic area of glabrous shiny skin found at macroscopic
inspection (Fig. 2A, inset). Of
the main supplying arteries, only the dorsalis pedis and its branches were
perfused down to the heel and sole (Fig.
2C). A short distance from its origin, the other great artery
divided into two main branches before undergoing further anastomosis into many
smaller branches (Fig. 2D). The
posterior tibial artery was occluded at the level of the popliteal space
(Fig. 2E).
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A feasibility study [6] of the use of our two-step approach was performed on animal cadavers and yielded promising results. For the first time, to our knowledge, all phases of the vascular system (arterial, parenchymatous, and venous) were visualized. Implementation of this method should enable precise documentation of the entire vascular system and diagnosis of vascular abnormalities. Mapping of the vascular system with postmortem angiography will be useful in the investigation of stab and gunshot wounds, in visualizing aneurysms, in pinpointing sources of bleeding, in locating ruptured bridging veins in shaken-baby cases, and in revealing occlusions of the coronary artery in cases of sudden cardiac death.
To adapt our method to human cadavers, we improved the technique used for the animal study. The odoriferous diesel oil was replaced with odorless paraffin oil, the viscosity of which was decreased to an optimal value of 24.39 mPa/s with a solvent (decane). As detailed elsewhere [6], the viscosity and lipophilic properties of the oil are crucial for its circulation after a perhaps long postmortem interval. The necessary attributes are satisfied with the odorless paraffin oil. The requisite properties of an oily liquid for postmortem angiography are well described [5–7]. The oil microembolizes the smallest arterioles and capillaries, and its penetration of these peripheral vessels depends on its viscosity. An oily liquid enters the venous system through small arteriovenous shunts, bypassing the arrested capillary microcirculation. In postmortem angiography, closure of the capillary microcirculation is of great importance because this system is highly susceptible to postmortem changes that enhance the permeability of the vessel walls. Hydrosoluble liquids are rapidly lost to the surrounding tissue through postmortem defects in the vessel wall, whereas oily liquids are retained by plugging the defects. The hydrophobicity of paraffin oil and of the contrast agent we used also impedes loss through breaks in the vessel wall [13]. Furthermore, oily liquids are known to be retained by vessels for at least 72 hours without extravasation [6–8].
Another advantage of oily liquids is that they flush out postmortem clots, which can give rise to artifacts. To avoid formation of air emboli, the tubes of the heart–lung machine have to be deaerated before use, which is a routine undertaking in the common use to which this apparatus is put. This heart–lung machine replaces the peristaltic pump used in our feasibility study [6]. With the heart–lung machine, it is possible to finely tune perfusion pressure. The machine was operated by a board-certified clinical perfusion scientist. With increasing experience and further optimization of the perfusion parameters, it should be possible to detect vascular leakage and occlusion on the basis of fluctuations in perfusion pressure. Once the site of injury has been located, the contrast agent can be injected specifically into the region of interest. In this pilot study, applied perfusion pressures of approximately 30 mm Hg for the upper extremity and approximately 50 mm Hg for the lower extremity simulated in vivo conditions. Further experiments, however, are needed to optimize postmortem perfusion parameters and enhance the quality of angiograms by improving separation of the arterial and venous phases. The images in this study revealed overlap of the two phases, which complicates radiologic diagnosis.
This pilot study showed our method is applicable to human cadavers. Our expectation of revealing vascular abnormalities was realized in the detection of occlusion of the posterior tibial artery in a case of advanced peripheral arterial occlusive disease and in a case of minute vascular leaks caused by venous injections. Our findings show that the method can be used for vascular diagnosis without autopsy. Such extensive and detailed mapping of the vasculature would never be possible in a classic autopsy. Furthermore, in contrast to existing techniques, the method can be used in situ without eliciting changes in the surrounding tissue. As evidenced by our depiction of a venous injection mark, retrograde perfusion of the venous system leads to optimal diagnostic visualization of the system. We found no artifacts that could have been attributed to interference with the venous valves. This kind of perfusion is not possible in clinical angiography.
On the basis of our findings with human cadavers, we believe that further development of our method is justified. The new perfusate can be used successfully, and replacement of the peristaltic pump with a modified heart–lung machine has improved the practicability of the method. The quality of perfusion, which is most important for the success of postmortem angiography, can be improved considerably with precise calculability of perfusion pressure and by the ease with which the administered liquid is quantified. With further developments, it should be possible not only to detect vascular occlusion and leakage but also to quantify the volume of the perfusate eluted in a particular time frame. With this knowledge and simulation of in vivo blood flow conditions, it should be feasible to quantify blood loss. This knowledge would help to gauge a person's ability to respond to and survive trauma. To date, such forensically important issues have been difficult to fathom.
Further applications of the method will include perfusion of the whole body. It is necessary to optimize perfusion and to find the most practicable approaches to the vascular system. To optimize this new method, a large number of cases will be necessary to gain experience. Radiologists, pathologists, and perfusionists will have to work together to find an optimal application of the two-step method. Working groups such as Virtopsy are scattered worldwide. They include the Office of the Armed Forces Medical Examiner, Washington, DC [16]; the Institute of Forensic Medicine, Copenhagen, Denmark [17]; and the Victorian Institute of Pathology, Sydney, Australia. These institutions have already installed CT scanners, and installations elsewhere have been planned for the next years. In Japan, the Society for Autopsy Imaging was founded in 2003. The demand for noninvasive autopsy techniques is high. For this kind of autopsy, visualization of the vascular system with postmortem angiography is indispensable. Until the introduction of our method, no practicable technique was forthcoming, to our knowledge. To permit other institutions to perform the method, a postmortem perfusion machine has been developed (modified HLM 20, Fumedica-Maquet), and a commercial set of tubes and perfusate will soon be available.
Minimally invasive autopsy techniques can replace the traditional approach. Especially in cultural circles in which autopsy is stigmatized or even forbidden, the minimally invasive approach can aid the judicial system without violating religious prohibitions. Further innovations in radiologic imaging techniques should promote the development of postmortem angiography.
The two-step postmortem angiographic method presented is undoubtedly practicable for human cadavers. After perfusion of the vascular system with paraffin oil to establish postmortem circulation, angiography can be performed with MDCT in which iodized oil is used as the contrast agent. The resulting images can reveal vascular occlusion and extravasation attributable to defects in the vessel walls. Postmortem angiography enables detailed examination of the vascular system not possible with conventional autopsy methods. The advent of a postmortem angiography is an important step toward the establishment of minimally invasive autopsy.
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