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DOI:10.2214/AJR.06.0787
AJR 2007; 188:832-838
© American Roentgen Ray Society

Review

Postmortem Angiography: Review of Former and Current Methods

Silke Grabherr1, Valentin Djonov2, Kathrin Yen1, Michael J. Thali1 and Richard Dirnhofer1

1 Institute of Forensic Medicine, University of Bern, IRM-Buehlstrasse 20, CH-3012 Bern, Switzerland.
2 Institute of Anatomy, University of Bern, Bern, Switzerland.

Received June 15, 2006; accepted after revision August 1, 2006.

 
Address correspondence to S. Grabherr (silke.grabherr{at}chuv.ch).

Supported by the Virtopsy Foundation, Bern, Switzerland.


Abstract
Top
 Abstract
Introduction
 Overview of Postmortem...
 Technical Aspects
 Indications for Postmortem...
 Methodologic Limitations
 Future Prospects
 Conclusions
 References
 
OBJECTIVE. Postmortem investigations are becoming more and more sophisticated. CT and MRI are already being used in pathology and forensic medicine. In this context, the impact of postmortem angiography increases because of the rapid evaluation of organ-specific vascular patterns, vascular alteration under pathologic and physiologic conditions, and tissue changes induced by artificial and unnatural causes.

CONCLUSION. In this article, the advantages and disadvantages of former and current techniques and contrast agents are reviewed.

Keywords: contrast media • conventional angiography • CT angiography • postmortem angiography • X-ray technology


Introduction
Top
 Abstract
 Introduction
Overview of Postmortem...
 Technical Aspects
 Indications for Postmortem...
 Methodologic Limitations
 Future Prospects
 Conclusions
 References
 
At the very beginning of the 16th century, Leonardo da Vinci and Jakobus Berengius were ostensibly the first to make use of prepared hollow anatomic structures. They produced wax casts of the heart chambers and the cerebral ventricles, and they used maggots to free these structures from the surrounding tissues [1].

Direct vascular injections were first performed by pioneers such as de Graaf, Ruysch, and Lower during the 17th and 18th centuries [1]. In 1857, Virchow developed a "lightning" vascular-injection technique, which was based on a graded increase in alcohol concentration and revealed fine details of the vascular architecture for the first time [2].

In 1899, 3 years after the discovery of X-rays, radiopaque materials were injected into the coronary arteries of isolated human hearts [1]. During the ensuing years, particularly during the first half of the 20th century, numerous contrast agents and injection techniques were introduced. However, only a few of these methods, such as the barium sulfate and silicon rubber techniques, have survived to the present day.


Overview of Postmortem Angiographic Techniques
Top
 Abstract
 Introduction
 Overview of Postmortem...
Technical Aspects
 Indications for Postmortem...
 Methodologic Limitations
 Future Prospects
 Conclusions
 References
 
For convenience, these techniques are subdivided according to the nature of the injection material: corpuscular preparations, oily liquids, hydrosoluble preparations, casts, and miscellaneous (see Table 1).


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  		TABLE 1: Postmortem Angiographic Techniques and Contrast Agents

 

Corpuscular Preparations
This type of preparation is the one most frequently used for postmortem angiography. It consists of a corpuscular radiopaque material, which is usually soluble in water. In 1907, menninge—a red lead oxide—was the first compound of this kind to be used in angiography [1, 3] (Fig. 1).


Figure 1
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  		Fig. 1 —Vascular system of lung, as revealed after injecting solution of menninge. (Reprinted with permission from Mitaya S. Aufbau und Gestalt der peripheren arteriellen Strombahn des kleinen Kreislaufs. Virchows Arch Path Anat 1939; 304:608-624 [3])

 
However, it was later superseded by barium sulfate, which was introduced in 1924 [4-8] (Fig. 2). Barium sulfate is usually injected as a warm solution in gelatin or agar. After cooling, gelatin permits the sectioning and histologic analysis of the injected organ. In 1938, Schlesinger [9] pioneered this technique to show the vasculature of the heart, and it has since been modified by many investigators, notably by Rodriguez and Reiner [10] in 1965. Several years later, in 1970, a finer-grained, aqueous preparation of barium sulfate, Micropaque (finely divided barium sulfate, Guerbet), was found to penetrate smaller vessels and even capillaries. Its use heralded the so-called microangiography technique [11].


Figure 2
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  		Fig. 2 —Whole-body angiogram of human fetus, which was prepared by perfusing solution of barium sulfate. (Reprinted with permission from Stoeter P, Voigt K. Radiological examination of embryonal and fetal vessels: technique and method of prenatal, postmortem angiography in different stages of gestation [in German]. Rofo 1976; 124:558-564 [6])

 
Other, less frequently used corpuscular preparations include aqueous bismuth chloride, introduced by Wedel et al. [12] in 1955; a gelatinous or agarous solution of potassium iodide, introduced by Plachta et al. [13] in 1955; and corn syurp (Karo, ACH Food Companies), introduced by Stein and Svare [14] in 1963. Each of these corpuscular preparations behaves similarly in the body. In 1969, Frik and Persch [15] noted that, in dislodging postmortem clots, the injection of these materials can avoid artifacts due to postmortem clots and that these preparations generate high contrast. Artifacts can be produced by the precipitation of the corpuscular particles themselves, either before or during imaging [16]. Obviously, not only the size of the particles but also the nature of the solvent is a crucial determinant of the caliber of vessels that can be penetrated. Micropaque, for example, will enter the capillary network only when water, not gelatin, is used as the solvent.

The advantages of corpuscular preparations include visualization of the microcirculation when dissolved in water and the ability to flush out postmortem clots. Disadvantages include extravasation when dissolved in water, no visualization of the microcirculation when dissolved in gelatin or agar, and precipitation-induced artifacts.

Oily Liquids
A list of the different types of oil that are suitable for injection into the vascular system was published by Schoenmackers [1] in 1960. However, oily contrast agent preparations have been used less frequently than other liquids for postmortem angiography. The first reported use of such an agent appeared in 1933 in which Parade [17] injected the commercially available Jodipin (iodized oil, Merck) to show the coronary arteries. Other oily preparations that have been used in angiography include Dionosil (propyliodone, Glaxo Laboratories), introduced in 1933 by Melnick et al. [18], and Lipiodol Ultra Fluide (iodized oil, Guerbet), introduced in 1974 by Pfeifer et al. [19] (Fig. 3). In 1968, Barmeyer [20] perfused the coronary arteries with a mixture of diesel oil and paraffin oil to measure the flow capacity. But for angiography, he preferred the use of Schlesinger's technique [9]. Except for our own investigations in 2005 [21] and 2006 [22], the last reported use of an oily liquid for postmortem angiography was in 1989 [23].


Figure 3
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  		Fig. 3 —Single-organ angiogram of kidney, which was prepared by injecting the liposoluble contrast agent Lipiodol Ultra Fluide (iodized oil, Guerbet). (Reprinted with permission from Pfeifer KJ, Klein U, Chaussy CH, et al. Postmortale Nierenvergröberungsangiographie mit fettlöslichem Kontrastmittel. Fortschr Röntegenstr 1974; 121:472-476 [19])

 
The potential of oily liquids in angiography was well described by Pfeifer et al. [19] in 1974. Like corpuscular preparations, they are able to flush out postmortem clots and can yield high-contrast angiographic images. Furthermore, they are retained by vessels for at least 72 hours without extravasation [22, 23]. However, they may also infiltrate damaged vessel walls and dislodge lipids from the wall as was speculated by Schoenmackers [1]. The viscosity of the oil is a critical determinant of the caliber of vessel that can be penetrated: low viscosity oils, such as diesel oil and paraffin oil, can lead to microembolism and occlusion of the microcirculation [22].

The advantages of oily liquids include their long intravascular retention time, no extravasation, that they can be used at a late postmortem stage, the interval between injection and imaging can be extended, and their ability to flush out postmortem clots. Their disadvantages include speculated infiltration of damaged vascular walls and dislodgement of lipids there from and viscosity-dependent visualization of the microcirculation.

Hydrosoluble Preparations
Hydrosoluble preparations are essential for in vivo angiography, but they are seldom used for a postmortem visualization of the vascular system. Their first reported application for this latter purpose was in 1866 [24]. Since the beginning of the 20th century, various water-soluble contrast agents have been tested, including formalin with added dyes [25], Cardiografin (diatrizoate meglumine, Bracco) [26], Hypaque (diatrizoate sodium, Sterling Winthrop) [27], Coloropaque (Pilot Chemical Company) [28], Gastrografin (diatrizoate meglumine, Mallinkrodt) [29], and Telebrix Gastro (ioxithalamate, Guerbet) [30]. Some authors such as Foote et al. [31] used water-soluble contrast agents, which have not been explained in detail (Fig. 4).


Figure 4
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  		Fig. 4 —Whole-body angiogram, revealed after injection of undefined water-soluble contrast agent. (Reprinted with permission from Foote GA, Wilson AJ, Steward JH. Perinatal post-mortem radiography: experience with 2500 cases. Br J Radiol 1978; 51:351-356 [31])

 
These hydrosoluble preparations diffuse rapidly through vessel walls, which is a useful property for embalming [32, 33] but not for postmortem angiography. The quality of the images, in terms of opacity, is poor [15, 23], and the vessels appear thinner than when corpuscular or oily preparations are used [15]. This latter phenomenon could reflect either incomplete filling of the vascular lumen with the hydrosoluble preparation or, alternatively, vascular dilatation in the presence of corpuscular and oily preparations [15].

The primary advantage of hydrosoluble preparations is that they are readily and speedily injectable. The disadvantages include rapid penetration of the vascular wall with associated edema of the surrounding tissues, poor radiopacity, and no flushing out of postmortem clots.

Casts
The use of casts dates back to the beginning of the 16th century [1]. The casting technique involves the injection of a suitable material into the vascular system, where it hardens. The surrounding tissue is then macerated to reveal the 3D vascular cast. Various casting materials have been tested over the years. In 1700, Bidloo used different metals with low melting temperatures, such as lead and mixtures of lead, bismuth, and cadmium [1]. In the 19th century and in the early part of the 20th century, celluloid and celloidin were used [1]. Later, synthetic resins and derivatives of rubber became popular. For postmortem angiography, the latter were used with a radiopaque compound. Other casting materials that have been used include nylon [34], neoprene latex [35], and polyester resin [36]. In 1954, Stern et al. [37] produced beautiful preparations of the coronary arteries using vinyl (Fig. 5). In 1981, Yonas et al. [38] developed a new technique that combined the injection of silicon rubber with xeroradiography of the cerebral vasculature.


Figure 5
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  		Fig. 5 —Vinylite cast of coronary arteries prepared by Stern et al. [37] in 1954. (Adapted and reprinted with permission from Stern H, Ranzenhofer ER, Liebow AA. Preparation of vinylite casts of the coronary vessels and cardiac chambers. Lab Invest 1954; 3:337-347 [37]

 
Since the introduction of the silicon rubber-lead oxide technique by Segerberg-Kottinen [39] in 1987, there has been only one reported use of another casting material [40]. Currently, the silicon rubber-lead oxide technique is still the most practiced method, and it permits the discernment of vessels down to 0.1 mm in diameter [41, 42]. For microangiography, special casting materials, such as Microfil (colored silicone rubber, Flow Tech) [43] and Mercox (prepolymerized methyl methacrylate, Ladd Research) [44], have been developed. Angiogenetic research is now highly important, and the use of casting materials is, therefore, essential as the newest developments show [45].


Figure 6
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  		Fig. 6 —Angiogram of testicular vessels, which were injected with mixture of menninge, turpentine oil, and Vaseline (petroleum jelly, Unilever). (Reprinted with permission from Cocchetti E, Donini I. La senilizzazione delle arterie del testicolo nell' uomo. Ateneo Parmense 1954; 25:318-336 [50])

 
Although the injection of casting materials can be tricky, the technique is widely used in postmortem angiography, and most of the complex mixtures applied are now available as ready-made commercial products. The advantages of casts include that artifacts are rare and the technique is good for single-organ studies. The disadvantages include shrinkage after hardening, the material cannot be flushed out after angiography, and the technique is impracticable for whole-body perfusion.

Miscellaneous
Some investigators have been highly imaginative in preparing their own mixtures [1]. In 1931, Hintze [46] reported on a preparation consisting of silicon arabicum and methylene blue. His rationale for the choice was that it was neutral and had viscosity and transudation characteristics that were similar to those of blood serum. Other exotic combinations include gelatin-menninge, calcium carbonate, linseed oil, and hydrogen sulfide [47]; barium, latex, and liquid ammonia [48]; barium, latex, and radioactive isotopes [49]; and menninge, terpentine oil, and Vaseline (petroleum jelly, Unilever) [50] (Fig. 6). Also Schlichter and Harris [51] mixed their own injection mass in 1949 as did Rissanen [52] in 1970. Most of these compositions were introduced in the first half of the 20th century. Since then, investigators have practiced less ingenuity.


Technical Aspects
Top
 Abstract
 Introduction
 Overview of Postmortem...
 Technical Aspects
Indications for Postmortem...
 Methodologic Limitations
 Future Prospects
 Conclusions
 References
 
Perfusion
The range of techniques used in postmortem angiography is as great as the diversity of the applied contrast agents. Most angiographic studies have been performed on single organs. In only a few instances have the vessels of an entire body been perfused.

Perfusion of single organs—Techniques for perfusion of single organs have included injection in situ, in which single organs have been injected with the contrast agent in situ and then removed for imaging [51, 53]. Another technique is injection after organ removal. This approach has been the most widely adopted, and the heart has been more exhaustively studied than any other organ. In most cases, Schlesinger's technique [9] has been applied: The freshly removed heart is first warmed in a water bath. The coronary arteries are cannulated, flushed with warm physiologic saline at a pressure of 150 mm Hg, and then perfused with a warm slurry of lead-agar or barium-gelatin at the same pressure.

The optimal pressure for injection is a matter of controversy. Schoenmackers [1] advised a pulsate pressure of 40-60 mm Hg, but other investigators have achieved better results using higher values ranging from 100 mm Hg [54] through 120-180 mm Hg [55] to 220 mm Hg [12]. Different techniques have been used to generate the necessary pressure head. These include gravity [56], pressure regulators [57] or roller pumps [22], or manual control [58, 59].

Some investigators have recommend chemical fixation [35, 60] or even decalcification [61] of the organ before injecting the contrast agent. Most authors agree that postmortem clots should first be flushed out; this is usually achieved by infusing saline at 38°C [14], as first suggested by Spalteholz [62] in 1907. On the other hand, several investigators have achieved good results without this precautionary measure [28]. Special perfusion techniques have been performed using kerosene [63] and a mixture of diesel oil and paraffin oil [20]. Hübner and Böhm [64] described a perfusion and fixation technique that is even more complex.

Whole-body perfusion—The few wholebody, postmortem angiographic studies that have been reported in the literature were conducted on animal embryos [6] and on human fetuses, embryos, and newborns [5, 46, 34] (Figs. 3 and 6). The first documented report of an angiographic study showing the arterial system of a whole adult human cadaver was published in 2005 [30]. In most instances, the perfusion techniques adopted were similar to those used for single organs. The method described by Stoeter and Voigt [6] in 1976 is an exception. These investigators proposed a radiologically controlled, discontinuous injection of the contrast agent, with angiography performed in the intervals. Using this approach, filling of the vascular system could be observed.

The first truly dynamic angiographic analysis of a whole body was reported by Grabherr [21] and Grabherr et al. [22]. In this instance, the postmortem circulation was established in adult dogs and cats by the continuous perfusion of an oily liquid. Multiple imaging at defined intervals permitted a dynamic visualization of the arterial, parenchymal, and venous systems.

Imaging
The following tools have been implemented to view suitably prepared vessels: macroscopic and microscopic inspection of 3D casts after maceration of the surrounding tissue, conventional radiography, xeroradiography, CT, MRI, micro-CT, and scanning electron microscopy. In the early pioneering days of angiography, technologic advancement permitted only the preparation of vascular casts. These casts were rendered visible by removing the surrounding tissue—first biologically, with maggots [1], and then later using aggressive chemicals [2]. After the discovery of X-rays, X-ray angiography and xeroradiography [38] then held precedence. Currently, MRI [65, 66] and especially CT [22, 30, 67] are the accepted diagnostic tools in postmortem angiography. With the advent of CT, it has once again become possible to visualize the vascular system spatially. Such a 3D overview was possible in the early pioneering days using the casting technique but was lost with the ascendancy of X-ray angiography. In the field of microangiography, micro-CT scanners are going to be implemented [43, 45], in addition to the use of scanning electron microscopy [44].


Indications for Postmortem Angiography
Top
 Abstract
 Introduction
 Overview of Postmortem...
 Technical Aspects
 Indications for Postmortem...
Methodologic Limitations
 Future Prospects
 Conclusions
 References
 
There are principally four types of investigation in which postmortem angiography is helpful: organ-specific analysis of vascular patterns and anatomic variations, pathologic and physiologic observations, changes induced by unnatural causes, and experimental testing of novel contrast agents.

Organ-Specific Analysis of Vascular Patterns and Anatomic Variations
The use of postmortem angiography in anatomic studies has a long history. And, as previously mentioned, the heart represents the most-studied organ in this respect. For example, postmortem angiography has been implemented to ascertain whether anastomoses exist between coronary arteries [20, 62]. And it has also been used to reveal the vasa vasorum of the aorta [51]. However, the vascular systems of many other organs, such as the testes [50]; regions, such as the lower extremities [68]; and tissues, such as the mesentery [69], have also been elucidated using this approach.

When low-molecular-weight contrast agents are applied, the microcirculation is revealed [11]. Such agents have often been used in dermatology to better appreciate the vascular support of skin flaps [12]. Microangiography of vascular casts is currently the most important research tool in the field of angiogenetics [43-45].

Pathologic and Physiologic Observations
Postmortem angiography has been used to study the vascular system not only under physiologic conditions but also under pathologic conditions, such as in arteriosclerotic coronary arteries [5]. It is also an important tool in the study of tumor vascularization [70]. And in forensic medicine, postmortem angiography has revealed splenic [71] and cerebral [41] aneurysms, subarachnoidal bleeding [72], esophageal varices [39], morphologic changes in the spinal arteries [42], and the rupture of bridging veins in a shaken-baby case [73].

Changes Induced by Unnatural Causes
In forensic medicine, postmortem angiography can be helpful in localizing the bleeding caused by unnatural injuries such as stab wounds and gunshots. It has also been used to investigate the effects of hanging on the vessels of the neck [56] and of electrical shock on vessels within affected regions of the skin [74].

Experimental Testing of Novel Contrast Agents
Although only one example of this indication exists in the literature [75], it may prove to be useful in screening potential contrast agents for in vivo angiography.


Methodologic Limitations
Top
 Abstract
 Introduction
 Overview of Postmortem...
 Technical Aspects
 Indications for Postmortem...
 Methodologic Limitations
Future Prospects
 Conclusions
 References
 
The quality of an angiogram depends greatly on the technique applied. But several general phenomena, which are not directly linked to the method used, can also compromise the quality of the images. Air bubbles, for example, can produce artifacts, but these artifacts can usually be avoided by careful injection. Incomplete filling of the vessels is another common problem. Investigators have attempted to overcome this difficulty by perfusing the vascular system with oil or saline before introducing the contrast agent and by injecting the contrast agent slowly and continuously. Obviously, the particle size of the contrast agent used will also have a bearing on the caliber of the vessel penetrated. After an IV injection, the microcirculation, and thereafter the arterial system, will be reached only if a material such as Micropaque is used [6]. Furthermore, viscous contrast media are less likely to penetrate the microcirculation than more fluid ones [22].

Another factor that can influence the result of postmortem angiography is the time elapsing between death and perfusion. Up to 24 hours, most methods are applicable. But thereafter, extravasation becomes an increasing problem. The death-to-perfusion time and the perfusion-to-radiography interval can be extended by using oily liquids [22], which are retained longer by vessels than nonoily ones.

Many of the described techniques are elaborate and time consuming, which explains why postmortem angiography has not become a routine undertaking in pathology and forensic medicine.


Future Prospects
Top
 Abstract
 Introduction
 Overview of Postmortem...
 Technical Aspects
 Indications for Postmortem...
 Methodologic Limitations
 Future Prospects
Conclusions
 References
 
In recent years, modern technologies, such as CT and MRI, have found their way into anatomy, pathology, and especially forensic medicine [65, 66]. In forensic medicine, these methods are used with a view to enhancing the quality of conventional autopsies. The vascular system has always been difficult to visualize, and these new tools have not lightened the burden of analysis. Large vessels can be observed with clarity [66], but smaller ones cannot. Consequently, postsurgical bleeding from such vessels may be overlooked. Nevertheless, in the further development of postmortem angiography, CT and MRI will be important tools.

Postmortem angiography is being used increasingly in forensic medicine [41, 42, 59, 60, 71, 73], and investigators, such as the Virtopsy project group in Bern (www.virtopsy.com) are actively engaged in developing convenient and minimally invasive techniques for this purpose. In the not-too-distant future, it should be possible to visualize in detail the vascular system of the entire body by these means [22, 30]. Indeed, it is already possible to establish a postmortem circulation that permits visualization of the arterial, parenchymal, and venous phases in comparison with clinical angiography [22]. And the 3D reconstruction of CT angiograms has revealed details and rendered possible measurements that were hitherto not even contemplated. The well-advised use of postmortem angiography will change our evaluation of the vascular system and help to improve the quality of postmortem anatomic, pathologic, and forensic diagnoses.


Conclusions
Top
 Abstract
 Introduction
 Overview of Postmortem...
 Technical Aspects
 Indications for Postmortem...
 Methodologic Limitations
 Future Prospects
 Conclusions
References
 
Postmortem angiography is a useful tool for analyzing the vascular system. Further improvements in technique will render it a valuable supplement to conventional autopsy methods.


References
Top
 Abstract
 Introduction
 Overview of Postmortem...
 Technical Aspects
 Indications for Postmortem...
 Methodologic Limitations
 Future Prospects
 Conclusions
 References
 

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