Hypostatic hemorrhages were found in the neck and/or scalp in all subjects. In subjects 1 to 3, hypostatic neck hemorrhages were present. Hypostatic scalp hemorrhages were found to some extent in all subjects, but were most prominent in subjects 2 and 5 (Fig. 5). In subject 1 (Fig. 1), the hypostatic neck hemorrhages were confluent and geographic, and involved the superficial soft tissue planes on the right anterior neck at the midline, the submental zone, and along the anterior border of the left sternomastoid muscle. Layered dissection also revealed extensive hemorrhage in the intermediate and deep strap muscle layers, mostly on the right side. In subject 2 (Fig. 2), there was diffuse intramuscular hemorrhage involving the right and left sternomastoid muscles with relative sparing of the other strap muscles of the neck. In subject 3 (Fig. 3), there was relatively minimal intramuscular hemorrhage with only focal hemorrhage in the left sternohyoid muscle and geographic hemorrhage into the subcutaneous fat of the left anterior shoulder. Subjects 4 (Fig. 4) and 5 failed to reveal any hypostatic neck hemorrhages.
The scalp hemorrhages were mostly petechial or punctate and uniformly distributed throughout the scalp (Fig. 5). Most of the hemorrhages were associated with markedly congested and distended blood vessels and some of the hemorrhages had a targetoid appearance (Fig. 5D).
The hypostatic neck hemorrhages had similar characteristics in the different subjects. The hypostatic neck hemorrhages involved both the endomysial and epimysial interstitial compartments of the strap muscles and were characterized by extensive extravasation of red blood cells (Fig. 6). In some areas, the hemorrhages had an angiocentric distribution with a dilated and congested vein in the center; however, most of the hemorrhages were confluent and extensively involved the interstitial space. In larger endomysial and perimysial hypostatic hemorrhages, there was a conspicuous increased concentration of interstitial neutrophils (Figs. 6C, D) simulating an acute inflammatory reaction. In areas of hypostatic hemorrhage with increased neutrophils, there were often extravascular aggregates of platelets (Fig. 6D).
The hypostatic scalp hemorrhages were found in all layers of the scalp but tended to concentrate in the reticular dermis (often with a perifollicular distribution), or at the galea (Fig. 7). The hypostatic hemorrhages of the reticular dermis were often associated with congested dermal blood vessels.
Postmortem hypostasis or lividity is defined as an intravascular phenomenon, but there is anecdotal evidence that postmortem hemorrhages can result from intense lividity. A detailed understanding of how and why this hemorrhagic form of lividity occurs is lacking, but it has significant medicolegal importance. For example, in cases with intense anterior lividity of the head and neck, pseudo-bruising could develop that confounds the diagnosis of subscalp bruising from blunt impact trauma and neck bruising in strangulation. This problem is not entirely theoretical—in some cases of disputed postmortem/antemortem neck hemorrhage, the issue has precipitated reviews of criminal convictions for murder and postconviction relief. Thus, the practical nature of the problems that arise from hypostatic hemorrhage makes the phenomenon worthy of careful consideration, including mechanistic analysis using experimental models. On this basis, the current cadaveric model was developed to create a system to study hypostatic hemorrhages, which can be induced under controlled conditions. It is hoped that this model will permit the macroscopic and microscopic features of hypostatic hemorrhages to be more fully defined and assist in developing methods to differentiate such hemorrhages from real bruising that occurs before death.
The initial general conclusion of this study is that postmortem hypostatic hemorrhages form after the progressive development of increasing gravitational hydrostatic pressure in an autolysing venous plexus. Specifically, as blood accumulates in the complex venous system of the neck, pressure increases within the vessel and blood leaks out of the autolysing blood vessel wall. However, it is highly probable that the development of extensive hypostatic hemorrhage requires an unusually rich venous plexus with complex anastomoses of thin-walled channels that are not well supported by extravascular connective tissues. If this hypothesis is correct, then the intense lividity of any part of the body with a venous plexus with these characteristics can form hypostatic hemorrhages. In fact, in addition to the jugular and scalp venous systems, there are other important venous plexuses that are of medicolegal interest, in terms of anatomic location, that can lead to the presence of forensically problematic hemorrhage: (i) pharyngeal (pharyngeoesophageal) venous plexus8; (ii) epidural (meningorachidian) venous plexus9,10; and (iii) communicating veins between the venous plexuses of the pelvic organs,11 including the rectal venous (hemorrhoidal) plexus.
The classic Prinsloo-Gordon hemorrhages (artifactual hemorrhages in the posterior pharyngeal wall) are well known to most pathologists and are probably the most common routinely encountered internal hypostatic hemorrhage.8 These hemorrhages are related to the perimortem distention and rupture of a series of veins in the prevertebral areas and in the adventitia of the posterior pharynx and superior esophagus known as the pharyngeal (pharyngoesophageal) venous plexus. Similarly, hemorrhages from postmortem distention and rupture of the meningorachidian venous plexus is the most likely explanation for the commonly observed spinal epidural hemorrhage12 that is found in some infants that die naturally and, to a lesser extent, adults. The meningorachidian venous plexus is a dense ramification of venous channels that almost entirely fills the anterior spinal epidural space. Intense lividity in the pelvic floor and perianal/perineal zone can also engorge the hemorrhoidal or rectal venous plexus causing a worrisome appearance of the anus after death. It is quite likely that factors beyond the geometry of the venous plexus (intercommunication of veins of the same caliber) are relevant to the development of hypostatic hemorrhages. At least 2 other anatomic concepts might be relevant. First, it seems likely that the angiosome concept might be useful to explain the distribution of hypostatic hemorrhages. The angiosome13–16 is a continuous 3-dimensional network of arteries and veins that roughly runs perpendicular to the skin surface, from superficial to deep (in contrast to a dermatotomy that represents innervation along the skin). Since blood pools under the influence of gravity, lividity fills blood vessels in adjacent angiosomes. Modeling blood pooling in angiosomes is probably more relevant than considering hypostatic congestion of named blood vessels when analyzing the patterns of hypostatic hemorrhage. In addition, venosomes (the venous portion of the angiosome)14 that are adjacent to each other may have watershed territories linked by communicating veins thereby enhancing hypostatic hemorrhage. Second, it may be that hypostatic hemorrhages principally occur at perivascular and interstitial spaces that have connective tissue that is not well supported by ground substance, matrix macromolecules, and collagen. This includes the simple intramuscular connective tissues such as the endomysium and perimysium of the strap muscles of the neck.17,18
Histologic examination of the postmortem hypostatic hemorrhages revealed true interstitial extravasation of red blood cells, in a pattern indistinguishable from antemortem hemorrhage. An entirely unanticipated finding was the presence of extravascular aggregates and interstitial “infiltrates” of neutrophils that closely resembled an acute inflammatory infiltrate associated with an early healing reaction. These extravascular collections of neutrophils likely represent the gravitational settling of nucleated cells in blood that is passively accumulating in the interstitial space. This is analogous to the formation of a “buffy coat” in blood samples in vitro, and postmortem blood clot in the heart chambers in situ where the cellular components of blood settles out from the fluid component under sedimentation. Another potential but less likely explanation would be postmortem leukocyte transmigration.
The reported model may allow for the development of histologic methods to differentiate real bruises from pseudo-bruising from hypostasis. Some areas for investigation include determining whether endothelial cell adhesion molecules are preferentially expressed only in injured blood vessels.19–21 In addition, there is evidence that platelets extravasated in antemortem bleeding are activated in the process and express adhesion molecules on the platelet membrane, whereas this may not occur in postmortem extravasation of blood. Therefore, a comparative immunohistochemical study of platelet and endothelial cell activation in real bruises and postmortem hypostatic hemorrhages could be elucidating and practically relevant.22
Although this experimental model of hypostatic hemorrhage has reasonable scope for further research, there are some potential limits. The model is limited by the types of human cadavers that are donated for medical research. Thus, it is necessarily the case that the subjects used in this research were elderly people with chronic disease. On this basis, the skin and soft tissue are not entirely representative of the entire age spectrum and not representative of the younger age range where difficulties with the postmortem diagnosis of neck compression often arise. Skin fragility and age-related changes in connective tissues may predispose to the development of hypostatic hemorrhages in the neck, similar to the predisposition to senile ecchymosis or purpura on the upper extremities during life. Despite these limitations, the model does allow the basic process of hypostatic hemorrhage to be probed. Another unexplained aspect of the present study was the fact that hypostatic neck hemorrhages could not be induced in all cadavers, despite the ability to concentrate the livor mortis in the neck and even form Tardieu spots. This indicates that additional poorly understood factors determine whether the hypostatic neck hemorrhages occur after postmortem prone positioning, ie, postmortem prone positioning and advancing postmortem interval is necessary but perhaps not sufficient to create hypostatic hemorrhages.
In conclusion, we have developed a model for the controlled induction of postmortem hypostatic hemorrhages in the neck. The macroscopic and microscopic appearances of the hypostatic neck hemorrhages can confound the postmortem diagnosis of strangulation. The model is a useful basis for studying parameters that will allow the differentiation of real bruising from postmortem pseudo-bruising such as epitopes related to platelet and endothelial cell activation. The results of the present study urge a caution when diagnosing strangulation in bodies with anterior neck lividity.
The authors thank Terry Irvine, Bill Wood, Jerry Topham, Tara Dunn, Patrick Kim, John Phu, and Dr. Noel McAuliffe for assistance.
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Keywords:© 2009 Lippincott Williams & Wilkins, Inc.
hemorrhage; homicide; artifact; strangulation; bruise; hypostasis