Postmortem Imaging-Guided Biopsy as an Adjuvant to Minimally Invasive Autopsy With CT and Postmortem Angiography: A Feasibility Study
Abstract
OBJECTIVE. Although postmortem CT suffices for diagnosing most forms of traumatic death, the examination of natural death is, to date, very difficult and error prone. The introduction of postmortem angiography has led to improved radiologic diagnoses of natural deaths. Nevertheless, histologic changes to tissues, an important aspect in traditional examination procedures, remain obscure even with CT and CT angiography. For this reason, we examined the accuracy of a minimally invasive procedure (i.e., CT angiography combined with biopsy) in diagnosing major findings and the cause of death in natural deaths.
MATERIALS AND METHODS. We examined 20 bodies in a minimally invasive fashion—namely, native CT, CT angiography, and biopsy—and compared the results to those obtained at subsequent autopsy and histologic analysis.
RESULTS. Regarding the major findings and the cause of death, the minimally invasive examination showed almost identical results in 18 of 20 cases. In one case, the severity of a cardiac ischemia was underestimated; in another case, the iliopsoas muscles were not biopsied, thus missing the diagnosis of discoid muscle necrosis and therefore a death due to hypothermia.
CONCLUSION. In light of increasing objections of the next of kin toward an autopsy and the necessity for medical examiners to assess the manner and cause of death, we think that the minimally invasive procedure described here may present a viable compromise in selected cases.
Introduction
In the last decade, postmortem imaging, especially that using CT, has gained increasing acceptance in the forensic field. Many groups in various countries have started to implement such procedures successfully [1–8].
By virtue of its capability in detecting and imaging osseous lesions, foreign bodies, and gas accumulations, postmortem CT has proved to be a useful tool in the examination of traumatic deaths. However, CT has certain limitations in the assessment of natural death. Vascular and organ pathologic abnormalities, for example, generally cannot be visualized accurately using native CT scans.
To address the problem of vascular pathologic abnormalities, postmortem angiography has been implemented with great success [9–13]. However, although the vascular bed could be visualized in detail and the results often surpassed those obtained by conventional autopsy, postmortem angiography does have certain limitations when addressing the cause of death (COD).
For example, postmortem angiography can show injuries to blood vessels in great detail and suffices to show an occlusion in a coronary or pulmonary artery, but it cannot deliver information regarding the cause of the occlusion. Atherosclerotic occlusions can be readily recognized with CT, but potentially lethal thrombotic occlusions cannot be differentiated from forensically irrelevant postmortem blood clots. Furthermore, atherosclerotic coronary occlusion, a finding that is frequently encountered at autopsy, may be irrelevant to the COD, because it can have existed for at least several weeks, months, or even years before the individual's death. Therefore, to assess the effect on an organ, for example the heart, one must also examine the structure of the tissue itself. At conventional autopsy, this is done macroscopically and very often also histologically.
Another problem in postmortem imaging is the vitality of an injury—that is, whether a lesion occurred during life or after death. The most common so-called vital reactions are hemorrhages, aspiration (e.g., blood, water, and gastric contents), inhalation of gases (e.g., carbon monoxide), embolism (e.g., fat, gas, and thrombi), or inflammatory responses. Although gas embolism and hemorrhages can be diagnosed with CT [14, 15], aspirated material can only be suspected, and inflammatory responses and fat embolisms are not detectable with CT. Traditional macromorphologic examination can usually discern between different aspirated materials, whereas microscopic findings of inflammation and diagnosis of fat embolism belong to the field of histology.
The accuracy of biopsy sampling has been shown before [16, 17]. However, to our knowledge, the possibility of diagnosing the COD by postmortem biopsy in combination with CT and postmortem angiography has not been examined to date.
To assess the diagnostic accuracy regarding the main findings and the COD, we compared the results of a minimally invasive approach (i.e., native CT, postmortem CT angiography, and biopsy) with those obtained in a conventional manner with autopsy and histologic analysis.
Materials and Methods
Inclusion Criteria
Of all the cases of extraordinary death (accidents, suicides, homicides, and cases of unknown cause and manner of death) delivered to our institute for forensic autopsy, we included 20 consecutive cases of unclear COD (i.e., no known medical history explaining the death) that displayed no signs of mechanical trauma and for which the case circumstances were indicative of a natural death. The mean age of the studied group was 56.4 years; the male-to-female ratio was 14:6 (Table 1). Ten of the cases were found dead at home, five died in a clinical institution, two died in vehicles without a crash, one died during sports (jogging), one died on a mountain, and one died at the workplace.
| Case No. | Age (y) | Circumstances of Death | Results of Histologic Analysis | Cause of Death | |||||
|---|---|---|---|---|---|---|---|---|---|
| Sex | Autopsy Findings | Radiology Findings | Biopsy Findings | Conventional | Minimally Invasive | ||||
| 1 | 68 | Male | Died at home | Cardiac hypertrophy, occluded stents, arteriosclerotic coronary stenosis, indurated lungs | Cardiac fibrosis, chronic blood aspiration, chronic interstitial pneumonia | Cardiac hypertrophy, stent occlusions in right circumflex artery and right coronary artery, atypic pneumonia | Cardiac fibrosis, chronic blood aspiration, chronic interstitial pneumonia | Cardiac arrest | Cardiac arrest |
| 2 | 60 | Female | Died at home | Atherosclerotic coronary occlusion, acute myocardial infarction, pulmonary congestion | Extensive contraction band necrosis, lungs congested | Occlusion of left anterior descending, pulmonary congestion, pleural effusions | Extensive contraction band necrosis, pulmonary edema | Myocardial infarction | Myocardial infarction |
| 3 | 63 | Male | Died on bus | Cardiac hypertrophy, sclerotic coronaries, stenosis proximal to left coronary artery, pulmonary edema | Single contraction band necrosis and slight fibrosis, pulmonary congestion and edema | Cardiac hypertrophy, sclerotic coronaries, stenosis proximal to left coronary artery, pulmonary edema | Slight myocardial fibrosis, pulmonary edema and congestion | Cardiac arrest | Cardiac arrest |
| 4 | 81 | Male | Died at home | Gastric content aspiration | Myocardial fibrosis, aspiration pneumonia | Aspiration pneumonia, pulmonary fibrosis positive | Slight myocardial fibrosis, slight pneumonia | Cardiac arrest due to pneumonia | Cardiac arrest |
| 5 | 78 | Male | Died in hospital | Cardiac hypertrophy, three-stem coronary artery disease, myocardial infarction scar, congested lungs | Myocardial fibrosis, single contraction band necrosis, pulmonary congestion | Three-stem coronary artery disease, cardiac hypertrophy, pulmonary congestion | Myocardial fibrosis, single contraction band necrosis, pulmonary emphysema | Cardiac arrest | Cardiac arrest |
| 6 | 58 | Male | Died in practice | Cardiac hypertrophy, occlusion of left anterior descending and circumflex arteries, pulmonary edema | Myocardial fibrosis, pulmonary edema | Cardiac hypertrophy, occlusion of left anterior descending and right circumflex arteries, pulmonary edema | Myocardial fibrosis | Cardiac arrest | Cardiac arrest |
| 7 | 52 | Male | Died at home | Small-cell carcinoma in lungs and locoregional lymph node, tumor erosion of pulmonary artery | Extensive small-cell carcinoma in lungs and regional lymph nodes | Small-cell carcinoma, tumor erosion of pulmonary artery, mediastinal lymphangitis | Extensive small-cell carcinoma in lungs | Exsanguination | Exsanguination |
| 8 | 33 | Female | Died at home | Pulmonary edema, reactive spleen | Lymphocytic myocarditis | Pulmonary edema, splenomegaly | Lymphocytic myocarditis | Cardiac arrest | Cardiac arrest |
| 9 | 15 | Male | Died at home | Central pulmonary thromboembolus, colitis ulcerosa | Colitis ulcerosa, fresh thromboembolus in pulmonary trunk | Central pulmonary thromboembolus, colitis ulcerosa | Colitis ulcerosa, fresh thromboembolus in pulmonary trunk | Right heart failure due to pulmonary thromboembolus | Right heart failure due to pulmonary thromboembolus |
| 10 | 78 | Female | Died in hospital | Intrathoracic hemorrhage, thrombotic occlusion of right coronary artery, pulmonary edema | Fibrosing alveolitis, proliferative state, pleuritis, pneumonic residues | Thrombotic occlusion of right coronary artery, intrathoracic hemorrhage, pulmonary edema, pneumonia | Fibrosing alveolitis, proliferative state | Cardiac arrest due to hemorrhage and coronary occlusion | Cardiac arrest due to hemorrhage and coronary occlusion |
| 11 | 82 | Male | Died in car | Thrombotic occlusion of right coronary artery, 90% stenosis of left anterior descending, pulmonary edema | Fresh thrombosis in coronary, pulmonary congestion | Thrombotic occlusion of right coronary artery, 90% stenosis of left anterior descending, pulmonary edema | Pulmonary congestion | Cardiac arrest due to coronary occlusion | Cardiac arrest |
| 12 | 55 | Male | Died at home | Cardiac hypertrophy | Pulmonary congestion | Cardiac hypertrophy, pulmonary congestion | Pulmonary congestion | Cardiac arrest | Cardiac arrest |
| 13 | 80 | Male | Died in hospital | Cardiac hypertrophy, coronary occlusion, free coronary bypasses | Myocardial fibrosis, pulmonary congestion | Cardiac hypertrophy, pulmonary congestion, coronary occlusion, free coronary bypasses | Myocardial fibrosis | Cardiac arrest | Cardiac arrest |
| 14 | 54 | Male | Died during sports | Thrombosis of right circumflex artery and right coronary artery, 90% stenosis of left anterior descending, pulmonary congestion | Fibrosis, single contraction band necrosis, pulmonary congestion | Thrombosis of right circumflex artery and right coronary artery, 90% stenosis of left anterior descending, pulmonary congestion positive | Fibrosis, single contraction band necrosis, pulmonary congestion | Cardiac arrest | Cardiac arrest |
| 15 | 57 | Male | Died at workplace | Cardiac hypertrophy, coronary stenoses, pulmonary congestion | Multiple contraction band necroses, fibrosis | Cardiac hypertrophy, coronary stenoses, pulmonary congestion | Fibrosis | Myocardial infarction | Cardiac arrest |
| 16 | 52 | Female | Died at home | Pulmonary thromboembolus | Fresh pulmonary thromboembolus | Pulmonary thromboembolus, coronaries normal | Fresh pulmonary thromboembolus | Right heart failure due to pulmonary thromboembolus | Right heart failure due to pulmonary thromboembolus |
| 17 | 49 | Male | Died at home | Cardiac hypertrophy, aortic dissection reaching left coronary ostium | Pulmonary congestion | Cardiac hypertrophy, aortic dissection reaching left coronary ostium | Pulmonary congestion | Cardiac arrest | Cardiac arrest |
| 18 | 46 | Female | Died at home | Large intracranial tumor, cerebral edema | Meningioma | Large intracranial tumor, cerebral edema | Meningioma | Central respiratory paralysis | Central respiratory paralysis |
| 19 | 31 | Male | Died on mountain | Cachexia, gastric erosions, extensive tuberculosis of lungs and spleen | Discoid necrosis of iliopsoas muscle; tuberculosis in lungs, spleen, liver, colon, trunk lymph nodes | Tuberculosis of lungs | Tuberculosis of lungs and spleen | Hypothermia | Cardiac arrest due to tuberculosis-associated cachexia |
| 20 | 36 | Female | Died during labor | Cerebral hemorrhages, pulmonary congestion | Massive embolism of amniotic fluid and fat | Cerebral hemorrhages, pulmonary congestion | Massive embolism of amniotic fluid and fat | Right heart failure | Cardiac arrest |
Investigations Applied
After thorough external inspection by a board-certified forensic pathologist, the corpses underwent CT. Scans were obtained with a Somatom Emotion 6 scanner (Siemens Healthcare) with 4 × 1.25 mm collimation. The reconstruction interval was 0.7 mm. We calculated 2D and 3D reconstructions using a Leonardo workstation with Syngo CT software (both from Siemens Healthcare).
Minimally invasive postmortem CT angiography was performed via unilateral access to the femoral blood vessels (femoral artery and vein). A modified heart–lung machine was used as injection pump for a close simulation of the intravital pressure conditions. A mixture of polyethylene glycol (PEG 200) and water-soluble contrast medium (iohexol, Omnipaque, GE Healthcare) was injected separately into the arterial and the venous system. CT scans were then obtained with the CT unit described in the previous paragraph.
Before the actual biopsy procedure, a 13-gauge introducer needle was placed under CT fluoroscopic control into the area of interest. Biopsy specimens were obtained with a Bard Magnum biopsy gun and a 14-gauge UltraCORE biopsy needle (all biopsy equipment was from Bard Biopsy Systems) (Fig. 1A, 1B). In every case, at least the heart and lungs were biopsied (two or more specimens of the left ventricle and four specimens of both lungs were analyzed). In addition, suspicious regions as identified by CT were also biopsied. The CT took only a few minutes to perform, and the entire CT-based angiography procedure (including access to the femoral vessels) required almost 1 hour. Depending on the extent of the biopsies (i.e., heart and lungs only or additional radiologically suspicious regions), the biopsy procedure took between a few minutes to almost half an hour.
After CT scanning and acquisition of biopsies, all corpses underwent full forensic autopsy. In addition, histologic examinations were performed on all vital organs (at least brain, heart, lungs, liver, and kidneys) and on case-relevant tissues identified by macromorphological findings. Formalin-fixed histology and biopsy samples were routinely stained with H and E and, in heart specimens, also with chrome aniline blue and were evaluated by a board-certified forensic pathologist. Ziehl-Neelsen staining was performed on one case in which tuberculosis-suspicious lesions were seen macro- and microscopically. Native lung specimens were stained with Sudan red III to detect a possible fat embolism.
Evaluation Process
The main results of autopsy and histologic analyses were compared with the main results obtained by radiology (native CT and angiography) and biopsy. The causes of death, as diagnosed by the conventional autopsy in combination with histologic analysis, were then compared with those deduced using the minimally invasive approach with radiology and biopsy. If relevant preexisting cardiac pathologic abnormalities could be found (e.g., significant cardiac hypertrophy or coronary stenoses or occlusions), but no findings pertaining to an immediately lethal condition (such as an acute myocardial infarction) were noted, the COD was deemed “cardiac arrest.”
Results
The results of the conventional approach with autopsy and histologic analysis were remarkably similar to those obtained using postmortem radiology augmented by biopsy (Table 1).
Main Findings
The aspiration pneumonia of case 4 was noted as being a “slight pneumonia” by biopsy. However, CT of this case correctly diagnosed aspiration pneumonia, thus equalizing the conventional results (as in the cases with pulmonary congestion or edema).
Another shortcoming of biopsy was the failure to detect pneumonic residues in case 10. The patient was admitted to hospital with pneumonia and treated accordingly. A diagnostic transthoracic biopsy was performed a few days before death. The major findings, an intrathoracic hemorrhage caused by the biopsy during hospitalization and a thrombotic coronary occlusion, were found in both the conventional and the minimally invasive examination procedures. However, histologic analysis showed pneumonic residues, whereas CT revealed pneumonia, and the biopsy missed such residues.
Biopsy missed a pulmonary congestion or edema noted by histologic analysis in two of nine cases. However, this finding was registered at CT examination, so the combination of both radiology and biopsy delivered the same results as autopsy and biopsy.
Contraction band necrosis proved to be more difficult to find with biopsy specimens. In case 3, biopsy missed the histologically found single contraction band necrosis; in case 15, biopsy only showed single instead of multiple contraction band necroses, as seen at histologic analysis.
Cause of Death
The COD as postulated by conventional methods was in almost complete accordance with that determined by the minimally invasive procedure (Figs. 2, 3, 4). Indeed, in 18 of 20 cases, both methods delivered identical results. However, in one case (case 15), biopsy only showed single contraction band necrosis, thus rendering the COD found by the minimally invasive method as a “cardiac arrest,” whereas histologic analysis revealed extensive contraction band necroses, therefore permitting the diagnosis of the COD as a “myocardial infarction.”
Another case (case 19), displayed a totally different COD by the minimally invasive technique than by the conventional procedure. In this case, the fully clothed frozen body of a man was found lying in snow in the mountains. Although both methods revealed extensive tuberculosis infection, the minimally invasive technique failed to detect gastric erosions. These erosions indicate a long agonal phase, which is, taking the incident scene into account, indicative of a hypothermic death. Furthermore, the iliopsoas muscles were not biopsied, which is why the discoid necrosis of these muscle fibers, a finding typical for hypothermia, was missed. This led to the erroneous determination of the manner of death in the minimally invasive examination to be natural, whereas autopsy proved this to be an accidental death due to hypothermia.
Discussion
Although CT alone did not suffice to diagnose all major findings detected by autopsy and histologic analysis, the combination of native CT, postmortem CT angiography, and biopsy, representing a minimally invasive approach, delivered remarkable results. Indeed, this minimally invasive approach led to the correct diagnosis of the COD in 18 (90%) of 20 cases. In one case, autopsy detected a myocardial infarction, a finding that was confirmed histologically. Although postmortem CT angiography displayed a thrombotic coronary occlusion, biopsy of the heart showed only a single contraction band necrosis, a finding that permitted only the vague diagnosis of the COD being a “cardiac arrest.” This underestimation of the severity of the ischemic damage may be overcome by selecting different areas of the heart, especially the papillary muscles, instead of the left ventricular wall, where, depending on the extent of the ischemia, no damage may be detected in the tiny biopsy sample. Targeted biopsy of such small structures is technically possible, as Aghayev et al. [17] showed when performing biopsy on peas in gelatin and corpses.
This sampling of regions of interest may increase the accuracy of histopathologic diagnosis. However, incidental findings not visible by CT or CT angiography, or macroscopic examination at autopsy, will be missed unless all (relevant) organs are examined histopathologically on a routine basis, as is standard procedure in clinical autopsies. Such an extensive microscopic examination is obviously hardly possible with postmortem biopsy, and incidental minor findings may therefore be missed in the minimally invasive examination.
In the remaining discrepant case regarding the COD, the man with tuberculosis who died due to hypothermia (case 19), the reason for the missed diagnosis is different. The autopsy was performed by an experienced forensic pathologist who knew which samples should be taken for confirmation of the suspected diagnosis. However, the biopsy was undertaken by a person with little forensic experience who omitted the biopsy of the iliopsoas muscles. The correct diagnosis, death due to hypothermia, was therefore not possible on the basis of minimally invasive examinations. This shortcoming highlights the necessity of a close collaboration between pathologists and radiologists in performing the proper examinations and thus arriving at the correct conclusions.
Such a close collaboration not only assists in making proper conclusions, but also may improve safety of the pathologists. For example, in case 19, the tuberculosis infection was unknown before the examinations. The surprise finding of a potentially lethal infection is not rare in forensic pathology, where, in contrast to clinical pathology, infections are frequent (i.e., in IV drug users) and a medical history is often unknown. Here, postmortem imaging in combination with biopsy may give important information as to the presence of certain contagious diseases such as tuberculosis, and thus help the pathologist to apply the necessary protection, such as special face masks, against such an infection.
Although this is an admittedly small study, we nevertheless believe that it highlights certain difficulties and advantages. The main advantage is that minimally invasive autopsy techniques are less objected to than conventional autopsies. The minimally invasive approach described here may serve as a compromise between this objection toward an autopsy and the physicians' need for information regarding pathologic conditions. Furthermore, minimally invasive postmortem examinations pose less risk of exposure of examiners to infectious agents than an autopsy.
However, certain drawbacks cannot be dismissed. For example, a discrete change in color or texture of an organ, an immensely important observation at autopsy, is obviously not visible in radiology. In these cases, the minimally invasive examiner will have to rely on blind chance biopsies of all important organs. Because of the small size of the biopsy specimen, tiny localized pathologic abnormalities not seen radiologically may be missed by chance sampling of organs.
Another problem is the time needed for a minimally invasive examination. An experienced pathologist will be able to perform a full autopsy in less time than with the minimally invasive technique. However, we believe that, with more experience and better equipment, these examinations will become more rapid and cheaper, very much like the development of laparoscopic surgical procedures.
We conclude from our study that the combination of CT, postmortem CT angiography, and biopsy is a valid tool to examine bodies in a minimally invasive fashion. A close collaboration between pathologists and radiologists is imperative for the correct sampling and diagnostic assessment and, therefore, for the success of such an undertaking.
Acknowledgments
We thank B. Nicolet for the staining of the biopsy and histology specimens and W. Bolliger for assistance in manuscript preparation.
Footnote
Address correspondence to S. A. Bolliger ([email protected]).
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© American Roentgen Ray Society.
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Submitted: March 12, 2010
Accepted: April 12, 2010
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