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Ultrasonography On The Non-Living. Current Approaches
Ultrasonography On The Non-Living. Current Approaches
Ultrasonography On The Non-Living. Current Approaches
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Use of Ultrasound in the Diagnostic Work-Up of Adult Intussusception – A Multicenter Retrospective Analysis View project
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1Department of Internal Medicine, Westküstenkliniken, Brunsbüttel, Germany, 2University of South Carolina School
of Medicine, Columbia, South Carolina, USA, 3Department of Pathology, Faculty of Medicine, University of
São Paulo, Brazil, 4Department of Radiology, Michigan Medicine, University of Michigan, USA, 5Department of
Periodontology and Oral Medicine, School of Dentistry, University of Michigan, USA, 6Department of Ultrasound,
Zhongshan Hospital, Fudan University, Shanghai, China, 7Department of Radiology, Hospital das Clínicas – School
of Medicine, University of São Paulo, Brazil, 8Beth Israel Deaconess Medical Center, Boston MA, USA, 9Department
Allgemeine Innere Medizin (DAIM), Kliniken Hirslanden Beau Site, Salem und Permancence, Bern, Switzerland,
10Johann Wolfgang Goethe Universitätsklinik Frankfurt, Germany.
Abstract
The vast majority of clinicians associate diagnostic ultrasound with a tool that is designed for the living patient. However,
it is of course possible to apply this imaging technology to evaluate the recently deceased patient for postmortem diagnosis,
or even just examine postmortem tissue. We describe several cases in which ultrasound-enabled providers obtain answers in
postmortem examinations and discuss potential future strategies and applications. In addition, we will also illustrate the use of
sonography in minimally invasive post-mortem tissue sampling (MITS), an approach that can be used in post-mortem mini-
mally invasive autopsies as well as for establishing ultrasound diagnostic parameters in new medical fields such as periodontal
and dental implant specialties.
Keywords: postmortem ultrasound; autopsy; imaging; cause of death; validation
es in which US enabled physicians to obtain answers to choice for postmortem imaging of neonates and paediat-
open diagnostic questions in postmortem examinations. ric cadavers [3]. By contrast, Roberts et al consider CT to
In addition, we will illustrate how US can assist in mini- be the method of choice in postmortem imaging because
mally invasive post-mortem tissue sampling (MITS) and discrepancies between autopsy and MRI are more com-
how several investigators used cadavers to evaluate diag- mon than between PMCT and autopsy [8].
nostic accuracy of certain ultrasound indications. Simonds et al [9] reported on the use of conventional
radiography in cadavers to detect fractures and foreign
Review of the literature bodies, positron emission tomography to detect tissue
changes especially in Alzheimer’s disease and Lewy
A review of the available literature showed that US body dementia and various uses of CT with stationary
appears to be particularly important in fetal and neonatal and mobile equipment. The working group reported that
postmortem diagnostics [3,4]. However, overall CT and US has so far been underrepresented in cadaver diagnos-
MRI or X-ray dominate the forensic literature. Heine- tics. MRI provides excellent images, but its availability
mann et al reported on the use of postmortem CT and and expense are significant limiting factors. The vastly
CT angiography between 2004 and 2014 [5]. CT is con- superior imaging provided by MRI has placed post-
sidered the standard method in postmortem imaging. It mortem US in a subordinate status in forensic medicine,
is less susceptible to interference from postmorten gas despite cost and availability advantages. This is mainly
formation than US. The biggest advantage over clinical due to the formation of gas on the corpus after few hours
autopsy is the detection of free air. Skeletal changes and and the resultant limitation to US wave propagation in
retained foreign bodies can also often be better detected. the body.
The strength of CT angiography lies primarily in the Egger et al [10] examined 119 cadavers for gas for-
detection of bleeding sources, even in postmortem ex- mation. They found gas formation mainly in the heart
aminations that are lacking an intrinsic blood pressure. and liver. Gas was initially detectable after 5-84 hours
Agreement between postmortem CT (PMCT) and clini- after death. In all cases of natural death, gas was found in
cal autopsy is nearly 90% if the reporting radiologist has the liver vessels and the heart simultaneously; in cases of
sufficient experience in post-mortem imaging [5]. death by gas embolism, gas was noted only in the heart.
Grabherr et al [6] reported on the use of X-ray in fo- Spaienza et al [11] reported on seven victims of a flood
rensic medicine dating back to 1896, the year an X-ray whom they examined with CT for postmortem intrahe-
of a hand was performed on a mummified Egyptian prin- patic gas formation. They found that gas first formed in
cess. Today, many forensic departments have mobile X- the portal vessels and then appeared in the hepatic veins.
ray machines to examine corpuses for radiopaque foreign Fischer et al [12] analyzed intrahepatic gas formation in
bodies or bony lesions. X-rays are also used to identify five male cadavers with non-traumatic causes of death
unknown deceased with the help of dental findings or lo- using a longitudinal study with CT scans at hourly in-
cating osteosynthetic material. The most common tech- tervals over a 24 hour period. They found an increase in
niques used today are PMCT, CT angiography and MRI. gas formation between the fourth and seventh hour after
A new development is the 3-D surface scanner. Blood death, after which conditions remained constant until the
and fluids can be well visualized in CT, even postmor- end of the study period. Intrahepatic gas is predominant-
tem, using this technique. Free air is also imaged without ly caused by mesenteric gas formation [13]. Detection
difficulty. However, interpretation is complicated by gas is possible by both CT and US. The first description of
formation, which begins a few hours after death. Free air portal venous gas was made in 1955 by Wolfe et al in six
can therefore only be detected up to a few hours after newborns that had died of intestinal necrosis [14].
death. The value of CT in cases of natural death is lim- The interference by gas formation and its rapid de-
ited. For example, ischemic heart disease in acute cardiac velopment raises questions regarding what potential
arrest cannot be detected by CT without angiography [6]. significance post-mortem US could have in clinical
MRI is also used in post-mortem imaging. Limita- adult medicine. A search of the literature on this topic
tions include the occurrence of gas, lack of circulation revealed a paucity of publications to date. Duarte-Neto
and low body temperature, which influences the behavior et al [15] described ten US-guided multiorgan punctures
of MR contrast agents. Gas leads to a complete loss of in patients with COVID-19 induced death. The first pub-
signal in MR. Gases formed by autolysis can significantly lished description of this method was in 2002 by Farina
interfere with imaging. On the other hand, the detection et al [16]. They compared US-guided puncture biopsies
of myocardial infarction is as good in postmortem MRI with conventional autopsies on 100 cadavers and found
as in living patients [7]. MRI is currently the method of a concordance rate of 83% for final diagnosis. An easily
Med Ultrason 2021; 0: 1-10 3
overlooked location and timing for postmortem US per- The transducers were protected during the examination
formance is in the emergency department, where deaths with sterile probe covers from Civco Medical Solutions.
may occur suddenly and unexpectedly. Even in older, The US device and the transducers were reprocessed af-
chronically ill patients, immediate postmortem US evalu- ter use according to the local hygiene recommendations.
ations can provide vital clues as to the cause of death
and critical education to clinicians. Some catastrophic Use of US in postmortem diagnosis
etiologies can be assessed with US and include proxi-
mal thoracic aortic dissections, pericardial effusion and Case 1
pneumothorax. Abdominal aortic aneurysm presence can An 87-year-old female patient presented via para-
raise its potential role in a death, even if intraabdominal medics due to a one-day increase in dyspnea, now at
or retroperitoneal fluid is not detected. US examination rest. She denied thoracic pain, cough, fever or chills, as
so quickly after death is unlikely to be encumbered by well as sweating and palpitations. The patient had been
gas formation. Evaluation of pleural cavities is easily discharged from the geriatric ward only 5 days ago. On
performed in search of fluid collections and assessment physical examination the patient was alert and oriented,
of the lower extremity deep venous system may reveal Glasgow Coma Scale 15, reduced general status body
the presence of deep venous thrombosis, thus suggesting habitus was obese, slight bilateral leg oedema. Her res-
pulmonary embolism as a potential cause of death if the pirations were equal on both lungs, percussion sound so-
clinical scenario is supportive. However, more direct evi- norous; heart sounds were regular and rhythmic without
dence of massive pulmonary embolism is unlikely to be murmurs, rub or gallops, norm frequent. Hemoglobin
reliable as blood can quickly gel in the cardiac chambers and white blood cell count, inflammatory parameters,
and lack of intracardiac pressure means acute signs of renal values, electrolytes and urine status were unre-
right heart strain will not be identified [5]. markable. The patient was diagnosed with heart failure,
Postmortem US in the pathology department has been treated conservatively and monitored overnight. After a
used to validate US findings in 20 patients to delineate stable course, the patient was transferred to the ward the
small organ structures, e.g., the adrenal glands [17] and following day. That next evening, the patient rapidly de-
perihepatic lymph nodes [18,19]. teriorated and had to be resuscitated. Cardiac resuscita-
Recently three cases in which post-mortem US within tion was unsuccessful. A post-mortem US was performed
three hours of death enabled the clarification of a previ- given the lack of clinical diagnosis and the unsuspected
ously unclear cause of death have been reported [20]. In clinical course. There were no signs of pulmonary embo-
all three cases, an autopsy could not be performed for lism (fig 1).
various reasons. The examinations were performed with Case 2
the GE S7 (GE Medical Systems Information Technolo- A 71-year-old male undomiciled and living alone in
gies, Freiburg i. Breisgau, Germany). Multifrequency the woods is brought in by the ambulatory emergency
transducers were used: a phased array (3-5 MHz), a mul- service for decreased responsiveness. Prehospital trans-
tifrequency linear array (6-15 MHz) and a sector trans- port time was approximately 40 minutes and the patient
ducer (2-4 MHz). A Mindray M7 with a phased array expired on the way, despite aggressive and constant re-
(2-5 MHz) transducer was also utilized for evaluation. suscitative efforts by paramedics. The family and the lo-
Fig 1. Postmortem a) echocardiography, after resuscitation was stopped: right atrium slightly dilated, the other cardiac cavities are of
normal width; b) US, after resuscitation was stopped: lower caval vein of normal width and c) left femoral vein perfusion detectable
after compression.
4 Thomas Thomsen et al Ultrasonography on the non-living. Current approaches.
Fig 3. Postmortem echocardiography, showing signs of massive acute pulmonary embolism. Subxiphoid (a) and four-chamber view (b).
Med Ultrason 2021; 0: 1-10 5
Fig 4. Lung ultrasound showing irregular, discontinuous pleural artefact, small supleural condensations and diffuses pulmonary
infiltration (a). Focus of acute pulmonary hemorrhage (hematoxylin-eosin stain, magnification 200 X) (b). Larva of Strongyloides
stercoralis in the alveolar lumen (c) (hematoxylin-eosin stain, magnification 400 X).
therapy was admitted in 2017 to investigate an episode showed marked thickening of intestinal walls. Needle
of fever, dyspnea and diarrhea. Investigation for tuber- pulmonary tissue sampling revealed foci of pulmonary
culosis was negative, but patient received treatment for hemorrhage and the presence of larvae of Strongyloides
syphilis and hepatitis B. In late 2019 the patient com- stercoralis perforating the pulmonary capillaries in the
pletely abandoned anti-retroviral therapy. Following lungs and intestinal mucosa (fig 4). The final diagnosis
medication cessation, he lost 12 kg and in October 2020 was established as systemic angioinvasive Strongyloi-
was admitted for progressive dyspnea and diarrhea. diasis in a patient with acquired immune deficiency syn-
X-ray revealed diffuse bilateral pulmonary infiltrates and drome and COVID-19 was excluded.
CT showed ground glass infiltrates with predominance Case 5
in basal portions of the lungs. The patient’s respiratory A 52-year-old female with a history of type I diabetes
status worsened, and he was intubated requiring progres- and immunosuppression due to a kidney pancreas double
sively higher levels of inspired oxygen. The patient rap- transplantation performed in 2008, now back on hemo-
idly deteriorated with worsening hemodynamic param- dialysis after renal transplant rejection, presented to the
eters despite broad-spectrum antibiotics and vasoactive hospital with progressive dyspnea and one episode of
drugs. The patient then developed massive respiratory haemorrhagic diarrhea. She eventually developed respir-
hemorrhage, which leads to cardiac arrest refractory to atory failure and was intubated and placed on mechani-
resuscitation efforts. The autopsy service received the cal ventilation. CT scans revealed bilateral ground glass
patient’s body with evident signs of weight loss. US of opacities affecting more than 50% of the lungs. RT PCR
the lungs revealed an irregular, discontinuous pleural for Sars-CoV-2 was positive in material sampled from
artefact, small supleural consolidations and diffuse pul- her trachea. She rapidly developed multiple organ failure
monary infiltration (white lung). Bowel US examination and septic shock refractory to broad-spectrum antibiot-
Fig 5. Ultrasound image showing thickened pleural line with irregularities next to areas of lung parenchyma in which is still possible
to identify A lines. Photomicrography showing alveolar septa thickening by fibrosis (arrow, hematoxylin-eosin stain, magnification
200 X) (b). Scattered epithelial cells with nuclear alterations compatible with viral infection (arrow) and foci of fibrin thrombi in
alveolar capillaries (dashed arrow, hematoxylin-eosin stain, magnification 200 X) (c).
6 Thomas Thomsen et al Ultrasonography on the non-living. Current approaches.
Fig 6. Ultrasound image of enlarged cervical lymph node (a); macroscopic view of a pulmonary embolus in a large branch of pulmo-
nary artery (embolus shown by an arrow) (b); microscopic view of pulmonary parenchyma, showing perivascular lymphatics dilated
by the presence of emboli of neoplastic epithelial cells exhibiting atypical nucleim cellular pleomorphism, organized as rudimentary
glandular acini. hematoxylin-eosin stain, 400 X magnification) (arrows points towards neoplastic emboli (c).
Med Ultrason 2021; 0: 1-10 7
transducers exist that might be helpful in the oral cavity. may need to be informed about soft-tissue, so may need
At first the forward looking endocavitary probe, second to be a forensic investigator or a forensic clinician. Fig-
the sideways looking (transducer cable in the lateral di- ure 10 demonstrates how well connective tissue, muscle,
rection), often intra-operatively used, hockey stick probe, nerve, and glands can be distinguished by US. While
as well as third, the also sideways looking but transducer such is known for medical US, it has previously been
cable in the elevational direction L30-8 array. This al- a challenge in dental due to probe dimensions and spa-
lows the transducer to image sagittal, transverse and cor- tial resolution. Of note is also the observed gas bubble
onal slices in the oral cavity (fig 8, fig 9). formation in cadaver tissues. Figure 11 shows frames re-
Case 8 corded during an elevational sweep from retro-molar to
The above mentioned soft-tissue imaging qualities molar region. A significant number of bubbles are seen,
were demonstrated in a study concerned with posterior most dominantly in the muscle tissue. These might either
mandible pertinent to clinical dentistry, e.g. oral, peri- be the result of previous freezing of the specimen or are
odontal and implant surgery [32]. While oral surgeons originating from the known postmortem gas formation
during the process of decomposition [1] (fig 10, fig 11).
Discussion