Pneumomediastinum and soft tissue emphysema of the neck in postmortem CT and MRI; a new vital sign in hanging?

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www.elsevier.com/locate/forsciint

Forensic Science International 153 (2005) 181–188

Pneumomediastinum and soft tissue emphysema of the neck in

postmortem CT and MRI; a new vital sign in hanging?

Emin Aghayev a,*, Kathrin Yen a, Martin Sonnenschein b, Christian Jackowski a,Michael Thali a, Peter Vock b, Richard Dirnhofer a

a Institute of Forensic Medicine, University of Bern, Buehlstrasse 20, 3012 Bern, Switzerlandb Institute of Diagnostic Radiology, University Hospital, 3010 Bern, Switzerland

Received 31 March 2004; accepted 3 September 2004

Available online 11 November 2004

Abstract

Spontaneous pneumomediastinum commonly occurs in healthy young men or parturient women in whom an increased intra-

alveolar pressure (Valsalva maneuver, asthma, cough, emesis) leads to the rupture of the marginal pulmonary alveoli. The air

ascends along the bronchi to the mediastinum and the subcutaneous space of the neck, causing cervico-fascial subcutaneous

emphysema in 70–90% of cases. Ninety-five forensic cases, including five cases of hanging, were examined using postmortem

multi-slice computed tomography (MSCT) and magnetic resonance imaging (MRI) prior to autopsy until December 2003. This

paper describes the findings of pneumomediastinum and cervical emphysema in three of five cases of hanging. The mechanism

of its formation is discussed based on these results and a review of the literature. In conclusion, when putrefaction gas can be

excluded the findings of pneumomediastinum and cervical soft tissue emphysema serve as evidence of vitality of a hanged

person. Postmortem cross-sectional imaging is considered a useful visualization tool for emphysema, with a great potential for

examination and documentation.

# 2004 Elsevier Ireland Ltd. All rights reserved.

Keywords: Virtopsy; Forensic radiology; Hanging; Pneumomediastinum; Emphysema; Vital reaction

1. Introduction

The finding of pneumomediastinum or mediastinal

emphysema means the evidence of air in the mediastinum.

It is an uncommon, infrequently reported entity, which is

well known in clinical medicine and is usually diagnosed on

the base of specific compliance and by the use of radiological

methods [1–3]. Spontaneous pneumomediastinum commonly

occurs in healthy young men or parturient women in whom

an increased intra-alveolar pressure (Valsalva maneuver,

* Corresponding author. Tel.: +41 31 631 84 11;

fax: +41 31 631 84 15.

E-mail address: [email protected] (E. Aghayev).

0379-0738/$ – see front matter # 2004 Elsevier Ireland Ltd. All rights r

doi:10.1016/j.forsciint.2004.09.124

asthma, cough, emesis) leads to the rupture of the marginal

pulmonary alveoli [4–6]. The air ascends along the bronchi to

the mediastinum and the subcutaneous space of the neck,

causing cervico-facial subcutaneous emphysema in 70–90%

of cases [7,8]. Inversely, pneumomediastinum following

cervico-facial emphysema is very rare and has been reported

as a complication after surgical procedures, head and neck

surgery, or after trauma to the face [9–12]. The most preferable

diagnostic tool for the detection of air in soft tissue is

computed tomography [3].

This group was evaluated for the findings of pneumo-

mediastinum and cervical emphysema. The value of post-

mortem imaging in these cases shall be discussed in the

following.

eserved.

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E. Aghayev et al. / Forensic Science International 153 (2005) 181–188182

2. Material and methods

The Institute of Forensic Medicine in Bern, in collabora-

tion with the Institute of Radiology of the University of Bern,

performs postmortem multi-slice computed tomography

(MSCT) and magnetic resonance imaging (MRI) of forensic

cases prior to traditional autopsy [13–18]. Ninety-five cases

with different diagnoses, including five cases of hanging,

were examined using MSCT and MRI till December 2003.

After exclusion of two cases with no extraluminal gas in the

neck and the mediastinum, three cases were left and are

described:

� C

Fi

(ar

of

ase 1: A 30-year-old male was found hanged on the slide

bar in a bathroom of a hotel. The hanging position was

incomplete and atypical. The strangling tool was com-

posed of a tripled loop of a telephone cable, a leather belt

and a shower hose with a metallic protective layer. Iso-

lated punctual congestive hemorrhages in the conjunctiva

of the left eye and two skin bruises below the chin, each

2 cm � 2 cm, were found. In the history, there was a long

period of drug consumption.

� C

ase 2: A 27-year-old male was found hanged under the

roof on a wooden beam in his house with a 1-cm thick rope

as a strangling tool. The hanging position was complete

and typical. Numerous punctual congestive hemorrhages

in the face, around the eyes and in the conjunctiva of both

eyes were present. No skin injuries were found. In the

history, depression had occurred explicitly since several

years.

� C

ase 3: A 23-year-old white male was found hanging on a

frame of a bridge. The hanging position was incomplete

and typical. The strangling tool consisted of single loop of

g. 1. 3D reconstruction of gas collections (gas structure VR) of case 1 sho

rows). The shape of these air collections reminiscent of sea corals, oriented p

the 3D reconstruction of lungs. Antero-posterior view of the 3D reconstr

a 5-mm thick rope. Isolated punctual congestive hemor-

rhages in the conjunctiva of both eyes were present.

2.1. Imaging

Imaging was performed 50 h after death in the first case

and approximately 24 h in the second and third cases. For

imaging, each body was wrapped in two radiologically

artefact-free body bags (Rudolf Egli AG, Bern, Switzer-

land).

Full body MSCT scanning was performed on a GE

Lightspeed QX/I unit (General Electric, Milwaukee, WI,

USA). Slice thickness was 1.2 mm. One thousand three

hundred and eighty axial cross-sections were acquired in

the first case, 2860 in the second and 1365 in the third case.

The duration of MSCT scanning was approximately 8 min

per case. A 3D volume rendering analysis using a protocol

for the segmentation of gas-tissue boundaries (gas structure

VR, Figs. 1, 3 and 5) on a dedicated workstation was

performed in each case. The gas structure VR protocol

generated a 3D model of all gas-tissue borderlines within

the scanned volume, based on density differences [19].

For MRI, we used a standardized protocol: in the axial

plane, T2-weighted SE sequences (TR/TE 4000/100 ms)

with a slice thickness of 3 or 4 mm and a gap of 1 mm were

systematically used, both without and with fat saturation.

Additionally, in the second case FSPGR (True-FISP, TR/TE

110/6, 4 ms, flip angle 608) and STIR (TR/TE 3700/14 ms,

TI 136 ms) sequences of the axial plane with slices of

4 mm and gaps of 1 mm were added, whereas in the

third case Tl-weighted SE (TR/TE 400/14 ms) and the

same STIR sequences as in second case in coronal

and axial planes were performed. MRI studies required

ws emphysema of the soft tissues of the mediastinum and neck

arallel to the trachea. Antero-posterior (a) and left-sided (b) views

uction of skull, neck and upper parts of thorax (c).

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E. Aghayev et al. / Forensic Science International 153 (2005) 181–188 183

Fig. 2. Axial MSCT (a) and T2-weighted MR (b) images of case 2 show massive cervical emphysema at the level of the thyroid gland (thick

arrows). Gas is mainly located behind the sternocleidomastoid muscles and in the spinal canal (long thin arrows).

approximately 2.5 h. Seven hundred and fifty images were

acquired in the first case and around 500 images in the

second and the third cases. Images were interpreted by

board-certified radiologists, retrospectively, with knowl-

edge of the autopsy findings, in the first and the third case

and prospectively, without knowledge of the autopsy find-

ings in the second case.

2.2. Autopsy

Autopsy was performed at 62 h in the first case and at

36 h after death in the second and the third case. An analysis

Fig. 3. 3D reconstruction of gas collections (gas structure VR) of the sku

interconnected gas cavities in the soft tissue of the neck and the mediast

of alcohol concentration in blood, including putrefaction

alcohol, was carried out in all three cases.

3. Results

3.1. Case 1

MSCT examination showed isolated gas in the brain

tissue and the beginning of gas formation in liver and spleen.

Cervical paratracheal soft tissue emphysema was found,

extending into the mediastinum. The 3D reconstruction

ll, neck (a) and thorax (b) of case 2 shows a complicated system of

inum (arrows).

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E. Aghayev et al. / Forensic Science International 153 (2005) 181–188184

Fig. 4. Bilateral photographs of cervical emphysema of case 2 at autopsy. Gas is located in the connective tissues of the neck (arrows).

using the gas structure VR protocol showed an accumulation

of gas within the soft tissues of the neck and mediastinum,

reminiscent of sea corals, oriented parallel to the trachea

(Fig. 1). All these findings stayed undetected in the autoptic

examination. Lesions of the mucosa of upper or lower

airways were found neither at imaging nor at autopsy.

Alcohol analysis in the blood was negative.

3.2. Case 2

MSCT and MRI examinations showed massive emphy-

sema in the cervical soft tissues, extending into the med-

iastinum down to the diaphragm. Gas was seen behind both

sternocleidomastoid muscles (Fig. 2), in paratracheal and

paralaryngeal regions, above the sternum and behind the left

clavicle. MSCT, furthermore, revealed air in the cervical

spinal canal (Fig. 2) and around both vertebral arteries.

Intravascular gas was not observed. 3D reconstruction using

the gas structure VR protocol showed a complex system of

interconnected gas cavities in the soft tissues of the neck

(Fig. 3), extending into the mediastinum. Autopsy confirmed

the findings of cervical emphysema and pneumomediasti-

num (Fig. 4). During dissection of the soft tissues of the neck

and the mediastinum there was a cracking noise under the

scalpel and dissecting the tissue layers was easier than

usually. Analysis of alcohol and putrefaction alcohol in

blood was negative.

3.3. Case 3

MSCT showed pneumomediastinum extending to the

diaphragm. Gas was localized behind the right sternoclei-

domastoid muscle, in the paratracheal region and bilaterally

to the thoracic aorta. Gas structure VR showed two corre-

sponding stripes of gas parallel to the aorta and some gas in

the right visceral space of the neck (Fig. 5). Gas was detected

in some abdominal vessels, such as liver vessels and portal

vein. These findings had not been detected at autopsy.

Neither by radiological examination nor by autopsy lesions

of the mucosa of the upper or lower airways were found.

Analysis of alcohol in blood, including putrefaction alcohol,

was negative.

4. Discussion

Hussarek and Wolf reported the first case of attempted

strangulation, where the finding of subcutaneous emphy-

sema was radiologically documented [2]. They also dis-

cussed the reason for the absence of this finding in

postmortem autoptic examination. The lack of availability

of radiological examination of strangled persons was stated

and suggested as reason for suspected underreporting [2]. In

clinical medicine, radiological examination of survived

attempted strangulation is performed regularly. Canizares

et al. reported a case of attempted hanging with subcuta-

neous cervical emphysema [1].

The detection of gas within the soft tissues is difficult at

autopsy and the findings of pneumomediastinum or cervical

emphysema are frequently missed. This hypothesis is sup-

ported by the absence of forensic literature mentioning

pneumomediastinum or cervical emphysema in cases of

hanging. In our cases 1 and 3, these findings stayed unde-

tected at autopsy.

Until several years ago, pneumomediastinum and cervi-

cal emphysema by hanging were not observed, unless the

victim survived, was hospitalized and underwent radiologi-

cal examination. The recent fast development of cross-

sectional radiological methods for clinical medicine also

allowed an implementation to forensic medicine; results

of the forensic application of MSCT and MRI have been

demonstrated in the literature [13–18]. Cross-sectional

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E. Aghayev et al. / Forensic Science International 153 (2005) 181–188 185

Fig. 5. 3D reconstruction of air collections (gas structure VR) of the thorax and neck of case 3 shows cervical emphysema of the right neck (thick

arrow) and pneumomediastinum (dotted arrow).

imaging offers recognized advantages to classical radio-

graphy by combining a fast, comprehensive examination

with the documentation of large areas of the body.

Using postmortem imaging, it was easily possible to

detect and document the gas collections within the soft

tissues. In our cases, the gas structure VR protocol of MSCT

data excelled by its 3D presentation of gas within the soft

tissues of mediastinum and neck (Figs. 1, 3 and 5), in the

second case, and even in the spinal canal. In MSCT images

only gas appears always as black due to negative Hounsfield

units [20] (Fig. 2a) and body tissues are graded according to

the gray tones. In MRI, gas also appears as black due to low

signal (Fig. 2b), but also ossification, metal artifact or major

vessel could appear as black and may lead to a pitfall. To rule

out postmortem gas formation by putrefaction and to prove

the vitality of mediastinal and cervical gas accumulation, the

following factors were taken into account:

1. n

egative results of alcohol analysis in the blood, includ-

ing putrefaction alcohol,

2. th

e absence of intravascular gas in the second case and the

presence of minimal cranial and abdominal intravascular

gas in the first case and minimal abdominal intravascular

gas in the third case,

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E. Aghayev et al. / Forensic Science International 153 (2005) 181–188186

3. t

he similar localization and pattern of distribution of gas

of pneumomediastinum and cervical emphysema in all

three cases, corresponding to the characteristics reported

of living cases in the literature,

4. t

he constant sharp upper limitation of emphysema at the

level of the strangulation mark,

5. t

he absence of gas in all other soft tissues of the body

(with the exception mentioned under 2 above).

Two pathophysiological mechanisms potentially explain

the presence of gas in the soft tissue in hanging. First, a

traumatic tear or rupture of lower or upper airways might

result from local violence or medical manipulation of the

airways. Second, from living persons it is known that the

strong and sudden increase of intra-alveolar pressure due to

the compression of the upper airways by strangulation may

break intrapulmonary barriers and cause air to leak and to

escape along bronchi into the connective tissues of the

mediastinum and neck [7,8,21]. Both mechanisms are com-

patible with the finding of air in the visceral space around the

trachea, esophagus and big vessels of the neck, the structures

serving as guides for air spread.

The proper traumatic cause of local subcutaneous

emphysema in hanging was reported in the literature

[22]. Non-traumatic pneumomediastinum and cervical

emphysema were extensively described only in living

patient after inhalational drug abuse [6,23,24], postopera-

tive vomiting [5] or as a spontaneous pneumomediastinum

[3,4,25]. Furthermore, Ito et al. reported a case of sponta-

neous pneumomediastinum in a trombonist [26]. He con-

cluded that the causative factors were the tenderness of

alveoli and repetitive over-inflation of the lung with intra-

alveolar pressures as high as 150 cm H2O during trombone

performance, which would result in alveolar rupture.

Grellner and Madea, studying pulmonary micromor-

phology in fatal strangulations, reported perivascular

and intra-alveolar hemorrhages, local dystelectasis and

focal emphysema [27] as frequent histological patterns

in 106 cases of fatal strangulation and hanging. They

verified focal emphysema as a histological finding in fatal

strangulation.

The mechanism of closing of the upper airways by

compression of the larynx or pharynx and pressing of the

tongue against the palate with an increase of intrathoracal

pressure, was assumed to be the main pathogenesis in our

three presented cases. The compression of the upper airways

in hanging results in attempted ‘‘breathing’’ movements

comparable to the Valsalva maneuver in living persons.

Exhalation against the closed glottis generally plays a

triggering role in the pathogenesis of pneumomediastinum

and cervical emphysema by hanging.

Vital reactions are essential elements of any everyday

forensic activity. In Switzerland, Austria and Germany, an

autopsy is often then indicated, when an external fault is

suspected. There is often a suicidal background in hanging,

and the evidence of vitality is an important step towards

clarification. Vital reactions are produced either by the

ongoing blood circulation system (e.g., congestive hemor-

rhage within the eye conjunctiva, air or fat embolism), by

ongoing respiration [28] (e.g., aspiration of blood [29],

gastric contents, foreign bodies), by a reaction requiring

an intact nervous system [30] (e.g., crow’s feet in electric

accident, in burning or an explosion [31], swallowing of

blood) or by an ongoing metabolism (e.g., evidence of

metabolized products of a poison in urine). Numerous

vitality reactions have been described in connection with

hanging [32–39], the most important ones being: congestive

hemorrhage in the conjunctiva of the eyes, hemorrhage into

the skin between two strangulation marks in case of several

loops, emulsification of fat cells, hemorrhage within the

point of attachment of neck muscles (especially the sterno-

cleidomastoid muscle) and hemorrhage accompanying lar-

yngeal fracture [40]. All these vital reactions are not

compulsary in hanging, and furthermore, they can also be

produced postmortem [32,38,40]. In contrast, pneumome-

diastinum and cervical emphysema are not produced by

blood circulation, but by attempted breathing after the

beginning of airway compression; therefore, they are more

reliable.

The frequency of pneumomediastinum and cervical

emphysema at postmortem MSCT and MRI examination

in hanging was three out of five examined cases. A larger

series of cases is needed to give a more accurate answer to

this question. According to our early experience, the use of

postmortem imaging methods, especially MSCT, should

allow an accurate detection of air in the body soft tissues

without difficulty.

5. Conclusions

1. Postmortem cross-sectional imaging is considered a use-

ful visualization tool, with a great potential for examina-

tion and documentation in forensic medicine.

2. T

he gas structure VR protocol of MSCT data excelled by

its 3D presentation of air within the soft tissues. Both

MSCT and MRI are able to diagnose gas within the soft

tissues, however, postmortem MSCT examination had

better visualization and is the more precise method in the

gas presentation as MRI.

3. In

hanged persons, the findings of pneumomediastinum

and cervical emphysema, after exclusion of putrefaction

gas in the soft tissues, might serve as an evidence of

vitality and thereby be of high relevance in forensic

medicine.

Acknowledgments

Supported by a grant from the Gerbert Ruef Foundation,

Switzerland. We are grateful to Elke Spielvogel, Karin

Zwygart and Vreny Beutler (Department of Diagnostic

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E. Aghayev et al. / Forensic Science International 153 (2005) 181–188 187

Radiology, University Hospital of Bern), and also to Roland

Dorn and Urs Koenigsdorfer (Institute of Forensic Medicine,

University of Bern) for the excellent help in data acquisition

during the radiological examination and forensic autopsy.

Particular thanks go to Naseem Malik for distinguish help in

translation.

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