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Laurent et al.
CT After Fatal Diving Accidents
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Special Articles
Original Research
Postmortem CT Appearance
of Gas Collections in Fatal
Diving Accidents
Pierre-Eloi Laurent 1, 2
Mathieu Coulange 3,4
Julien Mancini 5
Christophe Bartoli 6
Jacques Desfeux 6
Marie-Dominique Piercecchi-Marti 6
Guillaume Gorincour 1,2
Laurent PE, Coulange M, Mancini J, et al.
468
OBJECTIVE. The purpose of our study was to define the postmortem CT semiology of
gas collections linked to putrefaction, postmortem off-gassing, and decompression illness
after fatal diving accidents and to establish postmortem CT diagnostic criteria to distinguish
the different causes of death in diving.
SUBJECTS AND METHODS. A 4-year prospective study was conducted including
cases of death during diving. A hyperbaric physician analyzed the circumstances of death
and the dive profile, and an autopsy was performed. Subjects were divided into three groups
according to the analysis from their dive profile: decompression illness, death after decompression dive without decompression illness, and death after nondecompression dive without
decompression illness. Full-body postmortem CT was performed before autopsy.
RESULTS. The presence of intraarterial gas associated with death by decompression illness had a negative predictive value (NPV) of 100%, but the positive predictive value (PPV)
was only 54% because of postmortem off-gassing. The PPV reached 70% when considering
pneumatization of the supraaortic trunks. Pneumothorax, subcutaneous emphysema, and intraarterial gas, all of which are classic criteria for decompression illness diagnosis, are not
specific for decompression illness.
CONCLUSION. This study is the first to show that pneumothorax, subcutaneous emphysema, and intraarterial gas, all of which are classic criteria for decompression illness diagnosis, are not specific for decompression illness. Complete pneumatization of supraaortic
trunks is the best postmortem CT criteria to detect a fatal decompression illness when CT is
performed within 24 hours after death.
ross-sectional imaging has experienced an increasingly important role in legal medicine over
the past 10 years [1, 2]. In the
case of diving accidents, postmortem CT [3]
has facilitated the visualization of intravascular gas collections, which are difficult to
detect in autopsies [4]. The most frequent
cause of death in diving accidents is cardiovascular disease. Cold water leads to a redistribution of blood volume, with an increase
in cardiac work and sometimes cardiac decompensation [5, 6]. Drowning is also a frequent cause of diving fatalities but is often
secondary to technical incidents [7] or diving accidents. The third cause is decompression illness. Decompression illness includes
decompression sickness and arterial gas embolism secondary to pulmonary barotrauma
[8]. Decompression sickness is caused by
bubble formation (off-gassing) from dissolved inert gas. The solubility of the inert
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Subjects
Inclusion and exclusion criteriaAll diving accidents in scuba diving and apnea free-diving (also
called breath-hold diving) from September 2008 to
September 2012 in the Bouches-du-Rhne area (the
Postmortem CT
Before the autopsy, full-body CT was performed
on each subject with a 64-MDCT bi-tube scanner
(Definition, Siemens Healthcare). Postmortem CT
was performed in two sets: the first included the
head and neck; the second included the arms, thorax, abdomen, and legs. No contrast media was injected. The image acquisition was performed in the
dorsal decubitus position with the arms along the
body. The CT parameters for head and neck imaging were 140 kV; 320 mAs with dose modulation;
FOV, 240 mm; pitch, 0.4; and slice collimation,
1 mm. The CT parameters for full-body imaging (encephalon excluded) were 140 kV; 400 mAs
with dose modulation; FOV, 500 mm; pitch, 0.6;
and slice collimation, 1 mm. The reconstructions
and interpretations were performed with the Syngo
workstation (Siemens Healthcare).
Radiologic Interpretation
Two board-certified radiologists with experience in forensic radiology jointly analyzed the
radiologic data. The radiologists were blinded to
the circumstances of the accident and autopsy
findings. Each item in the analysis was recorded
as present or absent. The topography of the gas
collections was divided into the following categories: arterial examining the entire arterial system
including cerebral vascularization, left cardiac
cavities, and pulmonary veins; venous including
the entire venous system including cerebral vascularization, right cardiac cavities, and pulmonary arteries; and pleura including the presence
of pneumothorax.
To research postmortem CT diagnostic criteria that would lead to a CAGE diagnosis, two
supplementary criteria were defined [35]: complete pneumatization of the supraaortic trunks involving the left ventricle, aortic cross, and entire
supraaortic trunk up to and including the Willis
polygon completely filled with gas, without a visible blood-air level and pneumatization of the right
ventricle with the entire right ventricle completely
filled with gas. To document the effects of CPR,
the postmortem CT analysis also looked for subcutaneous emphysema limited to the thoracic area
and fractured ribs.
Study Groups
Study groups were formed according to the
data from the dive profile analysis, medical history, and autopsy. A consensus was obtained
from the forensic pathologists and the hyperbaric physician. Subjects were classified in one
of three groups on the basis of the circumstanc-
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Laurent et al.
es in which the accident took place and the information from existing literature, notably from
animal studies [30, 31], to study the gases respectively due to gas embolisms, postmortem
off-gassing, and putrefaction.
Decompression illness group (CAGE) The
decompression illness group consisted of subjects whose death was directly linked to CAGE.
We purposely chose not to distinguish between
deaths linked to severe decompression sickness
and barotrauma. Because the circumstances of
death are similar, there are few criteria to differentiate between them in the autopsy and dive profile analysis. The following criteria were chosen
for inclusion as decompression illness: dive profile analysis including decompression scuba dive
and fast ascent or diver did not follow advised
decompression stops; loss of consciousness during ascent or a few seconds after having come to
the surface; autopsy findings of cyanosis, bloody
foam at the mouth, hemotympanum, or presence
of a patent foramen ovale (predisposing factor);
and pathologic findings of alveolar hemorrhage or
rupture of interalveolar walls.
Decompression diving groupSubjects in the
decompression diving group did not experience a
decompression illness but experienced a decompression dive. The divers were respectful of the
recommended decompression stops during the ascent or the death occurred on the sea floor. The
following are the criteria for the classification of
the decompression diving group: lack of evidence
for a decompression illness, the accident occurred
during a scuba dive, and the dive necessitated decompression stops.
Nondecompression groupThe subjects in the
nondecompression dive group did not perform a
decompression dive and did not experience a decompression illness. Only putrefaction gas was
observed. The following are the criteria for the
classification of the nondecompression diving
group: lack of evidence for a decompression illness, no decompression dive, and the accident occurred while free diving (apnea).
Results
Subjects
We examined 20 fatalities from September 2008 to June 2012. Two divers
were excluded from the study because the
postmortem CT studies were performed
more than 72 hours after death (91 and
183 hours). In both cases, the delay in performing CT was due to difficulty in recovering the bodies. Eighteen subjects were
eventually studied, including four women and 14 men. All accidents occurred in
seawater. The results are presented in Tables 1 and 2. The median age was 47 years
(age range, 2374 years). The median dive
depth was 36 meters (range, 360 meters),
Statistics
Quantitative variables are presented in the form
of a median (minimummaximum). Categoric
variables were presented as counts (%). The three
study groups were compared with a Kruskal-Wallis analysis for quantitative variables and Fisher
exact test for categoric variables. The agreement
Age (y)
Sex
BMI
49
27
52
17
Cause of Death
4.0
53
CAGE
66
29
36
38
No
4.0
23
CAGE
42
52
25
16
No
4.5
68
CAGE
45
25
42
56
No
4.5
27
CAGE
74
25
38
18
No
6.0
24
CAGE
39
29
50
25
No
7.0
24
CAGE
59
32
33
51
No
55.0
75
CAGE
61
25
31
23
No
3.5
52
Cardiac failure
Cardiac failure
53
23
53
29
No
43.0
47
10
48
23
60
33
Yes
14.0
53
Drowning
11
42
29
60
33
Yes
14.0
51
Drowning
12
51
23
35
19
No
8.0
27
Cardiac failure
13
23
23
NR
NR
No
7.0
24
Drowning
14
28
25
20
No
8.0
21
Drowning
15
60
25
No
15.0
25
Drowning
16
37
30
No
28.0
43
Cardiac failure
17
37
23
NR
NR
No
48.0
50
Drowning
18
24
23
NR
NR
No
20.0
24
Drowning
NoteSubjects 13, 17, and 18 were free divers. BMI = body mass index, CPR = cardiopulmonary resuscitation, CAGE = cerebral arterial gas embolism, NR = not recorded.
a1 = CPR performed, 0 = CPR not performed.
470
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Group 1
Group 2
Group 3
49 (3974)
51 (4261)
33 (2360)
Total
47 (2374)
0.041
25 (22.651.9)
0.084
Maximum depth
38 (2552)
53 (3160)
3 (36)
36 (360)
NR
Duration of dive
26 (1756)
29 (1933)
3 (320)
25 (356)
NR
Delay before CT
4.5 (455)
14 (3.543)
17.5 (748)
8 (3.555)
0.112
27 (2375)
51 (2753)
27 (2150)
35 (2175)
0.176
NoteData are median with minimummaximum in parentheses. Significant difference was considered p <
0.05. Group 1 = decompression illness, group 2 = death after decompression dive without decompression
illness, and group 3 = death after nondecompression dive without decompression illness. BMI = body mass
index, NR = not recorded.
TABLE 3: CT Results
Containing Only Gas
Subject
Subcutaneous
Arterial Venous Supraaortic
Right Emphysema Limited PneumoGas
Gas
Trunks
Ventricle to Thoracic Area
thorax
Decompression illness
group
1
10
11
12
13
14
15
16
17
18
No decompression dive
group
Tested Criteria
Diagnostic criteria for decompression illnessTable 4 examines the presence or absence of postmortem CT criteria according to whether a decompression illness took
place. There was no statistically significant
link between the presence of arterial gas and
death by decompression illness (p = 0.054).
CAGE
(%)
Sensitivity
(%)
Specificity
(%)
PPV
(%)
NPV
(%)
Intraarterial gas
54.5
100
0.054
100
45.5
53.8
100
Pneumothorax
27.3
0.245
72.7
53.3
27.3
100
0.004
100
72.7
70
100
9.1
57.1
0.047
57.1
90.9
80
76.9
Right ventriclea
36.4
100
0.013
100
63.6
63.6
100
NoteCAGE = cerebral arterial gas embolism, PPV = positive predictive value (PPV), NPV = negative predictive value. Significant difference was considered p < 0.05.
aContaining only gas.
Discussion
Limitations
The main study limitation is the small
number of subjects in each group. This can
be explained by the prospective design of the
study as well as the relative rarity of diving
accidents. However, to our knowledge, this
is the largest study with as many subjects
and containing thorough data including a detailed description of the circumstances of the
accident, dive profile analysis, postmortem
CT, and autopsy.
The ages of the subjects included were
different within each group. The subjects in
group 3 were younger than the subjects in
the other groups. This can be explained by
the presence of three free divers in the nondecompression diving group. This sport is
mostly practiced by younger people. We also
think that the age difference between the
groups in the study did not modify our postmortem CT diagnostic criteria, specifically
the presence of intravascular gas collections.
CPR maneuvers were performed on 14
divers. CPR can generate artifact gas collections, which was shown in our animal
experiments [30] and in other studies [33,
40]. Even though the CPR performed never
successfully resuscitated the victims in this
study, it was necessary to perform CPR for
medicolegal and ethical reasons. Our study
described the real situations that confront
teams after a death while diving.
36
32
10
Depth (m)
15
20
24
20
16
30
12
35
40
472
10
Time (min)
15
20
28
25
25
Temperature (C)
Three criteria were systematically present after a death by CAGE (negative predictive value [NPV] = 100%): presence of intraarterial gas, complete pneumatization of
the supraaortic trunks and left ventricle and
pneumatization of the right ventricle (Fig. 2).
The complete pneumatization of the supraaortic trunks and the right ventricle had a
strong concordance ( = 0.886) because only
one discordance was observed.
Postmortem off-gassingWhen comparing the decompression and nondecompression dive groups, we observed a significant
difference concerning the presence of intraarterial gas. Nondecompression dives were
characterized by the absence of intraarterial
gas (p = 0.015).
CPR maneuversThe presence of subcutaneous emphysema limited to the thoracic
area (Fig. 3) was not statistically linked to
the practice of CPR maneuvers (p = 0.234).
The positive predictive value (PPV) was
100% for the practice of CPR maneuvers,
but the NPV was weak (30.8%). However,
rib fractures and subcutaneous emphysema
limited to the thoracic area were always associated ( = 1).
Death on sea floorTwo of the included subjects died on the sea floor at great
depths (60 meters). We observed a complete pneumatization of supraaortic trunks,
left heart ventricle, and right ventricle in
both subjects.
32 m/min
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Tested Criteria
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not with decompression illness. We previously showed this in an animal model [30].
We propose two postmortem CT diagnostic
criteria for a death by decompression illness.
First, complete pneumatization of the supraaortic trunks and left heart ventricle and decompression illness were statistically significantly linked (p = 0.004). The NPV was 100%,
and its presence is necessary to make this diagnosis. This sign also had a good PPV of 70%.
This criterion is therefore more relevant than
the presence of intraarterial gas, in which the
PPV was lower. In our study, the false-positive findings for complete pneumatization of
the supraaortic trunks were due to a long delay
before conducting postmortem CT or a death
on the sea floor in decompression diving. After a death on the sea floor, there is no pulmonary filtration of dissolved gas and much larger quantities of gas are released postmortem,
which explains the complete pneumatization of
vessels. In the late postmortem CT (case nine,
43 hours after death), the intravascular gas
quantities seen in the postmortem CT result in
an increase over time, as shown by the animal
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Laurent et al.
jects in the nondecompression diving group.
Intraarterial gas can therefore have three origins, which supports our hypotheses. The first
is decompression illness by barotrauma with
a rupture of the alveolar-capillary membrane
and arterial gas embolism, by severe desaturation accident with nitrogen bubbles breaking
through the pulmonary capillary filter with the
opening of intrapulmonary shunts [20, 21], or
by permeabilization of a patent foramen ovale
or any other right-to-left shunt [8, 17].
The second is postmortem off-gassing,
which is confirmed by the results of our animal study [30]. After exposing animals to hyperbaric conditions in a chamber and simulating the recommended decompression stops,
we observed arterial gas linked to postmortem off-gassing. To differentiate between
postmortem off-gassing and decompression
illness, we proposed to use the length of time
to CT appearance. We observed that in animal models, postmortem off-gassing occurred
3 hours postmortem [30]. We proposed a cutoff time of 3 hours before which arterial gas
that is observed can only correspond to decompression illness. However, in practice it
is difficult to perform postmortem CT within this delay, considering the time required
for rescue teams to recover, attempt to resuscitate, and transport the body. This adds to
off-gassing that occurs quickly when the dive
is deep and long. Therefore, it is difficult to
use the delay before gas appearance as a criterion. Nevertheless, to avoid the presence of
postmortem off-gassing and improve the relevance of a decompression illness diagnosis,
CT must be performed as early as possible.
The third is putrefaction gas, which does
not usually occupy the arterial topography if
CT is conducted within 24 hours postmortem. Subject 16 did show the presence of intraarterial gas because CT was performed 28
hours after death. Intraarterial gas was only
detected in subject 17, the subject with the
longest delay before CT (48 hours postmortem). These results also confirm the results
from our animal study in which no arterial
putrefaction gas was present on repeated CT
performed up to 24 hours after death [30].
Among the three possible causes, the analysis of intraarterial gas can affirm the presence of putrefaction gas [41] but does not
differentiate between decompression illness
and postmortem off-gassing.
Origin of Venous Gas
Our results, as expected, show an exclusive venous topography of putrefaction gases
474
Acknowledgments
The authors thank Pierre Champsaur,
Pierre Perich, Evelyne Basso, and all the CT
technologists.
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