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J Forensic Sci, 2019

doi: 10.1111/1556-4029.14010
CASE REPORT Available online at: onlinelibrary.wiley.com

PATHOLOGY/BIOLOGY

Benjamin Ondruschka,1 M.D.; Carsten Babian,1 M.D.; Martin Neef,2 M.D.; Johann Zwirner,1 M.D.; and
Marcus Schwarz,1 M.Sc.

Entomological and Cardiologic Evidence of


Time Since Death in Short Postmortem
Intervals

ABSTRACT: Estimating the time since death of the deceased is a main goal in forensic investigations, but this can be challenging due to con-
tradictory results derived from different investigations at the scene of death. We present a case of a 78-year-old woman, found dead in a small for-
est with broad-leaved trees, whose husband had a history of domestic violence. Routinely performed investigations, such as postmortem rectal
temperature and lividity, yielded inconsistent time since death results between only a few and longer than 20 h. This difficulty was most likely
caused by high ambient temperatures of up to 38.0°C, which negatively influenced the informative value of the applied nomogram method. Addi-
tionally, performed entomological investigation of fly maggots (Lucilia illustris) recovered from the corpse and the assessment of heart pacemaker
data revealed consistent and incontrovertible results. The presented case highlights the benefits of information provided by entomological investiga-
tions and data evaluation of cardiac implantable electronic devices and the combined use of the two techniques.

KEYWORDS: forensic science, acute kidney failure, cardiac implantable electronic devices, forensic entomology, pacemaker, postmortem
lividity, time since death

Time since death estimation is an important goal of forensic the police at 6 p.m. to report that her 78-year-old mother had
investigations at potential crime scenes but may be challenging been missing for more than 2 days. She was concerned that
in cases of putrefied cadavers or where different methodological her father could be involved in this issue as he was known to
techniques provide conflicting results (1). have been physically violent against his wife for several dec-
Until today, the classical method of death time estimation is ades. Furthermore, the father held a gun license and was
the measurement of the core body temperature and the compar- known to retain an old weapon. The police were unable to find
ison of this to ambient temperatures using nomograms. This a dead person in close proximity to the family house. The man
includes the addition of specific information, such as the cadav- explained that his wife had left the house without giving
eric body weight, clothing status, the movement of air around notice in the morning of that day and had not returned until
the corpse, and if the body was found in wet or dry conditions. the time he gave his testimony.
Furthermore, the existence and disappearance of livor mortis is The daughter began looking for her mother at 7 p.m., search-
the first true sign of death, the existence and re-establishment of ing several local spots in the area. She found her dead body 1 h
rigor mortis and examination of diverse supravital reactions are later lying supine on a forest floor about 300 m away from her
most commonly used by the forensic pathologists in external family’s house. The emergency doctor confirmed her death at
examinations of fresh corpses (2–4). However, additional ento- the scene. He attributed her cause of death to a traumatic head
mological and cardiologic investigations could be useful tools in injury as he noticed a bump on her forehead.
doubtful cases, but are mostly neglected in routine work to date.
Forensic Scene Investigation
Case Report The local investigation began in a small village next to Chem-
Case History nitz, Saxony, Germany after midnight at an ambient temperature
of 20.1°C. Due to the darkness, it was necessary for the fire bri-
During a phase of uncommonly hot summer days for the gade to install technical lighting. The deceased female was lying
region with ambient temperatures up to 38°C, a daughter called in supine position (Fig. 1). This area was located in a small for-
est with broad-leaved trees, such as willows and red alder. The
1
Institute of Legal Medicine, University of Leipzig, Johannisallee 28, forest was 30 cm above sea level.
D-04103 Leipzig, Germany. The “bump” on the forehead was visible as a separation of
2
Department of Cardiology, Division of Internal Medicine, Neurology and Der- the epidermis from the underlying dermis due to larval infiltra-
matology, University of Leipzig, Liebigstraße 20, D-04103 Leipzig, Germany. tion and movement (Fig. 2). The same phenomenon could be
Corresponding author: Benjamin Ondruschka, M.D. E-mail: benjamin.on-
druschka@medizin.uni-leipzig.de seen bilaterally at the groin. Further, moving larvae were found
Received 13 Nov. 2018; and in revised form 6 Jan. 2019; accepted 7 Jan. in a mask-like covering at the neck and along the hairline. Fly
2019. eggs were located at the corners of the eyes.

© 2019 American Academy of Forensic Sciences 1


2 JOURNAL OF FORENSIC SCIENCES

The physical examination did not reveal any relevant external


injury, such as traumatic head injuries or signs of asphyxiation.
Livor mortis was established on the back and was therefore con-
sistent with the supine position of the cadaver at the scene. The
lividity was fixed indicating that no shifting was possible. The
lividity did not disappear with thumb pressure (Fig. 3) but
reduced to a lesser intensity when pressure was applied with for-
ceps. The rigor mortis was fully established in all joints without
any re-establishment after initial testing. Testing of an idiomus-
cular contraction failed at the left biceps muscle. Finally, a body
core temperature of 35.8°C was recorded in the rectum.
The cause and manner of death remained unclear at the scene
without distinctive signs of involvement of third parties. The
time since death was inconclusive as certain signs of death
yielded a death time between 20 and 36 h prior to the investiga-
tion. On the contrary, the core body temperature remained near
FIG. 1––Scene of investigation at the time of arrival of the forensic staff. its initial value of 37.0°C indicating only a short interval since
death. However, very hot ambient temperatures during the post-
mortem interval could potentially have influenced the core body
temperature.

Autopsy Results
Full autopsy began 8 h after the investigation at the scene
ended. Its main findings were that the corpse suffered from a
hypertensive heart and kidney disease with a regular subclavicu-
lar pacemaker in situ. There was no evidence of relevant trau-
matic impact, only some minor abrasions were visible at the
elbows and knees. The kidneys were pale and with uremic odor.
Microscopic examination showed no severe signs of shock in
the kidneys but some tubular hyaline cylinders (Fig. 4). The
heart muscle showed disseminated fresh cell necrosis. Post-
mortem biochemistry revealed acute kidney failure, a normal
glucose metabolism, and no signs of acute inflammation
(Table 1). Toxicological blood analyses were negative for illicit
drugs and ethanol. Finally, a fatal kidney failure was declared as
natural cause of death.

Entomological Investigation
Numerous first instar larvae of the fly genus Lucilia were col-
lected from the accumulations at the face and groin of the corpse
together with one adult fly of Lucilia illustris during the scene
FIG. 2––Entomological infestation at the face and neck. The arrow points investigation which started at 1 a.m. These were the oldest sam-
at the bump reflecting a separation of the epidermis from the dermis due to ples collected and used for the following investigations. Given
larval movement.
that maggots were found at different body regions in the same

FIG. 3––Image representing absence of disappearance of postmortem lividity by thumb pressure.


ONDRUSCHKA ET AL. . POST-MORTEM ENTOMOLOGICAL AND CARDIOLOGIC INVESTIGATION 3

June to September. Fly eggs of other species could not be


detected.
Eggs of Lucilia illustris require less than 10 h, at an ambient
temperature of 35°C, to develop and hatch into first instar larvae.
Whilst the minimum interval for hatching at the average temper-
ature of 27°C is reported to be minimum 13 h according to
Wang et al. (6). An additional 10–12 h is required to reach the
second instar phase, which was already observed during autopsy
(6). The maggots sampled first at the scene were reared to their
adult stages until they reached fertility in a programmable cli-
mate chamber (KBF 240; Fisher Scientific GmbH, Schwerte,
Germany) at 22.0°C and 80% humidity as replicated growth
conditions. This temperature was selected as Wang et al. (6)
described that this fly species cannot complete its life cycle in
temperatures above 35°C. The flies had unrestricted access to
pig mincemeat until their oviposition. Directly after that, the
temperature was programmed as a controlled environment cabi-
net according to the data of the German Weather service to
FIG. 4––Kidney, stained with hematoxylin–eosin, indicating tubular swel- check development times and the first maggots hatched after
ling, and hyaline cylinders (scale bar: 50 lm). 10 h. We could identify second instar larvae not earlier than
10 h after hatching. The minimum time intervals for the first as
well as the second instar stages were, therefore, nearly congruent
with Wang et al. (6). Given that a dying person already attracts
TABLE 1––Results of postmortem biochemistry of the 78-year-old female
corpse found in a forest, using blood and cerebrospinal fluid (CSF) samples
attention of adult necrophagic flies and the body in question was
to determine potential functional causes of death. easy to access in the open environment (7), the first insect con-
tact should be close to the time point of death. Using the ento-
Chemicals (Postmortem) mological data, a minimum time since death was calculated with
Analyzed Substrate Result Reference Interpretation 10–13 h before investigation at the scene.
Creatinine CSF 3.0 mg/dL <2.5 mg/dL Acute kidney failure
Urea CSF 236.6 mg/dL <100 mg/dL
Cardiologic Investigation
HbA1c Blood 5.3% 4.8–5.9% Normal glucose
Glucose CSF 11.4 mg/dL metabolism The removal of a cardiac implantable electronic device posi-
Lactate CSF 380.2 mg/dL
Traub’s 391.6 mg/dL <500 mg/dL
tioned in a right subclavicular subcutaneous pocket was per-
sum formed carefully by placing an external permanent magnet to
C reactive CSF 5.6 mg/L 10 mg/L No inflammation avoid any self-endangerment by electric shock. After preparation
protein of the aggregate and its electrodes, both could be disconnected
by using a screwdriver specific to the device. Data evaluation
larval stage, it was not possible to declare the body region of was started the day after autopsy by using telemetric pacemaker
initial fly colonization. During autopsy, many more first and also software. The pacemaker aggregate type DDDR (Medtronic
second instar larvae of the fly genus Lucilia were caught. Some Sensiaâ, Dublin, Ireland) including electrodes and batteries was
of the larvae collected at the scene were cultivated at a climatic without malfunctions. Increasing atrial and ventricular tachycar-
chamber (KBF 240; Fisher Scientific GmbH, Schwerte, Ger- dia disturbances were recorded in the pacemaker’s internal mem-
many) until reaching the third instar and the adult phase and ory 2 days before the body was discovered. A final 14 h of
were afterward devitalized in hot water. Microscopic determina- lasting arrhythmia ultimately led to a persistent asystole 10 h
tion revealed that larvae and adults were from the species Lucilia before the start of the investigation. Since tachycardia arrhyth-
illustris only. mias have been documented repeatedly and in increasing time
Climate data from the 3 days prior to the time of external intervals, these dysfunctions were plausibly attributed to a cate-
examination of the deceased was obtained from the German cholaminergic reaction caused by another fatal disease rather than
Weather service in order to assess the potential settlement per- a sudden cardiac death in the sense of a malignant arrhythmia.
iod. This data were collected on a German Meteorological Office Finally, Fig. 5 summarizes the timeline of the case report with its
weather station approximately 700 m away from the scene loca- most relevant timepoints and results of the scientific investigations.
tion. The ambient temperatures were measured twice by the
police officers and further two times by the forensic staff on site, Discussion
and these were in close proximity to the data archived by the
German Weather service with small variances of 0.7°C. There- Although forensic entomological investigations are known for
fore, the weather station represents comparable values for the their benefits in determining longer postmortem intervals, they
outside temperature and rainfall of the location. The amount of are rarely requested in cases with fresh corpses (8). Additionally,
precipitation was 0.4 mm. The average temperature for the ques- postmortem investigation of pacemakers is infrequently used in
tionable postmortem period was 27.1°C with daytime maximum forensic pathology to date. Recent research indicates benefits of
values of 38.0°C. pacemaker reading in solving causes and noting time of death in
The insect fauna was typical of early postmortem periods for around two-thirds of all cases, irrespective of the putrefaction
the local region (5). Lucilia with its species Lucilia illustris is stage of the deceased (9,10). In the presented case, witness testi-
known to be an initial colonizer during summer months from monies were contradictory regarding the time interval of a
4 JOURNAL OF FORENSIC SCIENCES

40
Day 0 Day 1 Day 2 Day 3
35

Last seen alive by husband


Long-lasting tachycardia
30

25
Missed by daugther

Scene investigation
Single tachycardia

Police call: Missed


20

Found dead
15

Death time

Autopsy
10

05

00
Day 0; 4 p.m.

Day 0; 6 p.m.

Day 0; 8 p.m.

Day 0; 10 p.m.

Day 1; 12 p.m.

Day 1; 2 a.m.

Day 1; 4 a.m.

Day 1; 6 a.m.

Day 1; 8 a.m.

Day 1; 2 p.m.

Day 1; 4 p.m.

Day 1; 6 p.m.

Day 1; 8 p.m.

Day 2; 4 p.m.

Day 2; 6 p.m.

Day 2; 8 p.m.
Day 1; 10 a.m.

Day 1; 12 a.m.

Day 1; 10 p.m.

Day 2; 12 p.m.

Day 2; 2 a.m.

Day 2; 4 a.m.

Day 2; 6 a.m.

Day 2; 8 a.m.

Day 2; 10 a.m.

Day 2; 12 a.m.

Day 2; 2 p.m.

Day 2; 10 p.m.

Day 2; 12 p.m.

Day 3; 2 a.m.

Day 3; 4 a.m.

Day 3; 6 a.m.

Day 3; 8 a.m.

Day 3; 10 a.m.
ambient temperature (in °C) body temperature (in °C) average temperature of the maggots (in °C)
Core body temperature: < 3 hpm

Lividity: > 20 hpm

Rigor mortis: > 19 hpm

Idiomuscular contraction: > 13 hpm

Pacemaker: 10 hpm

Entomology: 10 - 13 hpm

FIG. 5––Graphic overview of local temperature profile at the scene obtained from the German Weather service with illustration of case-relevant points in the
time scale in the upper part. The horizontal black lines in the bottom part indicate the interval ranges in hours postmortem (hpm) from each of our evidence
types and highlights the contradictory results gathered by basic evaluation. The black vertical line illustrates the time point of forensic investigation at the
scene.

missing person between approximately 2 days and less than underestimated in relation to the discovery of the corpse at the
1 day. The related corpse investigation could not clarify the time scene. Higher core temperatures than expected in corpses
since death conclusively as signs of death yielded a much longer required greater understanding; yet, these may be explained by
time interval than the measured rectal body core temperature. In inflammatory diseases and fever. To date, it is still controversial,
the presented case, the lividity did not disappear on blunt thumb as to whether intense putrefaction processes and heat production
pressure which indicates a postmortem time of more than 20 h of fly larvae from friction can influence the core temperature of
(11). More recent data suggested that validity of such time cut- a corpse (14). Unfortunately, the mass core temperature of the
offs depends on the investigated body region (central or periph- maggots shown in accumulations initially at the head and the
eral) and the applied blunt force for the blanching test (12). inguinal regions of the body were not measured at the scene.
Given the inconsistency in the time since death estimation at The case report highlights the necessity of adequate storage of
scene, additional entomological and cardiologic investigations entomological traces at scene and at the beginning of the
were ordered. Cardiac data provided a more accurate time since autopsy, as well as the correct removal of any cardiac implanta-
death estimation in this case. Also, the entomological data con- ble electronic devices during evisceration, as these are shown to
firms that the corpse has been at the scene for the duration of be beneficial for time since death investigations, even in shorter
the egg stage, given that the larvae recovered from the scene postmortem intervals. In previous autopsies, we observed data
were first instar larvae only. The combination of the data from memory deletion, alarms, and error messages in pacemakers
both sources, entomology and cardiology, leads to the conclu- where electrodes have simply been cut during removal or the
sion that the postmortem interval is a minimum of 10 h before device was ripped out during high-speed accidents. Thus, valuable
the investigation took place. This result was in line with the forensic information might be missed if implanted devices are
statement given by the husband. removed in a destructive manner. Every pacemaker company
The estimation of time since death is one of the most impor- defines its own time intervals to retrieve previous data, but this
tant issues for forensic pathologists. This is because external could be up to 7 days. If this interval is passed, the devices in
examinations depend on several confounding aspects as men- question may be read by the manufacturers themselves. In our
tioned above. All these items are combined in a nomogram in experience, any failure of retrieval from the devices should not be
daily forensic routine and enable the time since death to be esti- restricted by longer intervals given that after death, there will be
mated with a certain standard deviation (13). Additional investi- only minute current flow and batteries of pacemakers are designed
gations of the external examination can subsequently refine the to last 8–10 years. Even after such intervals, pacemaker compa-
determined interval, as so-called “compound methods” (1). How- nies are able to read all important data with the help of their inter-
ever, the nomogram method is only applicable up to tempera- nal software.
tures of 37°C by convention and was therefore inconclusive in In the presented case, both additional investigations could
the given case where ambient temperatures were shown to solve the time of death potentially accurately and consistently
exceed this limit. Hot ambient temperatures might hold native and provide information of the manner of death (long-lasting
core body temperatures at a steady state or at least influence the tachycardia arrhythmias) in a functional death case due to acute
algor mortis. Therefore, the time of death determined might be kidney failure.
ONDRUSCHKA ET AL. . POST-MORTEM ENTOMOLOGICAL AND CARDIOLOGIC INVESTIGATION 5

6. Wang Y, Li LL, Wang JF, Wang M, Yang LJ, Tao LY, et al. Develop-
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