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Original Article

Proc IMechE Part H:


J Engineering in Medicine
2015, Vol. 229(5) 343–349
Necromechanics: Death-induced Ó IMechE 2015
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DOI: 10.1177/0954411915581409

of human tissues pih.sagepub.com

Pedro ALS Martins1,2, Francisca Ferreira1,2, Renato Natal Jorge1,2,


Marco Parente1,2 and Agostinho Santos3,4,5,6

Abstract
After the death phenomenon, the rigor mortis development, characterized by body stiffening, is one of the most evident
changes that occur in the body. In this work, the development of rigor mortis was assessed using a skinfold caliper in human
cadavers and in live people to measure the deformation in the biceps brachii muscle in response to the force applied by the
device. Additionally, to simulate the measurements with the finite element method, a two-dimensional model of an arm section
was used. As a result of the experimental procedure, a decrease in deformation with increasing postmortem time was
observed, which corresponds to an increase in rigidity. As expected, the deformations for the live subjects were higher. The
finite element method analysis showed a correlation between the c1 parameter of the neo-Hookean model in the 4- to 8-h
postmortem interval. This was accomplished by adjusting the c1 material parameter in order to simulate the measured experi-
mental displacement. Despite being a preliminary study, the obtained results show that combining the proposed experimental
procedure with a numerical technique can be very useful in the study of the postmortem mechanical modifications of human
tissues. Moreover, the use of data from living subjects allows us to estimate the time of death paving the way to establish this
process as an alternative to the existing techniques. This solution constitutes a portable, non-invasive method of estimating the
postmortem interval with direct quantitative measurements using a skinfold caliper. The tools and methods described can be
used to investigate the subject and to gain epidemiologic knowledge on rigor mortis phenomenon.

Keywords
Biomechanical testing, finite element method, rigor mortis, postmortem interval, necromechanics

Date received: 10 September 2014; accepted: 13 March 2015

Introduction makes muscles flaccid again, due to autolysis, that is,


self-digestion of the cell by its own enzymes, and
After the death phenomenon, the body undergoes a decomposition of muscle cells.1 The development of
series of modifications known as postmortem changes. rigor mortis is frequently studied in forensic medicine
One of the most evident modifications is body stiffen- to estimate the postmortem interval, and in the food
ing, known as cadaveric rigidity or rigor mortis. industry, it is used to access the tenderness of meat.
Rigor mortis occurs in all muscular tissues, and it is
caused by a decrease in the adenosine triphosphate
(ATP) levels, which cause the binding of the muscle
1
filaments of actin and myosin, with consequent stiffen- Faculdade de Engenharia, Universidade do Porto, Porto, Portugal
2
ing of the muscles.1,2 The phenomenon develops gradu- 3
INEGI-Universidade do Porto, Porto, Portugal
INMLCF, IP - Instituto Nacional de Medicina Legal e Ciências Forenses,
ally and at a variable rate, being influenced by several
Instituto Público
factors such as environmental temperature, physical 4
CENCIFOR - Centro de Ciências Forenses, Coimbra, Portugal
exercise before death and the cause of death.3,4 Usually 5
FMUP - Faculdade de Medicina do Porto
6
rigidity starts appearing 20 min after death and its UM-ESC - Universidade do Minho, Escola de Ciências da Saúde
intensity increases achieving a maximum around 6–12 h
Corresponding author:
postmortem (Hpm). The maximum or full rigor may Pedro ALS Martins, INEGI-Universidade do Porto, Campus da FEUP, Rua
last between 18 and 36 h.2 After that period, rigidity Dr. Roberto Frias, 404, 4200-465 Porto, Portugal.
gradually disappears.4,5 The disappearance of rigor Email: palsm@fe.up.pt

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344 Proc IMechE Part H: J Engineering in Medicine 229(5)

It is difficult to define an etiology of rigor mortis.


Environmental and individual variables, such as air tem-
perature, occurrence of physical exercise prior to death,
as well as race, gender, age and physical condition, are
some of the known factors influencing the onset and
evolution of rigor mortis.6 There is a wide range of inter-
individual variability, due to endogenous or exogenous
factors.7 Even without longitudinal studies on large ran-
dom samples, there are some thumb-rules regarding
many individual characteristics, which may allow us to
define a basic etiology of rigor mortis. In general, men
will have stronger rigor mortis than women since they Figure 1. Sketch of the Adipsmeter.
typically have larger muscle mass.8 For the same reason,
rigor may not be apparent or extremely hard to detect in software application, LipoSoft.14 The equipment was
age groups where low muscle bulk is typical, that is, in originally developed to assess the body fat percentage
the young and in the old.1,8 According to Van den by measurement of the skinfold thickness using a sim-
Oever,6 the muscular mass is the main factor influencing ple, portable, non-invasive and low-cost diagnostic sys-
the onset, resolution and degree of complete rigor. tem.15,16 The Adipsmeter is composed of a closed
Several studies exist in which the development of cylindrical body, two jaws ending with clamps, a han-
rigor mortis is evaluated. However, to the authors’ dle and a lever (Figure 1). The system incorporates
knowledge, no information can be found on the char- digital sensing and a wireless communication system
acterization of the mechanical properties’ modification with the software application.16
with the time elapsed since the death phenomenon. In The device ensures a constant pressure of 10 gf/mm2
contrast with Biomechanics, which includes the study between the clamp faces and skin. Using a load cell, the
of the mechanical properties of living-adaptable tis- force measured in the extremities of the device is of
sues,9 this study can more accurately be designated as a approximately 8.4 N, with an error smaller than 5% for
study on Necromechanics:11 the study of the change in the opening range (0–120 mm). A mechanical rotating
mechanical properties of biological tissues with the mechanism keeps the parallelism between the clamps
postmortem interval. faces for any jaw opening angle.15
Biological soft tissues present a highly nonlinear
mechanical behavior since they undergo large strains
with small applied stresses.12 For this reason, soft tissues Measurements on the cadavers
are often studied using hyperelastic concepts, having a
In this study, the Adipsmeter16 was used in human
behavior that can be compared to rubber-like and elas-
tomeric materials. Muscle tissue is usually considered as cadavers to measure the deformation in the biceps bra-
homogeneous and transversely isotropic due to the pre- chii muscle in response to the force applied by the
dominant unidirectional alignment of the muscle fibers device. The measurements were performed at the
and as incompressible due to the high water content. In North Branch of National Institute of Legal Medicine,
nonlinear mechanics, the response of the tissues is mod- I.P. (INML). All the procedures were subjected to the
eled using constitutive laws that are derived from a approval of the direction board of the institute and in
strain-energy density function or strain-energy function all cases the Portuguese law for investigation in cada-
(C).13 In the literature, there are several specific forms vers was respected. No post mortem harm was
of the strain-energy function that are frequently used inflicted. The measurements were performed both on
with variable efficiency to describe the elastic properties the left and right arms at 10 cm from the elbow joint
of hyperelastic materials. and with a distance of 9 cm between the two clamps.
In this study, a skinfold caliper was used in human To avoid inter-observer error, all the experimental data
cadavers to correlate the deformation measured using were collected by the same person after a period of
the device on the biceps brachii with postmortem time. adaptation to the technique. The corpses were kept at
The measurements were also performed in live people. room temperature and in supine position during the
Additionally, finite element simulations were imple- procedure. The values were recorded within 5 s using a
mented to simulate the measurements using a two- sampling frequency of 50 Hz. The device records the
dimensional (2D) model of a cross-section of the arm. distance between the two clamps. Initially, the clamps
were placed at the measuring position in contact with
the skin but without deforming the tissues to measure
Materials and methods the initial thickness. Subsequently, the device was
allowed to deform the tissues with its calibrated force.
Adipsmeter The thickness was measured while the load was being
The equipment used in this work consists of an adapted applied. Every measurement was repeated twice with a
Harpenden skinfold caliper, the Adipsmeter, and a brief interval (3–4 min), and the final thickness was an

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Martins et al. 345

average of both measurements. With these thickness the medial cross-section of the arm, which corresponds
values, the displacement at a certain hour postmortem to the area where the measurements were performed,
was calculated by the following expression: was chosen. Only the left arm was used for the simula-
tions. The real dimensions of the arm were obtained
Dd = lt  l0 through digital image analysis with the ImageJ soft-
with l0 being the initial thickness and lt the thickness ware, using the known dimension of the threaded holes
while the force was being applied, measured at a certain made to serve several purposes, such as to help in the
postmortem hour t. A decrease in the displacement alignment of the cuts.17
value with time indicates an increase in rigidity. The selected slice was manually segmented and the
To study the evolution of rigor mortis, the measure- contours of the different tissues that constitute the arm,
ments were performed every hour during 4 h (in some namely, the skin, fat, bone and the different muscles
cases during 5 h) starting from the first measurement. (biceps brachii, brachialis, and medial, long and lateral
The population of this study consisted of a total of 18 head of triceps brachii), were obtained. Afterwards, the
corpses, 6 females and 12 males, with an average age of contours were imported into the software ABAQUS
62.9 6 16.8 years, an average body mass index (BMI) of and the finite element mesh was created. The finite ele-
25.9 6 6.9 kg/m2 and a postmortem interval between 2 ment mesh consisted of 4281 four-node bilinear plane
and 13 Hpm. The exclusion parameters included death strain quadrilateral, hybrid, constant pressure elements
by drowning or fire, corpses with signs of cadaveric (CPE4H in ABAQUS). The clamps of the Adipsmeter
decomposition or with significant muscular atrophy were modeled as 2D analytic rigid shells, while con-
and corpses stored in the cold chamber prior to the straining the clamps’ rotations and their vertical move-
measurement. ment. The bone was considered as a rigid body. The
contact between the clamps and the skin was consid-
ered frictionless since the use of friction did not change
Measurements on live people the simulation results significantly. The simulation was
performed with an imposed load of magnitude equal to
To compare the values obtained in the corpses with the
the load applied by the device, 8.4 N. The final finite
strain value measured in live people, the measurements
element model can be observed in Figure 2.
were also performed in 58 volunteers, 31 females and
The material behavior for the different layers was
27 males, with an average age of 40.8 6 15.1 years and
assumed to be homogeneous, isotropic, hyperelastic
with an average BMI of 25.3 6 4.3 kg/m2. The proce-
and incompressible. Due to the presence of fibers, the
dure to obtain and analyze the data was identical to the
muscle behavior is normally assumed as transversely
one described previously. With these measurements,
isotropic, when a three-dimensional (3D) model is con-
the mean displacement value in the biceps brachii for
sidered. Since a plane strain condition is assumed, and
live people when subjected to the force applied by the
the muscle fiber orientation is perpendicular to the sec-
device was obtained. Additionally, this mean value also
tion considered in this study, as shown in Figure 2, the
gives an indication of the displacement expected to be
effect of the fibers was neglected and the muscles
measured at the moment of death, that is, a baseline
assumed as isotropic. To characterize the mechanical
deformation.
behavior of the muscle and adipose tissue layers, the
Both live volunteers and corpses were from the
neo-Hookean constitutive model was chosen following
North region of Portugal. There was no rigid control
the approach used by Tran et al.18 to estimate the
of race; nevertheless, both groups were highly domi-
material constants for the different layers based on
nated by Caucasians, as is typical of the demographics
indentation tests. In the neo-Hookean model, the
of the region.
strain-energy density function for isotropic and incom-
pressible materials19 is given by (1)
Finite element analysis
C = c 1 ð I 1  3Þ ð1Þ
In this work, the compression of the biceps brachii in
response to the force applied by the Adipsmeter was where I1 is the first scalar invariant of the right
analyzed and computationally simulated using the Cauchy–Green tensor and is given by I1 = tr(C). In this
finite element method (FEM) with a simplified model work, the adipose tissue was modeled with a c1 material
in ABAQUSÒ. For that purpose, a 2D model of the constant of 0.42 kPa. By comparing the numerical
arm was used to analyze the behavior of the tissues results with the displacements observed experimentally
when subjected to an applied load. The measurements for live people and for the interval of 4–8 Hpm, the
performed allowed us to estimate the mechanical prop- muscle tissue material constant c1 of the neo-Hookean
erties of the different layers. The geometry of the arm model was manually adjusted in order to obtain a good
was reconstructed from the images obtained from the agreement between the FEM simulation and the experi-
Visible Human Project. The cadaver used in this proj- mental results.
ect was a 38-year-old male with a BMI of 27.9 kg/m2. Regarding the skin layer, different properties
For this work, a slice of the thorax region containing obtained from the literature were tested and the one

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346 Proc IMechE Part H: J Engineering in Medicine 229(5)

Figure 2. Finite element model used. The different materials are presented in different colors: skin in green, adipose tissue in
white, muscles in red and bone in blue. The two clamps of the device are presented in black at the initial position of the simulation.

presenting more suitable results regarding the experi- negative slope of approximately 20.50) with increasing
mental data was chosen. In that sense, the skin was Hpm, which points to an increase in the rigidity. Data
modeled using the properties from Evans and Holt,19 for 3 and 9 Hpm were not included in the trend line cal-
which uses the Ogden material model to characterize culations, despite fitting the linear model reasonably
the mechanical properties of the skin. In this model, well, since sample size was approximately 50% of the 4-
the strain-energy function19 is expressed in terms of the to 8-Hpm interval. Data for 2 Hpm and in the interval
principal stretches (2) from 10 to 13 Hpm had to be discarded since the sam-
ple size was too small due to logistic constraints. In
X
N
mp  a a a  order to compare the displacement measured in the
Cðl1 , l2 , l3 Þ = l1 p + l2 p + l3 p  3 ð2Þ
p=1
ap corpses and in live people, the measurements were also
performed in 58 volunteers. A higher average displace-
The versatility of Ogden’s model lies on its extensibility ment value was measured in the live people
as additional terms, corresponding to additional para- (31.27 6 4.62 mm) in comparison to the values mea-
meter pairs ðmi , ai Þ : mi ai . 0, may be added depending sured in the cadavers, as expected. Additionally, a com-
on problem complexity. It is widely used in many parison between the values measured on the left and
engineering modeling applications of hyperelastic right sides of the same muscular group was performed.
materials. In this work, the skin layer was modeled As a result, no considerable difference was found in the
using m = 10 Pa and a = 26. evolution of rigor mortis on both sides of the body for
most of the measured cadavers. Nevertheless, the
obtained values differed in the muscular group side in
Results the majority of the population both in the corpses and
Adipsmeter measurements in the live people. A difference between both sides of the
body is not surprising since usually people do not have
At each hour of the postmortem interval considered
equally developed muscles on both sides of the body.
(2–13 Hpm), both left arm and right arm measurements
were taken. Using the data obtained from the 18 cada-
vers, an average of the displacements at each Hpm was
Finite element analysis
calculated. This method allowed correlating the experi- In order to correlate the modification of the mechanical
mental values with the postmortem time (Figure 3). properties with the postmortem time, the material para-
For Hpm with the highest number of cases meter c1 of the neo-Hookean model for the muscle
(4–8 Hpm), a trend line was drawn using a linear regres- layer was manually adjusted so that the simulation out-
sion of the type, displacement = m 3 Hpm + b. The comes corresponded to the total displacement observed
results show that the displacement diminishes (with a experimentally in the live people and in the corpses for

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Martins et al. 347

Figure 3. Graphical representation of the average displacement values (mm) obtained in the biceps brachii muscle for the live
people and for the corpses according to the postmortem time. The vertical black lines represent the standard deviation. The gray
points represent the postmortem hours with the highest number of cases; for these points, a linear trend line was drawn and the
respective equation is shown in the top right corner.

whether the displacement is symmetric on both clamps


since only the total displacement is measured. However,
the displacement of each clamp is most likely asym-
metric due to the thickness inhomogeneity of the differ-
ent layers, as occurs in the example used to reconstruct
the arm geometry. For that reason, the obtained result
seems to correspond to a realistic situation, and to com-
pare with the experimental results, only the total displa-
cement (sum of the displacement obtained for the right
and left clamps) was considered.

Figure 4. Variation in the muscle tissues c1 material parameter


for the neo-Hookean model in live people (Hpm = 0) and with Conclusion
the postmortem time.
After the death phenomenon, the body undergoes a
series of modifications known as postmortem changes.
the postmortem interval from 4 to 8 Hpm. In this work, The estimation of the postmortem interval is often
the properties of both the skin and adipose tissue layers made based on these modifications, such as rigor mor-
were assumed to remain unchanged during rigor mortis tis. In this work, rigor mortis development was assessed
evolution. As a result, the obtained values were using a skinfold caliper both in human corpses and live
adjusted to a linear regression including dispþlive and people. As a result, a decrease in the displacement val-
excluding disp-live; the value in the live people and the ues with the postmortem time was observed and a
obtained equations are shown in Figure 4. With this higher displacement value was obtained for live people,
result, it can be observed how the material parameter as expected.
c1 of the muscle changes with the postmortem time. It is clear in the data shown in Figure 3 that the
As an example, when running the FEM simulation increase in stiffness in the interval between 0 and 3 Hpm
imposing the load applied by the device, for the is very important. An ideal version of this work should
Hpm = 5 h, and with the material parameter include the study of that interval, as well as the time
c1 = 3.7 KPa, the obtained displacement was 14.3 mm interval at which cadaveric rigidity starts to subside
for the right clamp and 8.1 mm for the left clamp (18–36 h after the beginning of full rigor). The logistical
(Figure 5), which is in accordance with the values constraints of this work did not allow the inclusion of
obtained experimentally (Figure 3). these periods, which limits our understanding of the
The asymmetry in the displacements of the right and phenomena involved. However, we believe our methods
left clamps makes sense considering that on the right are adequate for the purpose of understanding the evo-
side, the layer of adipose tissue (which is the one with lution of rigor in the interval 4–8 Hpm.
lower rigidity) is thicker than on the left side. In the Even though one knows that a decrease in displace-
experimental data, it is not possible to distinguish ment is associated with an increase in rigidity, the

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348 Proc IMechE Part H: J Engineering in Medicine 229(5)

Figure 5. Reconstructed geometry after deformation resultant of an 8.4-N load applied on each clamp: (a) deformed geometry and
(b) maximum principal stresses distribution (MPa).

establishment of a relation between the measured val- This general approach does not account for individual
ues and a physical parameter that allows the characteri- variability but is a prototype of the technique to be
zation of the tissue mechanical behavior is of great used with every subject in future tests.
importance. This parameter might be the Young modu- The obtained results allow us to have a first insight
lus for elastic materials, or in the case of hyperelastic into how the mechanical properties of the muscular tis-
materials, it can be the parameters of the constitutive sue change with the postmortem time. Considering that
models. In this work, a first correlation between the when working with human cadavers several restrictions
muscle material parameter c1 of the neo-Hookean and ethical protocols need to be followed, the use of
model and the time since death was already achieved. minimal invasive procedures is of great importance
In order to take more assertive conclusions, the sample when dealing with human corpses. For that reason, the
size should be increased, since this study was carried proposed experimental procedure combined with a
out with a population of 18 cadavers. This would allow numerical technique can be very useful in the study of
obtaining a more accurate average displacement value the mechanical modifications of human tissues after
for each hour postmortem. death. This solution constitutes a portable, non-
In addition, the method could be improved by the invasive method of estimating the postmortem interval
implementation of an inverse FEM allowing the esti- with direct quantitative measurements using a skinfold
mation of the mechanical properties from the measured caliper. The tools and methods described can be used
experimental displacement in a more expeditious way. to investigate the subject and to gain epidemiologic
Constructing a specific 2D geometry for each cadaver, knowledge on rigor mortis phenomenon. Moreover,
for example by the estimation of the thickness of each the use of data from living subjects allows us to esti-
layer using ultrasound imaging, would result in more mate the time of death as shown in Figure 4. If the
accurate simulations. Therefore, the lack of support technique is able to provide an adequate degree of
imaging techniques (X-ray, computed tomography accuracy in larger validation tests, it may be considered
(CT) or ultrasound) is a limitation of this study. as an alternative to estimate the time of death.
Afterwards, applying in the different geometries, the
displacement obtained during the experimental mea- Declaration of conflicting interests
surements and using an optimization algorithm, the
material parameters for each layer could be estimated None declared.
for different postmortem hours, and not only for the
muscle layer, as in this work. For that purpose, the Funding
contribution of each layer to the final displacement xão para
This study was financially supported by Fundac
value should be studied. To mitigate this limitation, the a Ciência e a Tecnologia (FCT)—Portugal, through the
2D finite element model built on one level of the visual Fundo Europeu de Desenvolvimento Regional
human project was chosen taking into account the typi- (FEDER) under Grant SFRH/BPD/71080/2010 from
cal biceps size found on both cadavers and volunteers. Fundo Social Europeu (FSE) under programs POPH-

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Martins et al. 349

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