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Australian Journal of Forensic Sciences

ISSN: 0045-0618 (Print) 1834-562X (Online) Journal homepage: http://www.tandfonline.com/loi/tajf20

Reliability of weathering in the estimation of the


post-mortem interval of human remains buried in
coffins

Ines Buekenhout, Duarte Nuno Vieira & Maria Teresa Ferreira

To cite this article: Ines Buekenhout, Duarte Nuno Vieira & Maria Teresa Ferreira
(2016): Reliability of weathering in the estimation of the post-mortem interval of
human remains buried in coffins, Australian Journal of Forensic Sciences, DOI:
10.1080/00450618.2016.1257066

To link to this article: http://dx.doi.org/10.1080/00450618.2016.1257066

Published online: 23 Nov 2016.

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Download by: [Hacettepe University] Date: 19 January 2017, At: 05:31


Australian Journal of Forensic Sciences, 2016
http://dx.doi.org/10.1080/00450618.2016.1257066

Reliability of weathering in the estimation of the


post-mortem interval of human remains buried in coffins
Ines Buekenhouta, Duarte Nuno Vieirab and Maria Teresa Ferreirac,d
a
Laboratory of Forensic Anthropology, Department of Life Sciences, Faculty of Sciences and Technology,
University of Coimbra, Coimbra, Portugal; bFaculty of Medicine, University of Coimbra, Coimbra, Portugal;
c
Laboratory of Forensic Anthropology, Department of Life Sciences, University of Coimbra, Coimbra, Portugal;
d
Centre for Functional Ecology, University of Coimbra, Coimbra, Portugal

ABSTRACT ARTICLE HISTORY


Although the post-mortem interval (PMI) is essential in forensic Received 26 September 2016
sciences, dating skeletonized remains is a complex task for forensic Accepted 26 October 2016
scientists, not only because of the lack of reliable methods that
KEYWORDS
currently exist for its estimation but also due to the variability of the Forensic anthropology;
cadaveric decomposition process, which involves a series of factors. weathering; skeletonization;
Weathering and breakdown of remains progresses with time, from post-mortem interval;
cracking to loss of shape, and is accepted to occur in observable taphonomy
stages. When dealing with buried remains, these processes will take
longer because many of the most destructive agents will be shut out.
Burial represents a unique environment which has not been examined
often. This study analysed bone weathering (weight loss, grease,
degradation, fractures and flaking) of the atlas, axis, humerus, femur
and first metatarsal of 86 individuals recovered from a Portuguese
cemetery plot. Sex, age-at-death, burial period and storage period
were taken into account, but several problems may have affected the
outcome of the study. However, PMI estimation based on weathering
is not reliable, confirming that burial contexts create distinct micro-
taphonomic environments.

1.Introduction
Estimation of the post-mortem interval (PMI) is a fundamental aspect in forensic sciences.
Legally the establishment of PMI can determine the prescription or not of a crime and aid
in the reconstruction of the events surrounding the death of an individual. Despite repre-
senting a pertinent and significant question, the estimation of PMI is of particular difficulty,19
because decomposition involves a series of complex factors. The majority of cases rely upon
decomposition stages, anecdotal evidence and personal experience.2
Recently, there have been significant advances in this area, allowing us to better under-
stand cadaveric decomposition and the numerous endogenous factors (cause of death, sex,
body-build) and exogenous factors (deposition, temperature, precipitation, pH, soil) that
influence it.5,1015 While decomposition of soft tissues has been the focus of a number of

CONTACT Maria Teresa Ferreira mtsferreira@yahoo.com


2016 Australian Academy of Forensic Sciences
2 I. BUEKENHOUT ET AL.

studies,11,12,1619 several authors comment on the lack of research covering taphonomic


changes to skeletal remains and how it relates to PMI; the link still being very unsatisfactorily
defined.7,2023 Therefore, it is understood that the older human remains are, the more difficult
PMI estimation becomes.3,23 This is confirmed by the lack of reliable methods that currently
exist when only skeletal elements persist. As Vass et al.24 affirm, the post skeletonization
period of decomposition is most difficult to assess. This absence of adequate PMI estimation
tools in death investigations can lead to inaccurate PMI estimations and potentially to mis-
carriages of justice.
Taphonomy comprises a series of processes (biological and geological) which can affect
organic material after death.25,26 The taphonomic factor, where variability is the rule, greatly
influences the development of PMI estimation methods. As with soft tissue decomposition,
it is accepted that skeletal decay also occurs in observable stages but that the timing in
which the alterations take place are site-dependent.21,2729 This study will focus on weather-
ing, or response of the bone to its immediate environment,26 in a coffin-burial context in
Portugal. As suggested by Behrensmeyer,30 weathering will lead to a structural response by
skeletal elements mainly illustrated by fissuring, flaking and cracking of the bone surface
which develops progressively and leads to near destruction of bone. As such, there are
signs indicative or suggestive of a certain PMI. Bone weathering studies have been conducted
in different parts of the world,2022,3032 but weathering rates differ by region. Interestingly,
they have focused primarily on exposed remains. Since neither environment is static, burial
settings will lead to a difference in observed or expected results.33
When buried, decomposition of remains takes approximately eight times longer than on
ground surface,13 primarily because in environments where moisture, shade and low tem-
peratures prevail, decomposition and weathering will be slowed down. The rate of decay
depends also on burial depth: corpses buried deeply and/or in coffins will disintegrate at a
slower rate than those deposed within a shallow depression.10,19 Burial of remains also shuts
out destructive decaying agents such as insect and animal activity.22 Mant34 found that
airtight coffins and clothing tended to slow the decomposition rate of remains. Coffins ini-
tially protect human remains from direct contact with soil or substrate and organisms such
as plant roots and bacteria, but will eventually, due to gradual breakdown, allow the infil-
tration of various transformative agents such as minerals, plant roots, bacteria, water and
others.35 When in contact with a soil environment, chemical and physical alterations, or
diagenesis, of the tissue occurs.36 A coffin will also damage some portions of the skeleton
due to friction,35 making burial a specific and unique decomposition environment that has
been studied rarely.
The purpose of this study is to analyse if bone weight, grease presence, bone degradation,
post-mortem fractures or flaking are of value when establishing PMI of human remains, as
the development of inexpensive and expeditious PMI assessment methods is important. It
is known that the weight of a bone is an intrinsic property that has a significant influence
on a variety of taphonomic processes,37 and that it will decrease with time due to deminer-
alization. As for grease, Galloway et al.s17 and Behrensmeyers30 studies reveal that a bone
can still show surface grease even when cortical degradation is already observable. This
phenomenon has also been described by other authors such as Ubelaker.9 It is accepted
that the degree of degradation will increase with time,27,28 as will the extent of fractures and
flaking.
AUSTRALIAN JOURNAL OF FORENSIC SCIENCES 3

Another aspect of this study is to determine which bones are more durable in a coffin-
burial context, as larger skeletal elements are well known for their survival.20,21,38
In order to achieve this, 86 adult human remains from a single Portuguese cemetery plot
with different PMI were analysed. Data regarding age-at-death and sex of the individuals,
burial and storage periods were also taken into account.

2. Materials and methods


The sample consisted of 86 skeletons from the Twenty-first Century Identified Skeleton
Collection, housed at the University of Coimbra, Portugal (CEI/XXI). This collection contains
skeletal remains of Portuguese adult individuals of both sexes exhumed from the Capuchos
Cemetery, Santarm.39 The individuals were buried in coffins in graves (as opposed to coffins
in family tombs a reasonably common Catholic practice) with the following standard
dimensions: 2m long, 0.65m wide and 1.15m deep, and were only exhumed when
skeletonized.
The analysed individuals perished between 1995 and 2001, and were exhumed between
1999 and 2007. Females represent 51.2% (n = 44) of the sample, while males compose 48.8%
(n=42). Since the collection originated from cemetery remains, it reflects the Portuguese
demographic trend; therefore, the majority of skeletons are those of older individuals
(x=76.62, s.d.=14.98). The age-at-death of the female sample ranges between 50 and 97years
(x=76.62, s.d.=14.98); the male sample offers a larger age-at-death distribution, from 33 to
95years (x=71.38, s.d.=17.07). Table 1 presents the samples classification by age-group and
sex. The CEI/XXI contains skeletons with diverse PMI, which offers an excellent opportunity
to test this issue. Skeletons were not only subjected to a burial period but also to a storage
period at the Laboratory of Forensic Anthropology, University of Coimbra, before being
analysed for this study. The remains were deposited in plastic boxes, protected from direct
sunlight, humidity, soil and other extraneous factors. Table 2 presents the burial period and
timespan between exhumation and analysis, alongside the total PMI of the sample in years
by sex. Prior to this analysis, the skeletons were cleaned; the excess soil being removed with
soft toothbrushes. The atlas, axis, humerus, femur and first metatarsal were analysed. The
humerus and femur were selected to represent larger bones, while the atlas, axis and first
metatarsal were selected to represent smaller bones. Note also, that previous studies 7 have
not yet adequately investigated these smaller bones, and as such there is a need to better
understand their investigative importance when it comes to weathering.
The bones (left sided in paired cases) were assessed in terms of weight (scale SECA model
727; as a measure of bone density); presence or absence of grease; presence or absence of
degradation (wear and removal of bone segments) (Figure 1); presence or absence of frac-
tures (interruption of bone continuity) (Figure 2); and presence or absence of flaking (mar-
bling pattern and fine cracks on the outermost layer of the bone) (Figure 3). These weathering
factors were recorded in order to determine if they have an association with the PMI of buried
Table 1.Distribution by age group and sex.
Age group
Sex <40 4150 5160 6170 7180 8190 91100 Totals
Female 0 1 2 4 7 24 6 44
Male 4 2 3 7 11 12 3 42
Global 4 3 5 11 18 36 9 86
4 I. BUEKENHOUT ET AL.

Table 2.Timespan of the burial period, exhumation period and PMI by sex.
Years
Sex 4 6 7 10
Burial Female 0 40 4 0
Male 1 38 2 1
Years
6 7 8 9 10 11 15
Exhumation Female 4 21 10 2 6 1 0
Male 3 22 7 6 3 0 1
Years
12 13 14 15 16 17 19
PMI Female 4 19 12 2 4 3 0
Male 3 20 8 5 4 1 1

Figure 1.Example of degradation of the proximal epiphysis of the humerus (lateral view).

remains. The criteria were kept simple and readily observable so as to determine their poten-
tial importance for possible future study and more complex analysis.
Due to the fact that endogenous factors are also of importance in the process of decom-
position and skeletonization, sex and age-at-death were taken into account. Exogenous
factors are also considered to have an influence on decomposition rate. Santarm presents
a warm temperate climate with a hot and dry summer40 and the soil is sandy. Fine-textured
clay-rich soils can retard decomposition because their low rate of gas diffusion leads to low
oxygen-CO2exchange, allowing domination of anaerobes over aerobic microbes41 Note,
though, that coarser sandy soils, such as the soil at Santarm, can also retard decomposition
just as is observed in more finely-textured soils.41 Unfortunately, details of burial
AUSTRALIAN JOURNAL OF FORENSIC SCIENCES 5

Figure 2.Example of fracture on the diaphysis of the humerus (anterior view).

Figure 3.Example of flaking on the diaphysis of the humerus (posterior view).


6 I. BUEKENHOUT ET AL.

Table 3.Minimum, maximum, mean and standard deviation for bone weight by sex.
Minimum Maximum Mean Standard deviation
Bone weight (gr.) Female Male Female Male Female Male Female Male
Atlas 2 3 9 20 6 9 1.7 3.8
Axis 3 4 10 20 6 10 1.85 3.52
Humerus 32 60 108 188 61.8 117.9 18.5 28.8
Femur 106 194 374 526 207.36 330 62.185 77.84
First metatarsal 1 4 12 16 4.4 8.1 2.1 2.4

temperatures and pH estimation were not available. Since the climatic variations that
occurred during the years of burial were common to the 86 corpses, one can be reasonably
certain that these variations did not contribute significantly to the variations observed.
Statistically, the variables were studied using IBM SPSS Statistics 20, using Fishers exact
test and Pearsons correlation coefficient. In all tests a significance level of 95%, where p0.05,
was used.

3.Results
From the 86 individuals that were analysed, 84 humeri and femora were present, 83 first
metatarsals, 73 atlantes and 71 axes, comprising a total of 395 bones.

3.1.Weight
The average weight of the examined bones was higher for males than for females (Table 3).
For both sexes, the weight of the humerus, femur and first metatarsal decreased with increas-
ing age-at-death. As for the axis, this finding applied only to the female sample. The weight
of the atlas did not reveal a correlation with any of the variables in the study.
Variations in bone weight were not correlated with variations in PMI, burial and storage
period.

3.2.Grease
The majority of bones did not exhibit grease; each atlas and axis presented a dry surface. As
for humeri and first metatarsals, only three (PMI = 13 and 15years) and one (PMI = 13years)
bones, respectively, displayed a greasy surface. Femora presented a total of 13 individuals
with this feature, with PMI ranging between 12 and 17years.
Only femora appeared to have a relation with one of the variables in the study: the time
period between exhumation and analysis in other words, with the length of time they were
kept in the laboratory. Seemingly, the longer they were stored in plastic boxes, the drier their
surface became (Figure 4) (p = 0.05). No relation between PMI, burial period, sex, age-
at-death and presence or absence of grease on the femur was found.
Grease presence or absence was not correlated with PMI, burial and storage period, sex
and age-at-death for the axis, atlas, humerus and first metatarsal.
AUSTRALIAN JOURNAL OF FORENSIC SCIENCES 7

3.3.Degradation
As for wear and removal of bone segments, it is noteworthy that the atlas and axis presented
less degradation than the other bones in the study. Of the 73 axes, 55 displayed degradation
(PMI=12 to 19years) and 54 of the 71 axes also showed this feature (PMI=12 to 17years). On
the other hand, 83 of the 84 humeri (PMI=12 to 19years) as well as 83 of the 84 femora
(PMI=12 to 19years) and 68 of the 83 first metatarsals (PMI=12 to 17years) presented deg-
radation. Even though long bones seemed to be more affected by this attribute than verte-
brae, the femora and first metatarsals showed degradation primarily of both epiphyses while
the affected vertebrae manifested this attribute throughout the bone. With regard to humeri,
degradation was particularly present on the diaphysis and distal epiphysis.
Degradation of the first metatarsal seemed to be affected by age-at-death (p=0.028)
(Figure 5). The bones from individuals with an age-at-death over 51years appeared more
prone to degradation. Conversely, no relation between PMI, burial period, storage period,
sex and presence or absence of degradation on the first metatarsal was found.
For the axis, atlas, humerus and femur, degradation of bone surface was not related to
PMI, burial and storage period, sex or age-at-death.

3.4.Fractures
In this sample, fractures were more often present on humeri, femora and first metatarsals
than on vertebrae. Cracks were mostly longitudinal and of varying sizes, mostly affecting

Figure 4.Presence or absence of grease on the femora surface by time between exhumation and analysis
in years. N indicates sample size.
8 I. BUEKENHOUT ET AL.

Figure 5.Presence or absence of degradation on the first metatarsal surface by age-at-death in years. N
indicates sample size.

the diaphysis. Only three atlantes (PMI=13 and 14years) presented fractures, along with one
axis (PMI=13years), as opposed to nine humeri (PMI=12, 13 and 17years), 16 femora (PMI=12
to 19years) and 12 first metatarsals (PMI=12 to 16years).
For the atlas, axis, humerus, femur and first metatarsal, post-mortem fractures were not
correlated with PMI, burial and storage period, sex or age-at-death.

3.5.Flaking
Flaking was not a very common feature anywhere in the sample. Among the atlas samples,
two bones presented flaking (PMI=13years); while no axes exhibited this trait. Twenty-six
humeri presented flaking (PMI=12 to 19years, except 16); 11 femora (PMI=12 to 17years)
and one first metatarsal (PMI=13years) displayed this characteristic.
With regard to the humeri, the presence or absence of flaking was related to age-at-death
(p=0.000025), wherein the trait was more present in individuals who passed away at a
younger age (Figure 6). No correlation between PMI, burial period, storage period, sex or
presence or absence of flaking on the humerus was found.
Flaking was not correlated with PMI, burial and storage period, sex or age-at-death for
the atlas, axis, femur and first metatarsal.
AUSTRALIAN JOURNAL OF FORENSIC SCIENCES 9

Figure 6.Presence or absence of flaking on the humerus surface by age-at-death in years. N indicates
sample size.

4.Discussion
It seems that, in a burial context, larger bones (by mass) have a greater chance of recovery
than smaller bones, such as vertebrae, likely due to differences both in bone size and den-
sity.20,38 The first metatarsal was also present; probably because the individuals were buried
with socks and shoes, which assist preservation of foot bones.
Of the recovered and analysed bones, 86% (n=341) showed some sign of weathering,
predominantly in the form of degradation, which mostly affected the femur and humerus.
Fractures were observed mainly on long bones, along with flaking. The atlantes and axes
were less weathered but also less present. In consequence, larger bones such as femora and
humeri, besides being stronger and more resistant, seem to provide a better source of infor-
mation for the study of bone weathering patterns, as observed by Janjua and Rogers.20
As expected, it was found that the analysed bones had a higher average weight in the
male than the female sample; and younger individuals presented heavier bone elements.
This is consistent with Galloway et al.s38 and Lymans37 findings. However, the atlantes and
male axes did not follow this pattern: the vertebrae may suffer a weight loss that is less
significant and measurable than the weight loss observed in long bones. Long bones are
normally the object of forensic study and, being more robust than vertebrae, may present
a more significant as well as measurable rate of density loss. In addition, the shape of
long bones, consisting of a diaphysis and epiphyses, allows a greater loss of density in the
epiphyses.37,38 As for PMI estimations, it seems that a single bones weight cannot predict
10 I. BUEKENHOUT ET AL.

the PMI time period. Therefore, it could be of more interest to weigh a set of bones or the
skeleton as a whole.
This study revealed a relationship between grease and storage for the femur. In other
words, the shorter the storage period, the more likely it was for the femur to present grease.
Thus, one can affirm that the femur begins to dry as soon as it is stored, while when in contact
with soil the surface can experience rehydration due to humidity, as verified by Janjua and
Rogers.20 Thus, when studying buried remains, grease and soft tissue remnants do not seem
to present a reliable prospect for the estimation of time since death, because rehydration
can confuse the observer. However, as Pokines and Baker35 infer, and in agreement with this
study, when confronted with a bone bearing tissues or grease, then most likely it has been
recovered from a burial context.
Pokines and Baker35 observed the effect of coffins on degradation through friction, where
it occurs mainly on the epiphyses of long bones such as the femur and humerus. This explains
the higher degradation of epiphyses found on the femur and first metatarsal. The humerus
did not follow this rule: the greater degradation of the diaphysis and distal epiphyses may
be due to deposition of the proximal epiphyses on the scapulae, as bones can stack on each
other in enclosed spaces. Interestingly, when recovering remains that have decayed in coffins,
it seems that vertebrae show less degradation than long bones despite being the most
absent. Therefore, it seems that, once they begin to deteriorate, they quickly disintegrate,
probably due to their high trabecular bone consistency. This is in accordance with
Behrensmeyer,30 who stated that smaller bones will weather more slowly than larger bones,
but once they attain advanced stages of degradation the rate rapidly increases and these
smaller elements will weather much faster.
As for the first metatarsal, a significant result regarding degradation was found: degra-
dation of the first metatarsal revealed an association with age-at-death. This bone seems to
be more prone to degrade in individuals with an age-at-death of over 51years, perhaps
because the first metatarsal of these individuals may be more fragile and susceptible to
degradation. Ageing makes bones more fragile, which, in turn, facilitates degradation.
Despite the influence of intrinsic factors on bone degradation, no bones showed any asso-
ciation between degradation and PMI, making this attribute of little or no value in the esti-
mation of the referred interval. This was also reported by Rogers,6 who noted that degradation
of bones, in a study that lasted over 24months, did not follow a predictable pattern.
Fractures were perceived to be particularly present on long bones rather than on the
atlantes and axes. The anatomy of the latter may be more resistant to cracking even when
buried in a coffin with the presence of soil and humidity. Among the femur samples, fractures
were observed on 13, 14 and 17year-old remains, while the characteristic was not observed
on 15, 16 and 19year-old remains. A similar disparity in the appearance of fractures can be
observed in the humerus. Fractures were observed on 12, 13 and 17year-old remains but
not on 14, 15, 16 and 19year-old remains. Rogers6 also discussed the fact that the appearance
of fractures is quite variable over time, therefore, as much as this study revealed, this trait
does not seem of value when estimating the PMI of buried remains. Only 41 out of the 395
analysed bones presented fractures, confirming that it is not common for bones buried
inside coffins to crack. This may be due to the low temperatures one finds in deep burials;
Karr and Outram 29 reported that bones are more likely to fracture when exposed to high
temperatures.
AUSTRALIAN JOURNAL OF FORENSIC SCIENCES 11

Flaking was not as present as degradation, being observed mainly on the femur, humerus
and first metatarsal as per Cunningham et al.21 Among the humerus samples, an association
was found between age-at-death and flaking: the number of bones with this trait was higher
for individuals with a lower age-at-death. Degradation seemed more predominant on bones
from older individuals, therefore skeletal elements from younger individuals, being more
robust, may be more prone to flaking rather than suffering a total degradation of the cortical
bone. In other words, younger peoples stronger bones are more likely to reflect the stresses
that accompany decay by flaking. In the present sample, flaking was not a commonly
observed trait and as such it does not seem to be of help when estimating PMI of skeletons
that have been subject to lengthy burials. However, the cleaning method used may have
affected the presence of this characteristic. As such, the extent, location and/or pattern of
flaking may be worth researching further for PMI-indicating clues.
In no case was weathering a useful indication for estimating age of human remains buried
in coffins. Bone weathering is not significantly inhibited in burial contexts, such as coffin-
burial, in a temperate climate. As such, PMI estimation accuracy might benefit from research
into bone alteration including bone mass, grease presence and flaking as an effect of
decay. Such research should sample alteration in bones deposed in a wider range of both
burial and non-burial environments. Also, as observed, weathering of buried bones is influ-
enced by endogenous (sex, age-at-death) and exogenous (soil, humidity) factors, which
need to be taken into account, as well as other factors such as pH and temperature, among
others.

5.Conclusion
This study concluded that PMI estimation based on bone-weathering in coffin-buried
remains that were subjected to similar environmental conditions is not accurate. Therefore,
burial contexts create distinct micro-taphonomic environments23 where endogenous and
exogenous factors also play an important role. Along with many other authors, the authors
of this study also acknowledge that estimating PMI is a difficult task,19,23 while trying to
estimate it based on simple variables, such as weathering, can be very misleading.
Nevertheless, some setbacks during this research were experienced, which may have
influenced the outcome. Specifically, the sample consisted mainly of individuals with a PMI
of 13years. The samples were also subjected both to a coffin burial period and a storage
interval before the analysis took place. In addition, the study was limited to those factors
that were most easily identifiable when trying to investigate factors affecting decay, such
as sex, age-at-death, PMI, burial and storage period. Other factors such as coffin compo-
nents, cause of death, temperature and pH also play an important role in the rate of decay
but these data were unavailable. Recommendations for future studies include research on
a more diverse sample in terms of PMI and age-at-death, taking into account other intrinsic
factors, environmental factors and bone alterations that could lead to the construction of
predictive statistical models with practical applications in forensic anthropology.
On the basis of the results, one can argue that when trying to estimate the PMI based
solely on the decay rates of the remains, inaccuracies are likely to occur. So, weight, grease
presence, degradation, fractures and flaking do not seem promising for the estimation of
PMI of coffin-buried remains because interactions between known and unknown intrinsic
and extrinsic factors create unique micro-taphonomic environments that prevent acceptable
12 I. BUEKENHOUT ET AL.

PMI estimations based solely on the state of cadaverous decomposition. PMI estimations
should be the result of a holistic observation of the body and crime-scene whenever possible.
Regarding bone preservation, in this context femora, humeri and first metatarsals are more
resilient, whilst vertebrae are less present. In addition, as several soft tissue decomposition
studies have revealed, this research demonstrates that different environments present dif-
ferent influences on bone degradation, such as grease preservation.

Acknowledgments
The authors thank Lee Kimber.

Disclosure statement
No potential conflict of interest was reported by the authors.

Funding
The co-author Maria Teresa Ferreira was financed by Gerda Henkel Foundation (AZ 09/F/15).

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