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Potential groundwater pollutants from cemeteries

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Potential groundwater pollutants
from cemeteries
Science Report Potential groundwater pollutants from cemeteries
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groundwater, cemeteries, burials, ammonia, pollutants
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Science Report Potential groundwater pollutants from cemeteries 3
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eHead of Science
Science Report Potential groundwater pollutants from cemeteries
Executive Summary
This report provides background information on the likely types and concentrations
of potential groundwater pollutants that may arise from the practice of human burial
after death. It is intended as an update of a previous Agency report (P223) and is
for anyone who may need to consider the potential for groundwater pollution from
new or existing cemetery developments.
The report considers the components of the grave including organic and inorganic
body constituents and reviews the likely processes of decay which will liberate
these body constituents into the surrounding soil and groundwater. The likely
timescales for degradation are presented.
The information should help in the preparation of a groundwater risk assessment
for a particular site through providing background data to feed into that assessment.
Science Report Potential groundwater pollutants from cemeteries 5
Executive Summary ........................................................................................................4
1. Introduction ...............................................................................................................7
1.1 Scope 7
1.2 Context 7
2. Review of burial conditions and associated decay processes ............................. 8
2.1 Burial practices and sites 8
2.1.2 Green burials 8
2.1.3 Burial depth 9
2.1.4 Burial numbers per unit area and volumes 9
2.1.5 Embalming 10
2.1.6 Coffins and other non-body contents of the grave 11
2.2 Overview of body decay 11
2.2.1 Macrofaunal Influence on Decomposition. 13
2.2.2 Decay of the soft tissues 13
2.2.4 Decay of soft tissues – fats and the formation of adipocere 14
2.2.5 Bone 14
2.2.6 Factors Affecting Rate of Decomposition 15
2. 3 Environmental change in the vicinity of the grave 16
3. Potential groundwater pollutants from human burials........................................17
3.1 Potential pollutants 17
3.2 Mass transfer out of the grave 17
3.3 Ammoniacal nitrogen 17
3.3.1 Ammoniacal loading in the grave 17
3.4 Formaldehyde 18
3.4.1 Chemistry and action 18
3.4.2 Formaldehyde loading in the grave 18
3.4.3 Degradation of formaldehyde 19
3.4.4 Urea formaldehyde resins 19
3.5 Mercury 20
3.5.1 Mercury loading in the grave 20
3.6 Other metals 21
3.7 Pathogens 22
3.7.1 Pathogen loading in the grave 23
3.8 Phosphorus and Calcium 24
3.8.1 Loading in the grave 24
4. Natural attenuation processes for potential grave pollutants.............................25
Science Report Potential groundwater pollutants from cemeteries
4.1 Biodegradative routes and the availability of terminal electron acceptors in the grave
4.2 Decay and dissolution model 26
5. Risk assessment ......................................................................................................29
6. Discussion ............................................................................................................... 30
6.1 Suggested further work 30
References & Bibliography ..........................................................................................31
List of abbreviations .....................................................................................................34
Science Report Potential groundwater pollutants from cemeteries 7
1. Introduction
1.1 Scope
This report is intended as an aid to those involved in the development and management
of human burial sites and in particular medium to large-scale cemeteries. The document
provides an updated review of the potential pollution issues for groundwater associated
with such sites which may in turn feed into any risk assessment for considering the
environmental implications of a site. It follows on from, and replaces, an earlier report
(Environment Agency, 1999) and builds on some of the additional research which the
Agency has carried out with others in the intervening years (Trick, J, et al, 2002).
The report does not provide a detailed assessment for individual sites but rather is a
point of reference for anyone who may regulate, manage or indeed own such sites.
This report also does not consider animal burials in detail either in large scale incidents,
such as the disposal of carcasses following the outbreak of Foot and Mouth disease
(FMD) nor for the more prosaic, but increasingly common pet cemeteries. For the latter
one might consider that many of the issues and processes would be similar to human
burial sites though the precise details of, for example, body sizes, numbers per hectare
and time to skeleton will be different.
1.2 Context
The human body is made up of a multitude of elements and complex organic
substances. After death, these components return to the wider environment either
through the natural processes of decay or through human intervention for example in
cremation. This document is intended to consider the potential groundwater pollution
risks from areas of land used for multiple burials. Such areas are increasingly known by
a variety of names including cemeteries, graveyards, burial grounds and so on. A
scheme for the definition of such terms has been proposed (Rugg, 2000) but readers
should be mindful that the pollution risks to groundwater are based on the geophysical
and biogeochemical setting of the site and the source term involved rather than the title
or description on the gate. For our own part we have mostly used the term cemetery
intending to convey the impression of a planned site of burial for several to many bodies.
Several authors have commented that the cemetery in effect represents a specialised
form of landfill (Dent and Knight, 1998) and the practice of burial does come very close to
some current terminology in the arena of waste management. However, this comparison
is not entirely helpful and should be used with care, particularly in public discussions.
Certainly, there are some significant differences in the nature of a cemetery and the
concept that most readers may have of a landfill. In particular, the relative volume of soil
to waste and the liquid content are likely to be very different. Nevertheless, for existing
landfills at least the sites do share the common aspect of being a final resting-place for
organic and other material that has the potential to degrade and be transported in the
subsurface. Moreover, the attention paid elsewhere to the regulation of crematoria and
the atmospheric emissions from such establishments (Anon. 2001) shows that the
potential environmental impacts from the disposal of human bodies may need to be
carefully considered. Our focus is on the groundwater which may exist under a
Science Report Potential groundwater pollutants from cemeteries
2. Review of burial conditions and
associated decay processes
2.1 Burial practices and sites
Though it may initially seem that the existing arrangements and practices for the disposal
of the dead are completely established and unchanged for many years, this is not
necessarily the case.
For the great majority of the population there are two main choices for disposal of human
remains, to wit, burial or cremation. Nowadays cremation is considerably more common
than burial with almost 75% of funerals resulting in cremation in 2002 (Cremation Society
of Great Britain, 2003). An indication of the changes in fashion for cremation is that by
contrast in 1885 there were precisely 3 recorded cremations. Though more exotic
options such as burial at sea, launch of ashes into space or even conversion of ashes to
a diamond are available; such disposal would seem to pose little direct risk to
groundwater from the remains. Even more exotic options such as lyophilisation (“freeze-
drying”) followed by crushing, or alkaline hydrolysis in concentrated hydroxide followed
by disposal to foul sewer, have been proposed but are not commonly available in
England and Wales. To be clear, this report focuses solely on the impacts from burials
and the potential for groundwater pollution, cremations are not considered further as
there is a range of regulation and legislation specific to crematorium emissions.
As with any industry new techniques and procedures arise and customer demands can
change both in response to changing demographics and also in response to changing
environmental perceptions. Moreover, the ever increasing demand for development
land, public perceptions particularly from site neighbours and the fact that in some areas
of the country our cemetery capacity is fast filling up (London Planning Advisory
Committee) provide pressures for and against new cemetery developments. With a
current annual burial rate of 140,000 and an area of approximately 5m3 per burial (see
below) we need approximately 70 hectares of land per year for this purpose.
The Home Office has recently published a consultation (Home Office, 2004) on the
regulation and provision of cemeteries, which is intended as a first step to the reform of
some of the rather aged burial law. In particular, the consultation considered the
desirability of requiring local authorities to ensure that adequate cemetery space exists
(currently this is discretionary), as well as the issue of reuse of burial grounds. Note that
there are approximately 25,000 burial grounds across England and Wales (Home Office,
2004). The consultation is largely silent on the potential environmental pollution aspects
of any such new policies.
2.1.2 Green burials
In recent years that has been increasing interest in the uptake of “green” burials and this
was a focus in our earlier report. The term “green burial” can have many meanings
ranging from carrying out the funeral and burial as a close family (rather than using the
services of a funeral director) through some degree of environmental consideration (e.g.
Science Report Potential groundwater pollutants from cemeteries 9
use of a shroud or cardboard coffin in preference to a wooden coffin) to all the above
plus the use of a “natural” burial ground. These latter are often meadow or woodland
sites and are intended to be managed in a way that is environmentally or ecologically
responsible. The previous Agency report noted that in 1997 there were more than 50
“green” burial grounds operating in Great Britain, with 40 more potential sites making
applications for planning permission. More recently in 2003 the Natural Death Centre
has published a list of more than 180 natural burial grounds (Wienrich and Speyer,
2003) and suggest that 200 exist (Personal communication). For the purposes of this
report the most important features of such sites are that:
they may present a higher proportion of new development proposals than might be
supposed from the total number of such sites;
such sites may be more likely to prohibit the use of preservatives (either in embalming
of the corpse or in coffin construction) than more traditional sites;
the sites may allow a larger grave area and thus have a lower frequency of corpses
per hectare;
development proposals may come from individuals or small companies who are not
familiar with the Planning regime and unaware of groundwater considerations;
such sites commonly plant native tree or shrub species around or on top of the grave
thus providing different biological and recharge conditions through the grave.
However, despite the rapid increase in the numbers of these sites the total numbers of
such burials is currently only a small proportion of the total with a report of 1,270
occurring in 2002 out of a total burial and cremation tally of approximately 600,000 per
2.1.3 Burial depth
The depth to which coffins are buried depends in part on the nature of the site and the
anticipated use. A normal minimum of 1.4m may be deeper particularly where the grave
is expected to accommodate 2 or more burials. A table of grave depths for the
Danescourt cemetery was published and is repeated here.
Table 2.1 Depths of burial
Number of coffins Depth
in grave (m bgl)
1 1.40
2 1.83
4 2.74
2.1.4 Burial numbers per unit area and volumes
As the settings and usage of cemeteries can vary widely so too can the numbers and
proximity of bodies buried in a given area. In particular, the distribution of bodies within
natural burial grounds may be more variable than traditional municipal sites. Users of
this report may well have in mind a particular site and circumstance and should then
refer to the individual case rather than rely on approximations provided here.
For those who require some guidance, the numbers presented in the previous Agency
report remain valid. That is, traditional cemeteries may contain approximately 2,000
burials per hectare. Green burials would normally be expected to contain somewhat
Science Report Potential groundwater pollutants from cemeteries
fewer graves, at approximately 1,600 per hectare. However we note that perhaps the
earliest and most famous example of the latter at Carlisle was planned with only 440
graves per hectare (Wienrich and Speyer, 2003) so the green number may normally be
substantially less than that given above. Conversely, as the demand for green burials
appears to be growing it may be prudent to reflect that these sites may be very likely to
increase in size and perhaps density in years to come.
Using these numbers each grave would entail an area of approximately 5 m2 for
traditional cemeteries and from 6.3 to 23 m2 for the green sites.
It was noted above that the similarities between cemeteries and landfills are limited.
Certainly for most waste operations which we might consider landfills, the waste material
would normally be much more closely packed together with perhaps a shallow cover of
soil. For cemeteries this is clearly different; the bodies represent a very small proportion
of the total site volume and are distributed approximately evenly with significant
quantities of soil between them.
2.1.5 Embalming
The use of embalming in England and Wales is normally restricted to work intended to
provide cosmetic enhancement until burial or cremation and to inhibit decay until after
burial. Some also suggest that the process provides a disinfection of the body and
certainly there is some evidence of a decrease in numbers of cultivable bacteria in
formaldehyde treated bodies (Burke and Sheffner, 1976).
In essence, the process involves the injection of embalming fluid which is a solution of
formaldehyde into the blood vessels and abdomen. Other components of the fluid may
include surfactants to improve replacement of the original body fluid, antioxidants,
buffers, and pinkish dyes such as eosin or erythrosine (Mayer, 2000). However, these
components are normally in low concentration. The overall effect generates an improved
appearance by filling out the face and tissues and giving a more lifelike colour to the skin.
For example for a cemetery with 2,000 burials per hectare:
Interred mass = 2,000 x ( body mass 70kg + coffin mass 15kg)
170 tonnes
Interred volume = 2,000 x (coffin volume 2.1m(l) x 0.75m(w) x 0.4m(h))
1,260 cubic metres
(note this is quite a wide coffin, many may be significantly smaller)
By contrast:
Soil volume = (10,000m2 x 1.8m) – 1,260m3
16,740 cubic metres
Soil mass = 23,436 tonnes (assuming soil density of 1.4t.m-3)
That is, the graves represent less than 1% of the site mass and about 7% of the site
volume down to 1.8m depth.
Science Report Potential groundwater pollutants from cemeteries 11
The frequency of embalming is unclear, in the previous report it was noted that
embalming may be practiced on approximately 50% of bodies though others suggest
75% of bodies (Personal communication). The decision to embalm is often at the
discretion of the individual funeral director and may be more common where bodies are
to be viewed before burial or cremation. Indeed, it may be that in some instances the
decision of whether or not to embalm is tacit within the question of whether the body is to
be viewed.
2.1.6 Coffins and other non-body contents of the grave
The options for containing the body at burial range vary widely from simple shrouds or
even army surplus body bags to grand caskets of pine or hardwoods. Coffins and
shrouds may therefore be composed of less rapidly degraded materials than the corpses
which they enclose. Nevertheless, in modern burial practice most burials probably
involve chipboard and medium density fibreboard (MDF) coffins which may begin to
disintegrate rapidly in the ground compared with solid wooden boxes. Decay and
collapse of chipboard coffins is reported to be evident within one month of burial,
compared with 15 to 20 years in the case of pine or over 60 years for elm boxes, whilst
cardboard coffins are reported to collapse onto the cadaver almost immediately on
infilling the grave.
The use of MDF and chipboard as construction materials brings with it another source of
formaldehyde into the grave since these materials are themselves produced from
sawdust and wood fragments bonded with urea-formaldehyde resin or occasionally the
more expensive phenol-formaldehyde resin. Urea-formaldehyde resins are prepared as
colloids with a solids content of 65% and common usage levels may approximate to 8%
resin to wood fibre (Groom et al 1999). The environmental concerns around
formaldehyde in MDF are normally centred on off-gassing and inhalation in indoor air.
Hence environmental reports mostly consider air quality above a board, however, free
formaldehyde in MDF sawdust has been observed at approximately 350 micrograms per
gram (Leungprasert and Otten). Thus for a 15kg coffin this would imply 5.25g of free
formaldehyde. Note that the assumption of a 15kg coffin is an increase from the
previous Agency report. This comes from consideration of the properties (Wood Panel
Industries Federation, 2003) of the wood products used (Wood Panel Industries
Federation, 2002) and assumptions on the size and shape of coffins. Clearly this figure
will vary depending on the precise details of individual burials.
There is also the potential for metal and other objects to be interred in the grave; either
as worn jewellery or even grave goods. Moreover, a proportion of the population may be
expected to be interred with medical items such as orthopaedic implants or structures.
2.2 Overview of body decay
Previous environmental reports have often tended to consider the buried human corpse
as a largely elemental mass of potentially polluting substances. Inclusion of the
elemental composition (Table 2.2) (Forbes, 1987) in the previous Agency report further
emphasised this with the omission of the Oxygen data in the first edition of that report.
Science Report Potential groundwater pollutants from cemeteries
Table 2.2 Elemental composition of a human body based on a standard or
reference man of 70kg body weight
Element Mass (g)
Oxygen 43000
Carbon 16000
Hydrogen 7000
Nitrogen 1800
Calcium 1100
Phosphorus 500
Sulfur 140
Potassium 140
Sodium 100
Chlorine 95
Magnesium 19
Iron 4.2
Copper 0.07
Lead 0.12
Cadmium 0.05
Nickel 0.01
Uranium 0.00009
Total body mass 70000
However, this is plainly a simplification of the nature and state of these elements as they
are largely incorporated into organic compounds such as proteins, fats, bone etc. which
in turn will have a major influence on their degradation and decay. Table 2.3 shows a
summary of the structural aspects of a human body.
Table 2.3 Structural composition of a human body based on a standard or
reference man of 70kg body weight.
Tissue Mass (g)
Total body mass 70000
Skeletal muscle 28000
Adipose tissue 15000
Bone 5000
Cartilage 1100
Periarticular tissue 900
Marrow 3000
Skin 4900
Liver 1800
Brain 1400
The processes involved in decomposition of human remains have been extensively
studied is in the field of forensic anthropology. However, the focus is often on techniques
for dating the burial, for example in investigation of crime, rather than in elucidation of
mass transfer of potential pollutants (Mann et al, 1990). Very recently though, the
decomposition processes have been reviewed from the point of view of cemetery
pollution (Dent et al 2004). For our purposes the key to appreciating the potential for
Science Report Potential groundwater pollutants from cemeteries 13
pollution from cemeteries is an understanding of the release and transport of body
constituents into the wider environment. For example, doubtless during decomposition
some of the body will be degraded to gases (Iserson, 1994) which may then escape to
atmosphere, whereas other components may remain as long chain aliphatic compounds
which may be detected in the soil after more than a century (Spongberg and Becks,
2.2.1 Macrofaunal Influence on Decomposition.
In this report we shall concentrate on the microbial degradation of a buried corpse.
Certainly, where present, macrofauna can produce remarkably rapid decomposition as
evidenced by the 5 month skeletonisation of a body found in a heated house living room
(Schroeder et al, 2002). Alas, there is apparently little information available on the non-
microbial soil fauna that might be present at traditional cemetery grave depth, or the
effect they might have on the buried cadaver. This is probably because this is
considered to be well below the normal depth at which plant roots, soil macrofauna, and
mycorhizzal fungi function (Forbes et al, 2003). A study (Rodriguez and Bass,1985) on
unembalmed corpses buried at varying depths demonstrated that the decomposition rate
of the cadavers is highly dependent on the burial depth, environmental temperatures and
level of insect activity. Carrion insect activity including Calliphoridae (blow flies) and
Scarcophagidae (flesh flies) were noted in association with cadavers buried at 30cm
depth, with flies present on the grave surface, and observed burrowing down to the
cadaver through cracks in the soil. Eggs laid by adult flies on the grave surface hatched
to produce immature larvae, which were also observed migrating down to the cadaver to
feed. Beetle activity, principally of Scarabaeidae beetles, appeared to be limited to
above ground cadaver decomposition. However, digging and carrion insect activities
were limited to bodies buried at 30cm depth or above, with no insect activity found at
60cm. A body buried at 120cm was noted to have remained ‘very well preserved’
throughout the 12 months of the experiment.
Where cadaver macrofauna have been observed in shallow burials they are mainly of
necrophagous arthropods, which are insects with sense organs stimulated by organic
putrefaction gases that feed on decaying tissue. Approximately 10 insect families have
been identified as belonging to this group, among which the orders of Diptera (flies) and
Coleoptera (beetles) stand out particularly due to their activity and frequency on human
remains (Campobasso et al, 2001). The blowflies Calliphoridae and Muscidae are able
to colonise a corpse as quickly as 2-3 hours after exposure, with Sarcophagidae
following on, and are principle vectors of degradation because their short life cycle allows
a rapid elevation in numbers shortly after colonisation.
For the remainder of this report we have assumed that the traditional burial depths
examples in Table 2.1 above will be used and therefore that insect activity within the
grave need not concern us further.
2.2.2 Decay of the soft tissues
The processes effecting the degradation and ultimate disintegration of a corpse occur in
a series of stages often described as autolysis, putrefaction, liquefaction and
skeletonisation (Dent et al, 2004). These are indicative only though and should best be
considered as a series of overlapping processes.
Autolysis begins almost immediately after death and includes all manner of processes
that are natural ‘self destruct’ mechanisms (Fiedler and Graw, 2003) within individual
Science Report Potential groundwater pollutants from cemeteries
cells or within the wider body. These rely on the action of liberated enzymes or normal
body flora micro-organisms. Putrefaction normally begins between 48 and 72 hours after
death, although this will vary depending on the prevailing environmental conditions. The
body’s primary soft tissue constituents of proteins, fats and carbohydrates are broken
down by proteolysis, hydrolysis, and oxidation or more likely, fermentation. The
decomposition process continues with liquefaction, in which the tissues, softened during
putrefaction, degrade into a liquid mass. Skeletonisation is considered to be complete
when all of the soft tissue has been removed from the bones, which remain articulated by
2.2.4 Decay of soft tissues – fats and the formation of adipocere
After death, most bodies undergo putrefaction, in which the neutral fats of the
decomposing corpse undergo hydrolysis to fatty acids followed by either hydrogenation,
to form saturated rather than unsaturated fatty acids, or oxidation, yielding hydroxy-fatty
acids. Assuming sufficient water and enzymes are available this will continue until all of
the neutral body fat has been turned into liquefied fatty acids, which may be leached
from the coffin. Two notable alternatives to this are possible under the right conditions;
the dry decomposition referred to as mummification, and conversion of the body fat to a
waxy substance known as adipocere (Fiedler and Graw, 2003).
Adipocere is a grey-white soap like or waxy material known to form as a later post-
mortem change, resulting from the bacterial conversion of body fat into a lipid mixture.
The main constituents of adipocere are the saturated fatty acids (palmitic, stearic, and
myristic acids), with minor components comprising the unsaturated fatty acids (oleic and
palmitoleic acid depending on the extent of adipocere formation), triglycerides, hydroxy-
fatty acids and the salts of fatty acids (Forbes et al, 2003 and Stuart et al, 2000). If the
conditions under which the hydrolysis and hydrogenation of the fatty acids occurs are
right, adipocere will form as a result of the decay process, although the exact nature of
adipocere, and its mechanism of formation has yet to be elucidated. The formation of
fatty acids salts results from the reaction of fatty acids from the putrefaction process with
sodium and potassium present in tissue fluids at neutral or slightly alkaline intracellular
pH. If the body is then interred in soil or water with a high mineral content, cation
exchange process may result in the displacement of sodium and potassium by calcium
and magnesium ions, resulting in the formation of water insoluble soaps of the fatty
The formation of adipocere can occur in various soil types, and may begin as soon as 6
weeks post-mortem, although complete transformation will take many weeks or years
dependent on the burial and environmental conditions present, including temperature,
pH, clothing, and soil type.
2.2.5 Bone
Unsurprisingly, bone (including tooth enamel) is normally the most resilient and longest
lasting component of the body. It is comprised of several types of cells set within an
inorganic calcium and phosphorus matrix to give the bone strength (Van De Graaff and
Kent, 1998). In addition there is collagen, a structural protein. The relative proportions
of each vary within and between bones dependent on the position within the bone
structure or indeed the body. Overall, the bone mass may be considered as made up as
60% – 65% calcium hydroxyapatite and 35% protein (mostly collagen). The empirical
structure for hydroxyapatite is:
Science Report Potential groundwater pollutants from cemeteries 15
Bone dissolution is a slow process and hence the “time to skeleton” is a term used to
measure the degradation of all those other body components mentioned above.
Nevertheless the components of bone will slowly decompose; the protein content, mainly
collagen, is subject to proteolytic attack in the normal ways and loss of collagen would
normally render the remaining bone more brittle. Dissolution of the hydroxyapatite will
come primarily from acid attack of the structure and replacement of the calcium with
hydrogen ions. As such the rate will be dependent on the acidity of the surroundings and
skeletal material may be expected to show faster dissolution in acid soils than similar
material in neutral soils.
2.2.6 Factors Affecting Rate of Decomposition
Decomposition in the end relies on the rate of activity of degrading organisms and on the
rates of the (bio)chemical reactions involved. Hence intrinsic and empirical factors which
are seen to influence degradation rate include:
Age at death – decompositions occurs more slowly in newborn babies
Body mass index – decomposition may occur more rapidly in obese corpses
Cause of death – early and rapid onset of putrefaction tends to occur in people who
suffered wasting diseases, those suffering septic infections, and those suffering death
by asphyxia
Integrity of the corpse – any unhealed wounds or abrasions provide additional access
for soil bacteria
Burial depth – where shallow enough to allow macrofaunal attack
Principal among the site related factors are (Santarsiero et al, 2000):
Geological and hydrogeological characteristics of the soil, including soil type,
permeability and porosity.
Microbiological characteristics of the soil
Mechanical, structural, and resistance parameters of the soil,
Coffin or other container construction used
Land cover - land cover and topography will affect infiltration and water-logging will
retard decomposition.
Depth of the unsaturated zone – as well as acting as a barrier to contamination of an
underlying aquifer, this can also present a means for infiltration of oxygen that may aid
the decomposition process.
The interaction of these various factors can be complex, and is the subject of much study
in forensics in the determination of post-mortem interval. In general it is therefore difficult
to give a precise estimate of the length of time decomposition of the body would be
expected to take. However, unless interred in preservative environments, such as those
that would promote mummification (Polson et al,1985 and Janaway, 1997)
skeletonisation of the body would usually be expected to be complete within an interval
of approximately 10 years for burial in soil (Santarsiero et al, 2000) or 30 years for
entombment and this would normally be expected to apply to at least 80% of cemetery
Science Report Potential groundwater pollutants from cemeteries
2.3 Environmental change in the vicinity of the grave
The decay processes are noted to bring temporary increases in temperature above the
ambient ground temperature, though this increase is more pronounced where
macrofaunal decay is seen. Nevertheless, a corpse showing only microbial decay
exhibited a mean temperature increase of 3.4oC over the surrounding soil for a period of
about 5 weeks and beginning about 4 weeks after burial (Rodriguez and Bass, 1985).
This may well reflect the complete consumption of the readily available electron
acceptors such as oxygen and nitrate and hence a time period after which the decay
process proceeds at a slower rate.
The decay also appears to effect an increase in soil pH around or below the body
(Rodriguez and Bass,1985 and Reed,1958) ,with an increase of 2.1 units recorded.
Though the magnitude of this effect will depend in part on the buffering capacity of the
soil, from a pollution prevention view it may retard the movement of metals out of the
Science Report Potential groundwater pollutants from cemeteries 17
3. Potential groundwater pollutants
from human burials
3.1 Potential pollutants
In the following pages we review the potential components of human bodies that may
bring a pollutant risk to groundwater and derive likely loadings in the grave. We have
also considered the processes that can contribute to their attenuation in the subsequent
chapter. For some substances, such as ammonia, readers should also note that
additional Environment Agency guidance on subsurface attenuation already exists (Buss
et al, 2003).
3.2 Mass transfer out of the grave
Mass transfer of the end products of body degradation will occur in 2 main directions; up
and down. Volatile gaseous products such as carbon dioxide, methane, ammonia,
putrescine etc. will migrate towards the surface both by diffusion and advection. Soluble
and suspended components such as ammonium and micro-organisms will migrate down
through the subsurface entrained with recharge. Some lateral diffusion and dispersion
may also occur. Under normal circumstances the convection of soil gases may be
expected to provide relatively little gas exchange compared to diffusive transport (Jury et
al, 1991) although if the body temperature is elevated above that of the surrounding soil
this may change.
Unfortunately we have found no reports that quantify the extent to which gaseous and
soluble or colloidal products are formed from a human body.
3.3 Ammoniacal nitrogen
The previous Agency report focussed heavily on the potential of ammoniacal nitrogen to
move into the groundwater. Though understandable, this focus did affect presentation of
the data and led others to state incorrectly that Nitrogen is the second most abundant
element in the body; compare this with Table 2.2. Note also that this Nitrogen will mainly
be present as fixed Nitrogen in reduced -NH2 substituents of biological molecules such
as proteins and peptides.
3.3.1 Ammoniacal loading in the grave
Table 2.2 shows that the example human body of 70kg contains 1.8kg of Nitrogen. One
can also see from the section on coffins above that urea-formaldehyde resin might also
contribute fixed nitrogen and that approximately 500g could come from this source
(based on the molecular structure and mass of urea).
However, this ammoniacal content is not present as free ammonia nor as ammonium
ions in solution; rather, and for both the biological and resin derived terms, it is present
as a substituent of complex macromolecules which must degrade or be degraded in
order for ammonium ions to be released. Furthermore, some of the proteins such as
Science Report Potential groundwater pollutants from cemeteries
collagen and keratin will be present in structures noted for their resilience including bone,
cartilage, ligaments etc. Collagen, for example, is estimated to account for 35% of bone
dry mass and perhaps 50% for cartillage. Such proteins then will likely be amongst the
last degraded in the body both by virtue of their intrinsic secondary and tertiary structure,
and their shielded position deep within the body and bone. Based on the body
compositions above in Table 2.2 and the empirical structure of collagen (C244H385N77O72)
(Kramer et al, 1999)) this suggests about 470g of nitrogen will remain when the process
of skeletonisation is complete (with about 1250g of Carbon). Also, for the more
degradable proteins present in the major organs and skeletal muscle their
bioaccessibility to saprophytic micro-organisms may be less than ideal. For such
organisms ingress into, and progress through, the body may be slow and as such the
degradation rate may more likely be related to the accessible surface or volume rather
than the “lump” concentration of protein or body in the ground.
The degradation of proteins and peptides, when it occurs, is likely to result in the release
of amino-acids which may then enter anabolism for the degradative organism or more
likely undergo deamination and fermentation. The characteristic death odour
compounds of putrescine (NH2(CH2)5NH2 1,4-diaminobutane or butanediamine) and
cadaverine (NH2(CH2)5NH2) arise from the decarboxylation of amino-acids containing an
amine side group. These compounds undoubtedly account for a proportion of the
Nitrogen released from a body but that may be a small proportion and, in any event, we
have not found any reports that provide quantification.
3.4 Formaldehyde
3.4.1 Chemistry and action
Formaldehyde (HCHO, CAS: 50-00-0) is the simplest aldehyde and has a profound
biological effect in alkylating the amino or sulfhydryl side chains of amino acids. It may
thus destroy the nature, shape and activity of a wide range of proteins and inhibit amino
acid and protein biosynthesis. It can similarly alkylate the ring Nitrogen atoms of purine
and pyrimidine bases, constituents of nucleic acids.
Formaldehyde is highly soluble (solubility limit @550 g l-1) and reactive. It has a distinct
odour and the Henry's Law constant of 3.27x10-7 atm.m3 mol-1 and formaldehyde vapour
released to the atmosphere will photodegrade in sunlight in a few hours (Public Health
Service, U.S. Department of Health and Human Services, 1999).
Formaldehyde is an important industrial chemical with a wide range of uses in particular
as a feed stock to make other chemicals including resin glues. Hence it has been found
in wastewater from manufacturing and petrochemical plants (for example see: Sharma et
al 1994 and International Agency for Research on Cancer, 1982). In general,
formaldehyde has been considered an environmental risk to humans via inhalation since
the opportunities for environmental exposure through direct ingestion are rare.
3.4.2 Formaldehyde loading in the grave
As noted above there are two potential sources of formaldehyde in the grave, embalming
fluid and coffin manufacture. The loading from embalming was discussed in our earlier
report and can be summarised thus: 9 litres of 2% formalin solution provide 180g of
formaldehyde per body.
Science Report Potential groundwater pollutants from cemeteries 19
Urea formaldehyde resin used in pressed wood product manufacture is itself the product
of condensation reactions of methyloureas and, as such, is susceptible to the reverse
hydrolysis reactions (Conner, 1996) such as might be anticipated over the period of
disintegration of the coffin. Resins are typically made using molar ratio of
1:1.1:urea:formaldehyde; the resin is transported as a 65% (w/v) colloid and used in the
MDF and particleboard process at 10%(w/w) (Conner, 1996). Biological degradation of
the urea-formaldehyde resin will also tend to be via hydrolysis to yield the biologically
useful components urea and formaldehyde (see Glancer-Soljan et al, 2001 for example).
It is assumed that both abiotic and biotic degradation of the resin will therefore yield
formaldehyde. For a 15kg coffin then:
15kg coffin of which 1,500g resin
Mass ratio urea:formaldehyde::60:30
Hence 500g formaldehyde per coffin
The release period for this formaldehyde is uncertain and we have assumed that in
general it will be released by degradation of the coffin in the same time as decay of the
body soft tissues.
3.4.3 Degradation of formaldehyde
Formaldehyde is readily degraded by biological systems as long as the concentration is
not so high as to be completely toxic to the degrading organism. Indeed, it is a
component of central metabolism, particularly for organisms growing on C1 compounds.
In the environment plants (Schaeffner et al 2002), animals, fungi and bacteria (Adroer et
al, 1990) all exhibit formaldehyde degradation mechanisms. Recent isolation (Iwahara et
al, 2002) has shown that some soil fungi are able to degrade formaldehyde at
concentrations similar to that used in embalming fluid (i.e. 2% v/v) though it is unclear
how geographically widespread this ability may be. It is also clear that, whilst aerobic
conditions may provide the potential for more rapid bacterial degradation of
formaldehyde, anaerobic degradation can occur (Omil et al, 1999).
There is little literature on observed rates of formaldehyde degradation in cemetery soil
or groundwater. However, high efficiencies of formaldehyde removal (>>99%) from
wastewaters have been reported under both aerobic and anaerobic conditions (Garrido
et al, 2000). This would suggest that under grave conditions, where the availability of
other macro- and micro- nutrients is likely to be good, high efficiencies and rates of
formaldehyde degradation may also be expected.
3.4.4 Urea formaldehyde resins
Urea formaldehyde resins are formed in a two step process involving addition of
formaldehyde and urea to form methyloureas followed by condensation of these into low
molecular weight polymers.
Urea Formaldehyde Monomethylol urea
Science Report Potential groundwater pollutants from cemeteries
Interestingly, similar condensation products are used as slow release fertilisers for a
variety of applications, not least in bioremediation of hydrocarbon spills. They provide a
longer lasting source of fixed nitrogen and are known to be accessible to soil bacteria.
Enzymatic mechanisms for the reactions involved have recently been described (Jahns
et al, 2003). Equally, the condensation reaction used in manufacture is assisted by acid
catalysts which become trapped with the resin in the wood product. Rewetting of the
material causes reactivation of the catalyst and promotes the reverse hydrolytic reaction
to produce formaldehyde and urea (Conner,1996)..
3.5 Mercury
Mercury is considered here for completeness and in view of the likely increase in burial
content of this metal in the coming years. The main potential source for Mercury in
burials will be as amalgam in dental fillings.
The potential for atmospheric pollution with Mercury following cremation has long been
considered and was recently the subject of a consultation by Defra (Defra (2003)) based
on the need to abate release of dangerous substances under the OSPAR agreement.
Mercury is a metal which, in some forms, can be highly toxic to all orders of life.
Awareness of the human health impacts of mercury have led many countries to ever
increasing controls on its use and disposal. Moreover, the toxicology of Mercury and its
compounds has been recently reviewed (Environment Agency 2002).
The pollution and health risks from dissolution of mercury amalgams in dental fillings has
been a source of some controversy in recent years. Of particular interest has been the
control of wastewaters from dental practices (see for example Kunkel et al 1996) and
there are many reports of the slow release of mercury to intra-oral vapour and a few of
release into saliva solution (Leistevuo et al, 2002). The breakdown of dental amalgam
during life is caused by mechanical abrasion and (bio)chemical processes. These
contribute to a low level of mercury present in the body beyond the teeth and which is
normally excreted during life in the normal way. After death the mechanical abrasion
from mastication processes cease and thereafter there will be slow (electro)chemical
decomposition of the amalgam and dissolution into any surrounding aqueous phase.
3.5.1 Mercury loading in the grave
The composition of dental mercury amalgam fillings has varied over time and it is not
possible here to consider all recipes. A standard for the powder mix was published in
1978 (International Standards Organisation) and it is assumed that liquid mercury is
added to the solids mix in the ration of 1:1. Defra have estimated an average mercury
loading of 3g per body (Defra, 2003) though clearly this will vary between individuals.
Defra also noted that the amount of mercury released from crematoria is predicted to
increase by about two-thirds from 2000 to 2020 based on dental records and actuarial
data followed by a decrease back to 2000 emission levels around 2055.
There are no data on the release of mercury from dental fillings post mortem. However,
recently the release of mercury from dental amalgams into a flowing stream has been
studied (Okabe et al, 2003) which may be the closest approximation available to a
conservative approach for amalgam dissolution in the grave. The work observed that
dissolution is related to amalgam composition and solution pH. Over the 30 day leaching
Science Report Potential groundwater pollutants from cemeteries 21
experiments high initial leach rates fell rapidly and reached a steady state after a few
days. Mercury leaching was enhanced by low pH and was also dependent on the
formulation of amalgam used. Rates of mercury dissolution were approximately 0.03
micrograms per cm2 surface per hour. This allows some calculation of the Mercury loss
to the environment if a number of conservative assumptions about conditions and filling
sizes are made.
Mass of mercury per body = 3g (from above)
Density of mercury = (O'Neil et al, 2001).
Hence equivalent volume of Mercury = 0.2ml at s.t.p
Assume amalgam Mercury content = 50% v/v
Assume filling per body = 5 equal size
Hence volume per filling = ( 0.2ml x 2 ) / 5 = 0.08ml
Assume filling shape is spherical then volume of a sphere is given by
Hence rearranging and solving for sphere radius = = 0.26cm
And sphere surface area = 4 x
x (0.26)2 = 0.85 cm2
Mercury dissolution rate = 0.03 micrograms per cm2 surface per hour
Mercury grave dissolution rate = 0.03 x 0.85 x 5 x 8760 = 1.12 milligrams body-1 year –1.
3.6 Other metals
Depending on personal circumstance bodies at death may contain a variety of other
metals mostly of medical or jewellery origin. Apart from those present as biological
material (for example in the active site of many enzymes) the most obvious may be gold
in tooth fillings; however, a great many orthopaedic and other items contain high quality,
non-ferrous metals such as silver, platinum, palladium, cobalt etc. One estimate
suggests that UK cremations involve approximately 1,350 kg non-ferrous metals and
22,500 kg of orthopaedic residues each year (De Wit, 2002). Simple extrapolation would
suggest that burials therefore account for approximately 340 kg and 5,600 kg of each,
respectively. Thus a cemetery containing 1,000 burials may contain about 4kg of such
metals, on average.
Metal contamination around cemeteries is little studied, one case in the United States
(Spongberg and Becks, 2000) showed little elevation of soil metal concentrations except
for Arsenic which reached 8mg kg-1 presumably from 19th century embalming practices.
Science Report Potential groundwater pollutants from cemeteries
3.7 Pathogens
The issue of release of pathogens or potential pathogens from decomposing bodies is
often raised in consideration of cemetery developments. This concern most frequently
has centred around the possible transport of faecal organisms into nearby water bodies
including groundwater and indeed this was the principal burden of the Cemetery Clauses
Act 1847. In principle then it is possible to conceive of three scenarios for pathogen
escape from a buried corpse:
release of normal body flora, for example faecal organisms from the gut or skin or
mucosal membranes, which may then become opportunistic pathogens
release of existing pathogens from infections present at the time of death
release of pathogens which invade the body after burial.
Potential pathogens would include:
multicellular eukaryotic organisms e.g. worms
unicellular eukaryotic organisms and their resting stages e.g. Giardia, Cryptosporidium
bacteria, fungi and their spores
In 1998 the Agency completed a review of microbial contaminants in groundwater
(Environment Agency, 1998) which highlighted the lack of basic data on this topic and
there remain few studies on the microbial and pathogen circumstances around
For those organisms or agents which are explicit pathogens present as infections at the
time of death it is likely that after death the body becomes a relatively hostile
environment. The loss of body processes such as circulation and thermoregulation will
have profound effects on a pathogens own life and it seems likely that for most
organisms as a minimum the generation of new pathogens will cease shortly thereafter.
Certainly this will be the case for viruses which of course are incapable of replication
without a living host cell. There will also be the potential injection of toxic formaldehyde,
the bodies own cellular autolysis and attack from degradative organisms to contend with.
However, some organisms may potentially enter more hardy life cycle phases such are
spores or cysts. In summary it seems likely that the potential loading of explicit
pathogens will be limited to no more than the maximal loading at the time of death.
For organisms present as normal body flora the situation may be more complex. Many
organisms which inhabit the human body without harm may also become pathogens if
circumstances permit. Such opportunistic pathogens would include many species in the
gut, on the mucosa and skin. Such normal bacterial flora does flourish for a short period
after death as the control mechanisms maintained during life are lost and increases in
cultivable cell numbers of a few tenfold have been reported (Rose and Hackett, 1971).
In contrast, the practice of embalming may decrease the numbers of organisms present;
formaldehyde or formalin products are used in other countries to sanitise sewage sludge
before spreading (Godfree et al, 1983) but the comparison to embalmed bodies is
Science Report Potential groundwater pollutants from cemeteries 23
The movement of pathogens once in the groundwater may be rapid and in borehole
tracing experiments viruses for example are commonly observed to travel well in
advance of conservative tracers such as fluoroscein and rhodamine.
3.7.1 Pathogen loading in the grave
For organisms which are unable to replicate without a host the numbers at death
therefore represent a maximum grave loading. This would include human viruses and
most, if not all, eukaryotes. Hence only bacteria present a realistic threat of increasing
numbers post interment.
To date most concern about pathogen transport from burial sites has centred on the
traditional water quality parameters of enteric bacterial pathogens. For such enteric
organisms it is possible to consider the likely initial loading present in individuals for
whom the cause of death was something other than an enteric infection. The populations
of many bacteria and viruses in human faeces are around 106 per gram (Dahi,1990).
However, the dominant gut flora organisms such as Escherichia coli may be anticipated
at several log-fold more than this perhaps 109 per gram or more. These concentrations
may be multiplied by a few hundreds of grams of faecal material and gut contents that
may be anticipated in the body suggesting between 1011 and 1012 organisms.
Protozoan enteric pathogens such as Cryptosporidium and Giardia may also be present
in faeces though typically at lower concentrations perhaps 104 or 105 per gram.
Similarly, any multicellular parasites such as roundworms or flukes would be present at
even lower concentrations of perhaps 102 or 103 per gram faeces giving possible total
loadings of 104 or 105. These larger, more complex organisms may also present less of
a risk than the bacteria since their size may make transport through the subsurface more
difficult. Figure 3.1 shows a comparison of organism size and pore or fracture size in
geological formations.
Figure 3.1 Comparison of sizes of organisms and subsurface pores
Science Report Potential groundwater pollutants from cemeteries
For pathogens which invade the body after death or indeed for indigenous organisms
which actively degrade the body after death and which may then become opportunistic
pathogens the situation is even less clear. There is some evidence of the increase of
skin and mucosal flora post mortem (Burke and Sheffner, 1976) and this certainly seems
reasonable. The investigation of a cemetery in Wolverhampton showed an interesting
detection of Staphylococcus aureus in boreholes for which it is difficult to conceive of any
other environmental source (Trick et al, 2002). Initial loadings of such organisms may
be relatively modest by comparison with Escherichia coli for example, but if indeed they
contribute to decomposition then increases in cell numbers may be rapid and substantial.
With a distribution across the nasal and external surfaces of the body and the capacity
for aerobic, anaerobic and fermentative metabolism such organisms are well placed to
exploit the body.
Many soil bacteria which may play a part in decomposition are opportunistic pathogens,
Clostridium and Bacillus spp. in particular also provide the ability to enter a non-
vegetative phase which may both enhance longevity and transport characteristics.
However, there are no reports that quantify the concentrations of such organisms in the
3.8 Phosphorus and Calcium
3.8.1 Loading in the grave
The loading of these elements is given above in the section on body and bone
composition and it is clear that the bone accounts for the vast majority of both Calcium
(approximately 1100g) and Phosphorus (approximately 500g) in the body. Clearly there
are other physiological uses for these elements: Phosphorus in energy metabolism for
example and Calcium in signalling. Nevertheless the amounts used are insignificant for
our purposes in comparison with the bone mass.
The previous Agency (Environment Agency,1999) report assumed that Phosphorus
release from the body would occur in parallel with the release of soft tissue components.
However this would imply that the bone dissolution would be complete at the end of the
10 year period which is otherwise given as the “time to skeleton” period, which is clearly
inconsistent. This time to skeleton is a reasonable approximation in line with current
estimates (Iserson, 1994), however the time taken for the decomposition of the skeleton
itself will vary greatly depending in particular on the recharge conditions (i.e. how much
water flows over the remains) and on the pH of the grave.
Science Report Potential groundwater pollutants from cemeteries 25
4. Natural attenuation processes
for potential grave pollutants
4.1 Biodegradative routes and the availability of
terminal electron acceptors in the grave
The initial in-grave decomposition conditions are usually aerobic as a consequence of
the burial process. However, it is obvious that with the presence of a relatively large
degradable organic mass such as a body the available oxygen will be rapidly depleted
within the corpse itself. Moreover, the resupply of oxygen will be relatively slow due to
diffusion of soil gas from the atmosphere above or the soil surrounding the body or
carried by recharge. The grave model described by Dent et al (2004), suggests that
approximately 5 moles of gaseous molecular oxygen is initially available for aerobic
processes. In contrast the body carbon content of Table 2.2 above (16kg) implies that
perhaps 1,300 to 1,500 moles of molecular oxygen would be needed for complete
aerobic mineralisation of the organic carbon to carbon dioxide. Clearly then the oxygen
that is immediately available is insufficient and the body will rapidly become anaerobic.
Subsequent supply of oxygen will then depend on the availability of dissolved oxygen in
recharge, on diffusion of gaseous oxygen from the surface and laterally from the
surrounding soil. These processes will be subject to many, often competing, site-specific
factors. The amount of oxygen in recharge may be calculated assuming that the body
receives infiltration only from directly above and that oxygen is present at the normal
saturation level of 8 mg l-1. Hence even for an area with high recharge of 500mm,
for a grave area of 2.1m x 0.75m = 1.58 m2
with recharge of 500mm.yr-1
this implies a volume of 790 litres containing 8 mg l-1 Oxygen
that is, 6.3 g of Oxygen per year, only about one-fifth of a mole.
The diffusion of Oxygen from the surface or surrounding soil will be subject to Fick's Law
(Domenico and Schwartz, 1990) and may be highly site specific depending on both the
geological setting of the grave and the construction, compaction and cover of the grave
and surrounding soil. However, it is worth note that the diffusion rate will be affected
greatly by the water content of the soil and for high water content and indeed below the
water table the rate of oxygen supply will be greatly decreased.
Many of the commonly utilised alternative electron acceptors are likely to be present only
in very low initial concentrations in the grave. As discussed above, most of the nitrogen
present in the tissues will already be reduced as NH2 substituents. Similarly, though
sufur is a common component of organic molecules such as proteins this is normally as
sulfhydryl -SH side groups. For metals such as iron and manganese, these are present
in significantly lower quantities and again are likely to be present as already reduced
Science Report Potential groundwater pollutants from cemeteries
species. As soluble species likely to be present to some concentration in the overlying
soil both nitrate and sulfate may be expected to be carried to the body with recharge.
Site specific soil data may be available to assess the extent to which these electron
acceptors are present. However, for nitrate at least it seems unlikely that quantities
capable of promoting the anaerobic degradation of more than a few moles of carbon
would be present.
As a consequence of this model, two issues are apparent:
the body itself rapidly reaches an anaerobic state
the (re)supply of these common terminal electron acceptors may then occur at a
constant rate through diffusion and recharge
this implies a constant rate of electron transport dependent degradation rather
than first-order kinetics with rate dependent on organic concentration.
The remaining biodegradation possibilities rest on fermentation and methanogenesis.
Fermentation is the substrate level energy metabolism of organic substances and
typically results in the production of organic acids such as acetate, lactate and butyrate.
Fermentation of proteins and peptides will also produce amino acids which may then be
incorporated into cell carbon or deaminated to produce more organic acids (and
ammonia). Methane and carbon dioxide gases are produced as the end products from
methanogenesis and as gases may be quite mobile in the subsurface.
4.2 Decay and dissolution model
The previous Agency (Environment Agency, 1999) report proposed a first order “half-life”
approach to estimation of the pollutant flow for most of the components of the human
body. It was assumed that for the carbon content of the body approximately 25% of this
was not degraded within the time to skeleton but that all other components show a first
order decay based on the total amount present in the body.
We propose a number of changes to this model based on the discussions above of
contents and degradation paths whilst retaining other features such as decay timings,
hence we suggest:
skeletonisation of a buried corpse is assumed to take 10 years to complete.
though embalming with formaldehyde may retard the decay to some degree,
quantifiable effects data are not available and in view of the long timescales involved
(10 years) rates of decay for embalmed and unembalmed bodies are assumed to be
the same.
the previous Agency report suggested that “green” burials may provide relatively rapid
aerobic decay based on an assumed burial depth of 1.3m. However, this is still below
the maximum observed depth for macrofauna-mediated decomposition and we
suggest that decay rates for “green” and conventional burial sites should be assumed
to be the same.
temperature increase in the body is short duration and there is therefore no thermal
convection driver for soil gas mass transfer.
not all components will be readily degraded or solubilised during the skeletonisation
process. In particular,
phosphorus (phosphate) will be present overwhelmingly as hydroxyapatite in
bone and will mainly become accessible after the skeletonisation. Hence
Science Report Potential groundwater pollutants from cemeteries 27
phosphate dissolution will begin after 10 years of interment and will proceed with
bone dissolution.
calcium - as for phosphate
collagen content of the bones will also be unavailable until skeletonisation has
occurred. This will bring a further late phase of carbon and nitrogen loss
amounting to about 400g of the body nitrogen.
Mercury dissolution rates were calculated above and these should be used rather than
assume a half-life. This is an approximation with many uncertainties such as surface
access since as dissolution proceeds the contact surface area is likely to shrink thus
altering the dissolution rate.
The time for complete disappearance of the body including skeleton is unclear and
rather variable. Some cemeteries place time limits on the ownership of grave sites and
may reuse or move graves thereafter. For simplicity we have assumed below that this
“time to dust or removal” is 100 years but this is a somewhat arbitrary choice and
readers may wish to choose a different value.
Degradation of tissues based on aerobic respiration will be limited by oxygen
availability. This will be controlled by supply via dissolved oxygen in recharge or
gaseous diffusion. Both of these may be expected to be constant rates related to
depth, grave oxygen partial pressure, or recharge rate once the initial grave oxygen
content has been exhausted.
Degradation of tissues based on anaerobic respiration will be limited by availability of
electron acceptors. This will be controlled by dissolved supply via recharge and may
Advection and diffusion upwards
of gases CO2, CH4, N2, putrescine
Diffusion downwards
of O2
Recharge supply of
O2, NO3 and SO4
Diffusion of O2
Diffusion of CO2, CH4,
N2, putrescine etc
Aerobic degradation
Anaerobic degradation
Grave cut
Grave cut
Dissolved plume
Ground level
Figure 4.1 Transport of electron acceptors and degradation products
into and out of the grave
Science Report Potential groundwater pollutants from cemeteries
be expected to be provided at a constant rate.
Degradation of tissues based on fermentation will be limited by microbial access to
tissue surfaces and ability to force entry into compact or protected tissues such as
dense muscle, marrow etc. A suitable rate profile for such a complex problem is
unclear however, it is clear that the above factors are not related to the simple “lump”
concentration of organic material. We therefore propose a linear degradation rate for
this process.
Overall we therefore propose a constant linear rate for degradation of the body with
delays for those components that are known to be resistant or shielded in some way.
These considerations are summarised in a decay rate and timings table (Table 4.1
Table 4.1 Contaminant decay rates and timings
Contaminant Mass per
burial (g)
mass for
release (g)
start year
end year
Release rate
per burial
(g y-1)
Calcium 1100 1100 10 100 Zero-order 12.22
10 Zero-order 2480
Carbon 1200b1200b10 20 Zero-order 120
Zero-order 190
Nitrogen 400 400 10 20 Zero-order 40
Mercury 3 3 0 2600 Zero-order 1.12 x 10-3
Phosphorus 500 500 10 100 Zero-order 5.55
Formaldehyde 180 180 0 0.25
As a single
event NA
Formaldehyde 500d500d0 10 Zero-orderd50
a assumed from coffin of mass 15kg
b assumes that of the 16,000g body total then 1,200g are present in collagen in bone etc and so degraded after skeletonisation and
completely lost over the subsequent decade
c assumes that of the 1,800g body total then 400g are present in collagen in bone etc and so degraded after skeletonisation and
completely lost over the subsequent decade
d relies on catalytic hydrolysis of resin in situ
Science Report Potential groundwater pollutants from cemeteries 29
5. Risk assessment
The Agency has published widely on the assessment of pollution risks to groundwater. A
variety of tools and techniques are therefore available to assist in the understanding and
management of cemetery developments. The philosophy followed is one of using a
tiered approach common to much environmental risk assessment (DETR (2000)). This
is set out in more relevant detailed fashion in guidance on protection of groundwater
(Environment Agency 1999) and assessment of natural attenuation (Environment
Agency, 2000). We have not repeated the work here and readers should use this
document simply to assist their conceptual model construction and risk assessment.
Science Report Potential groundwater pollutants from cemeteries
6. Discussion
Despite the fact that we have been burying the dead for most, if not all, of our history and
beyond, our knowledge of the post-mortem processes and in particular the gross
distribution, transport and fate of body elements from the grave remains very limited.
This is increasingly important at a time when our existing cemeteries are fast filling up
and applications for new developments may be expected to become frequent. At a burial
rate of approximately 140,000 per year and with 2,000 graves per hectare we need 70
hectares of land every year for burials: about 100 football pitches.
In the absence of contrary quantifiable evidence much of our assessment was forced to
assume that the products of decay remain in the solid or dissolved phases and are not
transformed to gaseous products such as methane or molecular Nitrogen which may
diffuse into the atmosphere. This is undoubtedly a conservative assumption, there are
many processes which will act to bring about mass loss to the atmosphere, for example:
aerobic and anaerobic respiration to liberate carbon dioxide
evolution of reduced nitrogen compounds such as putrescine
reduction of ammonium under alkaline conditions to ammonia and subsequent
nitrification of ammonia to nitrate and then denitrification to nitrogen gas
Unfortunately, a good understanding of the extent and importance of each of these
processes and the rates at which they occur under a range of subsurface conditions is
currently lacking.
6.1 Suggested further work
If we are to improve our understanding of the risks that cemetery developments may
pose then there is a need for solid experimental science to quantify the processes
involved. Though much could be achieved with laboratory and lysimeter studies and
animal models eventually we would doubtless require some field scale evaluation.
Moreover, as the key decay and attenuation processes occur within, close to, or beneath
the body these are the areas that need to be investigated. Clearly this is a sensitive
issue which has meant that very few investigations have been carried out in the past or
the focus has been on crime investigation and forensic pathology rather than basic
understanding of the fate and transport of body elements in bulk.
Certainly it is possible to conceive laboratory and lysimeter experiments that could be
undertaken as PhD or post-doctoral studies in a standard academic frame.
Alternatively the Agency could seek partner organisations who already carry out
research in these areas to establish animal and or human burial research sites.
Science Report Potential groundwater pollutants from cemeteries 31
References & Bibliography
Adroer N., Casas C., de Mas C., Solà C. (1990) Mechanisms of formaldehyde
biodegradation by Pseudomonas putida. Appl. Microbiol. Biotechnol. 33, 217–220.
Agency for Toxic Substances and Disease Registry. Toxicological profile for
formaldehyde. Public Health Service, U.S. Department of Health and Human Services
Anon. (2001). Review of emissions from crematoria in the UK. Resurgam, 44 p81 - 127
Burke, P and Sheffner, A. (1976). The antimicrobial activity of embalming chemicals
and topical disinfectants on the microbial flora of human remains. Health Lab Sci. 13,
p267 – 270.
Buss, S, Herbert, A, Morgan, P and Thornton, S. (2003) Review of ammonium
attenuation in soil and groundwater. Environment Agency ISBN 1 84432 110 1
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List of abbreviations
CAS Chemical Abstracts Service. Maintain a standard reference index of chemicals
Defra Department of Environment, Food and Rural Affairs
DMF Dimethylformamide
FMD Foot and Mouth Disease
MDF Medium density fibreboard, used in coffin construction
pH negative log of the hydrogen ion concentration, a measure of acidity
Science Report Potential groundwater pollutants from cemeteries 35
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... Of the 370000 mgL -1 of formalin concentration, which was placed on dead biological specimens at Point C, only 149.24 to 175.10 mgL -1 were released or leached into the soil. The rest of formaldehyde concentration can be exposed to the atmosphere in gas state and would photodegrade in sunlight only in a few hours (Hart & Casper 2004). Hart and Casper (2004) reported that formaldehyde is highly soluble and reactive. ...
... The rest of formaldehyde concentration can be exposed to the atmosphere in gas state and would photodegrade in sunlight only in a few hours (Hart & Casper 2004). Hart and Casper (2004) reported that formaldehyde is highly soluble and reactive. The solubility limit for formaldehyde is 550000 mgL -1 . ...
... The highest efficiency of formaldehyde removal from wastewater was reported in both aerobic and anaerobic conditions (Garrido et al. 2000). This means that burial area of the dead biological specimen where the availability of macronutrients and micronutrients is good and very high efficiency, then the rates of formaldehyde degradation in soil may be expected to happen (Hart & Casper 2004). ...
Biomedical waste specifically anatomical specimens and body parts will be incinerated by a local incineration facility. However, the incineration of formaldehyde fixed specimen from hospitals poses hazardous effect to human and environment due to an exposure of highly toxic gases such as dioxins and furans. In addition, this practise is considered as non-shariah compliance by Muslim community. Thus, a safer and shariah-compliance option to dispose anatomical specimens through deep burial has been introduced. The concern has been raised on the side effect of the formaldehyde treated specimen to the environment. Formaldehyde is used widely for preservation of surgical and anatomical specimens. The formaldehyde toxicity specifically on the soil, soil water, soil animals and plants should be considered after the burial of the anotamical specimens. Thus, the aim of this study was to investigate the side effect of formaldehyde on soil after the burial of formalin fixed specimen on the environment. In this study, the amount of soil elemental distribution and formaldehyde concentration of pre-burial and post-burial of biological specimen were evaluated by using Energy Dispersive X-Ray Fluorescence (EDXRF) and Ultraviolet-Visible Spectrophotometer instrument, respectively. For EDXRF analysis at Point C, soil elemental distribution after burial of dead biological specimens has higher concentration compared to before the burial. The concentration of formaldehyde at Point C was higher after the burial of dead biological specimen compared to before burial, which exceeds the tolerable concentration recommended by the World Health Organisation (WHO).
... Groundwater, which is a vital water resource, has been historically reported to have lower pathogen loads than surface water because of the natural purification that occurs during natural adsorption and inactivation processes. The physical characteristics of porous media (i.e., soil geological and hydrogeological properties) play a key role in the dynamics of the pollutants released into the environment (Hart and Casper, 2004;Bivins et al., 2020;Paleologos et al., 2020). Some authors (Craun et al., 2010) have suggested that almost all waterborne disease dispersion is related to polluted groundwater and that pathogens can be transmitted from wastewater to groundwater through septic tanks, leaky sewers, and weak well nets. ...
Full-text available
Although the World Health Organization (WHO) announcement released in early March 2020 stated there is no proven evidence that the COVID-19 virus can survive in drinking water or sewage, there has been some recent evidence that coronaviruses can survive in low-temperature environments and in groundwater for more than a week. Some studies have also found SARS-CoV-2 genetic materials in raw municipal wastewater, which highlights a potential avenue for viral spread. A lack of information about the presence and spread of COVID-19 in the environment may lead to decisions based on local concerns and prevent the integration of the prevalence of SARS-CoV-2 into the global water cycle. Several studies have optimistically assumed that coronavirus has not yet affected water ecosystems, but this assumption may increase the possibility of subsequent global water issues. More studies are needed to provide a comprehensive picture of COVID-19 occurrence and outbreak in aquatic environments and more specifically in water resources. As scientific efforts to report reliable news, conduct rapid and precise research on COVID-19, and advocate for scientists worldwide to overcome this crisis increase, more information is required to assess the extent of the effects of the COVID-19 pandemic on the environment. The goals of this study are to estimate the extent of the environmental effects of the pandemic, as well as identify related knowledge gaps and avenues for future research.
... In addition, the high levels of microbial contamination including total and fecal coliform, fecal streptococcus, heterotrophic bacteria (22°C and 36°C), clostridia and proteolytic bacteria were found in most of the taken groundwater samples from three cemeteries [18]. Apart from all adverse effects of cemeteries on groundwater quality, in a study in 2004, Hart and Casper [19] came to the conclusion that higher burial depth of human corpses can increase the adverse effects of cemeteries on groundwater quality. Therefore, the depth of sampling from wells can be an important factor in the survey of cemetery effects on groundwater quality. ...
... This mode of water contamination is rare and not frequent. Groundwater pollution is mostly attributed to several anthropogenic activities such as irrigation return flow, industrial effluent, high water table in burial grounds and runoff especially in most urban settings of the world [33][34][35][36]. These approaches (hydrochemistry and microbial) have aided the deep understanding and differentiation between rock and water interactions and anthropogenic influences in water systems [37]. ...
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Groundwater samples were collected randomly from hand-dug wells in parts of Ado Ekiti metropolis and were subjected to its quality assessment and characterization. Physicochemical and bacteriological analyses were carried out following standard methods (APHA 2012). Hydrochemistry of the present study revealed relative mean concentration of the cati-ons in the order: Na + > Mg 2+ > Ca 2+ > K + , and that of the anions as Cl − > HCO 3 − > SO 4 2− > NO 3 − , respectively. The microbial test shows that E. coli tested positive in all the samples and their colonies are classified dominantly as satisfactory pollutant free state. Pollution index of groundwater results revealed an insignificant state of pollution of the groundwater. Deduction from the Pipers, Gibbs plots and chloro-alkaline indices results revealed the imprints of natural weathering, ion-exchange processes and anthropogenic activities influencing the groundwater quality. Factor analysis result also confirms the prevailing activities of natural geological forces and municipal contaminations acting on the groundwater. The hydrochemical processes coupled with the permeable nature of the aquifer media and high precipitation will influence groundwater flow and ultimately pose pollution risk to the aquifers and eventually the populace of these areas in years to come.
... The search of cemeteries and graveyards is a sensitive topic, making managing the search particularly important. Consideration of how to search burial grounds is already underway by teams throughout the world, with the United Kingdom as but one example: see (4). The main conflict however is between those who own or manage the land (usually state and church) and thus manage burials, and relatives of victims or the public, who wish to know what is buried where. ...
Burial grounds are commonly surveyed and searched by both police/humanitarian search teams and archaeologists. One aspect of an efficient search is to establish areas free of recent internments to allow the concentration of assets in suspect terrain. While 100% surety in locating remains can never be achieved, the deployment of a red, amber green (RAG) system for assessment has proven invaluable to our surveys. The RAG system is based on a desktop study (including burial ground records), visual inspection (mounding, collapses) and use of geophysics (in this case, ground penetrating radar or GPR) for a multi-proxy assessment that provides search authorities an assessment of the state of inhumations and a level of legal backup for decisions they make on excavation or not (‘exit strategy’). The system is flexible and will be built upon as research continues.
Studies on the impact of cemeteries on groundwater quality were initiated by van Haaren in 1951, and were occasionally undertaken in the 1970s and 1980s in Germany, the United Kingdom, Canada and South Africa. Regular studies only began in the late 1980s and were continued in the 1990s in Brazil, South Africa, Australia and Poland. On a smaller scale, this kind of research was also undertaken in other countries such as the USA, Portugal, and France. An overview of the results of those studies and focuses on the environmental conditions is presented, which according to current research, highlights the hazards associated with the significant chemical contamination of water.
Full-text available
Death to Dust: What Happens to Dead Bodies? provides the answers to the questions about corpses that professionals and layman alike want to, but were afraid to ask: What really does happen to a body after death? What does our culture do with corpses and what have other cultures done? How does a body really turn to dust? What happens during autopsies, dissection, embalming, cremation, and cryogenic preservation? How do we transport bodies and what does a medical examiner really do? How about the more bizarre uses for corpses, such as cannibalism, body snatching, and use in the secret rites of various cultures? In more than 800 pages, this book gives the latest information on organ and tissue donation and the arcane and secretive world of the funeral industry. We rarely speak about death—because it is the pornography of our culture and we know so little about it. This book sheds some light into dark corners of our society and proves that, once again, truth is stranger than fiction.
The disposal of sewage sludge to agricultural land has been accepted as a convenient and cost effective method by the water industry and farming community alike. However, sewage sludge by its nature is not a uniform product varying as a consequence of the compositon of the crude sewage and the methods of treatment. With minor exceptions it contains pathogenic microorganisms and parasites. In these circumstances the chemical disinfection of sewage sludge should be considered. This paper reports laboratory and field trials carried out with a formalin-based compound; DF 955. These trials were conducted using pathogens most likely to be a problem as a result of the agricultural use of sewage sludge, namely salmonellae and Taenia saginata, the beef tapeworm. Similarly the study was carried out in such a way as to simulate the practical use of this compound in order to detect adverse effects upon the soil microflora and vegetation.
This textbook provides an introduction to the study of hydrogeology, and maintains the process oriented approach of the earlier edition. The introduction is followed by chapters on: the origin of porosity and permeability; groundwater movement; equations of flow, boundary conditions and flow nets; groundwater in the basin hydrologic cycle; hydraulic testing; groundwater resources; stress, strain and pore fluids; heat transport in groundwater flow; solute transport; aqueous geochemistry; chemical reactions; colloids and microorganisms; mass transport equations; mass transport in natural groundwater systems and groundwater flow; contaminant hydrology; modelling of dissolved contaminant transport; multiphase fluid systems; remediation; and in situ destruction and risk assesment.
Selected strains of Pseudomonas putida, Pseudomonas cepacia, Trichosporon penicillatum yeast and the mixed culture of these three strains were used for aerobic degradation of formaldehyde and formic acid in the synthetic medium and waste water generated by melamine resins production. It has been shown that the mixed culture in the synthetic medium degrades 1000 mg/L of formaldehyde over 18-24 hours and 500 mg/L of formic acid over 12-18 hours. Aerobic degradation of wastewater from the production of melamine resins with the use of mixed bacterial and yeast culture was achieved in 24 hours with COD reduction of over 90 % and complete degradation of formaldehyde, methanol and butanol. The role of Trichosporon penicillatum yeast in the mixed culture, during aerobic degradation of formaldehyde in the synthetic medium and wastewater, was to form flocculent biomass that is self-precipitating.
This paper reports a study of dog carcass communities near Knoxville, Tennessee. Special emphasis has been given to the insects. The principal portion of the field work was conducted between May 7, 1951, and May 14, 1952. A total of 43 dog carcasses yielded significant information concerning seasonal distribution of carrion insects and seral stages in carcass communities. Carcasses were placed at intervals of about 2 weeks in hot weather and less frequently during cooler weather. The standard procedure was to place carcasses in pairs with respect to date of placement. One member of each pair was placed on the ground in a wooded area and the other was placed in similar manner in a non-wooded (pasture) area; this pairing of carcasses was designed to permit comparison of carcass communities in wooded areas with those in non-wooded areas. Frequency of field trips varied from thrice daily (on certain occasions during the hottest weather) to once in 12 days (during a period of coldest weather). Usually, however, trips were made at intervals of one week or shorter. The type of operations performed upon visiting a carcass varied; important operations frequently included 1) recording physical condition of the carcass, 2) measuring air temperature and temperature under the carcass, 3) measuring pH of soil under the carcass, 4) counting various arthropods seen, or estimating their abundances according to a 5-term scale, and 5) collection of arthropods.
Six strains of fungi that degrade formaldehyde were isolated from the soil. Strain no. 5 degraded formaldehyde concentrations as high as 2.0% within 20 days. Colonial and morphological properties indicated that strain no. 5 belongs to the genus Paecilomyces. This strain proliferated in medium containing 1.5% formaldehyde as the sole carbon source. The upper concentration limit of formaldehyde that permitted fungal growth was 2.4% and strain no. 5 degraded that concentration of formaldehyde completely within 55 days.