The usual process of corruption of the dead body begins at a variable time after death, but in an average temperate cli- mate may be expected to begin at about 3 days in the unre- frigerated corpse.
Even in temperate zones there can be a wide range of ambient temperatures, from below freezing to near blood heat. In the tropics, far higher temperatures are common- place, but in high latitudes or elevations, deep-freeze condi- tions can keep decomposition at bay indefinitely, as in the case of modern discoveries of prehistoric mammoths and medieval Esquimaux. It is therefore futile to attempt to construct a timetable for the stages of decomposition, except to point out salient markers for an undisturbed body in an
‘average’ indoor environment of about 18°C in temperate climates. From this approximate baseline the pathologist must then extrapolate for local variations appropriate to his climatic and geographical conditions.
Sequence of putrefactive changes
Whatever the time scale, the general order of corruption is similar, though the degree of advancement may vary between different areas of even the same corpse.
Usually the first external naked-eye sign is discoloration of the lower abdominal wall, most often in the right iliac fossa where the bacteria-laden caecum lies fairly super- ficially. Direct spread of organisms from the bowel into the tissues of the abdominal wall breaks down haemo- globin into sulphaemoglobin and other pigmented sub- stances. This discoloration spreads progressively over the abdomen, which in the later phase begins to become dis- tended with gas.
FIGURE2.10 Moderately early changes of decomposition, showing gaseous distension of scrotum and abdomen, and skin slippage and blistering in dependent areas. This was after about one week since death, but the changes vary greatly with environmental temperatures.
Putrefaction
At about this time, more generalized spread of bacteria begins to discolour the more moist tissues, which often comprise those dependent areas that show hypostatic col- oration and oedema. The face and neck become reddish, and begin to swell. The putrefactive bacteria, which largely origin- ate in the intestines and lungs, spread most easily in fluid so they tend to colonize the venous system, haemolysing the blood that stains the vessel walls and adjacent tissues. This gives rise to ‘marbling’, a branching outline of arborescent red, then greenish pattern in the skin, seen most clearly on the thighs, sides of the abdomen, and chest and shoulders.
This stage may be about one week in the ‘baseline’ timetable, where the corpse is in air at 18–20°C.
At or even before the stage of marbling, skin blisters may appear, at first on the lower surfaces of trunk and thighs where hypostatic oedema has loaded the tissues with fluid.
The upper epidermis becomes loosened, the so-called ‘skin- slippage’ giving rise to large, fragile sacs of clear, pink or red serous fluid. These may become so large that they are pen- dulous and soon burst, leaving areas of slimy, pink epider- mis. Where this skin change occurs in hairy parts, such as scalp, axilla and pubis, the hair becomes detached and will slide off on slight pressure. Gas formation will now become marked, with increased tension in the abdomen.
The scrotum and penis may swell up to remarkable size and the neck and face will become grotesquely bloated, making visual identification difficult or impossible. The pressure may cause the eye globes and tongue to protrude.
Purging of urine and faeces may occur due to the intra- abdominal pressure and, occasionally, a uterine prolapse may be extruded. There are recorded instances of pregnant
women having a macabre post-mortem ‘delivery’ of the fetus, from the same cause. Bloody fluid, which is tissue liquefaction stained by haemolysis, may leak from any ori- fice, especially the mouth, nostrils, rectum and vagina. By this stage, some 2–3 weeks may have elapsed since death.
To the inexperienced, this may suggest evidence of some lethal haemorrhage and many pathologists have been called to a scene of ‘crime’ because of the understandable concern of an investigating police officer that such bloody purging may be evidence of a violent mode of death. Pressure inside the chest due to gas formation in the abdomen may expel air, so that the fluids of decomposition in the trachea and bronchi may be blown into a bloody froth from the mouth and nostrils.
After several weeks, the reddish-green colour of the skin may deepen to a dark green or almost black, but there is marked variation in this aspect. Heavy maggot infestation will almost certainly have supervened except in winter condi- tions, and the destruction of skin by innumerable maggot holes and sinuses gives better access to other bacteria that may invade from the environment. The maggots secrete a proteolytic enzyme that speeds up the destruction of the tissues, in addition to the direct loss from the voracious appetites of these predators. Skin slippage causes shedding of the outer layers of the fingers and toes, making identification by fingerprints more difficult. Finger- and toenails last longer than the surrounding skin, but they too become loose and eventually fall out. Skin slippage may allow tattoos to become more visible and colourful for a time until the moist underlying dermis itself decomposes.
Internally, decomposition proceeds more slowly than at the surface. It is often quite surprising how valuable an
FIGURE2.11 Post-mortem decomposition of about 2 weeks’ duration in water in a summer temperature. There is ‘marbling’ of the skin where breakdown products of haemoglobin have stained the venous channels.
autopsy on a putrefying corpse can be, as the internal organs may be in far better condition than the exterior would sug- gest. Organs putrefy at markedly different rates. The lining of the intestine, the adrenal medulla and the pancreas autol- yse within hours of death, yet the prostate and uterus may still be recognizable in a partially skeletalized body a year later. The brain soon becomes discoloured, being a soft pinkish-grey within a week and liquefying within a month.
Meningeal haemorrhage and haematomata persist well, but apart from some tumours, non-haemorrhagic lesions in the brain substance vanish quite early.
The heart is moderately resistant, and examination of the coronary arteries for the degree of atheromatous stenosis may be well worthwhile for many months, though staining of the vessel walls by haemolysis makes recognition of mural throm- bosis difficult. Complete occlusion by firm ante-mortem
FIGURE2.12 Post-mortem decomposition showing putrefactive changes in the face, arms and trunk after one week in a warm room.
The illustration shows the contrast sometimes seen between one part of the body and another, as the legs are hardly affected. The face, neck and hands are swollen with gas, and the clothing is stained by leaking skin blisters. The tongue is protruding because of gas pressure from the tissues below. Death was due to carbon monoxide poisoning caused by faulty installation of a room heater.
FIGURE2.13 Almost complete destruction of the facial soft tissues by maggots. Post- mortem time about 2 weeks in a centrally heated apartment.
thrombus persists well. The heart may show a curious white granularity on the epicardial and endocardial surfaces, seen either during putrefaction or even on exhumation after a long interval. The nodules are a millimetre or less in size and are often called ‘miliary plaques’. They were investigated by Gonzales et al.(1954) who found that microscopically they consisted of calcium and soapy material. The origin is obscure, but they seem to be confined to the heart and to be some degenerative product of the cardiac tissue.
In obese people, the body fat (especially perirenal, omen- tal and mesenteric) may liquefy into a translucent, yellow fluid that fills the body cavities between the organs, and makes autopsy even more difficult and unpleasant.
Later putrefactive changes lead to the breakdown of the thoracic and abdominal walls, often hastened by the perforations of maggots and sometimes larger predators, such as rats and dogs. In some tropical countries, such as India and Sri Lanka, bodies left in the open are attacked by many animals, including monitor lizards, and in other parts of the world the indigenous fauna all contribute to the natural cycle that returns the body fats and proteins to the food chain.
After several months, the softer tissues and viscera pro- gressively disintegrate, leaving the more solid organs, such as uterus, heart and prostate, together with the ligamentous and tendinous tissues attached to the skeleton. Often some areas of skin persist, especially where protected by clothing or under the body against the supporting surface. Much depends upon the environment, as a corpse in the open air will suffer far more from rain, wind and especially animal predators, compared with one in a locked room.
Eventually, the body will be reduced to a skeleton, but for some time, ligaments, cartilage and periosteal tags will sur- vive. The season of year and the location will make a great difference to the time scale of skeletalization: a body dying outdoors in the late autumn will ‘survive’ longer through the cold winter and spring than one dying in the early summer.
The effects of animal predators are profound in terms of removing soft tissues from the bones. In broad terms, a corpse outdoors in a temperate climate is likely to be con- verted to a skeleton carrying tendon tags within 12–18 months, and to a ‘bare-bone’ skeleton within 3 years; there are, of course, numerous exceptions, depending mainly on the local environment. In closed conditions indoors, a body may never skeletalize, often being converted to a dried, partly putrefied, partly mummified shell.
Decomposition in immersed bodies
The old rule-of-thumb that bodies decay twice as fast in air as in water is grossly inaccurate, but emphasizes the slower rate of decomposition of immersed corpses. Though in mortuary practice ‘drowners’ are generally regarded as being the major source of offensively rotten bodies, this is usually because discovery and recovery is far later than in deaths on dry land. Water, in fact, slows up putrefaction, mainly because of the lower ambient temperature, and pro- tection from insect and small mammal predators.
The water also affects the usual processes of decay in that the epidermis becomes macerated and eventually detached, as described in the Chapter 16. Gas formation is the reason
Putrefaction
FIGURE2.14 Bloating of face and effusion of blood-tinged fluid from the nostrils and mouth. A body recovered from water, post- mortem time approximately 11 days.
for the inevitable flotation of an unweighted body, though the time of reappearance at the surface is extremely variable and certainly does not follow the speculative timetable of the older textbooks. The usual posture of a freely floating body is face down, as the head is relatively dense, and does not develop the early gas formation in the abdomen and thorax.
This lower position favours fluid gravitation and hence more marked decomposition, so that the face is often badly putre- fied in an immersed body, making visual recognition diffi- cult or impossible at an early stage. As stated, temperature is the major determinant of the rate of putrefaction. Though it
is usually claimed that the nature of the water in respect of sewage, for instance, is important, it is a minor factor as most of the micro-organisms responsible for decay come from the alimentary canal and respiratory passages of the body itself.
Decomposition in buried bodies
The rate of decay of bodies buried in earth is much slower than of those in either air or water. In fact the process of putrefaction may be arrested to a remarkable degree in cer- tain conditions, allowing exhumations several years later to be of considerable value. In this respect the prospect of an exhumation should never be dismissed on the grounds that because of the lapse of time, it is bound to be worthless.
It may turn out to be of little value, but this cannot be anticipated, and not infrequently the condition of the body may be surprisingly good.
The speed and extent of decay in interred corpses depends on a number of factors. If the body is buried soon after death, before the usual process of decay in air begins, putre- faction is less and may never proceed to the liquefying corruption usually inevitable on the surface. A lower tempera- ture, exclusion of animal and insect predators, and lack of oxygen are important factors. Although most bacteria originate in the intestine, there is less access for secondary invaders and the restriction of oxygen inhibits aerobic organ- isms. If the body is rotting before burial then, although the process slows down, it will still severely damage the corpse, as enzymatic and bacterial growth have had initial encourage- ment from a higher ambient temperature and free access of air, thereby producing conditions in which secondary FIGURE2.16 Adipocere formation in a body after 3 months in the
sea. Subcutaneous fat has been released from crustacean bites on the skin and has been converted into adipocere, which has been rolled by wave action within the clothing to form ovoid masses.
FIGURE2.15 Marine predation in a body after 3 months in the North Sea. The victim was from an oil rig and had floated on the surface in a life jacket. Much of the skin has been removed by crustaceans, and the arm muscles by larger fish who have cleaned out most of the body cavity.
Putrefaction
invaders (including anaerobes) can continue their work in a good culture medium that is already partly liquefied by the earlier stages.
Deep burial, as in the usual cemetery interment, pre- serves the corpse better than the shallow grave seen in some concealed homicides. The deep burial is colder (except in extremely cold weather), it excludes air better and, unless waterlogged, is not directly affected by rain.
The nature of the soil is not directly relevant except in its drainage and aeration properties. Heavy clay will exclude air and, if well above the water table, will exclude percolat- ing surface water. By contrast, light sandy soil may allow access of both air and rainwater, but will drain more effect- ively. The soil factor is less important than the topography in which it lies – in a valley floor or below the water table, waterlogging is inevitable, but on a well-drained hillside the grave may remain relatively dry.
Another factor that aids the preservation of legitimately buried corpses is the coffin. Though modern coffins are often of wooden laminate or chipboard, which rapidly dis- integrates when wet, any kind of coffin helps to exclude water and air for a time. A substantial, sound jointed coffin may last for years and the modern rarity of a sealed metal liner can keep a body in an excellent state of preservation for a long time.
A major factor that helps to slow decomposition is, of course, the absence of animal predation in burials. Again, if a corpse is buried before insect eggs are laid, the profound effect of maggot infestation is avoided. Rodents and larger mammals can only reach shallow burials, and in deep inter- ments the coffin has to be breached before even the limited fauna of that stratum can gain access.
As in all putrefaction, it is unrealistic to try to construct a timetable for the stages of decay in burials. The permutations of factors mentioned above make it impossible, especially where adipocere formation takes place, as described below.
The author (BK) has exhumed a chapel cemetery in the waterlogged peat of a Welsh valley and found not a trace of body, even skeleton, in graves with headstones confirming death only 20 years previously. By contrast, other bodies elsewhere were perfectly recognizable – and a standard autopsy could be carried out – one and a half years after death.
When bodies are buried in coffins in vaults, rather than in earth, then again there can be a variable rate of decay. Some bodies may develop adipocere, others may wholly or partly mummify.
There are many publications on this subject, mainly derived from the examination of historical sites or church crypts that have had to be cleared. The subject is of consid- erable interest but of limited forensic relevance.
FIGURE2.17 Decomposition in a body buried in a shallow grave for 6 months (see Figure 1.2). The soil had collapsed into cavities around the corpse, partly due to the weight of tractors passing over it. This allowed access to flies and discovery by a dog. The body is partly putrefied, but has some adipocere.
FORMATION OF ADIPOCERE
An important and relatively common post-mortem change is the formation of adipocere, a waxy substance derived from the body fat. The name was given to it by Fourcroy in 1789, being derived from ‘adipo’ and ‘cire’, to indicate its affinity with both fat and wax. In most instances the change of adipocere is partial and irregular, though occasionally almost the whole body may be affected. In small amounts, adipocere is more common than usually thought in buried or concealed corpses. It is caused by hydrolysis and hydro- genation of adipose tissue, leading to the formation of a greasy or waxy substance if of recent origin. After months or years have passed, adipocere becomes brittle and chalky. The colour can vary from dead white, through pinkish, to a grey or greenish-grey. The substance itself is off-white, but stain- ing with blood or products of decomposition can give it the red or greenish hues. The smell was accurately described by WED Evans (1962, 1963a, b) as being ‘earthy, cheesy and ammoniacal’.
The chemistry of adipocere has been studied extensively.
It contains palmitic, oleic and stearic fatty acids together with some glycerol, though the latter may have been leached out in older adipocere. These form a matrix for remnants of tissue fibres, nerves and muscles, which give some slight strength to the fats (see Mant and Furbank 1957). Crystals with radial markings can be found in the adipocere. Body fat at the time of death contains only about half of 1 per cent of fatty acids, but in adipocere, this may rise to 20per cent within a month and more than 70per cent in 3 months.
The formation of adipocere, as an alternative to total putrefaction, requires certain environmental conditions.
A body left exposed in air, unless the conditions are condu- cive to mummification, will undergo moist putrefaction if the temperature remains above about 5–8°C. In burials, immersion in water, and in incarceration in vaults and crypts, adipocere often forms to a greater or lesser extent.
It is usually taught that moisture is necessary for the process, and it is undoubtedly a fact that most adipocere formation occurs in immersed bodies and those in wet graves and damp vaults. Numerous cases have been described, how- ever, in which dry concealment also led to adipocere forma- tion and here it must be assumed that the original internal body water was sufficient for the hydrolysis to proceed.
It is said that some warmth is necessary for adipocere formation, but the process seems to occur even in deep
FIGURE2.18 Complete conversion of a body to adipocere. The body was recovered from a deep lake 8 years after disappearing in a boating accident during a heavy storm.
FIGURE2.19 Conversion of facial and orbital fat into adipocere after several months in water. There is also a penetrating wound on the forehead, obviously ante-mortem from the healing margins.
The body was eventually identified by obtaining hospital radiographs of the person suspected of being the victim; these matched post-mortem radiographs in respect of the injury and frontal sinus outlines.