Death is a grim topic for us all. The images many of us associate with it - the Grim Reaper, creaking coffins, skeletal limbs, willow trees and tombstones - are often unnerving, if not terrifying. As children we have been taught to connect grinning skulls and white bones with death and malevolent ghosts - something that remains with us for the rest of our lives.

And yet death is simply an integral part of life and nature. Trees shrivel up and die. Animals are slaughtered to feed those higher up on the food chain. Cells in our body die every day, to be replaced by new ones.

The purpose of this article is to inform, and not to horrify, the general public. If you are faint-hearted and are unable to endure highly graphic descriptions, it is highly advised that you do not proceed.

What is Death?

Death is the irreversible loss of the properties of living matter - that is to say, death is the cessation of life. It is when the body shuts down its machineries of life, never to start up again.

There are basically two phases of death: (1) somatic death, which is the cessation of the vital process, and (2) molecular death, which is the progressive disintegration of the body.

Somatic Death

Our body consists of billions of cells, all of which require two major components to live: oxygen and energy. The oxygen circulated to these cells by our blood is used in complex biochemical processes involving glucose or fatty acids to synthesise adenosine triphosphate (ATP) which, when broken down, releases a tremendous amount of energy.

Because oxygen is crucial to the cell system, oxygen loss is critical and, unless rapidly restored, will ultimately lead to cell death and disintegration.

The first thing to occur when a person dies is that their heart ceases to function¹. Because the function of the heart is to maintain blood flow in the circulatory system, when the heart stops beating, circulation of blood ceases as well. Simultaneously, the person ceases to respire, putting a stop to the input of fresh oxygen into the system. Without a supply of oxygen, the cells begin to die one by one.

The first cells to perish are those that are most sensitive to oxygen levels - the ganglionic cells in the central nervous system, responsible for transmission of information in the body. Brain death - the death of parts of the brain-stem, also known as the vital centres, involved in the maintenance of the respiratory and circulatory systems - occurs within minutes of anoxia². Death of less sensitive cells follow³. Aerobic metabolic processes within these cells cease, although certain anaerobic chemical processes may continue for several hours after death. Ultimately, however, when the body temperature falls and waste products accumulate, these processes too will fail.

Concomitant signs of death

1. Immediate signs

i. Pallor and loss of skin elasticity

ii. Changes in the eyes (ocular signs)

• Segmentation of retinal blood columns - Within one hour of death. In the eyes, the streams in the blood vessels become irregular and lumpy as red blood cells clump together, moving towards the optic disc and dropping over the edge of the cup. This becomes more prominent as the motion of blood decreases, and when blood movement ceases altogether, the columns remain unchanged. This sign may not always be present.

• Loss of pressure within the eyes (intra-ocular tension) - Within 24 hours of death.

• Tache noire de la sclérotique - Up to 2 days after death. This sign is only seen when the eyelids remain open after death. Spots - usually triangular, but sometimes round or oval - appear on the cornea, usually developing on the outer side before progressing to the inner side. They are usually initially yellow, but then turn brown and later black.

iii. Primary muscle flaccidity

As the muscles lose shape and contour, the body flattens over areas that are in contact with the surface on which it lies - usually the shoulder blades, buttocks and calves. This is known as 'contact flattening'. At this point, it is still possible for the muscles to respond to electrical stimuli.

i. Algor mortis (Cooling of the body)

The body temperature of a normal human being is approximately 37°C. Because the human body constantly loses heat by radiation, convection and vaporisation, heat must constantly be produced by the body through metabolic processes to maintain it at this temperature, so that vital enzymatic functions may continue. Thus when death occurs, heat production will gradually cease⁴, and the body will cool until it reaches the same temperature as the environment.

Many factors govern the cooling of the dead body. It is a common misconception that the cooling of a body follows Newton's law of cooling⁵. Furthermore, it is an equally common mistake to assume that body temperature is normal at the time of death.

The cooling of a body is affected by:

• The environment - A body will cool faster in a cool, humid environment with moving air than a warm, dry one.

• Body posture, physique and surface area - The greater the surface area exposed, the more quickly the body will cool. It has been reported that muscular activity seems to help determine the cooling rate as well - a body whose muscles have exhausted their supply of glycogen will produce minimal heat by the splitting of glycogen, and therefore cool more rapidly. Thin bodies and bodies of children and infants will also cool faster than that of an obese adult because of the surface area to body mass ratio. Furthermore, an obese corpse will take longer to cool because of the insulation provided by subcutaneous fat.

• Clothing - Clothing and covers will generally insulate the body against cooling.

• Body temperature at death - A person's body temperature may be normal or sub-normal at the time of death, depending on the cause of death. Damage to the heat- regulating centres of the body caused by pontine haemorrhage⁶ and similar lesions as well as severe infections may cause the body to be above 40°C at death. Indeed, fulminating infections may even cause the temperature of the body to rise for several hours after death.

ii. Livor mortis/Post-mortem hypostasis (Lividity)

When circulation of blood ceases, any subsequent movement of this liquid will be gravitational - that is to say, the blood will tend to flow downward. Consequently they will accumulate in capillaries and small veins in dependent parts of the body, and this is manifest as a purple or reddish-purple colour⁷ on the skin. This is known as lividity, and it is usually apparent within half an hour to two hours after death, fully developing within 12 hours⁸. It may be observed on the back of the torso and limbs, earlobes and tissue under fingernails of a corpse that has been laid on its back, initially appearing as a patchy mottling of the skin which subsequently spreads and produces extensive discolouration. If the corpse is autopsied, engorgement of the posterior portions of the brain, and parts of the lungs, stomach, liver, kidneys and intestines closest to the ground⁹ will also be observed. Sometimes the distended blood vessels within intense areas of lividity may rupture to produce a scatter of purple-black haemorrhages.

The extent of lividity depends on the volume of blood in circulation and how much blood has coagulated - for within 30-60 minutes after death, blood in most corpses become permanently incoagulable¹⁰. However, any pressure exerted upon areas of 'contact flattening' - even light pressure - will prevent gravitation of blood to these areas, and thus will manifest as patches of pale, bloodless skin. Once completely developed, movement of the body will no longer displace the blood.

iii. Rigor mortis (Stiffening of the body)

After initial flaccidity, the voluntary and involuntary muscles of the body will become stiff - a phenomenon we know as rigor mortis; dead bodies are usually called 'stiffs' because of this phenomenon. In life, the contraction and relaxation of muscles are caused by the sliding of the two muscle proteins actin and myosin within a given muscle unit¹¹ over one another. A muscle contracts when these two components slide into one another; muscle relaxation happens when they slide apart again. All of this is made possible by the splitting of the ATP molecule, which generates a stream of energy. When death occurs, oxygen is no longer being supplied to the cells, and the level of ATP is maintained solely by anaerobic splitting of glycogen. When this energy source becomes depleted, the myosin stays locked onto actin; when the body has completely run out of ATP, rigor mortis sets in.

Rigor mortis has been reported to commence, under average conditions, within three to four hours after death, and will disappear at 36-48 hours after death; however, the exact period and duration is highly variable. The onset of rigor mortis does not follow a constant or symmetrical order; however, it will typically develop in smaller muscles first - in the eyelids, face, lower jaw and neck, before moving on to the trunk and limbs¹². There is no measurable shortening of muscles unless the muscles have been subjected to tension prior to onset. When rigor mortis is fully developed, the joints of the body become fixed, and repositioning of the limbs is only possible by brute force - once broken, the rigor will not return, provided it is fully developed. It is traditionally accepted that rigor mortis passes off in the same sequence it developed, to secondary muscle flaccidity.

The period of development is influenced by factors such as:

• Temperature of the environment - High temperatures both accelerates the onset of rigor mortis and shortens its duration; if the temperature is below 10°C, development of rigor mortis is considered rare.

• Muscular activity prior to death - It has been observed that rigor mortis develops and passes quickly in an individual who died after prolonged muscular activity.

• Disease and unnatural death - Septicaemia and wasting diseases hasten the onset of rigor mortis; death by asphyxia tends to delay it. Similarly, death that is preceded by severe haemorrhaging causes rigor mortis to develop late.

A rare form of muscle stiffening, called cadaveric spasms, occurs at the moment of death. It is most commonly observed when the person has died violently - one who has committed suicide with an implement such as a knife or firearm, or been murdered. This may occur in death by drowning and poisoning as well. In many such cases, it involves only a certain group of muscles such as those of the forearm and hand, and usually involves an object tightly clutched in the hand of the victim - the suicide weapon, material from the assailant, or whatever might have been close to the victim at the time of death.

iv. Spontaneous movement

This is probably the most chilling manifestation of somatic death. The feet and legs of a corpse are seen to twitch or move hours after death has occurred. This is no doubt the kind of stuff that fuelled horror stories about the dead arising and wreaking havoc upon the living.

However, movement in the dead is caused by biochemical reactions and not vengeful spirits. Bardonnel et al (1936) reported such movements in a corpse that had been dead for 13 hours. The same phenomenon has been observed in corpses of people who died from cholera and yellow fever. The Frenchmen postulated that these spontaneous movements were caused by accumulation of carbon dioxide in the blood and muscles; however, this phenomenon only occurs in special circumstances such as high temperatures, extreme positions of the body when death occurred and increased tonus¹³ induced by certain poisons (the poison parathion was shown by Forster in 1964 to augment rigor mortis). On the odd occasion, when these gases reverberate against the vocal cords, noises may even be produced.

Molecular Death

Putrefaction

Putrefaction is the final marker for death, the final confirmation that life has departed. It is the gradual disintegration of the body into gases, liquids and salts by both bacterial activity and enzymes from our bodies. This process begins even as the cells in the body begin to die, but is usually not visible for at least several hours after death. The onset of putrefaction is determined by a variety of factors including atmospheric temperature, moisture and humidity (all of which affect microbial growth), age and pre-existing infection.

The mortal fear of hordes of worms descending upon one's body after burial is vivid and perhaps traumatic - but completely unfounded. In no way do worms enter the death scene at all, unless the corpse is buried directly in the soil, or the coffin falls apart in time. In fact, the final handlers of the body are those that have been with the person all his life - micro-organisms. It is perhaps by an ironic twist of nature that the first things to welcome a person into the world are also the last to see him go.

In life, humans cohabit with micro-organisms - those within the body and without. When blood circulation in the body ceases, the immune system slowly breaks down, as its components stagnate and die off one by one. Without the immune system to keep them in check, bacteria¹⁴ within the respiratory and gastrointestinal tract leave their habitats, penetrate the mucosal layers and rapidly invade the tissues. They are joined by other micro-organisms from the environment. There they will release enzymes that will break up the tissue into smaller, simpler components. Ruptured cells in the corpse release their own battery of enzymes, which collaborate with the microbes to slowly disintegrate the dead matter.

Sometimes flies and occasionally beetles will lay eggs on the corpse before interment. These eggs will hatch into maggots and larvae, which will subsequently feed upon the dead flesh. However, unlike the bacteria, these insect young require oxygen, and are buried alive with the corpse.

Tissue changes during putrefaction follows the following sequence:

1. Changes in tissue colour

The first visible sign of putrefaction is a green or greenish-red discolouration of the skin. As red blood cells burst, they release their haemoglobin¹⁵ load, which will diffuse through the walls of the blood vessels and stain the surrounding tissues red or reddish-brown. There they will undergo chemical changes to form various derivatives, including sulph-haemoglobin which discolours the tissue to a greenish-yellow, greenish-blue or greenish-black colour.

The discolouration starts at the skin of the anterior abdominal wall and spreads to the flank, chest, limbs and face in a marble vein-like pattern. By this time, about a week has elapsed since death. The skin will now be glistening and dusky reddish-green to purple-black in colour. Large sheets of epidermis - the top layer of the skin - will come lose with any light contact, revealing a moist, shiny pink base which, if it dries, becomes like yellow parchment.

2. Production of gases

Because the body will by now be anoxic, all metabolic activity taking place within it will be fermentative and will thus form various gases including methane, carbon dioxide, ammonia and hydrogen, as well as organic compounds such as butyric acid and mercaptans, which in combination gives the corpse a foul stench.

Blisters first form on the skin. These are of varying sizes, from less than 1 cm to about 20 cm, and are filled with dark fluids and putrid gases. These will burst upon the slightest touch, exposing the same moist pink base as described before.

Gas production begins to bloat the body, particularly in regions where the skin is loose¹⁶. It is the most rapid in the intestines, where the bulk of bacteria within the body are to be found. The gases formed cause the abdomen to distend and the pressure within to rise, sometimes forcing faeces out of the rectum and stomach contents through the nose and mouth. On the face, gas distension causes the eyelids to become swollen and tightly closed; the lips, swollen and pouting; the cheeks, puffed out, and the distended tongue, protruding between the lips. Bloodstained froth may also appear at the mouth and nostrils. Hair on the head and other parts of the body become loose at the roots, and may be easily pulled out.

By this time, fingernails and toenails readily detach along with large sheets of epidermis, usually forming complete 'gloves' and 'socks', and the body is incredibly swollen. Eventually, gas pressure within the body reaches its maximum and the abdominal cavity bursts open. It is now weeks after death.

3. Liquefaction of tissues

Elsewhere in the body, putrefaction continues. It begins with discolouration of the organs, and progresses to the liquefaction of the tissues. Body fats are converted to oleic, palmitic and stearic acids; proteins are ultimately broken down to amino acids, the building blocks of protein molecules. Little by little, the body is taken apart.

As a rule, body parts containing less muscle will liquefy faster than muscular organs. The eyeballs, stomach and intestines are the first to go. Small white granules called 'miliary plaques' will sometimes form on the outer surface of the heart. The heart itself becomes flabby and thin-walled. The spleen and lungs become mushy and friable, and gas formation causes the liver and brain to develop honey-comb patterns. The brain subsequently turns to mush. Generally the capsules of the liver, spleen and kidney will endure longer, turning into squashy bags filled with thick, turbid liquid. These will rupture in time as well.

Eventually, after all the soft parts are destroyed, the connective tissue and cartilage will disintegrate. All that will be left is the skeleton.

Saponification (Adipocere formation)

Sometimes putrefaction of a corpse does not lead to skeletonisation. Sometimes, during the breakdown of fat by hydrolysis and hydrogenation, conditions become too acidic for bacterial activity to continue. When this happens, the body fat remains as adipocere, a yellowish-white, greasy, waxy substance which smells of cheese, earth and ammonia. This substance floats on water, dissolves in hot alcohol and ether, and when burned produces a faint yellow flame.

Formation of adipocere, a natural form of preservation, is rare and requires a warm, moist environment as well as the participation of putrefactive bacteria including Clostridium welchii. It usually develops in subcutaneous tissues, especially in the cheeks, breasts and buttocks; on extremely rare occasions, the subcutaneous tissues of the entire body may be converted to adipocere. Viscera are very seldom involved. The adipocere will combine with mummified remains of muscles, fibrous tissues and nerves to form a naturally preserved corpse whose features are preserved. This takes upwards of 5 to 6 months¹⁷ after death, and the body may endure for years in this condition.

Mummification

Another modification of putrefaction is mummification, the desiccation of tissues and viscera after death. In conditions of dry heat and air currents - especially when saponification occurs - the body shrivels up into a dark leathery, parchment-like mass of skin and tendons surrounding the bone. The skin around the groin, neck and armpits will sometimes split due to shrinkage. Internal organs do not normally survive, but in special circumstances may be preserved. Anatomical features will be preserved in this condition.

The time required for complete mummification is highly variable, but in countries like Egypt where the climate is favourable, mummification may be advanced or complete within several weeks.

Aided disintegration: Cremation

Because of limited space in burial grounds, many people today have chosen cremation over interment. The changes that occur to these bodies differ greatly from those that are buried, and these changes occur over a period of several hours instead of months or years.

A body that is cremated - usually at about 926° Celcius (1,700°F) - is burned right down to the bones, first by charring, and then by complete combustion. Fat bodies ignite and burn more readily than muscular ones. As the skeleton emerges, the flames turn all sorts of brilliant colours as various salts and chemicals within the body are volatilised - sparks of blue-green from copper and purple from potassium amidst warm yellow and orange tongues of flame. The exposed bones will then turn black as the organic material is carbonised; later, these bones will fade from black to grey and finally to white. When this happens, the bones are said to be calcined and are very brittle. The skull may crack under the heat, and other bones may warp, twist and form tiny checkerboard or crescent patterns; however, for the most part the skeleton will remain intact.

These skeletal remains are then removed from the 'retort' or oven, and are then crushed to small fragments in a container by a heavy magnetic iron, and subsequently ground through a sieve about five millimetres in diameter before being placed in their final resting place.

In the end...

...Even if it means oblivion, friends, I'll welcome it, because it won't be nothing, we'll be alive again in a thousand blades of grass, and a million leaves... out there in the physical world which is our true home and always was.
- From 'The Amber Spyglass' by Philip Pullman.

It is a well-known joke that the only certain things in life are death and taxes. Unlike taxes, death really is inevitable - no matter how long-lived we are, death will claim us all one day. Perhaps it is the fear of disappearing forever that drives us to be edgy about death. Thus fear of death has become widespread in our society, has become ingrained in cultural taboos and superstitions. The media - especially the movie industry - on the other hand garners billions each year from books and films that frighten the living daylights out of the horrified but morbidly fascinated audience.

And yet death does not spell complete oblivion, for it completes the circuit for the circle of life. In the same manner that a tree falls to have many others rise in its place, so we take our turn in the self-preserving ecosystem that gave life to us. So much as we dread passing into the valley of the shadow, we may also take comfort in the knowledge that even as we perish and fade, we give the means for others to grow and live in our place.

References

• Freedman, AD. 1996. Death and Dying. The 1996 Grolier Multimedia Encyclopaedia.

• Gordon, I and HA Shapiro. 1975. Forensic medicine: A guide to the principles. Churchill Livingstone, Edinburgh.

• Knight, B. 1997. Simpson's forensic medicine (11th ed). Edward Arnold, London.

• Maples, WR and M Browning. 1994. Dead men do tell tales. Doubleday, New York.

• Polson, CJ, DJ Gee and B Knight. 1985. The essentials of forensic medicine (4th edition). Pergamon Press.

Further Reading

• Badonnel, M, E Fortineau and P Neveu. 1936. Ann. Med. Lég. 16:491-6.

• Forster, B. 1964. J Forens. Med. 11: 148.

• Spitz and Fisher. 1980. Medicolegal Investigation of Death (2nd ed). Thomas, Springfield, Illinois.

Other Resources on the Internet

• Contraction and rigor mortis

• Moyle Information Services for Law Enforcement: Death Investigation

• Postmortem changes and time of death

• Learn about Professor Gunter von Hagen's Body Worlds exhibition, the anatomical display of real human bodies.