Though the study of the rate of cooling of the dead human body is essentially an exercise in physiology, its potential use in determining the time since death have made it the most frequent topic for research in forensic medicine.
For more than one and a half centuries, papers have been published devoted to refining the problem further, which has obvious and important connotations in the investiga- tion of criminal deaths. Unfortunately, the vast amount of labour in this direction has not been rewarded by compar- able improvements in accuracy because of the permutations of factors that defeat exact calculation of the post-mortem interval. The history of this research is in itself extensive (Knight 1988) but a few cardinal points might be men- tioned here to mark the various phases of investigation.
Though the fact that a dead body becomes progressively colder after death has naturally been known since earliest times, scientific measurements were first published in the nineteenth century. Dr John Davey in 1839 recounted experiments with dead soldiers in Malta and Britain, using a mercury thermometer. Though this pioneer made no prac- tical contribution to the problem, some of his comments are remarkably pertinent across a gap of more than 150 years:
Much judgement, however and nice discrimination may be requisite on the part of the medical man, in appreciating the circumstances likely to modify temperature, so as to enable him when called upon for his opinion (of the time of death), to give one which will be satisfactory to the legal officers – and to himself – on reflection.
These cautionary words are just as applicable nowadays when, unfortunately, some doctors offer a time of death with a confidence often inversely proportional to their experi- ence. In 1863, Taylor and Wilkes wrote a classic paper which introduced many of the current concepts, such as the initial temperature plateau, the core temperature, heat gra- dient and the effect of insulation. Taylor was, of course, Alfred Swaine Taylor of Guy’s Hospital, author of the text- book that remained the definitive work on forensic medi- cine for almost a century. Later in the nineteenth century, Rainy of Glasgow first applied mathematical concepts to the problem and produced a formula for calculating the time of death. He also pointed out that Newton’s Law of Cooling did not apply to the human body. In 1887, Womack first
Estimation of the time since death by body cooling
used centigrade units, though his use of the now familiar temperature graphs was anticipated by Burman in 1880.
In this century, the most quoted papers were those by De Saram in Ceylon (De Saram et al.1955; De Saram 1957), who published careful and detailed measurements of con- trol cases obtained from executed prisoners. His data are still being studied and reworked. The names Fiddes and Patten are known to all those interested in this subject as, in 1958, they produced a paper that was a classic, as Taylor’s had been in the previous century. Using repeated temperature meas- urements they devised a percentage cooling method and explored complex theoretical aspects, such as the ‘infinite cylinder’ model, for the human body.
Marshall and his collaborators dominated the publica- tions in the 1960–1970 period, with papers that explored in depth the mathematical aspects and confirmed the double exponential or ‘sigmoid’ shape of the rectal cooling curve. In the last decade or so, many more papers and new techniques have been produced, with computer assistance increasingly used. Amongst these, Henssge and Madea in Germany have been predominant. Microwave and infrared thermography have been explored and the physics and mathematics of body cooling probed in such depth that often the scientist in the research group has difficulty in explaining the concepts to his medical collaborator. In spite of all this activity, practical methods of determining the time of death continue to lack accuracy. Though some recent publications offer firm advice and describe methods, they can do no more than provide a ‘time bracket’ of probability within which death is thought to have occurred.
Post-mortem cooling
Except where the environmental (ambient) temperature remains at or even above 37°C, the human body will cool after death. A uniform, homogeneous laboratory ‘body’ will cool according to Newton’s Law of Cooling, which states that the rate of cooling is proportional to the difference in temperature between the body surface and its surroundings.
Graphically represented, this will display the curve of a single exponential expression, not a straight line. A human body does not obey Newton’s Law, though the size of the discrep- ancy varies according to several factors. When death occurs, heat transfer within the body through the circulation ceases.
Metabolic heat production, occurring mainly in the muscles and liver, does not cease uniformly and some heat generation continues for a variable time. As soon as the supply of warmed blood ceases with cardiac arrest, the skin surface immediately begins to lose heat. The rate is variable because of clothing, posture and shielding against the supporting surface and, of course, the environmental temperature.
The centre or ‘core’ of the body cannot begin to cool until a ‘temperature gradient’ is set up by the cooling at the skin surface. As the tissues are poor heat conductors, this gradient takes a variable time to become established and therefore a thermometer placed near the core (usually in the rectum) will not register a fall for some time. This is the well-known ‘plateau’, which forms the upper flattened or slightly sloping part of the double exponential curve when
Temperature
(a)
(b) (c)
Time
FIGURE2.29 Cooling curves: the Newtonian single exponential curve (a) does not occur in practice, except on the surface of the body.
Because of the variable plateau (c), the true curve for deep core temperature (b) assumes a double exponential shape.
41ºC
37ºC
28ºC
Temperature
Time (f)
(e)(d) (a) (b)
(c) (g)
FIGURE2.30 Diagrammatic representation of some variables in body cooling curves: (a) average body, (b) obese body, (c) heavily clothed body, (d) thin body, (e) naked body, (f ) hypothermic body and (g) febrile body.
rectal temperatures are measured. If skin temperatures are used, as in some of the nineteenth century research, no plateau is found, and, using cranial temperatures taken through the nose, ear or skull, the plateau is less, as the core is nearer the surface.
The central part of the cooling curve approximates to Newtonian principles, being fairly straight or only a shal- low curve. As the temperature differential between the body and environment approaches zero, the graph again flattens off into a lower shelf. Unlike the laboratory body, the human body rarely reaches the ambient temperature unless the latter is at or near freezing. This is probably because enzyme and bacterial action starts during early decomposition and, much as a compost heap warms up, the temperature may actually rise a few days after death.
The typical rectal cooling curve then, is a ‘sigmoid’ shape or ‘double exponential’ curve. The part that is of use in forensic medicine is the central section showing the steepest fall. Theoretically, if one assumes that the body tempera- ture at the time of death was 37°C, then finding the point on this section corresponding to the measured rectal tem- perature should allow extrapolation back to the 37°C point which is at zero on the time scale, thus giving the post- mortem interval.
Unfortunately, a number of variables make this attractive proposition impossible to attain in practice. Not only are there variables, but the variables themselves often vary dur- ing the period before the body is discovered and examined.
For example, the ambient temperature may change markedly – perhaps several times – and often this may not be known to the examiner. Even opening doors and allow- ing draughts to play on the body will have profound effects on the cooling curve, which cannot be detected or corrected retrospectively.
Factors affecting the cooling curve
INITIAL BODY TEMPERATURE
This cannot be assumed to be 37°C and in fact is incapable of ever being measured in retrospect. Not only is there a difference between the rectal, liver, brain, axillary, mouth and skin temperatures in the living person, but the absolute values vary slightly from person to person and from time to time, even in health.
If the oral temperature is taken to be 37°C, then that in the axilla will be several degrees lower and that in the rec- tum at least one degree higher. There is a diurnal variation of almost 1°C, the temperature being lowest between 0200 and 0600 and highest between 1600 and 1800. Strenuous exercise raises the temperature by up to 3°C, which persists for up to 30 minutes after returning to rest.
When there is illness or trauma, much wider variations occur, which again are impossible to detect retrospectively.
In febrile illness from micro-organisms or parasitic infec- tions, the temperature may be 4 or 5°C higher. In the foren- sic context, infected wounds or a septic abortion are obvious examples. Cerebral (especially pontine) haemorrhage may also cause hyperthermia, as may some drug reactions. It is traditionally stated in many textbooks that asphyxia and strangulation cause agonal hyperthermia, but there is very little hard evidence for this, apart from anecdotal opinions passed from one author to another. One explanation may be that a homicide victim struggling desperately for life against strangulation will generate muscular heat as in any violent exercise, irrespective of an asphyxial mode of death.
At the other end of the scale, hypothermia is common even in temperate winters. Many victims of criminal assault may be left exposed before death and their temperature may be as much as 10°C lower than normal.
As virtually all methods and formulae for calculating the time of death depend upon the body temperature being 37°C, even a slight variation can introduce a funda- mental error.
THE BODY DIMENSIONS
The temperature gradient, which drives cooling, varies with the mass of the body and the surface area as well as with the conducting properties of the tissues. Some more complex calculations correct for mass:surface area ratio by means of nomograms (for example, those served by Henssge), but these can only be an approximation. The height and weight of the body must be known, which is often impossible at the scene of discovery. The amount of subcutaneous and abdom- inal fat will affect the insulating properties and hence the temperature gradient, but there is no way of assessing or correcting accurately for obesity. Oedema and dehydration both have a marked effect because of the high specific heat of water (see James and Knight 1965). In general, a thin person cools more quickly because of both the mass:surface area ratio and the lack of fatty insulation. Children have a larger surface area for a given body weight.
POSTURE
The loss of heat from the skin that drives the temperature gradient is affected by the access of air to the skin and the opportunity for radiation and convection. A body curled into a fetal position will expose much less surface than one in an extended, spread-eagled posture. Another factor is the amount of skin resting on the supporting surface and the nature of that surface. A body lying full length on its back will lose heat by conduction faster than one resting semi- prone, though radiation and convection may be facilitated.
Estimation of the time since death by body cooling
A body on a metal mortuary tray will cool more quickly than one lying on straw.
CLOTHINGANDCOVERINGS
All too obvious is the effect of external insulation by clothing or other coverings, even a hat. Radiation is a minor path- way for heat loss because of the low biological temperatures involved, but convection and conduction are markedly reduced by coverings. Even more confusion may be added when coverings actually contribute heat, such as an electric blanket left on after death. A duvet or ‘continental quilt’
will markedly retard cooling and in fact will accelerate decomposition to a considerable degree. Wet clothing will accelerate cooling, compared with dry coverings, because of the uptake of heat for evaporation.
THE AMBIENT TEMPERATURE
This is, of course, the major factor in cooling and, as was said at the outset, a body will not cool after death if the temperature of the environment is higher than the nominal 37°C, in fact, it may warm up. This may be climatic and seasonal, as in large areas of the world, not necessarily in the tropics. It may also be due to local heating, usually in dwellings or other buildings. This includes radiant heat from fires left burning near the body after death, electric blankets, or death in a house or vehicle fire. Where a victim dies in a warm bath then the whole cooling process is grossly distorted, the opposite of when immersion takes place in the cold water of baths, rivers, lakes or the sea.
AIR MOVEMENT AND HUMIDITY
Most skin cooling takes place by convection and conduc- tion with the adjacent air as the transporting medium. In still conditions, a layer of warm air clings to the skin, espe- cially if clothed or hairy, blocking the temperature differen- tial. Any air movement brings fresh cooler air into contact with the skin and encourages the gradient from the core.
The humidity is a less active factor, but damp air conducts heat more readily than dry. A body in a small space will cool more slowly than one exposed to the open air, as transfer of heat to the small volume of air will reduce the temperature differential.
THE MEDIUM AROUND THE BODY
This is usually air, but when it is water or (rarely) another fluid, skin cooling is far more effective. A body immersed in water, especially the moving water of a river or the sea, will rapidly lose heat, as is all too familiar during life when fatal hypothermia can occur within minutes in a cold sea. It is commonly stated that cooling is less rapid in contaminated
water (such as sewage) than in clean water, but this is hard to believe, given the same temperature for each type of medium.
As mentioned above, death in the warm water of a bath- tub reduces the cooling rate – and may even elevate the tem- perature, making any attempt at estimating the time of death futile.
HAEMORRHAGE
It is traditional to say that severe haemorrhage shortly before death causes more rapid cooling. As the estimation of the time of death is fraught with such inaccuracy, it is difficult to see how this opinion can have been derived. The volume of blood lost will reduce the mass of the body, but only in a minimal fashion. It may be that terminal bleeding may cause a shutdown of cutaneous circulation in an effort to maintain blood pressure and that this might encourage the early formation of the temperature gradient – but such vasoconstriction would relax immediately at death and play no part in post-mortem cooling.
Methods of measuring body temperature
Estimation of temperature by touching with the hand is a useful first manoeuvre when at the scene of a death. A hand placed on the forehead, face or exposed hand may give a first impression of whether death occurred recently or not. Even if these exposed areas are cold, feeling inside the clothing to touch the chest, abdomen or axilla may detect some heat, as may sliding a hand under the body where it is in contact with the supporting surface. These crude methods are com- bined with an estimate of rigor mortis to provide a prelim- inary screening of a recent, as opposed to a remote, time of death. Though conditions vary enormously, a body indoors will feel cold on exposed areas in 2–4 hours and in protected areas after some 6–8 hours. The traditional method of tak- ing the post-mortem temperature is by placing a mercury thermometer in the rectum. This must be a chemical thermo- meter (not a clinical instrument) or thermocouple, ideally reading from 0 to 50°C. The tip must be inserted to at least 10 cm above the anus, the instrument preferably having most of its gradations still visible when in situ. It should be left in place for several minutes for the reading to stabilize before being recorded. Where possible, it should be left in situfor multiple readings at intervals, though in operational circumstances (especially in criminal deaths) this may be difficult to arrange. There is considerable controversy about when such measurements should be carried out. It is often recommended that a doctor at the scene of death should measure the rectal temperature at once but logistic difficul- ties exist. Many cases where estimation of the time of death
is important are criminal or suspicious deaths. These will often be associated with at least the possibility of sexual or homosexual assaults, and it may not be practicable to inter- fere with clothing in the perineal area or to contaminate the anal and vaginal region before full trace evidence procedures are carried out, usually by police scene of crime officers or forensic scientists, which may include adhesive taping of the clothing and skin, and the retention of underclothes for seminal stains, etc.
To wrestle with tight clothing, perhaps at night, in inclement weather and in confined spaces, and to try to introduce a thermometer into the rectum in these circum- stances might ruin vital evidence of more importance than the admittedly uncertain calculations about time of death.
However, many pathologists and police teams do carry out this manoeuvre as a routine, but each pathologist must decide in every individual case, whether it is preferable to wait until the body is taken to the mortuary where proper, controlled undressing is possible.
This applies where pathology and criminalistic expertise is readily available, but it is acknowledged that in less ideal circumstances, when no such expertise is likely to appear within a few hours (if at all), then some doctor at the scene should take a temperature. The procedure must be tailored to the individual circumstances but where there is a possibil- ity of sexual interference, the rectum (and vagina) should be avoided until after full swabbing for semen and other
examinations are completed. Alternatives are to use the axilla, deep nasal passage or external ear for the insertion of a thermometer.
The technique of introducing a mercury or ‘rototherm’
thermometer through a stab wound in the abdomen to measure liver temperature is never justified. It inevitably leads to blood contamination of the skin and clothing and also leads to intraperitoneal bleeding that might be con- fused with existing internal injuries.
More modern measuring devices include thermocouples, which register temperature accurately with minimum stabil- ization time. They may be part of a compact electronic instrument, which has a digital readout, or they may be connected to a computerized recorder that can analyse several other sites at regular intervals (see Morgan et al. 1988).
Microwave thermography of brain and liver (see Al-Alousi et al.1986, 1994) and infrared monitoring of skin tempera- ture are at present research tools that may lead to practical devices in the future.
The use of thermometry in estimating the post-mortem interval
In spite of the great volume of research and publications already mentioned, accuracy in estimating the time since death from temperature remains elusive. The old rule-of- thumb was that the temperature fell at about 1.5°F/hour, something under 1°C/hour. Another rule-of-thumb was that the fall in °C from 37°C, plus three (to arbitrarily allow for the plateau), was equal to the time since death in hours.
For example, if a rectal temperature was found to be 32°C, then 37323 gave a post-mortem interval of 8 hours.
The only confidence that one could place in these methods was that they were almost always wrong and that, if the answer happened to be correct, it was by chance rather than science! To hope for a linear fall was against all the princi- ples of heat loss alluded to earlier. The first method took no account of the ‘plateau’ when rectal temperatures were used. This upper part of the double exponential curve is of variable length. If the body has been dead for some hours, serial temperature recordings fail to identify it, as the meas- urements begin on the steeper part of the curve, but where thermometry is begun soon after death, there is a variable flat area at the top of the sigmoid graph.
The length of the plateau has been discussed by several authors (see Shapiro 1965; Nokes et al.1985). Shapiro in particular has drawn attention to the invalidation of many formulae by the unknown length of the plateau. He claims that this can be as much as 4 hours ‘and is possibly consid- erably longer’. Marshall and Hoare (1962) admit that the plateau may be as long as 5 hours. The plateau is the result FIGURE2.31 Measuring the rectal temperature at the scene of a
murder. This should be done only after forensic procedures such as rectal swabbing have been completed. Normally the temperature should be taken at the mortuary where removal of clothing can be carried out with full photographic and forensic science monitoring.
In this case the body was unclothed at the scene and the circumstances did not warrant rectal swabbing.