Inside the 'dead zone': In an outdoor laboratory at Texas' Sam Houston State University, cadavers mummify in the summer's dry heat. Warning: This story contains graphic images. (Mo Costandi/Flickr)

Death brings life: This is what happens after you die

Moheb Costandi
Most of us would rather not know what happens to our bodies after death. But that breakdown gives birth to new life in unexpected ways.

'It might take a little bit of force to break this up," says mortician Holly Williams, lifting John's arm and gently bending it at the fingers, elbow and wrist. "Usually, the fresher a body is, the easier it is for me to work on."

Williams speaks softly and has a happy-go-lucky demeanour that belies the nature of her work. Raised and now employed at a family-run funeral home in north Texas, she has seen and handled dead bodies on an almost daily basis since childhood. Now 28, she estimates that she has worked on about 1 000 bodies.

Her work involves collecting bodies from the Dallas–Fort Worth area and preparing them for their funerals.

"Most of the people we pick up die in nursing homes," says Williams, "but sometimes we get people who died of gunshot wounds or in a car wreck. We might get a call to pick up someone who died alone and wasn't found for days or weeks, and they'll already be decomposing, which makes my work much harder."

John had been dead for four hours before his body was brought into the funeral home. He had been relatively healthy for most of his life. He had worked his whole life on the Texas oil fields, a job that kept him physically active and in pretty good shape. He had stopped smoking decades earlier and drank alcohol moderately. Then, one cold January morning, he had a heart attack at home, apparently triggered by unknown complications, fell to the floor and died almost immediately. He was just 57 years old.

Now, John lay on Williams's metal table, his body wrapped in a white linen sheet, cold and stiff to the touch, his skin purplish-grey – telltale signs that the early stages of decomposition were well under way.

A new ecosystem emerges
Far from being dead, a rotting corpse is teeming with life. A growing number of scientists view a corpse as the cornerstone of a vast and complex ecosystem, which emerges soon after death and flourishes and evolves as decomposition proceeds.

Decomposition begins several minutes after death with a process called autolysis, or self-digestion. Soon after the heart stops beating, cells become deprived of oxygen and their acidity increases as the toxic by-products of chemical reactions begin to accumulate inside them. Enzymes start to digest cell membranes and then leak out as the cells break down. This usually begins in the liver, which is rich in enzymes, and in the brain, which has a high water content.

Eventually, though, all other tissues and organs begin to break down in this way. Damaged blood cells begin to spill out of broken vessels and, aided by gravity, settle in the capillaries and small veins, discolouring the skin.

Body temperature also begins to drop, until it has acclimatised to its surroundings. Then rigor mortis – the stiffness of death – sets in, starting in the eyelids, jaw and neck muscles, before working its way into the trunk and then the limbs. In life, muscle cells contract and relax because of the actions of two filamentous proteins (actin and myosin), which slide along each other. After death, the cells are depleted of their energy source and the protein filaments become locked in place. This causes the muscles to become rigid and locks the joints.

During these early stages, the cadaveric ecosystem consists mostly of the bacteria that live in and on the living human body. Our bodies host huge numbers of bacteria; every one of the body's surfaces and corners provides a habitat for a specialised microbial community. By far the largest of these communities resides in the gut, which is home to trillions of bacteria of hundreds or perhaps thousands of different species.

The gut microbiome is one of the hottest research topics in biology; it's been linked to roles in human health and a plethora of conditions and diseases, from autism and depression to irritable bowel syndrome and obesity. But we still know little about these microbial passengers. We know even less about what happens to them when we die.

In August 2014, forensic scientist Gulnaz Javan, of Alabama State University in Montgomery, and her colleagues published the first study of what they have called the thanatomicrobiome (from thanatos, the Greek word for "death"). "Many of our samples come from criminal cases," says Javan. "Someone dies by suicide, homicide, drug overdose or traffic accident, and I collect tissue samples from the body. There are ethical issues [because] we need consent."

Most internal organs are devoid of microbes when we are alive. Soon after death, however, the immune system stops working, leaving them to spread throughout the body. This usually begins in the gut, at the junction between the small and large intestines. Left unchecked, our gut bacteria begin to digest the intestines – and then the surrounding tissues – from the inside out, using the chemical cocktail that leaks out of damaged cells as a food source. Then they invade the capillaries of the digestive system and lymph nodes, spreading first to the liver and spleen, then into the heart and brain.

Javan and her team took samples of liver, spleen, brain, heart and blood from 11 cadavers between 20 and 240 hours after death. They used two state-of-the-art DNA sequencing technologies, combined with bioinformatics, to analyse and compare the bacterial content of each sample.

The samples taken from different organs in the same cadaver were similar to each other but different from those taken from the same organs in the other bodies. This may be partly because of differences in the composition of the microbiome of each cadaver, or it might be caused by differences in the time elapsed since death. An earlier study of decomposing mice revealed that, although the microbiome changes dramatically after death, it does so in a consistent and measurable way. The researchers were able to estimate time of death to within three days of a nearly two-month period.

Javan's study suggests that this microbial clock may be ticking in the decomposing human body, too. It showed that the bacteria reached the liver about 20 hours after death and that it took them at least 58 hours to spread to all the organs from which samples were taken. Thus, after we die, our bacteria may spread through the body in a systematic way, and the timing with which they infiltrate first one internal organ and then another may provide a new way of estimating the amount of time that has elapsed since death.

"Degree of decomposition varies not only from individual to individual but also differs in different body organs," says Javan, "Spleen, intestine, stomach and pregnant uterus are earlier to decay, but on the other hand, kidney, heart and bones are later in the process."


Texas' Sam Houston State University runs an outdoor laboratory to study how the elements and insects affect the decomposition rates of bodies (Mo Constandi, Flickr)

Scattered among the pine trees in Huntsville, Texas, lie about half a dozen human cadavers in various stages of decay. The two most recently placed bodies are spread-eagled near the centre of the small enclosure. Much of their loose, grey-blue mottled skin is still intact and their ribcages and pelvic bones are visible between slowly putrefying flesh. A few metres away lies a fully skeletonised body with its black, hardened skin clinging to the bones as though it was wearing a shiny latex suit and skullcap.

Beyond other skeletal remains scattered by vultures, lies a third body in a cage of wood and wire. It is nearing the end of the death cycle, partly mummified. Several large brown mushrooms grow from where an abdomen once was.

For most of us the sight of a rotting corpse is, at best, unsettling and at worst repulsive and frightening, the stuff of nightmares. But this is everyday for the people at the  Southeast Texas Applied Forensic Science Facility. Opened in 2009, the facility is located in a 100-hectare area of the  Sam Houston State University (SHSU) National Forest. A 3.6-hectare plot of densely wooded land has been sealed off from the wider area and further subdivided, by 3m wire fences topped with barbed wire.

In late 2011, SHSU researchers Sibyl Bucheli and Aaron Lynne and their colleagues placed two fresh cadavers here, and left them to decay under natural conditions.

Once self-digestion is under way and bacteria have started to escape from the gastrointestinal tract, putrefaction begins. This is molecular death – the breakdown of soft tissues even further, into gases, liquids and salts. It is already under way at the earlier stages of decomposition but really gets going when anaerobic bacteria get in on the act.

Putrefaction is associated with a marked shift from aerobic bacterial species, which require oxygen to grow, to anaerobic ones, which do not. These feed on the body's tissues, fermenting the sugars in them to produce gaseous by-products such as methane, hydrogen sulphide and ammonia, which accumulate in the body, inflating the abdomen and sometimes other body parts.

This causes further discolouration of the body. As damaged blood cells continue to leak from disintegrating vessels, anaerobic bacteria convert haemoglobin molecules, which once carried oxygen around the body, into sulfhaemoglobin. The presence of this molecule in settled blood gives skin the marbled, greenish-black appearance characteristic of a body undergoing active decomposition.

Bloating is often used as a marker for the transition between early and later stages of decomposition, and another recent study shows that this transition is characterised by a distinct shift in the composition of cadaveric bacteria. Bucheli and Lynne took samples of bacteria from various parts of the bodies at the beginning and the end of the bloat stage.

They extracted bacterial DNA from the samples and sequenced it.

As an entomologist, Bucheli is mainly interested in the insects that colonise cadavers. She regards a cadaver as a specialised habitat for various necrophagous insect species, some of which see out their entire life cycle in and on the body.


Death becomes them: Southeast Texas Applied Forensic Science Facility staff (left to right) Kevin Derr, Joan Bytheway, Sybil Bucheli and Aaron Lynne explore the secrets of the dead. (Mo Costandi/Flickr)

When a decomposing body starts to purge, it becomes fully exposed to its surroundings. At this stage, the cadaveric ecosystem comes into its own – a hub for microbes, insects and scavengers.

Two species closely linked with decomposition are blowflies and flesh flies (and their larvae). Cadavers give off a foul, sickly-sweet odour, made up of a complex cocktail of volatile compounds that changes as decomposition progresses.

Blowflies detect the smell using specialised receptors on their antennae, then land on the cadaver and lay their eggs in orifices and open wounds.

Each fly deposits about 250 eggs that hatch in 24 hours, giving rise to small first-stage maggots. These feed on the rotting flesh and then moult into larger maggots, which feed for several hours before moulting again. After feeding some more, these larger, fattened maggots wriggle away from the body. They pupate and transform into adult flies and the cycle repeats until there's nothing left for them to feed on.

Under the right conditions, a decaying body will have large numbers of stage-three maggots feeding on it. This maggot mass generates heat, raising the inside temperature by more than 10°C. Like penguins huddling in the South Pole, individual maggots in the mass are constantly on the move. But whereas penguins huddle to keep warm, maggots move around to stay cool.

"It's a double-edged sword," Bucheli explains in her SHSU office, surrounded by large toy insects and a collection of ghoulish dolls based on the American cartoon series Monster High. "If you're always at the edge, you might get eaten by a bird, and if you're always in the centre, you might get cooked. So they're constantly moving from the centre to the edges and back."

The presence of flies attracts predators such as skin beetles, mites, ants, wasps and spiders, which feed on or parasitise the flies' eggs and larvae. Vultures and other scavengers, as well as large meat-eating animals, may also descend upon the body.

In the absence of scavengers, though, the maggots are responsible for removing the soft tissues. As Carl Linnaeus, who devised the system by which scientists name species, noted in 1767, "three flies could consume a horse cadaver as rapidly as a lion". Third-stage maggots will move away from a cadaver in large numbers, often following the same route. Their activity is so rigorous that their migration paths may be seen after decomposition is finished as deep furrows in the soil emanating from the cadaver.

In the relentless dry heat of a Texan summer, a body left to the elements will mummify rather than decompose fully. The skin will quickly lose all its moisture, so that it remains clinging to the bones when the process is complete.

The speed of the chemical reactions doubles with every 10°C rise in temperature, so a cadaver will reach an advanced stage of decomposition after 16 days at an average daily temperature of 25°C. By then, most of the flesh has been removed from the body, and the mass migration of maggots away from the carcass can begin.

The Egyptians learnt inadvertently how the environment affects decomposition. In the predynastic period, before they started building elaborate coffins and tombs, they wrapped their dead in linen and buried them in the sand. The heat inhibited the activity of microbes and burial prevented insects from reaching the bodies, so they were extremely well preserved. Egyptians began building elaborate tombs for the dead, to provide for their afterlife, but this had the opposite of the intended effect – separating the body from the sand hastened decomposition. And so they invented embalming and mummification.

Embalming involves treating the body with chemicals that slow down the decomposition process. The ancient Egyptian embalmer would first wash the body with palm wine and Nile water, remove most of the internal organs through an incision made down the left-hand side, and pack it with natron (a naturally occurring salt mixture found throughout the Nile Valley). He would use a long hook to pull the brain out through the nostrils, then cover the body with natron and leave it to dry for 40 days.

Initially, the dried organs were placed into canopic jars that were buried alongside the body; later, they were wrapped in linen and returned to the body. Finally, the body itself was wrapped in layers of linen, in preparation for burial. Morticians study the ancient Egyptian embalming method to this day.

Back at the funeral home, Holly Williams performs something similar so that family and friends can view their loved one at the funeral as they once were, rather than as they now are. For victims of trauma and violent deaths, this can involve extensive facial reconstruction.

Living in a small town, Williams has worked on many people she knew or grew up with – friends who overdosed, committed suicide or died texting at the wheel.

When her mother died four years ago, she did some work on her, too, adding the final touches by making up her face: "I always did her hair and make-up when she was alive, so I knew how to do it just right."

She transfers John to the prep table, removes his clothes and positions him, then takes several small bottles of embalming fluid from a wall cupboard. The fluid contains a mixture of formaldehyde, methanol and other solvents. It temporarily preserves the body's tissues by linking cellular proteins to each other and "fixing" them into place. The fluid kills bacteria and prevents them from breaking down the proteins as a food source.

Williams pours the bottles' contents into the embalming machine. The fluid comes in an array of colours, each matching a different skin tone. Williams wipes John's body with a wet sponge and makes a diagonal incision just above his left collarbone. She lifts the carotid artery and subclavian vein from the neck, ties them off with pieces of string, then pushes a thin tube into the artery and small tweezers into the vein to open up the vessels.

Next, she switches the machine on, pumping embalming fluid into the carotid artery and around John's body. As the fluid goes in, blood pours out of the incision, flowing down along the guttered edges of the sloped metal table and into a large sink.

She picks up one of John's limbs to massage it gently. "It takes about an hour to remove all the blood from an average-sized person and replace it with embalming fluid," Williams says. "Blood clots can slow it down, so massaging breaks them up and helps the flow of the embalming fluid."

Once all the blood has been replaced, she pushes an aspirator into John's abdomen and sucks the fluids out of the body cavity, together with any urine and faeces that might still be in there. Finally, she sews up the incisions, wipes the body down a second time, sets the facial features and redresses it. John is now ready for his funeral.

Embalmed bodies do eventually decompose. When, and how long it takes, depends largely on how the embalming was done, the type of casket in which the body is placed and how it is buried. Bodies are, after all, forms of energy, trapped in lumps of matter waiting to be released into the wider universe.

According to the laws of thermodynamics, energy cannot be created or destroyed, only converted from one form to another. In other words: things fall apart, converting their mass to energy while doing so. Decomposition is one final, morbid reminder that all matter in the universe must follow these fundamental laws.

It breaks us down, equilibrating our bodily matter with its surroundings, and recycling it so that other living things can put it to use.

Ashes to ashes, dust to dust.

This article was originally published by Wellcome on Mosaic,  mosaicscience.com

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