Their hearts are still beating. They urinate. Their bodies don’t decompose and they are warm to the touch; their stomachs rumble, their wounds heal and their guts can digest food. They can have heart attacks, catch a fever and suffer from bedsores. They can blush and sweat – they can even have babies.
And yet, according to most legal definitions and the vast majority of doctors these patients are thoroughly, indisputably deceased.
These are the beating heart cadavers; brain-dead corpses with functioning organs and a pulse. Their medical costs are astronomical (up to $217,784 for just a few weeks), but with a bit of luck and a lot of help, today it’s possible for the body to survive for months – or in rare cases, decades – even though it’s technically dead. How is this possible? Why does this happen? And how do doctors know they’re really dead?
Identifying the dead has never been easy. In 19th Century France there were 30 theories about how to tell if someone had passed away – including attaching pincers to their nipples and putting leeches in their bottom. Elsewhere, the most reliable methods included yelling a patient’s name (if the patient ignored them three times, they were dead) or thrusting mirrors under their noses to see if they fogged up.
Early attempts to test for signs of life included attaching pincers to nipples (Credit: Getty Images)
Suffice to say, the medical establishment wasn’t convinced about any of them. Then in 1846, the Academy of Sciences in Paris launched a competition for “'the best work on the signs of death and the means of preventing premature burials” and a young doctor tried his luck. Eugène Bouchut figured that if a person’s heart had stopped beating, they were surely dead. He suggested using the newly invented stethoscope to listen for a heartbeat – if the doctor didn’t hear anything for two minutes, they could be safely buried.
He won the competition and his definition of “clinical death” stuck, eventually to be immortalised in films, books and popular wisdom. “There wasn’t much that could be done, so basically anyone could look at a person, check for a pulse and decide whether they were dead or alive,” says Robert Veatch from the Kennedy Institute of Ethics.
But a chance discovery in the 1920s made things decidedly messier. An electrical engineer from Brooklyn, New York, had been investigating why people die after they’ve been electrocuted – and wondered if the right voltage might also jolt them back to life. William Kouwenhoven devoted the next 50 years to finding a way to make it happen, work which eventually led to the invention of the defibrillator.
The loss of heart beat was once considered a sign of death, but we now know this need not be the end (Credit: Getty Images)
It was the first of a deluge of revolutionary new techniques, including mechanical ventilators and feeding tubes, catheters and dialysis machines. For the first time, you could lack certain bodily functions and still be alive. Our understanding of death was becoming unstuck.
The invention of the EEG – which can be used to identify brain activity – dealt the final blow. Starting in the 1950s, doctors across the globe began discovering that some of their patients, who they had previously considered only comatose, in fact had no brain activity at all. In France the mysterious phenomenon was termed coma dépasse, meaning literally “a state beyond coma”. They had discovered the ‘beating-heart cadavers’, people whose bodies were alive though their brains were dead.
This was an entirely new category of patient, one which overturned 5,000 years of medical understanding in a single sweep, raising new questions about how death is identified and dredging up some thorny philosophical, ethical and legal issues to boot.
“It goes back and forth as to what people call them but I think patient is the correct term,” says Eelco Wijdicks, a neurologist from Rochester, Minnesota.
Beating heart cadavers should not be confused with coma patients or those in a vegetative state (Credit: Science Photo Library)
These beating heart cadavers should not be confused with other kinds of unconscious patients, such as those in a coma. Though they aren’t able to sit up and respond to the sound of their name, they still show brain activity, undergoing cycles of sleep and (unresponsive) wakefulness. A patient in a coma has the potential to make a full recovery.
A persistent vegetative state is decidedly more serious – in these patients the higher brain is permanently, irretrievably damaged – but though they will never have another conscious thought, again, they are not dead.
To qualify as a beating heart cadaver, the entire brain must be dead. This includes the “brain stem”, the primitive, tube-shaped mass at the bottom of the brain which controls critical bodily functions, such as breathing. But, somewhat disconcertingly, our other organs aren’t as troubled by the death of their HQ as you’d think.
Alan Shewmon, a neurologist from UCLA and outspoken critic of the brain death definition, identified 175 cases where people’s bodies survived for more than a week after the person had died. In some cases, their hearts kept beating and their organs kept functioning for a further 14 years – for one cadaver, this strange afterlife lasted two decades.
How is this possible?
In fact, biologically speaking, there has never been a single moment of death; each passing is really a series of mini-deaths, with different tissues dropping off at different rates. “Choosing a definition of death is essentially a religious or philosophical question,” says Veatch.
The brain uses up 25% of our body's oxygen, meaning it is the first organ to die after we stop breathing (Credit: Getty Images)
For centuries, soldiers, butchers and executioners have observed how certain body parts may continue twitching after decapitation or dismemberment. Even long before life support, 19th Century physicians related accounts of patients whose hearts had continued to beat for several hours after they stopped breathing.
At times, this slow decline can have alarming consequences. One example is the Lazarus sign, an automatic reflex first reported in 1984. The reflex causes the dead to sit up, briefly raise their arms and drop them, crossed, onto their chests. It happens because while most reflexes are mediated by the brain, some are overseen by “reflex arcs”, which travel through the spine instead. In addition to the Lazarus reflex, corpses also have the knee-jerk reflex intact.
Further along the life-death continuum, skin and brain stem cells are known to remain alive for several days after a person has died. Living muscle stem cells have been found in corpses which are two-and-a-half-weeks old.
Even our genes keep going long after we’ve taken our last breath. Earlier this year, scientists discovered thousands which spring to life days after death, including those involved in inflammation, counteracting stress and – mysteriously – embryonic development.
Beating heart cadavers can only exist because of this lopsided decline – it’s all dependent on the brain dying first. To get to grips with why this happens, consider this. Though the brain makes up just 2% of a person’s body weight, it sucks up a staggering 25% of all its oxygen.
Neurons are so high-maintenance in part because they are active all the time. They are constantly pumping out ions to create miniature electrical gradients between their insides and the surrounding environment; to fire, they simply open up the floodgates and let the ions flow back in.
The trouble is, they can’t stop pumping. If their efforts are stalled by a lack of oxygen, neurons are rapidly inundated with ions which build to toxic levels, causing irreversible damage. This “ischaemic cascade” explains why if you accidentally lop off a finger, it can usually be sewn back on, but most people can’t hold their breath for more than a few minutes without fainting.
Doctors now follow standard procedures to test for lingering signs of life (Credit: Science Photo Library)
Which brings us back to that perennial medical problem: if your heart’s still beating, how can doctors tell you’re dead? To begin with, doctors identified victims of coma dépasse by checking for the absence of brain activity on an EEG. But there was a problem.
Colleen Burns woke up just as doctors were about to remove her organs
Alarmingly, alcohol, anaesthesia, some illnesses (such as hypothermia) and many drugs (including Valium) can shut down brain activity, conning doctors into thinking their patient is dead. In 2009, Colleen Burns was found in a drug-induced coma and doctors at a hospital in New York thought she was dead. She woke up in the operating room the day before doctors were due to remove her organs (NB: it’s unlikely this would have gone ahead, because her doctors had planned additional tests before the surgery).
Several decades earlier in 1968, a group of esteemed Harvard doctors called an emergency meeting to discuss exactly this. Over the course of several months, they devised a set of foolproof criteria which would allow doctors to avoid such blunders and establish that beating heart cadavers were definitely dead.
The tests remain the global standard today, though some of them look uncannily like those from the 19th Century. For a start, a patient should be “unresponsive to verbal stimuli”, such as yelling their name. And though leeches and nipple pincers are out, they should remain unresponsive despite numerous uncomfortable procedures, including injecting ice-cold water into one of their ears – a technique which aims to trigger an automatic reflex and make the eyes move. This particular test is so valuable it won its discoverer a Nobel Prize.
Finally, the patient shouldn’t be able to breathe on their own, since this is a sure sign that their primitive brain is still going. In the case of Burns, the horrifying incident was only possible because her doctors ignored tell-tale signs that she was alive; she curled her toes when they were touched, moved her mouth and tongue and was breathing independently, though she was hooked up to a respirator. Had they followed the Harvard criteria correctly, they would never have declared her dead.
Cadaver donor management
You might expect all medical treatment to stop after someone is considered dead – even if they are a beating heart cadaver – but that’s not quite true. Today beating heart cadavers have spawned a strange new medical specialty, “cadaver donor management”, which aims to improve the success of transplants by tending to the health of the dead. The aim of the game is to fool the body into thinking everything is fine until recipients are lined up and their surgeons are ready.
In all, nearly twice as many viable organs – around 3.9 per cadaver– are retrieved from these donors compared to those without a pulse and they’re currently the only reliable source of hearts for transplant.
Beating heart cadavers may be given sophisticated treatments to preserve the organs for donation (Credit: Science Photo Library)
Intriguingly, the part of the brain that the body misses most is not its primitive stem or, as we’d like to think, the wrinkled seat of human consciousness (the cortex), but the hypothalamus. The almond-shaped structure monitors levels of important hormones, including those which regulate a person’s blood pressure, appetite, circadian rhythms, sugar levels, fluid balance and energy expenditure – then makes them, or instructs the pituitary gland to do so.
Instead the hormones must be provided by intensive care teams, who add just enough to an intravenous drip as and when they are needed. “It’s not just a case of putting them on a ventilator and giving them some food – it’s far more than that,” says Wijdicks.
Once the consent forms have been signed, dead patients receive the best medical care of their lives
Of course, not everyone is comfortable with the idea. To some, organ donor management reduces human beings to mere collections of organs to be stripped for parts. As journalist Dick Teresi cynically put it, once the consent forms have been signed, dead patients receive the best medical care of their lives.
These interventions are only possible because the Harvard tests promise to sort the dead and the living into neat boxes – but alas, yet again death is messier than we’d like to think. In a review of 611 patients diagnosed as brain dead using their criteria, scientists found brain activity in 23%. In another study, 4% had sleep-like patterns of activity for up to a week after they had died. Others have reported beating heart cadavers flinching under the surgeon’s knife and there have even been suggestions that they should be given an anaesthetic – though this is controversial.
The exact definition of death depends on our culture and religion (Credit: Getty Images)
To inject further controversy into the mix, some people don’t even agree with the definition in principle, let alone in practice. In the United States, many Orthodox Jews, some Roman Catholics and certain ethnic minorities – in total, around 20% of the population – like their dead with a flat-lining heart rate and cold to the touch. “There’s this group of people who quite militantly are offended when a doctor tries to pronounce death on someone that the family thinks are still alive,” says Veatch.
“Even with clinical death, there are disputes – for instance about how long it’s necessary for circulation to be lost before it’s impossible for it to be restored. We use five minutes in the US but there isn’t really good evidence that that’s the right number,” says Veatch.
At the heart of many legal struggles is the right to choose your own definition of death and when life support should be removed, issues Veatch is particularly passionate about. “I have consistently supported individuals who would insist on a circulatory definition, though that’s not the one I would use,” he says.
Where it gets particularly sticky is if the victim is pregnant. In these cases, the patient’s family have a heart-breaking choice to make. They can either accept that they’ve lost her unborn baby, or begin the intensive and often gruesome battle to keep her going long enough to deliver, which is usually when the foetus is about 24-weeks-old.
Back in 2013, Marlise Munoz was found unconscious at her home in Texas. Her doctors suspected that she had suffered a pulmonary embolism and discovered that she was 14 weeks pregnant. Two days later she was declared dead. Munoz was a paramedic and had previously told her husband that in case of brain death, she would not want to be kept alive artificially. He petitioned to have her life support removed – but the hospital refused.
A beating heart cadaver may still be able to sustain a growing foetus (Credit: Science Photo Library)
“In Texas there’s an automatic invalidation of a pregnant woman’s advanced directive. If she wanted them to withdraw life-sustaining treatment, then when she died that would not be allowed – that would be ripped up. She would be provided life-sustaining treatment,” says Christopher Burkle, an anaesthetist from Rochester, Minnesota who co-authored a paper on the subject with Wijdicks.
The circumstances are extremely rare, with only about 30 reported cases between 1982 and 2010, but the tug-of-war between the interests of the mother and those of her unborn baby begs the question: which human rights should we retain when we’re dead?
“In the US a dead patient still has rights to the protection of their medical information, for example. You can’t publish their medical record on the 6 o’clock news – a person who is dead has privacy rights in that respect. It’s not a huge jump to suggest that rights be maintained in other avenues for a dead person,” says Burkle.
And things may be about to get a lot more complicated. At the moment, doctors are bound by the “dead donor rule”, which asserts that no organs can be removed until a person is dead – that is, totally brain-dead or with a heart which has already stopped beating. But some people, including Veatch, think this should change.
They have proposed the “higher brain” definition, which means a person isn’t dead when their heart stops beating, or even when they stop breathing – a person is dead when they lose their “personhood”. Those with crucial parts of their brains intact and the ability to breathe independently would be dead so long as they could no longer have conscious thoughts.
By loosening up the definition a little further, transplant doctors would have access to a much larger pool of potential donors than they do at the moment and save countless lives.
Death isn’t an event, it’s a process – but after thousands of years of trying, we’re still searching for something more definitive. It doesn’t look like this is about to end any time soon.
Join 700,000+ Future fans by liking us on Facebook, or follow us on Twitter, Google+, LinkedIn and Instagram.
If you liked this story, sign up for the weekly bbc.com features newsletter, called “If You Only Read 6 Things This Week”. A handpicked selection of stories from BBC Future, Earth, Culture, Capital, Travel and Autos, delivered to your inbox every Friday.