Human hibernation: Secrets behind the big sleep

2014-05-07 13:32:07

Frank Swain

The extreme survival tricks of hibernating animals and the occasional human

could help us overcome life-threatening injuries, as Frank Swain discovers.

Imagine it: you have been rushed into the emergency room and you are dying.

Your injuries are too severe for the surgeons to repair in time. Your blood

haemorrhages unseen from ruptured vessels. The loss of blood is starving your

organs of vital nutrients and oxygen. You are entering cardiac arrest.

But this is not the end. A decision is made: tubes are connected, machines whir

into life, pumps shuffle back and forth. Ice-cold fluid flows through your

veins, chilling them. Eventually, your heart stops beating, your lungs no

longer draw breath. Your frigid body remains there, balanced on the knife-edge

of life and death, neither fully one nor the other, as if frozen in time.

The surgeons continue their work, clamping, suturing, repairing. Then the pumps

stir into life, coursing warm blood back into your body. You will be

resuscitated. And, if all goes well, you will live.

Suspended animation, the ability to set a person s biological processes on

hold, has long been a staple of science fiction. Interest in the field

blossomed in the 1950s as a direct consequence of the space race. Nasa poured

money into biological research to see if humans might be placed in a state of

artificial preservation. In this state, it was hoped, astronauts could be

protected from the dangerous cosmic rays zapping through space. Sleeping your

way to the stars also meant carrying far less food, water and oxygen, making

the ultimate long-haul flight more practical.

There has long been interest in whether suspended animation could allow

astronauts to survive missions to Mars and beyond (Science Photo Library).

One recipient of that funding was a young James Lovelock. The scientist would

dunk hamsters into ice baths until their bodies froze. Once he could no longer

detect a heartbeat, he would reanimate them by placing a hot teaspoon against

their chest (in later experiments, Lovelock warmed to the space-age theme by

building a microwave gun out of spare radio parts to more gently revive his

test subjects). These experiments on the flexibility of life would set him on

the path to his most famous work, the Gaia hypothesis of the world as a

living super-organism.

Adventurous as they were, these early experiments did not progress beyond the

animal stage, and astronauts were never frozen and revived with hot spoons. The

idea of transforming people into inanimate bars of flesh for long-distance

space travel remained in the realm of science fiction. Nasa s interest tailed

off with the end of the space race, but the seeds planted by Lovelock and his

colleagues continued to grow.

Cold storage

In 1900, the British Medical Journal published an account of Russian peasants

who, the author claimed, were able to hibernate. Existing in a state

approaching chronic famine , residents of the north-eastern Pskov region would

retreat indoors at the first sign of snow, and there gather around the stove

and fall into a deep slumber they called lotska . Waking once a day to wash

some hard bread down with water, the family took it in turns to watch the fire,

only rousing themselves fully once spring had broken. No trace of the sleepy

peasants of Pskov has ever emerged since, but the fantasy of human hibernation

persists, and very occasionally, something that looks very similar to it

crosses into reality.

A century later, Anna Bagenholm was on a skiing holiday in Norway when she

crashed head first into a frozen stream and became trapped under the ice. When

rescuers finally arrived, the Swedish radiologist had been submerged for 80

minutes, and her heart and breathing had stopped. Doctors at Tromso University

Hospital recorded a body temperature of 13.7C, the lowest ever observed in a

victim of accidental hypothermia. By all accounts she appeared to have drowned.

And yet, after careful rewarming and ten days spent in intensive care,

Bagenholm woke up. She went on to recover almost fully from her cold brush with

death. Under normal circumstances, even a few minutes trapped underwater would

be enough to drown a person, and yet Bagenholm had survived for over an hour.

Somehow the cold had preserved her.

It s not the first time the benefits of cold for traumatic injury have been

made apparent. As far back as the Napoleonic era, medics noted that wounded

infantrymen left out in the cold had better survival rates than the wounded

officers kept close to the fire in warmed tents. Therapeutic hypothermia is now

commonly used in hospitals to reduce injury in a wide variety of situations,

from surgery to helping infants recuperate following difficult births.

Lowering your body temperature slows your metabolic activity, about 5 7% for

every degree dropped. This in turn reduces the rate at which you consume

essential nutrients such as oxygen. Tissues that might become starved of oxygen

due to blood loss or cardiac arrest are thus protected. In theory, if we were

to keep reducing your temperature, eventually your biological processes would

come to a standstill. You would exist in a state of suspended animation. Like a

stopped clock, there d be nothing physically wrong with you all the

components inside would still be intact, simply stationary. All it would take

would be a little heat to set you in motion again.

Of course, it s not that simple. Hypothermia is dangerous. Your body wants to

be warm and will fight to remain that way. Throughout your life, it will

maintain a fairly constant temperature of around 37C. This requires great

effort. Your body must perform countless constant adjustments to balance heat

production with heat lost to the environment, working to keep your temperature

within a narrow band. If it drops too low, your blood is shunted away from the

exposed skin and gathers in your central torso while you shiver and huddle

under blankets. The effects of more severe cold are disastrous. At a body

temperature of around 33C just four degrees below normal your heartbeat

begins to flutter. At 25C, there s a risk it will stop altogether. And even if

you survive hypothermia, warming you up again can cause extensive kidney

damage.

Arctic ground squirrels make sure their bodily fluids don t freeze solid during

hibernation (Science Photo Library)

There are, however, certain species of animal that can endure far greater

spells of cold. The Arctic ground squirrel normally maintains a body

temperature similar to our own. But during hibernation, it can survive a core

temperature as low as 3C, carefully managing its super-cooled bodily fluids so

that it won t freeze solid. And Lovelock s hamsters could survive hypothermic

depths that would kill us. How animals survive these states is of great

interest to anyone hoping to unlock the secrets of suspended animation for

humans.

Staying alive

When is your comrade dead? asks Professor Rob Henning with a grin, quoting an

Army handbook he received as one of the Netherlands last draft of conscripts.

One: Is he rotting? Two: Is his head more than twenty centimetres from his

body? Like Lovelock, Henning has conducted experiments with hibernators that

have given him a flexible view of what constitutes being alive.

From the top floor of the Department of Clinical Pharmacy and Pharmacology at

the University Medical Centre Groningen (UMCG), a large window looks down on

the medieval city spread over a pancake-flat landscape. Below is a bustling

hospital, the region s hub for transplant surgery. It s also where Henning and

his team are uncovering the secrets of hibernation.

What we re doing here is biomimicry, says Henning, using these great

adaptations in nature to hijack them for the benefit of medicine.

Many animals can slow their metabolism to enter low-energy states: insects,

amphibians, mammals, birds and fish. In short periods, this condition

characterised by reduced body temperature and inactivity is known as torpor.

By stringing together many of these short sessions of torpor, animals can enter

the long-term dormancy we call hibernation. With this technique, small animals

such as mice, hamsters and bats can last out the cold famines of winter huddled

away, conserving energy.

Trained as an anaesthetist, Henning started hobbying in hibernation in the

1990s, but things took off in earnest when his research group was formed around

six years ago. If you think about hibernators, you have a lot of applications.

The most obvious ones are any type of major surgery, he explains. Blood loss

is the major cause of death during surgery, but in their hypothermic state,

hibernators can survive far worse injuries than they can at normal body

temperatures. This is partly because tissues are protected at low metabolic

rates, and partly because the heart is pumping blood at a fraction of the rate

it usually does.

A dormouse in torpor. It will spend up to three quarters of its life asleep,

hibernating (Science Photo Library)

But a resistance to cold and blood loss isn t the total sum of hibernators

incredible endurance. Although it resembles a very long lie-in, hibernating is

not a simple matter of sleeping through the cold. It s a gruelling marathon of

hypothermia, starvation and disease susceptibility. To endure these sufferings,

the animals that practice it have developed a suite of adaptations to protect

mind and body.

Before a long hibernation, animals eat their way into obesity, essentially

becoming type 2 diabetic. Unlike in humans, this does not result in the

thickening of artery walls that leads to heart disease. Some species will stop

eating two or three weeks before hibernation, suddenly resistant to the pangs

of hunger even while maintaining their regular level of activity.

While a human can lie in bed for a week before muscles begin to atrophy and

blood clots form, hibernators will endure months without moving. During

hibernation, the microbiome the community of bacteria living in an animal s

digestive tract is battered by cold and the sudden lack of food. Hibernators

lungs become covered with a thick deposit of mucus and collagen like those seen

in people with asthma, and their brains show changes that resemble those of

early-stage Alzheimer s. Some species lose memory during hibernation. Most

surprising of all, some show symptoms of sleep deprivation when they finally

wake. And yet, hibernators are able to counter all of these issues to bounce

back in spring, often without any long-term ill effects.

Thicker than water

UMCG is a half-kilometre complex of buildings so tightly huddled together that

it s possible to walk from the grand foyer at one end to the bicycle racks at

the other without stepping outside. One of these buildings is the animal

laboratory.

In a tiny room set away from the main corridor, Henning s doctoral student

Edwin de Vrij and his colleague are tending to a rat laid prone on a bed of

ice. A tangle of fine tubes and wires surrounds the animal, delivering

life-preserving fluids and carrying away precious data. A spool of paper

inching from one machine shows that from a frenetic 300 beats per minute, the

rat s heart rate has slowed to just 60. The red numbers glowing on another show

that the rat s internal temperature has dropped more than 20 degrees to 15C.

Clicking like a metronome, a ventilator delivers steady breaths to the

anaesthetised rodent. As a non-hibernator like us, the rat cannot survive deep

hypothermia without medical assistance. If you cool them down, nerve impulses

will be slower, and muscles have a harder time in the cold, so it s quite

physiological that they have a harder time breathing, explains de Vrij. This

isn t the case for true hibernators or some other non-hibernating mammals,

for that matter. Somehow hamsters can maintain adequate breathing, he says.

We don t have to ventilate them.

As well as inducing hibernation in hamsters (a process that takes weeks of

gradual adjustment in climate-controlled rooms to mimic the onset of winter),

the UMCG team also induce forced hypothermia states like that of our rat,

chilling the animals rapidly until they fall into a state of metabolic

suspension.

Today, de Vrij is searching for platelets, which are essential for blood

clotting to prevent bleeding. Hibernating animals avoid getting blood clots

despite their lack of activity, an ability that comes down partly to a curious

change in the hypothermic body: as they cool, platelets disappear from the

blood. Nobody yet knows where they go, but their prompt reappearance on

rewarming has de Vrij convinced that they are preserved somewhere in the body,

rather than being absorbed and later resynthesised. Surprisingly, this change

also happens even in non-hibernators, including rats and occasionally human

victims of hypothermia.

Platetets (pink) are vital for blood clotting, and could play a key role in

helping animals survive during hibernation (Science Photo Library)

The shared characteristics of different hibernators mean it s likely that these

species have inherited fragments of protective mechanisms against cold,

inactivity, starvation and asphyxiation from common ancestors and developed

these into a comprehensive low-metabolic syndrome. There are even hints that we

humans might, to some extent, retain some of these abilities. For a long time,

there was no evidence that primates could hibernate. But in 2004, a species of

Madagascan lemur was shown to practice regular bouts of torpor. If you look at

the lemur and look at us, we share about 98% of our genes, says Henning. It

would be very strange if the tools of hibernation were all packed into that 2%

difference.

As their body temperature drops, hibernators also remove the lymphocytes (white

blood cells) from their blood and store them in the lymph nodes. And within 90

minutes of awakening, these reappear. This damping down of the immune system

prevents a general inflammation in the body during rewarming the very thing

that would cause humans and other non-hibernators to suffer kidney damage.

However, it s a risky strategy, leaving animals unable to mount an immune

defence while hibernating. The fungus responsible for white-nose syndrome,

currently wiping out bat colonies in the USA, takes advantage of this

vulnerability, infecting the bats while they are dormant. In response, the bats

frequently exit hibernation and rewarm to fight off the pathogen the

high-energy cost of these interruptions ultimately killing them.

Funny smell

Knowing how hibernators control these changes in their blood could have

immediate and far-reaching benefits for us. As well as improving our ability to

survive hypothermia and cold suspended-animation states, stripping the blood of

white blood cells could prevent the aseptic sepsis caused by heart lung

machines, in which activation of blood cells as they pass through the

life-support equipment triggers a body-wide immunological reaction. Transplant

organs, often chilled for transport, would also benefit from better

cryoprotection. And we could increase the shelf-life of our blood stocks we

still haven t figured out how to store donated blood platelets at low

temperatures, so blood donations can only be kept a week before they must be

used or thrown away due to the risk of bacterial infection.

The UMCG team took a giant leap towards achieving these goals quite by accident

after a student left a culture of hamster cells in a fridge at 5C. After a week

the hamster cells were still alive, and smelling of rotten eggs. The student

poured the medium surrounding the cells over a separate batch of cells from a

rat, suspecting the smelly cells might have secreted some kind of protective

agent. She placed them in the same fridge and waited. Normally, refrigerating

rat cells would quickly kill them, but after two days they were still alive.

The team is investigating several compounds that might be responsible for this

cryopreservation. One is an enzyme known as cystathionine beta synthase (CBS),

which stimulates the production of hydrogen sulphide, the molecule that gives

rotten eggs their characteristic whiff. If hamsters are injected with a

chemical to inhibit CBS, they can no longer enter torpor, and those that were

forced into hypothermic states suffered the kind of kidney damage one would

expect in non-hibernators like us.

Of over a hundred compounds Henning s team has investigated, many had no

effect, but a few did, conferring long-term cold protection to cell samples.

The team has already patented one of these compounds, Rokepie, as an additive.

This would allow cells that normally need to be kept at 37C, such as those from

humans or mice, to be stored in the refrigerator, either for transport or so

experiments can be put on hold during weekends and busy periods.

The leading cryopreservation molecules extracted from hibernators are

incredibly potent, and it seems they work by eliciting changes in the cells

themselves whether these are from hibernators or not. If so, this offers

further evidence that we still possess some tools that could help endure

hypothermia and low metabolic states.

For now, applying the lessons they ve learned from hibernators wholesale onto

humans is not within the remit of Henning s group. The space race is long over,

and Nasa is not awarding major grants to develop suspended animation. However,

the US Army is.

Golden hour

If you look anywhere near a trauma bay, things are pretty chaotic, says

Professor Sam Tisherman. It s controlled chaos, but the chaos mainly comes

from the fact you never know what s going on with the patient.

In frenetic hospital emergency wards, it s often not possible for doctors to

identify the problem, fix it and keep the patient alive all at the same time.

Patients suffering uncontrolled blood loss, for example, may go into cardiac

arrest. When this happens, surgeons must fight the clock to stop the bleeding

before they can start resuscitation efforts. Somebody rolls in and they re

basically dying, says Tisherman. We re quickly trying to resuscitate them,

and figure out what s wrong with them, and repair injuries all at the same

time. This is the fundamental underpinning of trauma medicine: you are always

against the clock.

Tisherman wants to buy doctors a little more time. He believes that by inducing

hypothermia we can extend the golden hour in which surgeons battle to save

the lives of critically injured patients. To do this, he s pushing human

endurance of hypothermia far beyond its normal limits.

After graduating from MIT in 1981, Tisherman built a career in critical care

medicine. He won a Lifetime Achievement Award in Trauma Resuscitation Science

from the American Heart Association in 2009, and is now an Associate Director

of the Safar Center for Resuscitation Research in Pittsburgh. It was founded by

Peter Safar, the Austrian physician who popularised the kiss of life , CPR,

and drove the creation of the Resusci Anne doll used in teaching it. At

Pittsburgh, Safar created the world s first intensive care training programme.

His lifelong aim was to save the hearts and brains of those too young to die.

The procedure that Tisherman is pioneering is called emergency preservation and

resuscitation. His work is supported through the US Army s Telemedicine and

Advanced Technology Research Center, which funds research on topics as niche as

advanced prosthetics and robots to carry wounded soldiers out of the

battlefield.

Some of his surgeons will already be familiar with hypothermic techniques,

having routinely chilled patients to the low 30s or high 20s. For procedures

that require zero blood flow, cardiac surgeons will even cool patients to

around 15C, the point at which their heart stops.

Surgeons performing a cardiac operation using hypothermic protection of the

patient in Russia in 1979 (Science Photo Library)

Tisherman is planning to cool patients to this point, and perhaps even further,

chilling them to such a degree that the entire body enters a kind of suspended

animation. During this time, they will have no heartbeat, no breathing and no

discernible brain activity. In fact, they ll have no blood, either it will be

drained and replaced with ice-cold saline, the only way to cool a human fast

enough to avoid tissues becoming damaged as they struggle to remain

functioning. Tisherman calls this state hypothermic preservation .

The procedure has already been demonstrated successfully in the lab, reviving

dogs that had lain suspended in cold states for up to three hours. Trials are

now moving to a clinical setting. Surgeons, anaesthetists and perfusionists at

Massachusetts General Hospital have even undergone training for the pioneering

surgery. But no one knows when a suitable patient will arrive through the

doors. That is in fact one of the issues they face: by the nature of trauma,

patients won t be able to give informed consent for the procedure. Because of

this, Tisherman s group has engaged in a wide community consultation to let

citizens in the area know the programme was going on. The study had to be

signed off personally by the Secretary of the Army, the highest-ranking

civilian official in the organisation.

Beyond that lie further obstacles. Amid the frantic activity of the emergency

room, Tisherman must make sure that a team of trauma surgeons can work in

concert with cardiac surgeons and perfusionists armed with pumps and bags of

chilled saline, an additional layer of complexity in an already chaotic

environment. And although cooling affects all tissues equally, it is not

without secondary effects. The blood factors responsible for clotting are also

inhibited by the cold. This creates problems controlling bleeding during the

rewarming phase. The surgeons, too, will suffer from the cold, as both the

patient and the room itself will be chilled during the procedure. Yet the cold

is only a tool; the end goal is metabolic suspension.

In the future, emergency preservation and resuscitation could be extended to

those suffering heart attacks or exposure to poisons, or any critical care

situation where time is a factor. Cooling is the most powerful way of

suppressing metabolism we have, says Tisherman, If we can either decrease the

needs of the tissues or improve oxygen delivery to the tissues then everything

will be okay.

Although animals in the laboratory were able to recover from three hours in

this suspended state, the first human patients to experience it will only be

put under for a third of that. An hour should be enough to repair the

bleeding, Tisherman says. The cooling period doesn t necessarily have to

cover the entire surgery. For those wanting to travel to distant stars, going

beyond that hour is, sadly, out of the question for now. We re not trying to

freeze the dead, Tisherman chuckles, just buy enough time to save the living.