Lazarus syndrome man pronounced dead comes back to life for two days

A man came back to life - like the Biblical Lazarus - half an hour after doctors told
his family he had died.
Michael Wilkinson, 23, 'died' in hospital of a previously undiagnosed heart
condition after his mother found him collapsed in bed.
Doctors failed to revive the roofer and pronounced him dead, and he was given the
last rites.
But 30 minutes later medics found a pulse and told relatives he was actually alive.
Lazarus syndrome: Michael Wilkinson died of a previously undiagnosed heart
condition. But 30 minutes after he was pronounced dead, medics found a pulse
Mr Wilkinson, from Preston, was transferred to the intensive care unit at Royal
Preston Hospital in Lancashire where he survived for two days following an
emergency operation. He then died on February 3rd this year.
An inquest heard that his return to life was known as Lazarus syndrome - the
spontaneous return of circulation after attempts to resuscitate fail. There have only
ever been 38 cases recorded worldwide.
The syndrome takes its name from the biblical story of Lazarus, who was raised
from the dead by Jesus.
At time of Mr Wilkinson's death, his mother Susan Horrigan, 44, said: 'It was as if
he had been taken away from me, then given back only to be taken away again.'
John Whittaker, A&E consultant, told the inquest at Preston Magistrates Court:
'When we pronounce him dead that is not a small thing, you make absolutely
certain.
'The decision to pronounce him dead was because we had worked on him for 15
minutes and come to the end of what we could do.
'There is a phenomenon known as Lazarus syndrome. It is incredibly rare. There
have only been 38 cases of this ever in the world.'
He said Michael's pulse restarting was probably due to the drugs he had been
given.
Assistant Dept Coroner Derek Baker, addressing Mrs Horrigan, said: 'You received
this tragic news Michael had died then prepared yourself to deal with this tragedy.
'Then you were told a pulse had been found. How long after was that? One hour,
two hours?'
She replied: 'About half an hour.'
The inquest heard Mr Wilkinson died of cardiac arrest leading to organ failure. The
coroner recorded a verdict of death by natural causes.
A post-mortem examination carried out at the Royal Blackburn Hospital found he
had an undiagnosed heart condition, in which his left ventricle had become
abnormally thickened.
Mr Wilkinson had been drinking with his family in Preston the evening before he
was found collapsed but tests showed alcohol was not a factor in his death. They
also ruled out drug use or any physical trauma.
Speaking after the inquest, Mr Wilkinson's grandmother Carole Bolton, 66, said:
'He was lovely, people used to say he was a good-hearted lad.
'He was good-hearted and it was his heart that took him. We would like to thank
staff at the Royal Preston Hospital. They could not have done more.'
 'Dead' Brazilian boy 'sits up in coffin at his own funeral and asks for WATER
before lying back down lifeless'
 Kelvin Santos stopped breathing during treatment for pneumonia and was
declared dead on Friday
 On Saturday he allegedly sat up in his coffin and asked his father for a glass
of water
 A two-year-old boy sat up in his coffin and asked for water before laying
back down again lifeless, according to a Brazilian news website.
 In a case that seems almost too incredible to be true, ORM claimed that
Kelvin Santos stopped breathing during treatment for pneumonia at a
hospital in Belem, northern Brazil.
 He was declared dead at 7.40pm on Friday and his body was handed over
to his family in a plastic bag.
 Two-year-old Kelvin Santos was declared dead on Friday after he stopped
breathing during treatment for pneumonia
 The child's devastated family took him home where grieving relatives held a
wake throughout the night, with the boy's body laid in an open coffin.
 But an hour before his funeral was due to take place on Saturday the boy
apparently sat up in his coffin and said: 'Daddy, can I have some water?'.
 The boy's father, Antonio Santos, said: 'Everybody started to scream, we
couldn't believe our eyes. Then we thought a miracle had taken place and
our boy had come back to life.
 'Then Kelvin just laid back down, the way he was. We couldn't wake him. He
was dead again.
 Mr Santos rushed his son back to the Aberlardo Santos hospital in
Belem,where the doctors reexamined the boy and confirmed that he had no
signs of life.
 He said: 'They assured me that he really was dead and gave me no
explanation for what we had just seen and heard.'
 The boy's family decided to delay the funeral for an hour in the hope that he
would wake up again, but ended up burying him at 5pm that day in a local
cemetery.
 Devastated: Kelvin's father Antonio Santos claims his son was a victim of
medical negligence
 Convinced that his son was victim of medical malpractice, Mr Santos has
now registered a complaint with the police who have launched an
investigation
 He said: 'Fifteen minutes after rushing him away for resuscitation, they came
and told me he was dead and handed me his body. Perhaps they didn't
examine him properly. Dead people don't just wake up and talk. I'm
determined to find out the truth.'
 The local state department today confirmed the boy had been admitted to
hospital in a critical condition and was declared dead after suffering cardiac-
respiratory failure.

The Lazarus phenomenon

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DEFINITION

The Lazarus phenomenon is described as delayed return of spontaneous circulation (ROSC)

after cessation of cardiopulmonary resuscitation (CPR). This was first reported in the
medical literature in 1982, and the term Lazarus phenomenon was first used by Bray in
1993.1,2 The term was coined from the story of Lazarus, who was resurrected by Christ four
days after his death.

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METHODS

Literature Review

We searched Medline, Pubmed and Google Scholar using the words ‘Lazarus
phenomenon’, ‘cardiopulmonary resuscitation’ and ‘spontaneous return of circulation’.
Even though we retrieved more articles from Google Scholar than Medline or Pubmed, we
had to screen a large number of articles (more than 14,000) to select the appropriate ones.
We scrutinized all the articles to identify cases where cessation of CPR was followed by
spontaneous return of circulation.

So far 38 cases of delayed ROSC have been published in the medical literature.1-28 The
majority of the articles appeared in the anaesthetic and intensive care journals. Cases
described include both in-hospital and out-of-hospital arrests. We collected information on
diagnoses at the time of arrest, duration of CPR, cardiac rhythm when CPR was stopped
and time taken for ROSC, and the final outcome (Table 1).

Diagnoses at the time of cardiac arrest

Of the 38 cases described, 13 had myocardial infarction and eight had obstructive airways
disease. Other diagnoses include ruptured abdominal aortic aneurysm, pulmonary artery
rupture, gastrointestinal haemorrhage, hyperkalaemia due to renal failure, trauma, digoxin
toxicity, sepsis and overdose with opiates and cocaine.

Resuscitation details

The duration of CPR ranged from 6-75 minutes, with an average duration of 27 minutes.
The duration of CPR was not documented in seven patients. When CPR was stopped, 23
patients were in asystole, 12 were in pulseless electrical activity and one was in ventricular
fibrillation, and the rhythm was not known in two patients (not mentioned in the reports).

Time to return of spontaneous circulation

ROSC occurred within 10 minutes of stopping CPR in 82% of cases (23 out of 28 patients),
with a mean delay of 7-8 minutes. The time taken for ROSC is unknown in 10 patients.
Three of these patients were only found to be alive (one in the mortuary) after being left
unattended for several minutes, and in seven the data was unavailable from the case
reports.2,5,9,12,18,28 However, the time interval could only be an approximation because
patients were not always closely monitored following termination of CPR, with a few
exceptions.16

Outcome

Seventeen patients (45%) achieved good neurological recovery following ROSC. Three of
these patients subsequently died during their hospital stay due to sepsis and pulmonary
embolism and 14 (35%) were eventually discharged home with no significant neurological
sequelae.

Seventeen patients (45%) did not achieve neurological recovery following ROSC and died
soon after. The outcome is not known in four patients (10%). There was no significant
correlation between the outcome and duration of CPR, time interval for ROSC or the
diagnosis.

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PROPOSED MECHANISMS

The exact mechanism of delayed ROSC is unclear and it is possible that more than one
mechanism is involved. Dynamic hyperinflation of the lung causing increased positive end
expiratory pressure (PPEP) is one of the proposed mechanisms, which has some supporting
evidence in patients with obstructive airways disease.

Positive end expiratory pressure

Rapid manual ventilation without adequate time for exhalation during CPR can lead to
dynamic hyperinflation of lungs. Dynamic hyperinflation may lead to gas trapping and an
increase in the end-expiratory pressure (called auto-PEEP) leading to delayed venous
return, low cardiac output and even cardiac arrest in patients with obstructive airways
disease.9,29,30
The link between mechanical ventilation of patients with obstructive ventilatory defects and
circulatory failure was first demonstrated in 1982.31 One report describes a patient with
respiratory failure due to asthma whose blood pressure was undetectable five minutes after
initiating artificial ventilation with a tidal volume of 700 mL and respiratory rate of 25
breaths per minute. Even after inotropes the systolic blood pressure did not exceed 70 mm
Hg. The ventilator was adjusted to a respiratory rate of six breaths per minute and a tidal
volume of 400 mL and the blood pressure gradually rose to 126/84 mm Hg.29

The physiology of severe auto-PEEP is similar to pericardial tamponade, where circulation

can only be restored after removing the obstacle to cardiac filling. Auto-PEEP is a possible
cause of pulseless electrical activity (PEA), and rapid ventilation during CPR should be
avoided. Hypovolaemia and decreased myocardial contractility could exaggerate its effect
on venous return and cardiac output. Some authors recommend discontinuing the
ventilation transiently for 10 to 30 seconds in PEA to allow venous return.9

It is tempting to apply this theory even to patients without obstructive airways disease.
Dynamic hyperinflation can theoretically happen in any situation where rapid manual
ventilation is carried out. One could argue that in the presence of decreased cardiac
output—as in myocardial infarction and hypovolaemia—dynamic hyperinflation could
compromise the cardiac output even more, leading to cardiac arrest.

Even though auto-PEEP due to dynamic hyperinflation seems most plausible and has some
evidence in patients with obstructive airways disease, this alone would not explain all cases
of delayed ROSC. In one report, CPR was terminated after 30 minutes and the patient was
in asystole. Because the patient had MRSA and CPR was performed without proper
infection control measures, the physician involved in the CPR went to shower and change
clothes, leaving the patient still being ventilated in the intensive care unit. Returning five
minutes later, he found the patient with a perfusable rhythm. The patient died two days
later.14

Delayed action of drugs

Some authors suggest delayed action of drugs administered during CPR as a mechanism for
delayed ROSC.8It is possible that drugs injected through a peripheral vein are inadequately
delivered centrally due to impaired venous return, and when venous return improves after
stopping the dynamic hyperinflation, delivery of drugs could contribute to return of
circulation. In some cases, however, drugs are actually administered through a central line.
Even though this theory is plausible it would be impossible to either prove or disprove.
Hyperkalaemia

There are few reports of delayed ROSC in the presence of hyperkalaemia.8,10 It is a well-
known fact that intracellular hyperkalaemia could persist longer, rendering the myocardium
retractile for long periods of time. There is a report on a 68-year-old lady with cardiac
arrest due to hyperkalaemia who did not respond to CPR and conventional treatment up to
100 minutes, but later responded to dialysis and made a complete recovery.32 So even
though prolonged cardiac arrest refractory to conventional treatment could respond to
dialysis, it is unlikely that hyperkalaemia on its own could explain delayed ROSC after
cessation of CPR.

Myocardial stunning

Prolonged myocardial dysfunction can occur following myocardial ischaemia, taking up to

several hours before normal function returns.33 Of the 38 cases, 13 had myocardial
infarction, and at least seven had hypovolaemia which could have contributed to transient
myocardial ischaemia and stunning.

Transient asystole

Asystole or PEA following countershock of prolonged VF is common and occurs in around

60% of patients.34 Even though restoration of circulation occurs in 16% of patients, the
prognosis is poor: only 0-3% are discharged alive. It is possible that asystole or PEA after
countershock could be transient before a perfusable rhythm restores circulation. Transient
asystole following defibrillation would explain at least one case, where CPR was
interrupted after a last cardioversion attempt resulting in asystole, and ROSC occurred soon
after.11 However, transient asystole would not explain delayed ROSC in majority of patients
in whom the duration of asystole was much longer. In another case, CPR was stopped while
the patient was still in ventricular fibrillation and haemodynamic activity returned few
moments later.11 The authors of the case rightly point out that CPR should not be halted in a
patient with ventricular fibrillation.

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CONSEQUENCES OF DELAYED RETURN OF SPONTANEOUS CIRCULATION

Delayed ROSC can lead to serious professional and legal consequences. Questions will be
asked about whether CPR has been conducted properly and whether it was stopped too
soon. The medical team might be accused of negligence and incompetence and even be
sued for damages if a patient survives with severe disability.26,28,35 A doctor involved in
resuscitation and certification of death followed by delayed ROSC has recently been
accused of culpable homicide.
The conduct of ALS can only be assessed from the case record, so it is vital to record the
events during cardiac arrest as accurately as possible. When to discontinue CPR is still a
medical decision and so it is absolutely essential to get a consensus from the arrest team
and to document the reason for termination of CPR. Some authors recommend
measurement of end-tidal carbon dioxide during CPR. Values above 10-15 mmHg indicate
a favourable prognosis and should preclude termination of CPR.36,37 This technology is not
widely available outside the intensive care setting, but should be considered in difficult
clinical situations. Whether this would identify patients in whom delayed ROSC might
occur is nevertheless questionable.

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HOW WOULD ONE RECOGNIZE DEATH?

It is important to realize that death is not an event, but a process. The conference of
Medical Royal Colleges in the UK advocated that death is a process during which various
organs supporting the continuation of life fail.38 Cessation of circulation and respiration is
such an example. The physical findings to support this—absence of heartbeat and
respiration—are the traditional and the most widely used criteria to certify death. Since
these findings alone are not a sign of definitive death, it is quite possible to declare death in
the interval between cessation of CPR and delayed ROSC.

Because delayed ROSC occurred within 10 minutes in most cases, many authors
recommend that patients should be passively monitored for at least 10 minutes following
unsuccessful CPR. During that period the family should be informed that CPR had been
stopped because of poor response and further efforts are not in the best interests of the
patient. It should also be mentioned that the patient is being closely monitored to establish
death beyond any doubt. Death should not be certified in any patient immediately after
stopping CPR, and one should wait at least 10 minutes, if not longer, to verify and confirm
death beyond doubt. This is in line with what was said by W H Sweet in 1978: ‘the time
honoured criteria of the stoppage of the heart beat and circulation are indicative of death
only when they persist long enough for the brain to die.’39

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NON-MEDICAL LITERATURE

Newspapers

In addition to medical literature, there are many newspaper articles, websites and a few
anecdotes in medical journals describing patients who were certified dead, but later found
to be alive (Table 2). Many of these articles refer to these incidents as ‘Lazarus
phenomenon’. There is even a movie called Lazarus phenomenondescribing two cases of
resurrection after death. However, the authenticity of one of these cases has been
questioned.
Lazarus Syndrome: Or how - as one British woman's just proved - waking
from the dead is more common than you think
The idea that we can defeat death and return to life has inspired and horrified
mankind since ancient times. Our culture is filled with tales of miraculous
resurrections — from Lazarus and Christ to Doctor Who and Harry Potter.
But it is equally riddled with horror stories of people pronounced dead who awake
buried or with crematorium flames licking at their bodies.
The Victorians were so anxious about being buried alive that undertakers sold
'safety coffins' with bell pulls, alarms and breathing pipes. Their fear — called
taphophobia — was anything but irrational. In the days before brain scans and
heart monitors, it was an all too real problem.
Unusual: Tasleem Rafiq's recovery has baffled doctors at the Royal Berkshire
Hospital in Reading, who are describing it as 'a miracle,' according to her family
In 1905, the eccentric British social reformer William Tebb documented 149 known
cases of live burials and ten of bodies waking up during dissection. So concerned
was Tebb that he founded the London Association for the Prevention of Premature
Burial, to raise public awareness.
Medical advances mean the misdiagnosis of death has become a rarity. But even
today, the dead can still return to life.
This week it emerged that Tasleem Rafiq, a mother of four from Reading, is alive
and well, even though her heart stopped for 45 minutes.
After Mrs Rafiq, 52, suffered a heart attack, medics tried to resuscitate her at
home, in the ambulance and at the Royal Berkshire Hospital with no success.
As the despairing family gathered around her body, Mrs Rafiq twitched.
This was not the involuntary movement of a corpse, which can occur following
attempts at resuscitation. Within minutes she was awake. Within a day she was
sitting up and sharing jokes.
The hospital disputes the family's account and insists they never told them she was
actually dead.
Nevertheless, her case has highlighted a rare and contentious phenomenon,
Lazarus Syndrome, where supposedly dead patients recover after attempts to
revive them have been abandoned.
Though disputed by some doctors, the issue raises disturbing questions about how
we diagnose death.
Patients are declared dead only with the onset of brain death — when electrical
activity in the brain stops. It is diagnosed through an absence of independent
breathing, a lack of eye movement, fixed or dilated pupils and no reflexes.
With modern technology, brain death should be easy to identify. But in rare cases,
doctors get it hopelessly wrong.
After Mrs Rafiq collapsed, an ambulance was called and medics took her to
hospital (stock image)
In 1996, Daphne Banks, a farmer's wife from Huntingdon, attempted suicide by
drug overdose on New Year's Eve. She was declared dead by doctors at
Hinchingbrooke Hospital in the early hours of New Year's Day, only for an
undertaker to rescue her from the mortuary slab 34 hours later after hearing her
snoring.
Her husband pronounced his wife's salvation 'a miracle'.
Equally miraculous was the case of the Egyptian chauffeur who rose from the
dead. In July 1997, Abdel-Sattar Badawi was laid in a coffin and taken to the
mortuary of a hospital in Menoufia.
Doctors had declared him dead, but he was in a deep coma, and after 12 hours he
woke up. Mr Badawi, then in his 60s, said: 'I shouted for someone to come and
rescue me. When no one heard me I started to chant verses from the Koran to
seek God's pardon.'
Unable to see anything, he pushed open the lid of the coffin (luckily it had not been
screwed down) and found himself surrounded by corpses.
Confused and anxious, he climbed out and continued to shout for help.
Three hospital staff came into the morgue and were confronted by Mr Badawi
waving and chanting.
A male nurse collapsed with a heart attack and died from shock. As Mr Badawi left
the hospital, he vowed never to return. Who can blame him?
Earlier this year another Egyptian, Hamdi Hafez al-Nubi, a 28-year-old waiter, was
declared dead after suffering a heart attack at work.
His relatives took his body home and prepared it for burial in his village of Naga al-
Simman in Luxor. However, a doctor sent to sign the death certificate was
surprised to find the body was warm. Closer checks revealed Mr al-Nubi had a
pulse. He was revived, and the funeral turned into a celebration.
Egypt seems to have suffered its unfair share of animated corpses, but such cases
occur the world over.
In April, a Chinese woman aged 95 climbed out of her coffin six days after she
'died'. Li Xiufeng was thought to be dead when a neighbour found her motionless in
bed.
She was placed in a coffin at her home so friends and relatives could pay their last
respects.
The day before the burial, the neighbour called round to discover the coffin was
empty. He was even more stunned to discover the sprightly corpse sitting in the
kitchen, cooking a restorative meal.
Steve Moore has compiled some of the more bizarre incidents of resurrection for
his book Back From The Dead And 350 Other Stories Of Amazing Luck.
He tells the story of Gerry Allison, whose body was making its way through Los
Angeles in a hearse in 1977 when a tyre burst. The hearse careered into the
window of a rival funeral parlour.
The doors flew open and the coffin toppled out. Passers-by saw Mr Allison, in a
shroud, walk out of the wreckage. Doctors believe the crash brought him out of a
deep coma.
Then there was Fagili Mukhametzyanov, who woke up at her funeral last year, and
promptly died of shock.
Mrs Mukhametzyanov, 49, had been pronounced dead by doctors in Kazan,
Russia, after a heart attack at home.
As relatives filed past her open coffin, she started to scream. She lived for only
another 12 minutes before dying — this time permanently. Her case is not
untypical. Often patients who come back to life are left with severe brain and organ
damage and never recover their health.
Michael Wilkinson, a roofer from Preston, Lancashire, 'died' in hospital in 2009
aged 23 from a previously undiagnosed heart condition. But after he was given the
last rites, doctors found a pulse. Mr Wilkinson was transferred to intensive care at
Royal Preston Hospital, where he survived for two more days.
Lazarus Syndrome is rare. In 2010, a paper in Critical Care Medicine by
researchers from McGill University, Montreal, identified 32 reported cases.
All involved the spontaneous revival of apparently dead heart attack patients after
attempts to resuscitate them.
The evidence was limited, but enough to convince the authors that more study into
the phenomenon was needed.
Some believe it may be caused by the delayed delivery of adrenaline injected to
revive a patient after a heart attack.
Another theory is that attempts at resuscitation create a build-up of pressure in the
chest. After 'death', the released pressure allows the heart to expand, which
somehow kick-starts it.
Other doctors are wary about labelling an unlikely series of events a 'syndrome'.
Harley Street consultant cardiologist Duncan Dymond says: 'I have never seen
anything like that, and I have been qualified for 40 years.'
Though these events occur only on rare occasions, they raise questions about how
long doctors should wait before declaring a patient dead.
Indeed, at a time when controversy is raging around the Liverpool Care Pathway
— which allows NHS doctors to stop medication for patients they believe are close
to death — such cases should give us pause for thought about the powers of the
human body to cling to life.
Until Lazarus Syndrome has been fully explained — or discounted — it may make
sense to follow the example of George Washington.
The American president was so concerned about misdiagnosis that he ordered his
doctors not to bury him for at least two days after he was declared dead, giving him
ample time to effect a dramatic resurrection. Unfortunately for him, we are still
waiting.
George Washington was so concerned about misdiagnosis that he ordered his
doctors not to bury him for at least two days after he was declared dead