Articles
 

                    Near-death experience in survivors of cardiac arrest: a prospective study in the
                    Netherlands
 

                    Pim van Lommel, Ruud van Wees, Vincent Meyers, Ingrid Elfferich
 

                    Division of Cardiology, Hospital Rijnstate, Arnhem, Netherlands (P van Lommel
                    MD); Tilburg, Netherlands (R van Wees PhD); Nijmegen, Netherlands (V Meyers
                    PhD); and Capelle a/d Ijssel, Netherlands (I Elfferich PhD)
 

                    Correspondence to: Dr Pim van Lommel, Division of Cardiology, Hospital Rijnstate, PO
                    Box 9555, 6800 TA Arnhem, Netherlands (e-mail:pimvanlommel@wanadoo.nl)

                    Summary
                    Introduction
                    Methods
                    Results
                    Discussion
                    References

                    Summary
 

                    Background Some people report a near-death experience (NDE) after a life-threatening
                    crisis. We aimed to establish the cause of this experience and assess factors that
                    affected its frequency, depth, and content.

                    Methods In a prospective study, we included 344 consecutive cardiac patients who
                    were successfully resuscitated after cardiac arrest in ten Dutch hospitals. We compared
                    demographic, medical, pharmacological, and psychological data between patients who
                    reported NDE and patients who did not (controls) after resuscitation. In a longitudinal
                    study of life changes after NDE, we compared the groups 2 and 8 years later.

                    Findings 62 patients (18%) reported NDE, of whom 41 (12%) described a core
                    experience. Occurrence of the experience was not associated with duration of cardiac
                    arrest or unconsciousness, medication, or fear of death before cardiac arrest. Frequency
                    of NDE was affected by how we defined NDE, the prospective nature of the research in
                    older cardiac patients, age, surviving cardiac arrest in first myocardial infarction, more
                    than one cardiopulmonary resuscitation (CPR) during stay in hospital, previous NDE, and
                    memory problems after prolonged CPR. Depth of the experience was affected by sex,
                    surviving CPR outside hospital, and fear before cardiac arrest. Significantly more patients
                    who had an NDE, especially a deep experience, died within 30 days of CPR (p<0·0001).
                    The process of transformation after NDE took several years, and differed from those of
                    patients who survived cardiac arrest without NDE.

                    Interpretation We do not know why so few cardiac patients report NDE after CPR,
                    although age plays a part. With a purely physiological explanation such as cerebral
                    anoxia for the experience, most patients who have been clinically dead should report one.

                    Lancet 2001; 358: 2039-45

                    See Commentary
 

                    Introduction
 

                    Some people who have survived a life-threatening crisis report an extraordinary
                    experience. Near-death experience (NDE) occurs with increasing frequency because of
                    improved survival rates resulting from modern techniques of resuscitation. The content of
                    NDE and the effects on patients seem similar worldwide, across all cultures and times.
                    The subjective nature and absence of a frame of reference for this experience lead to
                    individual, cultural, and religious factors determining the vocabulary used to describe and
                    interpret the experience.1

                    NDE are reported in many circumstances: cardiac arrest in myocardial infarction (clinical
                    death), shock in postpartum loss of blood or in perioperative complications, septic or
                    anaphylactic shock, electrocution, coma resulting from traumatic brain damage,
                    intracerebral haemorrhage or cerebral infarction, attempted suicide, near-drowning or
                    asphyxia, and apnoea. Such experiences are also reported by patients with serious but
                    not immediately life-threatening diseases, in those with serious depression, or without
                    clear cause in fully conscious people. Similar experiences to near-death ones can occur
                    during the terminal phase of illness, and are called deathbed visions. Identical
                    experiences to NDE, so-called fear-death experiences, are mainly reported after
                    situations in which death seemed unavoidable: serious traffic accidents, mountaineering
                    accidents, or isolation such as with shipwreck.

                    Several theories on the origin of NDE have been proposed. Some think the experience is
                    caused by physiological changes in the brain, such as brain cells dying as a result of
                    cerebral anoxia.2-4 Other theories encompass a psychological reaction to approaching
                    death,5 or a combination of such reaction and anoxia.6 Such experiences could also be
                    linked to a changing state of consciousness (transcendence), in which perception,
                    cognitive functioning, emotion, and sense of identity function independently from normal
                    body-linked waking consciousness.7 People who have had an NDE are psychologically
                    healthy, although some show non-pathological signs of dissociation.7 Such people do
                    not differ from controls with respect to age, sex, ethnic origin, religion, or degree of
                    religious belief.1

                    Studies on NDE1,3,8,9 have been retrospective and very selective with respect to
                    patients. In retrospective studies, 5-10 years can elapse between occurrence of the
                    experience and its investigation, which often prevents accurate assessment of
                    physiological and pharmacological factors. In retrospective studies, between 43%8 and
                    48%1 of adults and up to 85% of children10 who had a life-threatening illness were
                    estimated to have had an NDE. A random investigation of more than 2000 Germans
                    showed 4·3% to have had an NDE at a mean age of 22 years.11 Differences in estimates
                    of frequency and uncertainty as to causes of this experience result from varying
                    definitions of the phenomenon, and from inadequate methods of research.12 Patients'
                    transformational processes after an NDE are very similar1,3,13-16 and encompass
                    life-changing insight, heightened intuition, and disappearance of fear of death.
                    Assimilation and acceptance of these changes is thought to take at least several
                    years.15

                    We did a prospective study to calculate the frequency of NDE in patients after cardiac
                    arrest (an objective critical medical situation), and establish factors that affected the
                    frequency, content, and depth of the experience. We also did a longitudinal study to
                    assess the effect of time, memory, and suppression mechanisms on the process of
                    transformation after NDE, and to reaffirm the content and allow further study of the
                    experience. We also proposed to reassess theories on the cause and content of NDE.
 

                    Methods
 

                    Patients
 

                    We included consecutive patients who were successfully resuscitated in coronary care
                    units in ten Dutch hospitals during a research period varying between hospitals from 4
                    months to nearly 4 years (1988-92). The research period varied because of the
                    requirement that all consecutive patients who had undergone successful
                    cardiopulmonary resuscitation (CPR) were included. If this standard was not met we
                    ended research in that hospital. All patients had been clinically dead, which we
                    established mainly by electrocardiogram records. All patients gave written informed
                    consent. We obtained ethics committee approval.

                    Procedures
 

                    We defined NDE as the reported memory of all impressions during a special state of
                    consciousness, including specific elements such as out-of-body experience, pleasant
                    feelings, and seeing a tunnel, a light, deceased relatives, or a life review. We defined
                    clinical death as a period of unconsciousness caused by insufficient blood supply to the
                    brain because of inadequate blood circulation, breathing, or both. If, in this situation, CPR
                    is not started within 5-10 min, irreparable damage is done to the brain and the patient will
                    die.

                    We did a short standardised interview with sufficiently well patients within a few days of
                    resuscitation. We asked whether patients recollected the period of unconsciousness,
                    and what they recalled. Three researchers coded the experiences according to the
                    weighted core experience index.1 In this scoring system, depth of NDE is measured with
                    weighted scores assigned to elements of the content of the experience. Scores between
                    1 and 5 denote superficial NDE, but we included these events because all patients
                    underwent transformational changes as well. Scores of 6 or more denote core
                    experiences, and scores of 10 or greater are deep experiences. We also recorded date
                    of cardiac arrest, date of interview, sex, age, religion, standard of education reached,
                    whether the patient had previously experienced NDE, previously heard of NDE, whether
                    CPR took place inside or outside hospital, previous myocardial infarction, and how many
                    times the patient had been resuscitated during their stay in hospital. We estimated
                    duration of circulatory arrest and unconsciousness, and noted whether artificial
                    respiration by intubation took place. We also recorded type and dose of drugs before,
                    during, and after the crisis, and assessed possible memory problems at interview after
                    lengthy or difficult resuscitation. We classed patients resuscitated during
                    electrophysiological stimulation separately.

                    We did standardised and taped interviews with participants a mean of 2 years after CPR.
                    Patients also completed a life-change inventory.16 The questionnaire addressed
                    self-image, concern with others, materialism and social issues, religious beliefs and
                    spirituality, and attitude towards death. Participants answered 34 questions with a
                    five-point scale indicating whether and to what degree they had changed. After 8 years,
                    surviving patients and their partners were interviewed again with the life-change
                    inventory, and also completed a medical and psychological questionnaire for cardiac
                    patients (from the Dutch Heart Foundation), the Utrecht coping list, the sense of
                    coherence inquiry, and a scale for depression. These extra questionnaires were deemed
                    necessary for qualitative analysis because of the reduced number of respondents who
                    survived to 8 years follow-up. Our control group consisted of resuscitated patients who
                    had not reported an NDE. We matched controls with patients who had had an NDE by
                    age, sex, and time interval between CPR and the second and third interviews.

                    Statistical analysis
 

                    We assessed causal factors for NDE with the Pearson 2 test for categorical and t test
                    for ratio-scaled factors. Factors affecting depth of NDE were analysed with the
                    Mann-Whitney test for categorical factors, and with Spearman's coefficient of rank
                    correlation for ratio-scaled factors. Links between NDE and altered scores for questions
                    from the life-change inventory were assessed with the Mann-Whitney test. The sums of
                    the individual scores were used to compare the responses to the life-change inventory
                    in the second and third interview. Because few causes or relations exist for NDE, the null
                    hypotheses are the absence of factors. Hence, all tests were two-tailed with significance
                    shown by p values less than 0·05.
 

                    Results
 

                    Patients
 

                    We included 344 patients who had undergone 509 successful resuscitations. Mean age
                    at resuscitation was 62·2 years (SD 12·2), and ranged from 26 to 92 years. 251 patients
                    were men (73%) and 93 were women (27%). Women were significantly older than men (66
                    vs 61 years, p=0·005).The ratio of men to women was 57/43 for those older than 70 years,
                    whereas at younger ages it was 80/20. 14 (4%) patients had had a previous NDE. We
                    interviewed 248 (74%) patients within 5 days after CPR. Some demographic questions
                    from the first interview had too many values missing for reliable statistical analysis, so
                    data from the second interview were used. Of the 74 patients whom we interviewed at
                    2-year follow-up, 42 (57%) had previously heard of NDE, 53 (72%) were religious, 25
                    (34%) had left education aged 12 years, and 49 (66%) had been educated until aged at
                    least 16 years.

                    296 (86%) of all 344 patients had had a first myocardial infarction and 48 (14%) had
                    undergone more than one infarction. Nearly all patients with acute myocardial infarction
                    were treated with fentanyl, a synthetic opiod antagonist; thalamonal, a combined
                    preparation of fentanyl with dehydrobenzperidol that has an antipsychotic and sedative
                    effect; or both. 45 (13%) patients also received sedative drugs such as diazepam or
                    oxazepam, and 38 (11%) were given strong sedatives such as midazolam (for intubation),
                    or haloperidol for cerebral unrest during or after long-lasting unconsciousness.

                    234 (68%) patients were successfully resuscitated within hospital. 190 (81%) of these
                    patients were resuscitated within 2 min of circulatory arrest, and unconsciousness lasted
                    less than 5 min in 187 (80%). 30 patients were resuscitated during electrophysiological
                    stimulation; these patients all underwent less than 1 min of circulatory arrest and less
                    than 2 min of unconsciousness. This group were only given 5 mg of diazepam about 1 h
                    before electrophysiological stimulation.

                    101 (29%) patients survived CPR outside hospital, and nine (3%) were resuscitated both
                    within and outside hospital. Of these 110 patients, 88 (80%) had more than 2 min of
                    circulatory arrest, and 62 (56%) were unconscious for more than 10 min. All people with
                    brief cardiac arrest and who were resuscitated outside hospital were resuscitated in an
                    ambulance. Only 12 (9%) patients survived a circulatory arrest that lasted longer than 10
                    min. 36% (123) of all patients were unconsciousness for longer than 60 min, 37 of these
                    patients needed artificial respiration through intubation. Intubated patients received high
                    doses of strong sedatives and were interviewed later than other patients; most were still
                    in a weakened physical condition at the time of first interview and 24 showed memory
                    defects. Significantly more younger than older patients survived long-lasting
                    unconsciousness following difficult CPR (p=0·005).

                    Prospective findings
 

                    62 (18%) patients reported some recollection of the time of clinical death (table 1). Of
                    these patients, 21 (6% of total) had a superficial NDE and 41 (12%) had a core
                    experience. 23 of the core group (7% of total) reported a deep or very deep NDE.
                    Therefore, of 509 resuscitations, 12% resulted in NDE and 8% in core experiences. Table
                    2 shows the frequencies of ten elements of NDE.1 No patients reported distressing or
                    frightening NDE.
 

                                                  WCEI score*
                                                                   n
                     A No memory
                                                  0
                                                                   282 (82%)
                     B Some recollection
                                                  1-5
                                                                   21 (6%)
                     C Moderately deep NDE
                                                  6-9
                                                                   18 (5%)
                     D Deep NDE
                                                  10-14
                                                                   17 (5%)
                     E Very deep NDE
                                                  15-19
                                                                   6 (2%)
                     WCEI=weighted core experience index. NDE=near-death experience. *A=no NDE,
                     B=superficial NDE, C/D/E=core NDE.
                     Table 1: Distribution of the 344 patients in five WCEI classes*
 
 
 

                     Elements of NDE1
                                                 Frequency (n=62)
                     1 Awareness of being dead
                                                 31 (50%)
                     2 Positive emotions
                                                 35 (56%)
                     3 Out of body experience
                                                 15 (24%)
                     4 Moving through a tunnel
                                                 19 (31%)
                     5 Communication with light
                                                 14 (23%)
                     6 Observation of colours
                                                 14 (23%)
                     7 Observation of a celestial landscape
                                                 18 (29%)
                     8 Meeting with deceased persons
                                                 20 (32%)
                     9 Life review
                                                 8 (13%)
                     10 Presence of border
                                                 5 (8%)
                     NDE=near-death experience.
                     Table 2: Frequency of ten elements of NDE
 
 

                    During the pilot phase in one of the hospitals, a coronary-care-unit nurse reported a
                    veridical out-of-body experience of a resuscitated patient:

                    "During a night shift an ambulance brings in a 44-year-old cyanotic, comatose man into
                    the coronary care unit. He had been found about an hour before in a meadow by
                    passers-by. After admission, he receives artificial respiration without intubation, while
                    heart massage and defibrillation are also applied. When we want to intubate the patient,
                    he turns out to have dentures in his mouth. I remove these upper dentures and put them
                    onto the 'crash car'. Meanwhile, we continue extensive CPR. After about an hour and a
                    half the patient has sufficient heart rhythm and blood pressure, but he is still ventilated
                    and intubated, and he is still comatose. He is transferred to the intensive care unit to
                    continue the necessary artificial respiration. Only after more than a week do I meet again
                    with the patient, who is by now back on the cardiac ward. I distribute his medication. The
                    moment he sees me he says: 'Oh, that nurse knows where my dentures are'. I am very
                    surprised. Then he elucidates: 'Yes, you were there when I was brought into hospital and
                    you took my dentures out of my mouth and put them onto that car, it had all these bottles
                    on it and there was this sliding drawer underneath and there you put my teeth.' I was
                    especially amazed because I remembered this happening while the man was in deep
                    coma and in the process of CPR. When I asked further, it appeared the man had seen
                    himself lying in bed, that he had perceived from above how nurses and doctors had been
                    busy with CPR. He was also able to describe correctly and in detail the small room in
                    which he had been resuscitated as well as the appearance of those present like myself.
                    At the time that he observed the situation he had been very much afraid that we would
                    stop CPR and that he would die. And it is true that we had been very negative about the
                    patient's prognosis due to his very poor medical condition when admitted. The patient
                    tells me that he desperately and unsuccessfully tried to make it clear to us that he was
                    still alive and that we should continue CPR. He is deeply impressed by his experience
                    and says he is no longer afraid of death. 4 weeks later he left hospital as a healthy man."

                    Table 3 shows relations between demographic, medical, pharmacological, and
                    psychological factors and the frequency and depth of NDE. No medical, pharmacological,
                    or psychological factor affected the frequency of the experience. People younger than 60
                    years had NDE more often than older people (p=0·012), and women, who were
                    significantly older than men, had more frequent deep experiences than men (p=0·011)
                    (table 3). Increased frequency of experiences in patients who survived cardiac arrest in
                    first myocardial infarction, and deeper experiences in patients who survived CPR outside
                    hospital could have resulted from differences in age. Both these groups of patients were
                    younger than other patients, though the age differences were not significant (p=0·05 and
                    0·07, respectively).
 

                                            Frequency of NDE
                                                                          Depth
                                            NDE
                                                         No NDE
                                                                    p
                                                                          of NDE
                                            (n=62)
                                                         (n=282)
                                                                          (n=62)
                     Categorical factors
                     Demographic
                     Women
                                            13 (21%)
                                                         80 (28%)
                                                                    NS
                                                                          0·011
                     Age* <60 years
                                            32 (52%)
                                                         96 (34%)
                                                                    0·012
                                                                          NS
                     Religion? (yes)
                                            26 (70%)
                                                         27 (73% )
                                                                    NS
                                                                          NS
                     Education?? Elementary
                                            10 (27%)
                                                         15 (43%)
                                                                    NS
                                                                          NS
                     Medical
                     Intubation
                                            6 (10%)
                                                         31 (11%)
                                                                    NS
                                                                          NS
                     Electrophysiological
                                            8 (13%)
                                                         22 (8%)
                                                                    NS
                                                                          NS
                     stimulation
                     First myocardial
                                            60 (97%)
                                                         236 (84%)
                                                                    0·013
                                                                          NS
                     infarction
                     CPR outside hospital§
                                            13 (21%)
                                                         88 (32%)
                                                                    NS
                                                                          0·027
                     Memory defect after
                                            1 (2%)
                                                         40 (14%)
                                                                    0·011
                                                                          NS
                     lengthy CPR
                     Death within 30 days
                                            13 (21%)
                                                         24 (9%)
                                                                    0·008
                                                                          0·017
                     Pharmacological
                     Extra medication
                                            17 (27%)
                                                         70 (25%)
                                                                    NS
                                                                          NS
                     Psychological
                     Fear before CPR?§
                                            4 (13%)
                                                         2 (6%)
                                                                    NS
                                                                          0·045
                     Previous NDE
                                            6 (10%)
                                                         8 (3%)
                                                                    0·035
                                                                          NS
                     Foreknowledge of NDE?
                                            22 (60%)
                                                         20 (54%)
                                                                    NS
                                                                          NS
                     Ratio-scaled factors
                     Demographic
                     Age (mean [SD], years)*
                                            58·8 (13·4)
                                                         63·5 (11·8)
                                                                    0·006
                                                                          NS
                     Medical
                     Duration of cardiac
                                            4·0 (5·2)
                                                         3·7 (3·9)
                                                                    NS
                                                                          NS
                     arrest (mean [SD], min)
                     Duration of
                                            66·1 (269·5)
                                                         118·3 (355·5)
                                                                          NS
                     NS
                     unconsciousness
                     (mean [SD], min)
                     Number of CPRs (SD)
                                            2·1 (2·5)
                                                         1·4 (1·2)
                                                                    0·029
                                                                          NS
                     Data are number (%) unless otherwise indicated. CPR=cardiopulmonary resuscitation.
                     NS=not significant (p>0·05). *3 missing values. ?n=74 (data from 2nd interview, 35
                     NDE, 39 no NDE). ?2 missing values. §10 missing values.
                     Table 3: Factors affecting frequency and depth of near-death experience (NDE)
 
 

                    Lengthy CPR can sometimes induce loss of memory and patients thus affected reported
                    significantly fewer NDEs than others (table 3). No relation was found between frequency of
                    NDE and the time between CPR and the first interview (range 1-70 days). Mortality during
                    or shortly after stay in hospital in patients who had an NDE was significantly higher than in
                    patients who did not report an NDE (13/62 patients [21%] vs 24/282 [9%], p=0·008), and
                    this difference was even more marked in patients who reported a deep experience (10/23
                    [43%] vs 24/282 [9%], p<0·0001).

                    Longitudinal findings
 

                    At 2-year follow-up, 19 of the 62 patients with NDE had died and six refused to be
                    interviewed. Thus, we were able to interview 37 patients for the second time. All patients
                    were able to retell their experience almost exactly. Of the 17 patients who had low scores
                    in the first interview (superficial NDE), seven had unchanged low scores, and four
                    probably had, in retrospect, an NDE that consisted only of positive emotions (score 1).
                    Six patients had not in fact had an NDE after all, which was probably because of our wide
                    definition of NDE at the first interview.

                    We selected a control group, matched for age, sex, and time since cardiac arrest, from
                    the 282 patients who had not had NDE. We contacted 75 of these patients to obtain 37
                    survivors who agreed to be interviewed. Two controls reported an NDE consisting only of
                    positive emotions, and two a core experience. The first interview after CPR might have
                    been too soon for these four patients (1% of total) to remember their NDE, or to be willing
                    or able to describe the experience. We were therefore able to interview 35 patients who
                    had had an affirmed NDE, and 39 patients who had not.

                    Only six of the 74 patients that we interviewed at 2 years said they were afraid before CPR
                    (table 3). Four of these six had deep NDE (p=0·045, table 3). Most patients were not
                    afraid before CPR, as the arrest happened too suddenly and unexpectedly to allow time
                    for fear.

                    Significant differences in answers to 13 of the 34 items in the life-change inventory
                    between people with and without an NDE are shown in table 4. For instance, people who
                    had NDE had a significant increase in belief in an afterlife and decrease in fear of death
                    compared with people who had not had this experience. Depth of NDE was linked to high
                    scores in spiritual items such as interest in the meaning of one's own life, and social
                    items such as showing love and accepting others. The 13 patients who had superficial
                    NDE underwent the same specific transformational changes as those who had a core
                    experience.
 

                     LIfe-change inventory questionnaire
                                                                        p
                     Social attitude
                     Showing own feelings
                                                                        0·034
                     Acceptance of others*
                                                                        0·012
                     More loving, empathic*
                                                                        0·002
                     Understanding others*
                                                                        0·003
                     Involvement in family*
                                                                        0·008
                     Religious attitude
                     Understand purpose of life*
                                                                        0·020
                     Sense inner meaning of life*
                                                                        0·028
                     Interest in spirituality*
                                                                        0·035
                     Attitude to death
                     Fear of death*
                                                                        0·009
                     Belief in life after death*
                                                                        0·007
                     Others
                     Interest in meaning of life
                                                                        0·020
                     Understanding oneself
                                                                        0·019
                     Appreciation of ordinary things
                                                                        0·0001
                     NDE=near-death experience. 35 patients had NDE, 39 had not had NDE. 1 value
                     missing for patients wih NDE in all categories; *2 values missing for patients with NDE
                     (ie, n=33).
                     Table 4: Significant differences in life-change inventory-scores16 of patients
                     with and without NDE at 2-year follow-up
 
 

                    8-year follow-up included 23 patients with an NDE that had been affirmed at 2-year
                    follow-up. 11 patients had died and one could not be interviewed. Patients could still
                    recall their NDE almost exactly. Of the patients without an NDE at 2-year follow-up, 20
                    had died and four patients could not be interviewed (for reasons such as dementia and
                    long stay in hospital), which left 15 patients without an NDE to take part in the third
                    interview.

                    All patients, including those who did not have NDE, had gone through a positive change
                    and were more self-assured, socially aware, and religious than before. Also, people who
                    did not have NDE had become more emotionally affected, and in some, fear of death had
                    decreased more than at 2-year follow-up. Their interest in spirituality had strongly
                    decreased. Most patients who did not have NDE did not believe in a life after death at
                    2-year or 8-year follow-up (table 5). People with NDE had a much more complex coping
                    process: they had become more emotionally vulnerable and empathic, and often there
                    was evidence of increased intuitive feelings. Most of this group did not show any fear of
                    death and strongly believed in an afterlife. Positive changes were more apparent at 8
                    years than at 2 years of follow-up.
 

                     Life-change inventory
                                                2-year follow-up
                                                                 8-year follow-up
                     questionnaire
                                                NDE
                                                        no NDE
                                                                 NDE
                                                                         no NDE
                                                (n=23)
                                                        (n=15)
                                                                 (n=23)
                                                                         (n=15)
                     Social attitude
                     Showing own feelings
                                                42
                                                        16
                                                                 78
                                                                         58
                     Acceptance of others
                                                42
                                                        16
                                                                 78
                                                                         41
                     More loving, empathic
                                                52
                                                        25
                                                                 68
                                                                         50
                     Understanding others
                                                36
                                                        8
                                                                 73
                                                                         75
                     Involvement in family
                                                47
                                                        33
                                                                 78
                                                                         58
                     Religious attitude
                     Understand purpose of life
                                                52
                                                        33
                                                                 57
                                                                         66
                     Sense inner meaning of life
                                                52
                                                        25
                                                                 57
                                                                         25
                     Interest in spirituality
                                                15
                                                        -8
                                                                 42
                                                                         -41
                     Attitude to death
                     Fear of death
                                                -47
                                                        -16
                                                                 -63
                                                                         -41
                     Belief in life after death
                                                36
                                                        16
                                                                 42
                                                                         16
                     Others
                     Interest in meaning of life
                                                52
                                                        33
                                                                 89
                                                                         66
                     Understanding oneself
                                                58
                                                        8
                                                                 63
                                                                         58
                     Appreciation of ordinary things
                                                78
                                                        41
                                                                 84
                                                                         50
                     NDE=near-death experience. The sums of all individual scores per item are reported
                     in the same 38 patients who had both follow-up interviews. Participants responded in a
                     five-point scale indicating whether and to what degree they had changed: strongly
                     increased (+2), somewhat increased (+1), no change (0), somewhat decreased (-1),
                     and strongly decreased (-2). Only in the reported 13 (of 34) items in this table were
                     significant differences found in life-change scores in the interview after 2 years (table
                     4).
                     Table 5: Total sum of individual life-change inventory scores16 of patients at
                     2-year and 8-year follow-up
 
 
 
 

                    Discussion
 

                    Our results show that medical factors cannot account for occurrence of NDE; although all
                    patients had been clinically dead, most did not have NDE. Furthermore, seriousness of
                    the crisis was not related to occurrence or depth of the experience. If purely physiological
                    factors resulting from cerebral anoxia caused NDE, most of our patients should have had
                    this experience. Patients' medication was also unrelated to frequency of NDE.
                    Psychological factors are unlikely to be important as fear was not associated with NDE.

                    The 18% frequency of NDE that we noted is lower than reported in retrospective
                    studies,1,8 which could be because our prospective study design prevented
                    self-selection of patients. Our frequency of NDE is low despite our wide definition of the
                    experience. Only 12% of patients had a core NDE, and this figure might be an
                    overestimate. When we analysed our results, we noted that one hospital that participated
                    in the study for nearly 4 years, and from which 137 patients were included, reported a
                    significantly (p=0·01) lower percentage of NDE (8%), and significantly (p=0·05) fewer deep
                    experiences. Therefore, possibly some selection of patients occurred in the other
                    hospitals, which sometimes only took part for a few months. In a prospective study17 with
                    the same design as ours, 6% of 63 survivors of cardiac arrest reported a core
                    experience, and another 5% had memories with features of an NDE (low score in our
                    study); thus, with our wide definition of the experience, 11% of these patients reported an
                    NDE. Therefore, true frequency of the experience is likely to be about 10%, or 5% if based
                    on number of resuscitations rather than number of resuscitated patients. Patients who
                    survive several CPRs in hospital have a significantly higher chance of NDE (table 3).

                    We noted that the frequency of NDE was higher in people younger than 60 years than in
                    older people. In other studies, mean age at NDE is lower than our estimate (62·2 years)
                    and the frequency of the experience is higher. Morse10 saw 85% NDE in children, Ring1
                    noted 48% NDE in people with a mean age of 37 years, and Sabom8 saw 43% NDE in
                    people with a mean age of 49 years; thus, age and the frequency of the experience seem
                    to be associated. Other retrospective studies have noted a younger mean age for NDE:
                    32 years,9 29 years,6 and 22 years.11 Cardiac arrest was the cause of the experience in
                    most patients in Sabom's8 study, whereas this was the case in only a low percentage of
                    patients in other work. We saw that people surviving CPR outside hospital (who
                    underwent deeper NDE than other patients) tended to be younger, as were those who
                    survived cardiac arrest in a first myocardial infarction (more frequent NDE), which
                    indicates that age was probably decisive in the significant relation noted with those
                    factors.

                    In a study of mortality in patients after resuscitation outside hospital,18 chances of
                    survival increased in people younger than 60 years and in those undergoing first
                    myocardial infarction, which corresponds with our findings. Older people have a smaller
                    chance of cerebral recovery after difficult and complicated resuscitation after cardiac
                    arrest. Younger patients have a better chance of surviving a cardiac arrest, and thus, to
                    describe their experience. In a study of 11 patients after CPR, the person that had an
                    NDE was significantly younger than other patients who did not have such an
                    experience.19 Greyson7 also noted a higher frequency of NDE and significantly deeper
                    experiences at younger ages, as did Ring.1

                    Good short-term memory seems to be essential for remembering NDE. Patients with
                    memory defects after prolonged resuscitation reported fewer experiences than other
                    patients in our study. Forgetting or repressing such experiences in the first days after
                    CPR was unlikely to have occurred in the remaining patients, because no relation was
                    found between frequency of NDE and date of first interview. However, at 2-year follow-up,
                    two patients remembered a core NDE and two an NDE that consisted of only positive
                    emotions that they had not reported shortly after CPR, presumably because of memory
                    defects at that time. It is remarkable that people could recall their NDE almost exactly
                    after 2 and 8 years.

                    Unlike our results, an inverse correlation between foreknowledge and frequency of NDE
                    has been shown.1,8 Our finding that women have deeper experiences than men has been
                    confirmed in two other studies,1,7 although in one,7 only in those cases in which women
                    had an NDE resulting from disease.

                    The elements of NDE that we noted (table 2) correspond with those in other studies
                    based on Ring's1 classification. Greyson20 constructed the NDE scale differently to
                    Ring,1 but both scoring systems are strongly correlated (r=0·90). Yet, reliable
                    comparisons are nearly impossible between retrospective studies that included selection
                    of patients, unreliable medical records, and used different criteria for NDE,12 and our
                    prospective study.

                    Our longitudinal follow-up research into transformational processes after NDE confirms
                    the transformation described by many others.1-3,8,10,13-16,21 Several of these
                    investigations included a control group to enable study of differences in transformation,14
                    but in our research, patients were interviewed three times during 8 years, with a matched
                    control group. Our findings show that this process of change after NDE tends to take
                    several years to consolidate. Presumably, besides possible internal psychological
                    processes, one reason for this has to do with society's negative response to NDE, which
                    leads individuals to deny or suppress their experience for fear of rejection or ridicule.
                    Thus, social conditioning causes NDE to be traumatic, although in itself it is not a
                    psychotraumatic experience. As a result, the effects of the experience can be delayed for
                    years, and only gradually and with difficulty is an NDE accepted and integrated.
                    Furthermore, the longlasting transformational effects of an experience that lasts for only a
                    few minutes of cardiac arrest is a surprising and unexpected finding.

                    One limitation of our study is that our study group were all Dutch cardiac patients, who
                    were generally older than groups in other studies. Therefore, our frequency of NDE might
                    not be representative of all cases--eg, a higher frequency could be expected with
                    younger samples, or rates might vary in other populations. Also, the rates for NDE could
                    differ in people who survive near-death episodes that come about by different causes,
                    such as near drowning, near fatal car crashes with cerebral trauma, and electrocution.
                    However, rigorous prospective studies would be almost impossible in many such cases.

                    Several theories have been proposed to explain NDE. We did not show that
                    psychological, neurophysiological, or physiological factors caused these experiences
                    after cardiac arrest. Sabom22 mentions a young American woman who had complications
                    during brain surgery for a cerebral aneurysm. The EEG of her cortex and brainstem had
                    become totally flat. After the operation, which was eventually successful, this patient
                    proved to have had a very deep NDE, including an out-of-body experience, with
                    subsequently verified observations during the period of the flat EEG.

                    And yet, neurophysiological processes must play some part in NDE. Similar experiences
                    can be induced through electrical stimulation of the temporal lobe (and hence of the
                    hippocampus) during neurosurgery for epilepsy,23 with high carbon dioxide levels
                    (hypercarbia),24 and in decreased cerebral perfusion resulting in local cerebral hypoxia
                    as in rapid acceleration during training of fighter pilots,25 or as in hyperventilation followed
                    by valsalva manoeuvre.4 Ketamine-induced experiences resulting from blockage of the
                    NMDA receptor,26 and the role of endorphin, serotonin, and enkephalin have also been
                    mentioned,27 as have near-death-like experiences after the use of LSD,28 psilocarpine,
                    and mescaline.21 These induced experiences can consist of unconsciousness,
                    out-of-body experiences, and perception of light or flashes of recollection from the past.
                    These recollections, however, consist of fragmented and random memories unlike the
                    panoramic life-review that can occur in NDE. Further, transformational processes with
                    changing life-insight and disappearance of fear of death are rarely reported after induced
                    experiences.

                    Thus, induced experiences are not identical to NDE, and so, besides age, an unknown
                    mechanism causes NDE by stimulation of neurophysiological and neurohumoral
                    processes at a subcellular level in the brain in only a few cases during a critical situation
                    such as clinical death. These processes might also determine whether the experience
                    reaches consciousness and can be recollected.

                    With lack of evidence for any other theories for NDE, the thus far assumed, but never
                    proven, concept that consciousness and memories are localised in the brain should be
                    discussed. How could a clear consciousness outside one's body be experienced at the
                    moment that the brain no longer functions during a period of clinical death with flat
                    EEG?22 Also, in cardiac arrest the EEG usually becomes flat in most cases within about
                    10 s from onset of syncope.29,30 Furthermore, blind people have described veridical
                    perception during out-of-body experiences at the time of this experience.31 NDE pushes
                    at the limits of medical ideas about the range of human consciousness and the
                    mind-brain relation.

                    Another theory holds that NDE might be a changing state of consciousness
                    (transcendence), in which identity, cognition, and emotion function independently from the
                    unconscious body, but retain the possibility of non-sensory perception.7,8,22,28,31

                    Research should be concentrated on the effort to explain scientifically the occurrence
                    and content of NDE. Research should be focused on certain specific elements of NDE,
                    such as out-of-body experiences and other verifiable aspects. Finally, the theory and
                    background of transcendence should be included as a part of an explanatory framework
                    for these experiences.

                    Contributors
 

                    Pim van Lommel coordinated the first interviews and was responsible for collecting all
                    demographic, medical, and pharmacological data. Pim van Lommel, Ruud van Wees, and
                    Vincent Meyers rated the first interview. Ruud van Wees and Vincent Meyers
                    coordinated the second interviews. Ruud van Wees did statistical analysis of the first and
                    second interviews. Ingrid Elfferich did the third interviews and analysed these results.

                    Acknowledgments
 

                    We thank nursing and medical staff of the hospitals involved in the research; volunteers
                    of the International Association of Near Death Studies; IANDS-Netherlands; Merkawah
                    Foundation for arranging interviews, and typing the second and third interviews; Martin
                    Meyers for help with translation; and Kenneth Ring and Bruce Greyson for review of the
                    article.
 

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