Near-death Experience in Survivors of Cardiac Arrest: a Prospective Study in the Netherlands

Pim van Lommel et al.

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Summary

Background Some people report a near-death experience (N.D.E) 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 N.D.E and patients who did not (controls) after resuscitation. In a longitudinal study of life changes after N.D.E, we compared the groups 2 and 8 years later.

Findings 62 patients (18%) reported N.D.E, 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 N.D.E was affected by how we defined N.D.E, the prospective nature of the research in older cardiac patients, age, surviving cardiac arrest in first myocardial infarction, more than one cardiopulmonary resuscitation (C.P.R) during stay in hospital, previous N.D.E, and memory problems after prolonged C.P.R. Depth of the experience was affected by sex, surviving C.P.R outside hospital, and fear before cardiac arrest. Significantly more patients who had an N.D.E, especially a deep experience, died within 30 days of C.P.R (p less than 0.0001). The process of transformation after N.D.E took several years, and differed from those of patients who survived cardiac arrest without N.D.E.

Interpretation We do not know why so few cardiac patients report N.D.E after C.P.R, 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.

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)

Introduction

Some people who have survived a life-threatening crisis report an extraordinary experience. Near-death experience (N.D.E) occurs with increasing frequency because of improved survival rates resulting from modern techniques of resuscitation. The content of N.D.E 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}

N.D.E 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 N.D.E, 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 N.D.E 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. Other theories encompass a psychological reaction to approaching death, or a combination of such reaction and anoxia. 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. People who have had an N.D.E are psychologically healthy, although some show non-pathological signs of dissociation. Such people do not differ from controls with respect to age, sex, ethnic origin, religion, or degree of religious belief.

Studies on N.D.E have been retrospective and very selective with respect to patients. In retrospective studies, 5 to 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% and 48% of adults and up to 85% of children who had a life-threatening illness were estimated to have had an N.D.E. A random investigation of more than 2000 Germans showed 4 to 3% to have had an N.D.E at a mean age of 22 years. 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. Patients' transformational processes after an N.D.E are very similar 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.

We did a prospective study to calculate the frequency of N.D.E 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 N.D.E, and to reaffirm the content and allow further study of the experience. We also proposed to reassess theories on the cause and content of N.D.E.

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 to 92). The research period varied because of the requirement that all consecutive patients who had undergone successful cardiopulmonary resuscitation (C.P.R) 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 N.D.E 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, C.P.R is not started within 5 to 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. In this scoring system, depth of N.D.E is measured with weighted scores assigned to elements of the content of the experience. Scores between 1 and 5 denote superficial N.D.E, 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 N.D.E, previously heard of N.D.E, whether C.P.R 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 C.P.R. Patients also completed a life-change inventory. 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 N.D.E. We matched controls with patients who had had an N.D.E by age, sex, and time interval between C.P.R and the second and third interviews.

Statistical analysis

We assessed causal factors for N.D.E with the Pearson chi squared test for categorical and t test for ratio-scaled factors. Factors affecting depth of N.D.E were analysed with the Mann-Whitney test for categorical factors, and with Spearman's coefficient of rank correlation for rational-scaled factors. Links between N.D.E 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 N.D.E, 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 (S.D 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 N.D.E. We interviewed 248 (74%) patients within 5 days after C.P.R. 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 N.D.E, 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 opioid 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 milligrams of diazepam about 1 h before electrophysiological stimulation.

101 (29%) patients survived C.P.R 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 unconscious for longer than 60 min, and 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 C.P.R (p =0.005).

WCEI=weighted core experience index. NDE=near-death experience. *A=no NDE, B=superficial NDE, C/D/E=core NDE.

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 N.D.E and 41 (12%) had a core experience. 23 of the core group (7% of total) reported a deep or very deep N.D.E. Therefore, of 509 resuscitations, 12% resulted in N.D.E and 8% in core experiences. Table 2 shows the frequencies of ten elements of N.D.E. No patients reported distressing or frightening N.D.E.

: Table 1 summary: The vast majority of the 344 patients fall into the No memory class, with 282 patients or 82 percent scoring 0 on the WCEI. The remaining patients are distributed across four other classes with much lower frequencies, ranging from 2 percent for Very deep NDE, with scores of 15 to 19, up to 6 percent for Some recollection, with scores of 1 to 5.

Table 2 summary: Positive emotions and awareness of being dead are the most frequent elements of near-death experiences among 62 participants, reported by 56 percent and 50 percent respectively. Other common experiences include meeting with deceased persons at 32 percent and moving through a tunnel at 31 percent. The least frequently reported elements are the presence of a border at 8 percent and life review at 13 percent.

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 C.P.R. 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 C.P.R. 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 C.P.R. 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 C.P.R 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 C.P.R. 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 N.D.E. No medical, pharmacological, or psychological factor affected the frequency of the experience. People younger than 60 years had N.D.E 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 C.P.R 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).

Table 3 summary: Factors influencing the frequency and depth of near-death experiences, or NDEs. For the frequency of NDEs, significant factors include being under 60 years of age, which occurred in 52 percent of the NDE group versus 34 percent of the no NDE group, and having a first myocardial infarction, seen in 97 percent of the NDE group compared to 84 percent of the no NDE group. Other significant frequency factors include a lower rate of memory defects after lengthy CPR, a higher rate of death within 30 days, and a higher likelihood of having a previous NDE. In terms of ratio-scaled factors for frequency, the NDE group had a significantly lower mean age of 58.8 years compared to 63.5 years in the no NDE group, and a higher average number of CPRs at 2.1 versus 1.4. Regarding the depth of NDE, the only significant factors identified were CPR performed outside the hospital, death within 30 days, and fear before CPR.

Lengthy C.P.R can sometimes induce loss of memory and patients thus affected reported significantly fewer N.D.E's than others (table 3). No relation was found between frequency of N.D.E and the time between C.P.R and the first interview (range 1 to 70 days). Mortality during or shortly after stay in hospital in patients who had an N.D.E was significantly higher than in patients who did not report an N.D.E (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 less than 0.0001) [9%], p less than 0.0001).

NDE=near-death experience.

Longitudinal findings

At 2-year follow-up, 19 of the 62 patients with N.D.E 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 N.D.E), seven had unchanged low scores, and four probably had, in retrospect, an N.D.E that consisted only of positive emotions (score 1). Six patients had not in fact had an N.D.E after all, which was probably because of our wide definition of N.D.E 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 N.D.E. We contacted 75 of these patients to obtain 37 survivors who agreed to be interviewed. Two controls reported an N.D.E consisting only of positive emotions, and two a core experience. The first interview after C.P.R might have been too soon for these four patients (1% of total) to remember their N.D.E, or to be willing or able to describe the experience. We were therefore able to interview 35 patients who had had an affirmed N.D.E, and 39 patients who had not.

Only six of the 74 patients that we interviewed at 2 years said they were afraid before C.P.R (table 3). Four of these six had deep N.D.E (p =0.045, table 3). Most patients were not afraid before C.P.R, 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 N.D.E are shown in table 4. For instance, people who had N.D.E 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 N.D.E=near-death experience. 35 patients had N.D.E, 39 had not had N.D.E.

: Significant differences in life-change inventory scores between patients with and without near-death experiences at a 2-year follow-up. The most notable p-values are found in religious attitudes, specifically interest in spirituality at 0.035, sense of inner meaning of life at 0.028, and understanding the purpose of life at 0.020. Other significant differences occur in social attitudes, such as showing own feelings at 0.034, and in other categories like interest in the meaning of life at 0.020 and understanding oneself at 0.019. The smallest p-value recorded is for the appreciation of ordinary things at 0.0001.

1 value missing for patients with N.D.E in all categories; *2 values missing for patients with N.D.E (that is, n=33).

N.D.E 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 N.D.E underwent the same specific transformational changes as those who had a core experience.

8-year follow-up included 23 patients with an N.D.E that had been affirmed at 2-year follow-up. 11 patients had died and one could not be interviewed. Patients could still recall their N.D.E almost exactly. Of the patients without an N.D.E 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 N.D.E to take part in the third interview.

All patients, including those who did not have N.D.E, had gone through a positive change and were more self-assured, socially aware, and religious than before. Also,

N.D.E=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). people who did not have N.D.E 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 N.D.E did not believe in a life after death at 2-year or 8-year follow-up (table 5). People with N.D.E 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.

Table 5 summary: Life-change inventory scores for patients who experienced a near-death experience, or NDE, compared to those who did not. Generally, the NDE group showed higher scores across most life-change categories at both the two-year and eight-year follow-ups. Notable findings include a strong decrease in the fear of death for the NDE group, which moved from negative 47 at two years to negative 63 at eight years. By the eight-year mark, the NDE group showed particularly high scores in appreciation of ordinary things at 84 and interest in the meaning of life at 89, both of which exceeded the scores of the no NDE group. Spiritual interest also saw a significant increase for the NDE group, rising from 15 at two years to 42 at eight years, while the no NDE group remained negative at negative 41.

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.

Discussion

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

The 18% frequency of N.D.E that we noted is lower than reported in retrospective studies, which could be because our prospective study design prevented self-selection of patients. Our frequency of N.D.E is low despite our wide definition of the experience. Only 12% of patients had a core N.D.E, 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 N.D.E (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 study 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 N.D.E (low score in our study); thus, with our wide definition of the experience, 11% of these patients reported an N.D.E. 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 C.P.R's in hospital have a significantly higher chance of N.D.E (table 3).

We noted that the frequency of N.D.E was higher in people younger than 60 years than in older people. In other studies, mean age at N.D.E is lower than our estimate (62·2 years) and the frequency of the experience is higher. Morse saw 85% N.D.E in children, Ring noted 48% N.D.E in people with a mean age of 37 years, and Sabom saw 43% N.D.E 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 N.D.E: 32 years, 29 years, and 22 years. Cardiac arrest was the cause of the experience in most patients in Sabom's study, whereas this was the case in only a low percentage of patients in other work. We saw that people surviving C.P.R outside hospital (who underwent deeper N.D.E than other patients) tended to be younger, as were those who survived cardiac arrest in a first myocardial infarction (more frequent N.D.E), 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, 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 C.P.R, the person that had an N.D.E was significantly younger than other patients who did not have such an experience. Greyson also noted a higher frequency of N.D.E and significantly deeper experiences at younger ages, as did Ring.

Good short-term memory seems to be essential for remembering N.D.E. 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 C.P.R was unlikely to have occurred in the remaining patients, because no relation was found between frequency of N.D.E and date of first interview. However, at 2-year follow-up, two patients remembered a core N.D.E and two an N.D.E that consisted of only positive emotions that they had not reported shortly after C.P.R, presumably because of memory defects at that time. It is remarkable that people could recall their N.D.E almost exactly after 2 and 8 years.

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

The elements of N.D.E that we noted (table 2) correspond with those in other studies based on Ring's classification. Greyson constructed the N.D.E scale differently to Ring, 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 N.D.E, and our prospective study.

Our longitudinal follow-up research into transformational processes after N.D.E confirms the transformation described by many others. Several of these investigations included a control group to enable study of differences in transformation, 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 N.D.E 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 N.D.E, which leads individuals to deny or suppress their experience for fear of rejection or ridicule. Thus, social conditioning causes N.D.E 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 N.D.E 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 N.D.E 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 N.D.E 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 N.D.E. We did not show that psychological, neurophysiological, or physiological factors caused these experiences after cardiac arrest. Sabom mentions a young American woman who had complications during brain surgery for a cerebral aneurysm. The E.E.G 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 N.D.E, including an out-of-body experience, with subsequently verified observations during the period of the flat E.E.G.

And yet, neurophysiological processes must play some part in N.D.E. Similar experiences can be induced through electrical stimulation of the temporal lobe (and hence of the hippocampus) during neurosurgery for epilepsy, with high carbon dioxide levels (hypercarbia), and in decreased cerebral perfusion resulting in local cerebral hypoxia as in rapid acceleration during training of fighter pilots, or as in hyperventilation followed by valsalva manoeuvre. Ketamine-induced experiences resulting from blockage of the nmda receptor, and the role of endorphin, serotonin, and enkephalin have also been mentioned, as have near-death-like experiences after the use of L.S.D, psilocarpine, and mescaline. 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 N.D.E. 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 N.D.E, and so, besides age, an unknown mechanism causes N.D.E 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 N.D.E, 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 E.E.G Also, in cardiac arrest the E.E.G usually becomes flat in most cases within about 10 s from onset of syncope. Furthermore, blind people have described veridical perception during out-of-body experiences at the time of this experience. N.D.E pushes at the limits of medical ideas about the range of human consciousness and the mind-brain relation.

Another theory holds that N.D.E 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.

Research should be concentrated on the effort to explain scientifically the occurrence and content of N.D.E. Research should be focused on certain specific elements of N.D.E, 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

We thank nursing and medical staff of the hospitals involved in the research; volunteers of the International Association of Near Death Studies; I.A.N.D.S-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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