Context While the adoption of practice guidelines is standardizing many aspects
of patient care, ethical dilemmas are occurring because of forgoing life-sustaining
therapies in intensive care and are dealt with in diverse ways between different
countries and cultures.
Objectives To determine the frequency and types of actual end-of-life practices
in European intensive care units (ICUs) and to analyze the similarities and
differences.
Design and Setting A prospective, observational study of European ICUs.
Participants Consecutive patients who died or had any limitation of therapy.
Intervention Prospectively defined end-of-life practices in 37 ICUs in 17 European
countries were studied from January 1, 1999, to June 30, 2000.
Main Outcome Measures Comparison and analysis of the frequencies and patterns of end-of-life
care by geographic regions and different patients and professionals.
Results Of 31 417 patients admitted to ICUs, 4248 patients (13.5%) died
or had a limitation of life-sustaining therapy. Of these, 3086 patients (72.6%)
had limitations of treatments (10% of admissions). Substantial intercountry
variability was found in the limitations and the manner of dying: unsuccessful
cardiopulmonary resuscitation in 20% (range, 5%-48%), brain death in 8% (range,
0%-15%), withholding therapy in 38% (range, 16%-70%), withdrawing therapy
in 33% (range, 5%-69%), and active shortening of the dying process in 2% (range,
0%-19%). Shortening of the dying process was reported in 7 countries. Doses
of opioids and benzodiazepines reported for shortening of the dying process
were in the same range as those used for symptom relief in previous studies.
Limitation of therapy vs continuation of life-sustaining therapy was associated
with patient age, acute and chronic diagnoses, number of days in ICU, region,
and religion (P<.001).
Conclusion The limiting of life-sustaining treatment in European ICUs is common
and variable. Limitations were associated with patient age, diagnoses, ICU
stay, and geographic and religious factors. Although shortening of the dying
process is rare, clarity between withdrawing therapies and shortening of the
dying process and between therapies intended to relieve pain and suffering
and those intended to shorten the dying process may be lacking.
While the principle that dying patients should be treated with respect
and compassion is broadly accepted among health care professionals, medical
practices for end-of-life care differ around the world. In the United States,
medicine has moved from a paternalistic model to one that promotes autonomy
and self-determination.1,2 Patient
expectations and preferences now help shape end-of-life practices, limiting
the use of technologies that may prolong dying rather than facilitate recovery.1,2 In Europe, patient-physician relationships
are still somewhat paternalistic.3-5
Different cultures and countries deal in diverse ways with the ethical
dilemmas arising as a consequence of the wider availability of life-sustaining
therapies.3,4,6 Some
have not adopted the Western emphasis on patient autonomy or methods of terminating
life support.3,4,6 In
the past, patients died in intensive care units (ICUs) despite ongoing aggressive
therapy.7 Theoretical discussions7 and
attitudes of critical care professionals concerning these issues have been
reported.4,8,9 In
North America, observational studies documenting physician behavior have noted
changes in the modes of patient deaths10-17 and
an earlier abandonment of life-sustaining treatments.10 Although
European observational studies have demonstrated withholding or withdrawing
of life-sustaining treatments in 6% to 13.5% of patients admitted to the ICU
and in 35% to 93% of dying patients, the results have come from individual
countries.5,17-21 The
overall incidence of end-of-life practices in European ICUs is not known.
Furthermore, no studies have been conducted to date comparing different European
countries or regions to verify whether reported variations from questionnaire
respondents4 are accurate.
End-of-life actions in ICUs include withholding or withdrawing life-sustaining
therapies,5,7-21 and
in Europe, community studies have described active euthanasia in the Netherlands22 and Belgium.23 At
the time this study was conducted, euthanasia was legally practiced in only
1 European country, but withdrawing life-sustaining therapies was common.5,19,21 It is not known whether
regional variations in attitudes toward use of euthanasia has any influence
on local ICU practice.
The objectives of this large multicenter study were to observe and describe
actual end-of-life practices in ICUs of several European countries, to determine
their overall incidence, to document variations in the pattern of practice,
and to analyze similarities and differences in terms of variables that might
explain the findings.
All consecutive adult patients admitted to the ICU who died or had any
limitation of life-saving interventions in the ICU from January 1, 1999, to
June 30, 2000, were studied prospectively. Patients were followed until discharge
from ICU, death, or 2 months from the decision to limit therapy.
Definitions of End-of-Life Categories
End-of-life categories were defined prospectively to enable the classification
of each patient into 1 of 5 mutually exclusive categories: cardiopulmonary
resuscitation (CPR); brain death; withholding life-sustaining treatment; withdrawing
life-sustaining treatment; and active shortening of the dying process. Withholding treatment was defined as a decision that was
made not to start or increase a life-sustaining intervention. Patients not
undergoing CPR were classified as withholding therapy. Withdrawing treatment was defined as a decision that was made to actively
stop a life-sustaining intervention presently being given. Active shortening of the dying process was defined as a circumstance
in which someone performed an act with the specific intent of shortening the
dying process; these acts did not include withholding or withdrawing treatment
although withholding or withdrawing could occur prior to SDP. Examples included
an intentional overdose of narcotics, anesthetics, or potassium chloride. Cardiopulmonary resuscitation was defined as a death despite
use of ventilation and cardiac massage, that is, failed or unsuccesful CPR. Brain death was defined as a documented cessation of cerebral
function and meeting the criteria for brain death.
The term "shortening of the dying process" was used instead of active
euthanasia because Dutch investigators insisted that the term "active euthanasia"
could not include most ICU patients who could not request the action. Several
other terms were considered, but shortening of the dying process was accepted
by all investigators as it describes the intent, the action that occurs, and
is a more neutral term that physicians might more readily record. In addition,
as some investigators might still be reluctant to admit to shortening of the
dying process, another question was added to evaluate the highest possible
incidence of actions that might be considered active euthanasia (although
most of these actions were probably not active euthanasia). For each patient,
physicians were asked whether any other action (not forgoing therapy) taken
to relieve patient suffering may have contributed to the patient's death.
In each institution, the senior intensivist responsible for patient
care and for end-of-life decisions determined the end-of-life practice and
was responsible for filling out the study data form. A hierarchy for categorizing
patients used the more active mode of limitation if more than 1 was recorded.
Patients were classified as "withhold" only if that was the sole limitation
made, as "withdraw" if treatment was both withheld and withdrawn, and as "shortening
of the dying process" if withholding or withdrawing and shortening of the
dying process decisions were involved. Patients who died without a treatment
limitation either underwent CPR that was unsuccessful or were diagnosed with
brain death. If a patient underwent successful CPR before withholding or withdrawing
life-sustaining therapies, or was considered brain dead after withholding
or withdrawing therapies, the patient was categorized as withholding or withdrawing
according to the prioritization given above.
Ethical and Legal Considerations
No interventions or treatments were given, withheld, or withdrawn from
patients as part of this observational study. Countries and centers were coded
for the purpose of anonymity and study patients were numbered consecutively
to ensure confidentiality and to allow clinicians to report practices of questionable
legality. Individual institutional ethics committee approval with a waiver
of informed consent was required and obtained from each participating institution.
Potential French centers could not participate as they could not obtain approval
from their ethics committee.
Study Centers and Data Collection
National representatives of the Ethics Section of the European Society
of Intensive Care Medicine were asked to coordinate the study for each country
and find several other ICUs in each respective country from a variety of institutions.
Coordinators finalized definitions, data forms, and procedures (including
a manual) for the study, and then met with principal investigators from each
national center to explain the study, to describe inclusion and exclusion
criteria, and to instruct on how to complete the forms. The forms were tested
for reliability by giving them to investigators to complete for hypothetical
test cases initially and again after 2 weeks. Agreement between the initial
and repeat administrations was evaluated by κ coefficient of reliability,
an interrater measure of agreement beyond chance. A value of 0.75 is considered
excellent agreement, values between 0.40 and 0.75 are taken to represent fair
or good agreement. Values of coefficients were above 0.6. Additional procedures
to improve validity and consistency included actual test cases from centers
before the study started, concurrent audit and feedback throughout the study,
case audits, site visits, and an Internet site with frequently asked questions
and meetings among investigators. Not all centers enrolled patients during
the entire 18-month study.
The study data form included patient and institutional characteristics.
Patient characteristics were sex, age, religious affiliation, ICU admission
diagnosis, chronic disorders, type of end-of-life category, specific therapies
limited, the method of shortening of the dying process (if relevant), whether
interventions (other than forgoing life-sustaining treatments or shortening
of the dying process) to relieve patient suffering may have contributed to
patient mortality, and dates and times of (1) ICU admission, (2) death or
discharge, and (3) decisions to limit therapy. Institutional data included
country, hospital mortality rate, number of ICU admissions, practice (academic
or nonacademic [private, public, or other]), and physician religious affiliation.
Countries were divided into 3 geographic regions prior to data analysis:
northern (Denmark, Finland, Ireland, the Netherlands, Sweden, and United Kingdom),
central (Austria, Belgium, Czechia, Germany, and Switzerland), and southern
(Greece, Israel, Italy, Portugal, Spain, and Turkey). The mean number of ICU
admissions per month was used to categorize each institution by its turnover
as small (≤30), intermediate (31-60), or large (≥61). The institutional
variable practice was dichotomized into academic/nonacademic.
For each patient the main outcome variable was the end-of-life category.
Univariate associations of end-of-life categories with the nonnumerical variables,
sex, diagnosis, chronic disorder, region, practice, and religion were tested
using the χ2 test. When any cell had an expected frequency
less than 5, an exact P value substituted the asymptotic
one routinely calculated. Time lapse between 2 events (length of stay in the
ICU, time from ICU admission until first limitation, time from the first decision
to limit treatment until death, or time from the decision for the most active
form of limitation of therapy until death) were shown to be in all cases very
skewed and significantly deviated from normality by Lilliefors test. Descriptive
statistics for those variables include medians and interquartile range (IQR),
and differences among groups determined by region, practice, or religion were
tested using the nonparametric Kruskal-Wallis rank test.
A multiple logistic regression was used to examine and test the associations
of the odds for treatment limitations with the factors age, sex, diagnosis,
chronic disorder, ICU length of stay, region, practice, and turnover. The
outcome variable was the dichotomy "any limitation" (including withholding,
withdrawing, or shortening of the dying process) vs "failed CPR." Collinearity
of physician's religion and region prevented the inclusion of both variables
in the model. The cumulative probability of death as a function of time from
the most active limitation adjusted for age, sex, diagnosis, practice, turnover,
and region was obtained using a Cox proportional hazards model.
Statistical analyses were performed using SPSS version 10 (SPSS Inc,
Chicago, Ill) and StatXact version 4 (StatXact-Cytel Software Corp, Cambridge,
Mass). A test was considered significant if P<.05.
All P values reported are 2-sided. Funding sources
had no involvement in the above methods.
During the study, 31 417 patients (range, 111-3118 patients per
center) were admitted to ICUs in 37 centers located in 17 countries over 13.5
months (range, 1-18 months). Of the 31 417 patients, 4280 died or had
life-sustaining treatments limited in some fashion. Of the 4280 patients,
32 were excluded, 27 were younger than 13 years old or were of unknown age,
and 5 had no end-of-life information. Thus 4248 patients (13.5% of those admitted
to ICUs) comprised the study population. Patient characteristics including
age, sex, ICU admission diagnoses, religion, and mortality are shown in Table 1.
Limitation of life-sustaining therapy occurred in 3086 (72.6%) of 4248
patients, that is, 9.8% of ICU admissions and 76.0% of dying patients (3086/4058).
The frequency of the different end-of-life categories together with the mortalities
and range of percentages in the countries for the 4248 patients are shown
in Table 2. Of the 3086 patients,
2734 (88.6%) received mechanical ventilation and at least 1815 (58.8%) were
receiving vasopressor agents at the first limitation of therapy. Withholding
preceded or accompanied withdrawal of therapy in 1335 of 1398 patients (95.4%)
who underwent withdrawing treatment. All patients who underwent shortening
of the dying process already had previous therapies withheld or withdrawn.
Shortening of the dying process was used at 9 centers in 7 countries. A large
proportion of the patients who underwent shortening of the dying process was
reported in 1 center. Of the 94 patients who underwent shortening of the dying
process, types of medications were available for all patients and doses used
for shortening of the dying process were available for 50 patients. Treatment
modalities used for the patients who underwent shortening of the dying process
included administration of opiates or benzodiazepines alone or in combination,
with 4 patients also receiving muscle relaxants and 6 receiving barbiturates.
Potassium chloride was not used in any of the shortening of the dying process
cases. The most commonly used opiate was morphine (administered to 73 patients
alone or combination), ranging from 5 to 200 mg. The most commonly used benzodiazepine
was diazepam (administered to 54 patients alone or combination), ranging from
20 to 200 mg. The most common combination was morphine and diazepam (administered
to 43 patients). The median dosage for morphine was 13.4 mg/h and for diazepam
was 13.8 mg/h. Doses of opiates and benzodiazepines were no higher than mean
doses used with withdrawing treatment in previous studies12,14 in
22 of the 50 patients and were within the ranges of doses used in all but
5 patients. In 8 of 94 patients, the drug doses given would unlikely lead
to death. Withdrawal of endotracheal tubes occurred in 17 of 94 patients (18.1%)
who underwent shortening of the dying process and 125 (8.9%) of 1398 patients
who underwent withdrawal of treatment (P = .01).
None of these withdrawals occurred in patients who received muscle relaxants.
One hundred thirty-nine of 2992 patients (4.6%) who did not undergo shortening
of the dying process had actions taken other than forgoing therapies, which
were classified by investigators as given to relieve patient suffering but
which may have contributed to patient mortality.
The median (IQR, 25th to 75th percentiles) length of stay in the ICU
for all study patients was 4.0 (1.0-11.1) days, and the median (IQR) time
from ICU admission until the first limitation was 2.8 (0.6-9.8) days. The
median (IQR) time from the first decision to limit treatment until death was
14.7 (2.9-54.7) hours. The median (IQR) time from the decision for the most
active form of limitation of therapy until death was 6.6 (1.5-31.7) hours
for all patients, 14.3 (2.2-67.1) hours for withholding, 4.0 (1.0-17.2) hours
for withdrawing, and 3.5 (1.5-8.5) hours for shortening of the dying process
(P<.001) patients. The predicted probability of
death over time for the different limitations, adjusted for age, sex, diagnosis,
practice, turnover, and region is shown in Figure 1. The respective probabilities of death within 24, 48, and
72 hours were 50%, 61%, and 68% for withholding, 80%, 89%, and 93% for withdrawing,
and 93%, 97%, and 99% for shortening of the dying process.
The distribution of patients by region was 1505 (35.4%) in the northern,
1209 (28.5%) in the central, and 1534 (36.1%) in the southern region. The
frequency of the end-of-life categories by region is shown in Table 2. In the southern European countries, CPR was used more (30.1%)
and withdrawing (17.9%) and shortening of the dying process (0%) were used
less frequently than those in the central (17.9%, 33.8%, 6.5%) or northern
(10.2%, 47.4%, 0.9%) countries (P<.001). The median
(25th-75th percentiles) length of stay in the ICU was 2.3 (0.8-7.2) days in
the northern countries, significantly shorter than those in the central and
southern countries (5.0 [1.6-13.1] days and 5.9 [1.6-13.9] days, respectively; P<.001). The median time (IQR) from ICU admission until
the first limitation was 1.6 (0.4-5.2) days in the northern, 3.3 (0.7-11.7)
days in the central, and 5.7 (1.5-13.8) days in the southern countries (P<.001).
Withdrawal of life-sustaining treatment occurred more often if the physician
was Catholic (41.2%), had no religious affiliation (35.6%), or Protestant
(44.4%) (based on completed questionnaires) than if they were Jewish (15.7%),
Greek Orthodox (13%), or Moslem (23.7%) (P<.001)
(Table 3). Use of CPR and withholding
treatment showed differences based on physician's religion. Patient religious
affiliations were Catholic (30%), Protestant (24%), Jewish (6%), Greek Orthodox
(6%), none (3%), Moslem (2%), other (2%), and unknown (27%). Differences in
CPR use, withholding, and withdrawing therapy based on patient religious affiliations
were similar to those found for physicians (data not shown). Multivariate
analyses revealed more withholding and withdrawing therapies than use of CPR
as patient age and days in ICU increased, in northern countries, in ICUs with
intermediate patient turnover, and in patient acute and chronic diagnoses
(Table 4). Withholding treatment
alone also was more common than CPR use in northern and central countries
(P<.001).
This is the first observational study to date to evaluate multiple countries
for the various ICU end-of-life practices, to examine religion as a factor
in end-of-life practices, to study time to death after different types of
therapeutic limitations, and to speculate about a lack of clarity between
therapies intended to relieve pain and suffering in patients and those intended
to shorten the dying process or cause death.
The study demonstrates that end-of-life actions are routine in European
ICUs. Life support was limited in 73% of study patients and 10% of ICU admissions.
Both withholding and withdrawing of life support seem to be accepted by most
European intensivists while shortening of the dying process, despite occurring
in a few cases, remains rare. The study provides useful data for physicians
and families for approximate times to death after various limitations. This
information should help those involved with the dying patient prepare for
the inevitable outcome.
The choice of limiting therapy rather than continuing life-sustaining
therapy was related to patient age, acute and chronic diagnoses, number of
days in ICU, frequency of patient turnover, region, and physician religion.
Previous studies have shown greater limitations for elderly patients,14,17,18,21 severity
of illness scores,5,17,21 length
of ICU stay,14,18,21 and
certain diagnostic categories such as cirrhosis, severe cardiac and respiratory
failure, organ system failure, cancer, and cardiac arrests.5,18 The
greatest frequency of limitations in the present study occurred for acute
neurologic diseases and human immunodeficiency virus for chronic disorders.
The northern region had more limitations, decreased CPR use, less time until
a limitation of treatment was determined, and perhaps consequent shorter ICU
stays. Regional differences may be related to religious differences that were
closely intertwined.
Physician and patient religion showed significant differences in use
of end-of-life therapies. These differences may be because of the varying
religions and cultures of European countries. A large US study failed to show
regional differences.13 Religious affiliation
was not evaluated,13 but the greater differences
in Europe may be related to more religious homogeneity within European countries
than the United States. Responses to bioethical issues have been shown to
vary throughout Europe.24 In the only other
large international multicenter study on ICU practices, differences in CPR
directives were observed depending on country; religion was not evaluated.17 Religious affiliations have been shown to influence
physician attitudes toward withdrawal of life support in hypothetical situations.4,22,25 Catholic physicians
were less willing to withhold or withdraw therapy4,22,25 ;
and in 1 study, Jewish physicians were more willing to limit therapy 8 and in another study less willing.25 The
present study demonstrated that physicians who were Protestant, Catholic,
or with no religion more frequently used withdrawal of life-sustaining treatments
than physicians who were Greek Orthodox, Jewish, or Moslem. A previous Israeli
study with only Jewish physicians demonstrated only withholding and no withdrawing
of life-sustaining treatments.20
Several factors account for the great variability in the end-of-life
categories between countries. First are the different religions and cultures
noted herein. Second, physician values and practices seem to differ from country
to country.3,4,6 Major
variations were noted for both continuation and limitation of life-sustaining
treatment. The rate for CPR use was 48% and for withdrawing treatment 5%,
which may indicate inordinate continuation of treatment, whereas rates for
CPR use of 5% and for withdrawing of 69% may signify insufficient energetic
care. Cook et al17 have noted variability in
medical centers within cities. Another possible explanation for the differences
between countries and regions may relate to the difference in case mix. Finally,
the variability may be related to the ongoing evolution of end-of-life practices7,10 occurring at different rates and to
different degrees among various countries.13
The conventional ethical view is that there is no moral distinction
between withholding and withdrawing life-sustaining therapies.26,27 This
belief is not universal,11 and some health
care professionals are more reluctant to withdraw than withhold therapies.4,8 This study indicates that both withdrawing
and withholding of life support have widespread acceptance in Europe. The
present study, however, demonstrates clinical differences between withholding
and withdrawing treatments: withdrawal of therapy was associated with earlier
and more frequent mortality. Previous studies in which questionnaires were
used or which had smaller numbers of patients led to similar conclusions.5,28 Another possible explanation for this
finding is that withdrawal of therapy occurred in more unstable patients.
At the time of this study, euthanasia was illegal in all European countries,
although legally pardoned in the Netherlands. A previous study also noted
euthanasia in Belgium,23 but evidence of euthanasia
in ICU practice was not available. This study confirms that active shortening
of the dying process, although reported in the ICUs of 7 countries, remains
rare. One possible reason for the infrequent use of active shortening of the
dying process in ICUs may be the dependency of ICU patients on life support.
Withdrawing or withholding life-support often leads to death thus minimizing
any perceived need for shortening of the dying process. The fact that all
shortening of the dying process therapies were preceded by withholding or
withdrawing and that the time course until death was similar for shortening
of the dying process and withdrawing might mean that a process of withdrawal
is observed for a while and then actions are taken to shorten the life of
the patient. If physicians were shortening the dying process from the outset,
a quicker death may have been observed.
Whether or not shortening of the dying process is considered euthanasia
is controversial. Active euthanasia includes the intent to cause death plus
the action that causes death. The purpose of shortening of the dying process
was to specify an action that directly caused the intentional death of the
patient. Discussions with investigators reporting shortening of the dying
process decisions confirmed that hastening death was the intention in all
shortening of the dying process cases. A small number of physicians have used
shortening of the dying process for intent, but without actions causing death
most likely because the definition for shortening of the dying process emphasized
the intent to shorten the dying process without specifying (except for examples)
specific actions required to cause death. The majority of cases of shortening
of the dying process can be equated with euthanasia as physicians showed intent
and actions that caused death.
The distinction between therapies intended to relieve pain and suffering
and those intended to shorten the dying process or hasten death may not be
so clear or easily determined. Differentiation may be difficult as intentions
are subjective and private and only self-reporting or an analysis of extreme
actions will be determinant.29 In fact, most
end-of-life decisions have multilayered intentions that are complex, ambiguous,
and often contradictory.30 It is unclear how
many physicians around the world who withdraw treatments and give therapies
to relieve pain or suffering also intend to shorten the dying process. Some
physicians give much larger doses of medications than are required for relief
of pain or suffering so that the patient can die with dignity, but do not
call this euthanasia. The present findings that doses of opioids and benzodiazepines
reported for shortening of the dying process treatment with the intent to
cause death were in the same range as those used for symptom relief in earlier
studies12,14 and leading to death
within similar times as in patients undergoing withdrawing treatment, leads
to the speculation that the distinction between treatments to cause death
and to relieve suffering in dying patients may be unclear. It is recognized
that absolute doses may not be indicative of euthanasia as prior exposure,
tolerance, and duration of medications are important. That the distinction
is not sharp is further supported by the fact that 5% of the patients (not
receiving shortening of the dying process treatment) received therapies that
may have contributed to mortality, raising the possibility that the adjunct
drugs contributed to death in some non–shortening of the dying process
cases too.
Strengths of the present study include the prospective design and enrollment
of a large number of consecutive patients from 37 ICUs in 17 countries, evaluation
of all limitations and deaths in all admitted patients, analysis of the apparent
reasons for the findings, and direct reporting of actions rather than theoretical
responses to a questionnaire. Anonymity and contemporaneous documentation
probably resulted in honest and more accurate reporting. However, the present
study has limitations. The patients studied may not be representative of the
ICU population of each European country. Since only 1 to 4 centers participated
from each country, it was recognized a priori that the participating ICUs
did not necessarily represent the practices of all ICUs in that country. Therefore,
regions were evaluated. In addition, participants by their special interest
in ethical issues may not necessarily share the attitudes of unselected ICU
physicians. Severity scores of the patients were not analyzed. Underreporting
of practices for fear of legal ramifications cannot be excluded. The findings
of the present study do reflect what physicians from different countries say
they do.4
Despite the importance of end-of-life physician practices, many related
questions remain unanswered. For instance, what are the perspectives of physicians,
nurses, patients, and families regarding the ICU and potential dying experiences
in different countries with different cultures? The present group has started
such a study. Only with knowledge of actual physician behavior, such as that
observed in this study, can future studies hope to ask the appropriate questions
and then can proper public debate occur.
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