End-of-Life Issues in the Intensive Care Unit

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218 End-of-Life Issues in the Intensive Care Unit

Nicholas S. Ward, J. Randall Curtis, Mitchell M. Levy

In the last century, the process of dying changed dramatically. Previously, doctors simply did all they could for a patient, and when their treatments failed, the patient died, almost always at home. However, with the advent of more sophisticated medical technologies, even patients with severe organ failure can be kept alive. Unfortunately, with this progress has come a new set of complex medical, ethical, and societal issues.

In the United States, about 80% of people now die in healthcare facilities (60% in acute care facilities),1 despite the fact that about 90% of Americans polled say they would prefer to die at home.2 This disparity is due to two factors: (1) many people die while undergoing treatments meant to postpone death—treatments that are often futile; and (2) many families are unable to care for a dying person or are uncomfortable having a loved one die at home. The net result is that most people will die in a hospital or other healthcare facility, and many of them will undergo high levels of medical care before death. A recent study showed that about 20% of Americans will die in an intensive care unit (ICU) or be admitted to an ICU just before death.3

Two conclusions can be drawn from the preceding information. One is that a tremendous amount of health care is being delivered to dying patients. This has been reflected in several studies, such as that of Cher and Lenert, which showed that a relatively large percentage of Medicare expenditures goes to treat patients in the last weeks of their lives.4 The other conclusion is that doctors have to learn a new set of skills that were not necessary in the past. They need to be able to recognize patients who are going to die despite medical care and help decide which of the almost limitless supply of medical therapies available are appropriate and which are not. Physicians need to guide their patients through a maze of medical options in an attempt to balance preservation of life with quality of life—a daunting task, to say the least.

image How Are Critically Ill Patients Dying?

In 1995, a landmark study in end-of-life issues was published. This was the first large-scale attempt to define how seriously ill people die in American hospitals. In a two-part study involving 4301 seriously ill, hospitalized patients, the investigators examined multiple aspects of end-of-life care and found major shortcomings in current practice. Only 47% of the time did the physician know when a patient wanted to avoid cardiopulmonary resuscitation (CPR), and the incidence of dying with moderate or severe pain was 50%.5

More insight into the dying experience came in subsequent studies that showed that the vast majority of ICU deaths occur only after a decision to limit life support has been made.6,7 In two important studies, Prendergast and coworkers helped define how patients die in ICUs.6,8 In their first study, they compared deaths in their ICU from two periods, 1987 to 1988 and 1992 to 1993, to determine how often CPR was performed before death and how often limits were placed on life support before death.9 Their data showed that the incidence of CPR before death had declined from 49% to 10% and that the incidence of withholding or withdrawing life support had increased from 51% to 90% of all ICU deaths.

In an effort to benchmark their data with the rest of the country, the same investigators then did a large follow-up study 1 year later. They collected data from more than 6000 patient deaths occurring in 131 ICUs in 38 states over a 6-month period and analyzed the data for the incidence of various limits on life support. They found that on average, only 25% of patients dying in ICUs were given CPR before death. About 70% of patients had some restriction on life support, and almost 50% of patients had some medical therapy withheld or withdrawn before death.6

The other striking piece of data to emerge was the degree of variability that existed among ICUs. The incidence of patients dying with full aggressive measures ranged from 4% in one ICU to 79% in another. Likewise, the incidence of withdrawing life support ranged from 0% to 79%, depending on the ICU. These data clearly show that although the overall practice of limiting life support in ICUs in the United States is common, there is tremendous variability from place to place in end-of-life care.

In 2003, a study examined deaths in 31 ICUs in 17 European countries. Overall, the percentage of patients dying with some limits on life support was 72.6%, which was very similar to studies done in the United States. As in the American studies, there was also tremendous variability in practices among the different ICUs, with rates of CPR before death ranging from 5% to almost 50%.9

image What Accounts for Variability in Practice?

It should not be surprising that there is so much variability in a practice as multidimensional as end-of-life care. Even the standard practice of medicine varies from institution to institution. The decision to limit or not limit life support is generally a complex one that may reflect the personal biases of both physician and patient. Many attempts have been made to find patterns among different types of physicians and patients that can explain the variation. For example, one study showed that university-based physicians are more likely than community-based physicians to write do-not-resuscitate (DNR) orders and withhold or withdraw life support.10 A similar study showed that patients without private physicians in the ICU were more likely to undergo active withdrawal of life support.11 Unfortunately, studies like this are hard to interpret unless one knows the contexts in which these decisions were made. An increased tendency to withhold life support from a terminally ill patient may reflect a weaker physician-patient relationship or a stronger one based on the patient’s preferences.

Other studies have sought to explain variation by culture, race, or religion.12–16 Although such factors may play a role in these important decisions, and there may be some general trends in decision patterns, there is enough variation even within cultures, races, or religions to indicate that one cannot generalize this information to a given individual. Physicians need to be cognizant of the fact that their patients may have markedly different views of optimal end-of-life care, regardless of their culture, religion, or race.

image Predicting Outcomes

A central problem complicating end-of-life decisions is the difficulty of predicting outcomes in critically ill patients. The combination of multiple coinciding medical problems and rapidly changing clinical status can make this a very difficult task. Essentially, two objective tools are available to a physician when trying to determine the prognosis of a critically ill patient: published outcomes and severity scores. Both can be helpful, yet have limitations. In addition, the role of a physician’s personal experience is important but can also have important limitations.

Severity Scores

Severity scores have been available for almost 3 decades, and much has been learned in that time. In most severity score algorithms, data are collected during the first 24 hours of admission and are then used to compile a score that predicts the risk of death during hospitalization. Many of these scoring systems were developed by reviewing data from thousands of ICU patients and employing logistic regression models to choose some important input variables. Other variables were simply chosen based on presumed clinical value. These scores were then validated prospectively on patients.

Unfortunately, there are several problems with these severity score–based systems. First, they make predictions based on hospital outcomes at the time of their creation. Thus, as medical treatments improve, the scores must be updated. In the 1970s, for example, acute respiratory distress syndrome (ARDS) had a hospital mortality approaching 80%, so its presence might justifiably increase a patient’s severity score. Presently, ARDS has about 40% hospital mortality. Thus, a severity scoring system using the diagnosis of ARDS, or even components of the diagnosis such as hypoxemia, would have to be adjusted. Some commercially available proprietary severity scoring systems, such as the Acute Physiology and Chronic Health Evaluation (APACHE) methodology, are updated and revalidated on a regular basis to avoid this problem, but many that are widely used today, such as APACHE II, are based on patient data collected as many as 2 or 3 decades ago.

Another problem with using severity scores is that most models derive their predictions from factors present at or shortly after admission to the ICU and do not provide updated mortality estimates as the patient’s condition changes. Further, severity scores often give intermediate mortality estimates such as 60% instead of a clear yes-or-no answer. Even these numbers are subject to confidence intervals. Perhaps the most glaring problem of using severity scores is that they say nothing about morbidity, disability, or survival after hospitalization. These factors are often just as important as risk of death in making end-of-life decisions. A patient may accept a 30% chance of survival if it were followed by a high quality of life, but not accept a 70% chance of survival if it were likely to entail a poor quality of life.

Outcome Data

Many of the same problems encountered with severity scores characterize the use of outcome data. Although published outcome studies are an essential tool for clinicians in predicting a course of illness, they suffer from two major problems. One is that the population studied for a particular illness may not share the same characteristics as a particular patient. For example, in a large multicenter clinical trial of a new therapy for sepsis, the mortality rate in the control (untreated) arm was 31%.17 It is important to note, however, that this trial excluded patients with conditions such as renal failure, liver failure, pancreatitis, acquired immunodeficiency syndrome (AIDS), and a variety of other comorbid conditions, thus limiting the usefulness of these data for prognostic purposes.

Another problem with using outcome data, similar to the severity scores, is the rapidity with which therapies can change and improve. In four published studies by different authors between 1981 and 2000 examining the mortality of Pneumocystis carinii pneumonia in ICU patients, the mortality decreased from 86% to approximately 50%.18 Similar changes in outcome over time have been reported with a variety of other illnesses, such as ARDS, as treatments have improved.

image Caring for Families in the Intensive Care Unit

Impact of Family Meeting

Relatives, partners, and friends often provide support and care for a patient, which for some will include the responsibility of surrogate decision making. Surrogate decision makers are often under an enormous amount of emotional stress, and decision making during these circumstances can be difficult. In addition, one study revealed that despite discussions with ICU physicians, only half of families of critically ill patients adequately understood their loved ones’ diagnoses, prognoses, or treatments.19 Despite this, clinicians and health systems often neglect the care of the family as part of the overall care of a patient. Therefore, clinician-family communication is an important component of good quality care. In addition, effective clinician-family communication reduces the stress on family members of critically ill patients and improves the family members’ level of understanding. This is of critical importance in the ICU because if the patient’s family is under significant distress, their ability to provide surrogate decision making may be impaired, and the medical decisions they make may not accurately reflect the wishes of the patient.

In addition to the multitude of data showing that the way we communicate with families has a significant impact, there are also data showing that interdisciplinary team communication has a significant impact on important patient and family outcomes. Observational studies show increased survival, shorter lengths of stay, and improved patient satisfaction when there is good nursing-physician communication.20 In addition, patients and families have reported that interdisciplinary communication is an important part of good end-of-life care, and most studies of interventions that have improved end-of-life care include an interdisciplinary team in the intervention. Unfortunately, some ICU family meetings occur only between the physician and the family. Underutilization of the many professionals involved with a critically ill patient’s care is a common mistake. Care of ICU patients is provided by a large interdisciplinary team that includes consulting physicians, nurses, social workers, and members of the clergy. These healthcare providers often know the patient and family from different perspectives, and holding a meeting without attempting to have all relevant members present can result in miscommunication and may result in missed opportunities to provide families with the best possible resources.

Family Outcomes: Anxiety, Depression, Posttraumatic Stress Disorder

An important problem with critical care delivery systems is dissatisfaction among family members. There is also evidence to suggest that our current approach causes anxiety, depression, and posttraumatic stress disorder (PTSD) among family members. Many critical care units only conduct family meetings after it is clear that an ICU patient is actively dying, but it is important to meet with all ICU families early in the ICU stay, because family caregivers are under a high level of emotional and physical stress. In fact, family members of patients who survive the ICU are more dissatisfied with communication in the ICU than family members of patients who die.21 This likely reflects the fact that family members of ICU patients experience an important unmet need with regard to regular and systematic communication with ICU clinicians. Several interventions have been shown to improve family satisfaction: time spent with physicians,22 timing of family meetings, and open visiting hours.23

image Who Decides?

Decision Making about Life-Sustaining Treatments

As stated earlier, the vast majority of people will die with some limit on life support in place, whether in or out of an ICU. Unfortunately, the patient can rarely participate in these decisions. Most studies show that someone else makes the decision to limit a dying patient’s life support 60% to 70% of the time.7,24 Therefore, the burden of these difficult decisions falls to a proxy (a legal delegation) or a surrogate (a nonlegal delegation). Most often, this is a family member.

The process of surrogate decision making is fraught with problems. Although most would agree that family or friends of the patient are the best people to make such decisions, several studies have shown that patients rarely discuss specific treatment options with their proxies, and surrogate decisions correlate poorly with what the patient would actually want done.25,26 Further, in a study by Hare et al., it was shown that surrogates often place greater emphasis on certain aspects of dying such as pain and suffering than patients do; patients are more concerned with burdening their families and the amount of time left to live.19

Legal Issues

In the United States, all 50 states now recognize the legality of a patient’s right to refuse medical treatment, although there remains some controversy and confusion about specific issues. The legal issues involved in proxy decision making can also be a source of great confusion. Perhaps realizing that it is impossible to account for the many possible family and social relationships involved, most states have few laws dealing with the issue of surrogate decision makers and have purposely kept the codes vague and malleable.27 Most states accept a properly drafted written advance directive as sufficient legal guidance to limit life support. Unfortunately, most advance directives or living wills are too vague in their language, using phrases such as “terminal illness” and “little chance of recovery,” which are subject to interpretation. Diseases such as chronic obstructive pulmonary disease and congestive heart failure may be considered terminal illnesses by some people but not by others. Some people may consider diseases such as early-stage lung cancer not imminently terminal.

Nevertheless, these directives can be of great help. They can help prevent futile or unwanted care when no other surrogate is available. They may be useful in family decision making when dealing with an unconscious patient facing potentially futile care. The previously stated wishes of the patient in an advance directive can help with feelings of guilt or uncertainty regarding end-of-life decisions. They can also be helpful when there is disagreement between surrogates about a course of action. Because a surrogate, by definition, is an agent representing what the patient would decide if he or she were able, the advance directive can be a helpful guide.

Sometimes advance directives can be a source of discord, such as when the written directive differs from what a surrogate decides. In most states, the law recognizes a properly drafted and witnessed directive as the legal opinion that should be followed; however, many physicians are wary of ignoring the requests of a living surrogate, especially if it is a spouse or other close family member. In situations like this, attempts should be made to build consensus among all parties before making any decision. Most state laws regarding written advance directives also allow for some flexibility in the physician’s obligation to follow them. They often state that if a physician feels that the directive is of questionable validity or if he or she feels ethically unable to follow the directive, it is not binding.

Patient Autonomy Versus Medical Paternalism

A central problem with the end-of-life decision-making process is defining the role of the physician. Usually the physician’s role is a combination of educator and adviser, but this is not always the case. In the past, physicians were more likely to dictate courses of action or treatment plans for their patients, a concept referred to as medical paternalism. In many parts of the world, medical decisions continue to be made this way with little input from the patient or family. In these cultures, patients are often comfortable with this kind of decision making. More recently in the United States, the concept of patient autonomy has dictated medical decision making. In the extreme form of patient autonomy, the physician’s role is only to educate the patient about the problem and offer available treatment plans, along with their risks and benefits. The patient then independently chooses a course of action. Under this model, it is the obligation of the physician to provide the medical information necessary for the patient to have the appropriate knowledge for informed decision making. The physician plays no part in the decision making. Many physicians use this model of practice today, or something similar to it, believing it empowers patients and frees them from physician bias.

Although many patients desire autonomy, when it comes to decisions about life-sustaining therapy in the ICU, often the decisions fall to the surrogate. In the extreme, the autonomy model may make family members feel like they are being abandoned and may place unnecessary stress on the family. Over the same time period, much of the rest of the world used a model of decision making in the ICU that has been called parentalism (the non-sexist version of paternalism), in which physicians are the medical decision makers, with little or no input from the patient or family. In this latter extreme version, the patient and family are informed about the treatment patients will receive, and often only involved in decision making when the patient wishes to forgo treatment.

In contrast to both of these approaches, many physicians and patients believe the physician is obliged to be involved in the decision-making process and often to recommend a course of action. The physician thus offers several possible courses of action but makes specific recommendations. This model is referred to as shared decision making and may well represent an ideal blending of the autonomous and parentalistic approach. In this model, caregivers do their best to understand the wishes of their patients. This is accomplished through a process of genuine listening to family members and eliciting their understanding of the wishes of their loved one, then combining that knowledge with the clinician’s best guess about the likely prognosis and outcome. Through this process, a clinician can proactively offer an opinion about the appropriate course of therapy. In 2005, five European and North American critical care societies issued a joint statement supporting the model of shared decision making when caring for ICU patients.28 Ultimately, it is up to each individual physician to determine the degree of involvement warranted in end-of-life decisions.

There are multiple components of the shared decision model that are essential for an even exchange of information and a truly joint decision made in concert with the patient and family. Table 218-1 describes in detail the components of shared decision making, and the use of these components is further elaborated in the following strategies for family meetings.

TABLE 218-1 Shared Decision Making

Dimensions of Shared Decision Making Example Physician Behaviors and Questions
Providing medical information and eliciting patient values and preferences Discuss the nature of the decision.
What are the essential clinical issues we are addressing?
Describe alternatives.
What are the clinically reasonable choices?
Discuss pros/cons.
What are the pros and cons of the treatment choices?
Discuss uncertainty.
What is the likelihood of success of treatment, and how confident are we in this estimate?
Assess understanding.
Is the family now an “informed participant,” with a working understanding of the decision?
Explore the patient’s values/preferences.
What is known about the patient’s medical preferences or values? What is important to the patient?
Exploring family’s preferred role in decision making Discuss the family’s role.
What role should the family play in making the decision?
Assess desire for others’ input.
Is there anyone else the family would like to consult?
Deliberation and decision making Explore “context.”
How will the decision impact the patient’s life?
If the family is to participate in decision making, elicit family opinion about the best treatment choice.
What does the family think is the most appropriate decision for the patient?

Adapting Shared Decision Making to Fit Each Patient and Family

Although the shared decision-making model is the preferred model in many ICU settings, each patient and family is unique; as circumstances and prognosis change, the role the family wishes to play may change. Therefore the initial meeting should often be one that models shared decision making, but after the exchange of information regarding the status of the patient and the patient’s treatment preferences, it is important to assess the role the family wishes to play in the decision-making process. The family may not wish to partake in the decision-making process, and the process will then shift toward the parentalism model. If the family wishes to be closely involved, then the decision-making process should be a shared process in which physicians give prognostic information and, based on that information and discussion of the patient’s values, offer to provide a recommendation on treatment decisions.

It is important to recognize that the decision-making model is a dynamic process that may change several times throughout the course of an ICU stay. As patients become more critically ill and the prognosis is more certain, the physician should be willing to take on a more active role in the decision-making process to relieve the family of the burden of decision making in these circumstances. Whichever decision-making model is utilized, it must be one that is responsive to the needs of the family. Research suggests that physicians often have one model of decision making they use for all patients.29 The physician and interdisciplinary team must be prepared to adapt this model to fit the individual patient and family.

Most interventions that have shown to be beneficial in improving care for ICU patients follow a standard procedure or protocol. Using such a protocol will encourage consistency across the ICU and help prevent oversights and miscommunication. This was recently tested in a randomized controlled trial which demonstrated decreased symptoms of anxiety and depression through use of a protocolized family conference intervention.30 Obviously, communication with families cannot be performed in a manner that is so overprotocolized the team comes across as rigid and uncaring. Each individual patient and family is different and must be treated individually—but with key components applied in an individualized way. A mnemonic was developed that features five key elements to help guide clinicians in communicating with families: VALUE. This mnemonic is described in Table 218-2 and has been shown to result in improved family outcomes.31

TABLE 218-2 VALUE: Five-Step Approach to Improving Communication with Families in the ICU

V Value family statements.
A Acknowledge family emotions.
L Listen to the family.
U Understand the patient as a person.
E Elicit family questions.

image Conclusion

Clearly, the process of dying is changing. Although the physician has always had an important role to play, that role has also changed. Today’s physician not only must be adept at administering comfort measures but also must decide when to initiate those measures rather than other therapies aimed at prolonging life. Because the dying process frequently involves the healthcare system, physicians in these settings need to have good end-of-life skills. The model of decision making in the ICU is evolving. A model in which decision making is shared among physicians, patients, and families is emerging as a compassionate alternative to the two extremes of autonomy and parentalism. Failure to address these issues will result in patients getting more futile care at the expense of their own comfort and increased costs to the healthcare system.

Key Points

1 A majority of deaths occur in healthcare institutions such as hospitals and ICUs as opposed to home. Studies now show that the vast majority of patients who die in the hospital do so only after some limitation has been placed on life-sustaining treatments. Other studies show that ICUs, and even physicians, can vary greatly in the frequency with which they limit or withdraw life support.
2 Many studies have tried to demonstrate what accounts for the dramatic variability in end-of-life practices. Various patient characteristics such as ethnicity, and physician characteristics such as community-based versus university-based status, may impact these decisions, but these factors do not explain all the variability.
3 Currently, most decisions to limit life support are not made by the patient. This raises problems regarding surrogate decision making. Clearly identifying one legal surrogate can be difficult, and most state laws in the United States give few specifics about who can qualify as a surrogate decision maker. Usually the decision to limit life support is made by the healthcare team in association with the family.
4 One of the greatest barriers to delivering optimal end-of-life care is the ability to predict patient outcomes. Two common tools that aid in this are validated severity scores and published outcome data. However, both are fraught with potential error and should not automatically be relied on as accurate predictors of morbidity and mortality.
5 Throughout the world, cultures and people differ in their beliefs about how important medical decisions should be made. Some favor a decision-making model in which the physician makes the majority of the decisions—often referred to as medical paternalism. In the latter half of the 1990s, the United States has been characterized by a model that favors the patient (or surrogate) as the primary decision maker—referred to as patient autonomy. Both systems have advantages as well as drawbacks, and a physician must consider the patient’s and family’s perspectives on decision making.

Annotated References

Cook DJ, Guyatt GH, Jaeschke R, et al. Determinants in Canadian health care workers of the decision to withdraw life support from the critically ill. JAMA. 1995;273:703-708.

This prospective study identifies several factors that influence the decision to withdraw life support. The most important factors were likelihood of surviving the current episode, likelihood of long-term survival, premorbid cognitive function, and patient age.

Curtis JR, Rubenfeld GR. Managing death in the ICU. New York: Oxford University Press; 2000.

This comprehensive textbook has contributions from many authors and includes practical suggestions for end-of-life care, as well as philosophical pieces.

Danis M, Federman D, Fins JJ, et al. Incorporating palliative care into critical care education: principles, challenges, and opportunities. Crit Care Med. 1999;27:2005-2013.

This well-written overview describes the fundamental principles of palliative care in the ICU and offers concrete suggestions for building an educational curriculum.

Danis M, Mutran E, Garrett JM. A prospective study of the impact of patient preferences on life-sustaining treatment and hospital cost. Crit Care Med. 1996;24:1811-1817.

In this prospective study, patients were asked about life-support preferences and then followed for 6 months. Of interest, there was no significant association between patient desire for life support and the use of these therapies.

Johnson D, Wilson M, Cavanaugh B, et al. Measuring the ability to meet family needs in an intensive care unit. Crit Care Med. 1998;26:266-271.

A survey instrument was used to identify the top needs of families of critically ill patients. Continuity of caregiver communication was identified as a priority.

Prendergast TJ, Luce JM. Increasing incidence of withholding and withdrawal of life support from the critically ill. Am J Respir Crit Care Med. 1997;155:15-20.

This important prospective study describes how patients die in ICUs and documents a dramatic increase in the practice of limiting some form of life-support measures in several hospitals over a 5-year period.

SUPPORT principal investigators. A controlled trial to improve care for seriously ill hospitalized patients: the Study to Understand Prognoses and Preferences for Outcomes and Risks of Treatments (SUPPORT). JAMA. 1996;274:1591-1598.

In two consecutive 2-year periods, a prospective observational study documented major shortcomings in communication, the frequency of aggressive treatment, and the characteristics of death in the hospital. An intervention study using a nurse to facilitate communication and clinical care of the dying demonstrated essentially no improvement in outcomes.

Thompson BT, Cox PN, Antonelli M, et al. Challenges in end-of-life care in the ICU: statement of the 5th International Consensus Conference in Critical Care: Brussels, Belgium, April 2003: executive summary. Crit Care Med. 2004;32:1781-1784.

A summary of the results of an international consensus conference on end-of-life care in which the shared decision model is well described.

Lautrette A, Darmon M, Megarbane B, et al. A communication strategy and brochure for relatives of patients dying in the ICU. N Engl J Med. 2007;356:469-478.

A seminal publication in end-of-life care. This randomized controlled trial tested an intervention that included administration of a bereavement pamphlet and standardized family meetings. The results demonstrated a significant reduction in symptoms of anxiety, depression, and posttraumatic stress disorder among families of patients who died in the ICU.

References

1 Field M. Approaching Death: Improving Care at the End of Life. Washington, DC: National Academies Press; 1997.

2 Knowledge and Attitudes Related to Hospice Care [National Hospice Organization Survey]. Princeton, NJ: 1996.

3 Angus DC, Barnato AE, Linde-Zwirble WT, et al. Use of intensive care units at the end of life in the United States: an epidemiologic study. Crit Care Med. 2004;32:638-643.

4 Cher DJ, Lenert LA. Method of Medicare reimbursement and the rate of potentially ineffective care of critically ill patients. JAMA. 2001;278:1001-1007.

5 SUPPORT principal investigators. A controlled trial to improve care for seriously ill hospitalized patients: The Study to Understand Prognoses and Preferences for Outcomes and Risks of Treatments (SUPPORT). JAMA. 1995;274:1591-1598.

6 Prendergast TJ, Claessens MT, Luce JM. A national survey of end-of-life care for critically ill patients. Am J Respir Crit Care Med. 1998;158:1163-1167.

7 Faber-Langendoen K. A multi-institutional study of care given to patients dying in hospitals: Ethical and practice implications. Arch Intern Med. 1996;156:2130-2136.

8 Prendergast TJ, Luce JM. Increasing incidence of withholding and withdrawal of life support from the critically ill. Am J Respir Crit Care Med. 1997;155:15-20. (see comments)

9 Sprung CL, Cohen SL, Sjokvist P, et al. End-of-life practices in European intensive care units: The Ethicus Study. JAMA. 2003;290:790-797.

10 Bach PB, Carson SS, Leff A. Outcomes and resource utilization for patients with prolonged critical illness managed by university-based or community-based subspecialists. Am J Respir Crit Care Med. 1998;158(5 Pt 1):1410-1415.

11 Kollef MH, Ward S. The influence of access to a private attending physician on the withdrawal of life-sustaining therapies in the intensive care unit. Crit Care Med. 1999;27:2125-2132.

12 Hopp FP, Duffy SA. Racial variations in end-of-life care. J Am Geriatr Soc. 2000;48:658-663.

13 McKinley ED, Garrett JM, Evans AT, Danis M. Differences in end-of-life decision making among black and white ambulatory cancer patients. J Gen Intern Med. 1996;11:651-656.

14 Mebane EW, Oman RF, Kroonen LT, Goldstein MK. The influence of physician race, age, and gender on physician attitudes toward advance care directives and preferences for end-of-life decision-making. J Am Geriatr Soc. 1999;47:579-591.

15 Levin PD, Sprung CL. Cultural differences at the end of life. Crit Care Med. 2003;31(5 Suppl):S354-S357.

16 Vincent JL. Cultural differences in end-of-life care. Crit Care Med. 2001;29(2 Suppl):N52-N55.

17 Bernard GR, Vincent JL, Laterre PF, et al. Efficacy and safety of recombinant human activated protein C for severe sepsis. N Engl J Med. 2001;344:699-709.

18 Mansharamani NG, Garland R, Delaney D, Koziel H. Management and outcome patterns for adult Pneumocystis carinii pneumonia, 1985 to 1995: Comparison of HIV-associated cases to other immunocompromised states. Chest. 2000;118:704-711.

19 Azoulay E, Chevret S, Leleu G. Half the families of intensive care unit patients experience inadequate communication with physicians. Crit Care Med. 2000;28:3044-3049.

20 Truog RD, Campbell ML, Curtis JR, et al. Recommendations for end-of-life care in the intensive care unit: A consensus statement by the American Academy of Critical Care Medicine. Crit Care Med. 2008;36:953-963.

21 Wall RJ, Curtis JR, Cooke CR, Engelberg RA. Family satisfaction in the ICU: Differences between families of survivors and non-survivors. Chest. 2007;132:1425-1435.

22 Gries CJ., Curtis JR., Wall RJ., Engelberg RA. Family member satisfaction with end-of-life decision making in the ICU. Chest. 2008;133(3):704-712.

23 Lee MD, Friedenberg AS, Mukpo DH, Conray K, Palmisciano A, Levy MM. Visiting hours policies in New England intensive care units: strategies for improvement. Crit Care Med. 2007;35(2):497-501.

24 Lynn J, Teno JM, Phillips RS, et al. Perceptions by family members of the dying experience of older and seriously ill patients. SUPPORT investigators: Study to Understand Prognoses and Preferences for Outcomes and Risks of Treatments. Ann Intern Med. 1997;126:97-106. (see comments)

25 Hare J, Pratt C, Nelson C. Agreement between patients and their self-selected surrogates on difficult medical decisions. Arch Intern Med. 1992;152:1049-1054.

26 Sulmasy DP, Terry PB, Weisman CS, et al. The accuracy of substituted judgments in patients with terminal diagnoses. Ann Intern Med. 1998;128:621-629.

27 Sabatino CP. The legal and functional status of the medical proxy: Suggestions for statutory reform. J Law Med Ethics. 1999;27:52-68.

28 Thompson BT, Cox PN, Antonelli M, et al. Challenges in end-of-life care in the ICU: statement of the 5th International Consensus Conference in Critical Care: Brussels, Belgium, April 2003: executive summary. Crit Care Med. 2004;32:1781-1784.

29 White DB, Malvar G, Karr J, Lo B, Curtis JR. Expanding the paradigm of the physician’s role in surrogate decision-making: An empirically derived Framework. Crit Care Med. 2010;38:743-750.

30 Lautrette A, Darmon M, Megarbane B, et al. A communication strategy and brochure for relatives of patients dying in the ICU. N Engl J Med. 2007;356:469-478.

31 Cook DJ, Guyatt GH, Jaeschke R, et al. Determinants in Canadian health care workers of the decision to withdraw life support from the critically ill. JAMA. 1995;273:703-708.

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