BENEFITS OF PALLIATIVE CARE AT THE END OF LIFE

Most of the studies designed to determine the benefits of palliative care/hospice at the end of life have been done in the cancer setting. However, an increasing number of researchers are focusing on palliative care interventions for patients with other life-limiting diseases. The field of palliative care/hospice research is still growing, and meta-analyses of palliative care studies have been difficult because of variations in methodology and in the focus and extent of services [44]. Increasingly, studies are showing benefit to palliative care/hospice in terms of quality of life, satisfaction with care, and end-of-life outcomes, as well as cost-effectiveness.
A systematic review published in 2008 indicated weak evidence of benefit for palliative care/hospice; the results demonstrated significant benefit of specialized palliative care interventions in four of 13 studies in which quality of life was assessed and in one of 14 studies in which symptom management was assessed [29]. However, the authors of the review noted that most of the studies lacked the statistical power to provide conclusive results, and the quality-of-life measures evaluated were not specific for patients at the end of life [29]. Other research has shown that palliative care intervention was associated with significantly better quality of life and greater patient and/or family caregiver satisfaction [44,45,46]. Data to support benefit in reducing patients' physical and psychologic symptoms have been lacking [44]. Such symptoms were significantly improved when patients received care delivered by palliative care specialists [28].
Surveys of patients' family members also demonstrate a benefit of palliative care. The Family Assessment of Treatment at the End of Life (FATE) survey was developed to evaluate family members' perceptions of their loved one's end-of-life care in the Veterans Administration (VA) healthcare system. FATE consists of nine domains: well-being and dignity, information and communication, respect for treatment preferences, emotional and spiritual support, management of symptoms, choice of inpatient facility, care around the time of death, access to VA services, and access to VA benefits after the patient's death. Using the assessment tool, researchers found that palliative care and hospice services were associated with significantly higher overall scores compared with usual care [47].
In addition to the benefits for patients, palliative care offers benefit to patients' family members. According to a survey of bereaved family members, a significantly higher proportion of respondents had their emotional or spiritual needs met when the patient received palliative care (compared with "usual care") [48]. Palliative care also led to a significant benefit in terms of family members' self-efficacy; that is, more family members knew what to expect when the patient was dying, felt competent to participate in the care of the dying person, and felt confident in knowing what to do when the patient died [48]. Other studies have shown benefit for caregivers through positive effects on caregiver burden, anxiety, satisfaction, and the ability to "move on" more easily after the patient's death [45,49].

The most surprising benefit of palliative and hospice care is a survival advantage. A 2007 study showed that hospice care extended survival for many patients within a population of 4,493 patients with one of five types of cancer (lung, breast, prostate, pancreatic, or colorectal cancer) or heart failure [50]. For the population as a whole, survival was a mean of 29 days longer for patients who had hospice care than for those who did not. With respect to the specific diseases, heart failure was associated with the greatest increase in survival (81 days), followed by lung cancer (39 days), colorectal cancer (33 days), and pancreatic cancer (21 days) [50]. There was no survival benefit for patients with breast or prostate cancer.

The survival advantage for patients with lung cancer has been found in other studies. In one of these studies, patients with metastatic nonsmall-cell lung cancer who received early palliative care (within 3 weeks after enrollment in the study) lived significantly longer than patients who received standard oncology care (11.6 months vs. 8.9 months), even though aggressive care was used less frequently in the group receiving early palliative care [51]. Quality of life was also significantly better for patients receiving early palliative care [51]. Similarly, a retrospective study found a slight survival advantage to hospice care among older individuals (>65 years) with advanced lung cancer [52]. These results led the American Society of Clinical Oncology (ASCO) to publish a Provisional Clinical Opinion in which it states that concurrent palliative care and standard oncologic care should be offered to people with metastatic nonsmall cell lung cancer at the time of initial diagnosis [53]. The ASCO Opinion also notes that although the evidence of survival benefit is not as strong for other types of cancer, the same approach should be considered for any patient with metastatic cancer and/or high symptom burden [53].
The cost of care at the end of life is a controversial issue because of the disproportionate costs incurred for care within the last 2 years of life and the wide variation in costs related to the aggressiveness of care across healthcare facilities [54]. The simple act of discussing end-of-life issues can help patients and families better understand options, leading to reduced costs. In a study of 603 patients with advanced cancer, costs in the last week of life were approximately $1,000 lower for patients who had end-of-life discussions with their healthcare providers compared with patients who did not have such conversations [55].
Several studies have documented the cost-effectiveness of hospice and palliative care. A meta-analysis published in 1996 showed that hospice care reduced healthcare costs by as much as 40% during the last month of life and 17% over the last 6 months [56]. A later study demonstrated little difference in costs at the end of life, with the exception of costs for patients with cancer, which were 13% to 20% lower for those who had received hospice care than for those who had not [57]. In a study of 298 patients with end-stage organ failure diseases, in-home hospice care significantly reduced healthcare costs by decreasing the number of hospitalizations and emergency department visits [45]. The strongest evidence of cost savings is found in a 2007 study in which hospice use reduced Medicare costs during the last year of life by an average of $2,309 per hospice user [58]. As was found earlier, the cost savings were greater for patients with cancer than for those with other diagnoses [58]. The greatest cost reduction (about $7,000) was associated with a primary diagnosis of cancer and length of stay of 58 to 103 days [58]. The maximum cost savings was much lower (approximately $3,500) for other life-limiting diagnoses but with a similar length of stay (50 to 108 days) [58].
Palliative care consultations also reduce costs. A review of data for Medicaid beneficiaries (with a variety of life-limiting diagnoses) at four hospitals in New York showed that hospital costs were an average of $6,900 lower during a given admission for patients who received palliative care than for those who received usual care [59]. The reduction in costs was greater ($7,563) for patients who died in the hospital compared with those who were discharged alive [59].

CHALLENGES TO OPTIMUM DELIVERY OF PALLIATIVE CARE AT THE END OF LIFE

Despite the many benefits of palliative care and hospice, referrals are usually not timely and often are not made at all [60,61,62,63,64,65]. Many challenges contribute to the low rate of optimum end-of-life care.

Among the most important barriers to the optimum use of palliative care at the end of life are the lack of well-trained healthcare professionals; reimbursement policies; difficulty in determining accurate prognoses; and attitudes of patients, families, and clinicians.

Lack of Well-Trained Healthcare Professionals

Education in medical school and training programs focuses on life-prolonging methods, and the important role of palliative care traditionally has not been sufficiently addressed [66]. Students who have participated in mandatory courses in palliative medicine have noted that they are better prepared to care for dying patients [67]. Efforts to enhance education have resulted in the development of more than 300 primary care residency programs that offer palliative medicine as part of the curriculum and 72 postgraduate medical fellowship programs in palliative care [68,69]. In addition, hospital-based palliative care programs have integrated the eight NCP domains into graduate courses and residencies for physicians and registered nurses, and certifications in palliative care have become available for physicians, nurses, and social workers [5]. More than 2,100 physicians obtained certification in hospice and palliative medicine from the American Board of Hospice and Palliative Medicine between 1996 and 2006. In 2006, subspecialty certification in hospice and palliative medicine was established for 10 Boards within the American Board of Medical Specialties. The first exam was held in 2008, and 1,274 physicians earned certification in hospice and palliative medicine; with the next exam in 2010, the number of physicians earning certification nearly doubled, with physicians in internal medicine earning the most subspecialty certifications (Table 3) [70].

NUMBER OF PHYSICIANS CERTIFIED IN SUBSPECIALTY OF HOSPICE AND PALLIATIVE MEDICINE, 2010

American Board Specialty	No. of Physicians
Internal medicine	1,849
Family medicine	835
Pediatrics	100
Anesthesiology	59
Psychiatry and neurology	49
Emergency medicine	34
Surgery	26
Obstetrics and gynecology	21
Radiology	20
Physical medicine and rehabilitation	18
Total	3,011

Table 3

Source: [70]

Initiatives to enhance the knowledge and skills of nurses have included graduate nursing programs in palliative care, instructional resources for nursing educators, communication skills training for nurses, and educational programs for home care professionals, as well national certifications [5,71]. Nearly 18,000 nurses are Board-certified in hospice and palliative nursing [72].

Reimbursement Policies

Medicare reimbursement for hospice care became available when the Medicare Hospice Benefit was established in 1982, and reimbursement through private health insurances soon followed [33]. Reimbursement for hospice enabled more people with life-limiting disease to receive palliative care at home and in hospice units: the number of hospices in the United States has increased steadily, from 158 Medicare-certified hospices in 1985 to 5,150 in 2010 [1]. Despite the positive impact of the Medicare Hospice Benefit, the benefit has impeded timely referral because of its policy disallowing concurrent hospice care and life-prolonging treatment (Table 4). The eligibility requirements of the benefit explicitly state that "the focus of hospice is on care, not cure," and in order to receive reimbursement for hospice services, patients must sign a statement that they will forego curative treatment [33]. This requirement frightens some patients or their families, who subsequently view hospice as "giving up." Furthermore, the restriction does not account for palliative treatments that serve a dual purpose of palliating symptoms and prolonging life; for example, treatments used to optimally treat heart failure are the same as those used for palliation [73]. At present, there are no Medicare regulations that specify which treatments are considered palliative, and this lack of clarity has led to variation in what treatments individual hospice programs offer. Hospice care may be denied to patients receiving palliative chemotherapy or radiotherapy, and this may result in many people not choosing hospice. Although oncology experts have noted that radiotherapy is an important component of palliative care for many people with metastatic cancer, only 3% of people receiving hospice care receive radiation therapy; expense and the need to transport patients were the primary barriers [74,75,76]. Other palliative interventions, such as chemotherapy, blood transfusions, total parenteral nutrition, and intravenous medications, may not be economically feasible for small hospices but may be possible at larger ones [77,78,79].

MEDICARE HOSPICE BENEFIT

Variables	Criteria
Benefits (covered services)	Services of physicians; nurses; social workers; dietary counselors; physical, occupational, language, and speech therapists; hospice aides and homemakers; grief and loss counselors Medications for symptom control (small co-payment may be necessary) Medical equipment and supplies Short-term inpatient or respite care (small co-payment may be necessary)
Nonreimbursable services	Care from a provider not arranged by the hospice medical team Room and board Care in an emergency room or inpatient facility, unless arranged by hospice medical team Ambulance transportation, unless arranged by hospice medical team
Period of care	Two 90-day periods, followed by unlimited number of 60-day periods
Restrictions	Signed acknowledgment that treatment (including medications) directed at curing the terminal disease cannot be carried out Certification by physician at the beginning of each period of stay that the prognosis is 6 months or less

Table 4

Source: [33]

Many have suggested that the hospice model should change to allow for integration of disease-directed therapy [80,81]. The Affordable Care Act of 2010 stipulates that the Centers for Medicare & Medicaid Services implement a 3-year demonstration project to evaluate concurrent hospice care and disease-directed treatment [81]. This project represents a significant change to the eligibility criteria and, while the change has the potential to improve access to hospice care, careful assessment of the effect of concurrent treatment on use of hospice as well as on quality of life, quality of care, survival, and costs is needed [81].

The Medicare Hospice Benefit criterion of a life expectancy of 6 months or less has also affected the timeliness of referral to hospice because of the aforementioned challenges in predicting prognosis. Many hospices were accused of fraud and were assessed financial penalties when government review found documentation of patients who received hospice care for longer than 6 months. As a result, many clinicians delayed hospice referral because of their lack of confidence in their ability to predict survival within 6 months. However, the 6-month regulation has been revised, and a penalty is no longer assessed if a patient lives beyond 6 months if the disease runs its normal course [33].

Unfortunately, reimbursement for end-of-life care discussions is not as straightforward as for hospice care. An effort to establish government reimbursement for discussions of end-of-life care options, including hospice care and advance directives, sparked a political storm that led to the removal of the proposed reimbursement from the health care reform bill of 2011. Some have noted that clinicians can be reimbursed for end-of-life discussions by using time-based Evaluation and Management (E&M) codes [82]. According to E&M guidelines, these codes can be used "when counseling and/or coordination of care dominates (more than 50%) the physician/patient and/or family encounter" services [83,84].

Difficulty in Prognostication

To make appropriate referrals to hospice, clinicians must be able to determine accurate prognoses, at least within the 6-month timeframe required for reimbursement. However, prognostication is a complex issue, and is a primary barrier to hospice use [85,86,87,88,89,90,91,92]. Studies have found that physicians typically overestimate survival, and one study found that physicians overestimate prognosis both in determining it and in communicating it to the patient [93,90,94]. The difficulty in determining the risk of death within a specific time period not only affects the ability of clinicians to make appropriate referrals to hospice but also impedes the ability of patients and families to make necessary end-of-life decisions, with many patients not fully understanding the severity and progressive nature of the disease [95].

Several factors contribute to physicians' difficulty in prognostication, including a desire to meet the patient's needs (for a cure or prolongation of life) and a lack of reliable prognostic models [78,94,96]. Perhaps the most important factor contributing to prognostic difficulty is the variations in disease trajectories, which have been characterized as a short period of evident decline, long-term limitations with intermittent serious episodes, and a prolonged decline (Figure 5) [8,31,97].

TYPICAL DISEASE TRAJECTORIES AND SERVICE NEEDS OVER TIME FOR ELDERLY PATIENTS

Figure 5

Source: [8] Reprinted, with permission from Lynn J, Adamson DM. Living Well at the End of Life. Adapting Health Care to Serious Chronic Illness in Old Age. Santa Monica: Rand; 2003

How difficult it is to determine a prognosis depends on the disease trajectory. Determining a prognosis in the cancer setting was once clear-cut because of the short period of evident decline, but advances in cancer therapies have made it more difficult to estimate a prognosis. Studies have shown rates of accurate prognosis of 20%, with survival usually overestimated, up to a factor of five [90,93]. The unpredictable course of organ-failure diseases, with its long-term limitations and acute exacerbations has always made prognostication difficult [61,86,98,99]. In a survey of cardiologists, geriatricians, and internists/family practitioners, approximately 16% of respondents said they could predict death from heart failure "most of the time" or "always" [86]. Predicting survival for people with the third type of trajectory (prolonged decline) is extremely difficult because of the wide variation in progressive decline. The prognosis for dementia can range from 2 to 15 years, and the end-stage may last for 2 years or more [100,101].

To help facilitate more timely referrals to hospice, the NHPCO established guidelines for determining the need for hospice care, and these guidelines were adopted by the Health Care Finance Administration to determine eligibility for Medicare hospice benefits [73]. Other prognostic models have been developed, such as the SUPPORT model, the Palliative Prognostic (PaP) Score, and the Palliative Prognostic Index (PPI) [11,102,103,104]. Most were developed for use in the cancer setting and for hospitalized patients, and their value beyond those settings has not been validated [78,92]. In addition, the PaP and the PIP will identify most patients who are likely to die within weeks but are much less reliable for patients who have 6 to 12 months to live [92]. A systematic review showed that the NHPCO guidelines, as well as other generic and disease-specific prognostic models, were not adequately specific or sensitive to estimate survival of at least 6 months for older individuals with nonmalignant life-limiting disease, especially heart failure, COPD, and end-stage liver disease [96].

Most prognostic tools for organ-failure diseases are used to estimate the risk of dying and to select patients for treatment, not to determine when end-of-life care should be initiated. Several models have been established to determine prognosis for heart failure; the one used most often is the Seattle Heart Failure model, which represents the most comprehensive set of prognostic indicators to provide survival data for 1, 2, and 5 years [105,106]. Newer evidence-based recommendations for estimating survival in advanced cancer have been published, as has a nomogram; however, use of the nomogram for hospice referral is limited, as it estimates survival at 15, 30, and 60 days [78,107].
For estimating prognosis in advanced dementia—a condition with the most challenging disease trajectory—the Advanced Dementia Prognostic Tool (ADEPT) has been shown to be better than the NHPCO guidelines in identifying nursing home residents with advanced dementia at high risk of dying in 6 months [108]. However, the ability of ADEPT to identify these patients is modest [108]. Lastly, the Patient-Reported Outcome Mortality Prediction Tool (PROMPT) was developed to estimate 6-month mortality for community-dwelling individuals 65 years or older with self-reported declining health over the past year; the model shows promise for making appropriate hospice referrals, but the model needs validation [109].
In addition to the low reliability of these models, another problem is that the clinician's prediction of survival remains integral, as it is one element in prognostic models, sometimes representing as much as half of a final score [107]. Other variables include performance status, laboratory data, and quality of life scales.
Researchers continue to evaluate prognostic variables to establish criteria for prognosis, especially disease-specific criteria. In its guidelines for palliative care, the Institute for Clinical Systems Improvement distinguished between the clinical indicators that should prompt palliative care and those that should prompt hospice referral (Table 5) [110].

COMPARISON BETWEEN PALLIATIVE CARE AND HOSPICE

Condition	Palliative Care	Hospice
Debility/failure to thrive	More than 3 chronic conditions in patient older than 75 years of age Functional decline Weight loss Patient/family desire for low-yield therapy Increasing frequency of outpatient visits, emergency department visits, hospitalizations	Documentation of clinical progression of disease Eastern Cooperative Oncology Group status test result of 3 or more No desire for aggressive treatment Not a candidate for aggressive treatment Frequent emergency room visits/frequent hospitalizations
Cancer	Uncontrolled signs and symptoms due to cancer or treatment Introduced at time of diagnosis if disease terminal Introduced when disease progresses despite therapy	Any patient with metastatic or inoperable cancer
Heart disease	Stage III or IV heart failure despite optimal medical management Angina refractory to medical or interventional management Frequent emergency department visits or hospital admissions Frequent discharges from implanted defibrillators despite optimal device and antiarrhythmic management	Heart failure symptoms at rest Ejection fraction less than 20% New dysrhythmia Cardiac arrest or syncope Frequent emergency room visits for symptoms
Pulmonary disease	Oxygen-dependent, O2 saturation less than 88% on room air Unintentional weight loss Dyspnea with minimal to moderate exertion Other pulmonary diagnoses (e.g., pulmonary fibrosis, pulmonary hypertension)	Dyspnea at rest Signs or symptoms of right heart failure O2 saturation less than 88% PCO2 greater than 50 Unintentional weight loss
Dementia	Behavioral problems Feeding problems, weight loss Caregiver stress Frequency of emergency department visits Increased safety concerns	Unable to walk, bathe or dress self without assistance Incontinence Less than six intelligible words Frequent emergency department visits
Liver disease	Increased need for paracentesis for removal of ascitic fluid Increased confusion (hepatic encephalopathy) Increased safety concerns Symptomatic disease	International normalized ratio greater than 5 Albumin less than 2.5 g/dL Refractory ascities Spontaneous bacterial peritonitis Jaundice Malnutrition and muscle wasting
Renal disease	Dialysis Stage IV or Stage V chronic kidney disease	Not a candidate for dialysis Creatinine clearance of less than 15 mL/minute Serum creatinine greater than 6 mg/dL
Neurologic	Stroke Parkinson's disease Amyotrophic lateral sclerosis Multiple sclerosis	Frequent emergency room visits Albumin less than 2.5 g/dL Unintentional weight loss Decubitus ulcers Homebound/bed confined

Table 5

Source: [110]

This difficulty in determining prognosis has a negative impact on the appropriate timing of hospice referrals. Although the use of hospice has increased over the past decades, the timing of referral has not changed significantly since the mid-1980s [111]. The average length of hospice care is much lower than the 6 months allowed by the Medicare benefit; in 2010, the average length was approximately 67 days, and the median duration (a more accurate reflection because it is not influenced by outliers) was 20 days [1]. In addition, approximately 35% of patients died (or were discharged) within only 7 days [1]. Studies have indicated that the benefits of hospice increase as the duration of care increases, and such services as bereavement counseling, palliative care, and respite for caregivers is best when hospice care is provided for 4 to 8 weeks, a longer period of time than the median stay [58,112].
Longer durations of hospice services are also linked to family members' perceptions of the quality of care. According to the findings of 106,514 surveys from 631 hospices in the United States, 11% of family members thought their loved one was referred "too late" to hospice; this perception was associated with more unmet needs, higher reported concerns, and lower satisfaction [113].
In contrast to the restrictions on access to hospice, there are no restrictions on access to palliative care. Referrals for palliative care should be made on the basis of actual or expected symptoms at any time during the disease continuum; referrals should not be made on the basis of prognostic models [78,96]. Referrals for specialist palliative care should be made when treatment goals change from curative to palliative [114,115]. A consensus report from the Center to Advance Palliative Care provides guidance for identifying patients with a life-limiting illness who are at high risk of unmet palliative care needs [115]. The report includes criteria for referral for palliative care assessment at the time of hospital admission and during each hospital day (Table 6) [115]. Experts in nonmalignant life-limiting diseases are calling for earlier palliative care consultation. Such consultation before implantation of a left ventricular assist device as destination therapy is recommended, as it has been shown to improve the quality of care and advance care planning [116,117]. Guidelines for renal and respiratory diseases note that all patients with these diseases should be offered palliative care services, and the integration of palliative care specialists into liver transplantation teams has been suggested [118,119,120].

CRITERIA FOR PALLIATIVE CARE ASSESSMENT AT THE TIME OF HOSPITAL ADMISSION AND DURING HOSPITAL STAY

At Time of Hospital Admission
Primary criteria*	A potentially life-limiting or life-threatening condition AND Not surprised if the patient died within 12 months More than one admission for same condition within several months Admission for difficult physical or psychologic symptoms Complex care requirements (e.g., functional dependency, complex home support for ventilator/antibiotics/feedings) Failure to thrive (decline in function, feeding intolerance, or unintended decline in weight)
Secondary criteria†	A potentially life-limiting or life-threatening condition AND Admission from long-term care facility Older age, with cognitive impairment and acute hip fracture Metastatic or locally advanced incurable cancer Chronic use of home oxygen use Out-of-hospital cardiac arrest Current or past hospice program use Limited social support No history of advance care planning discussion/document
During Hospital Stay
Primary criteria*	A potentially life-limiting or life-threatening condition AND Not surprised if the patient died within 12 months More than one admission for same condition within several months Stay in intensive care unit of 7 days or more Lack of documentation of goals of care Disagreements or uncertainty among the patient, staff, and/or family about major medical treatment decisions, resuscitation preferences, or use of nonoral feeding or hydration
Secondary criteria†	A potentially life-limiting or life-threatening condition AND Awaiting, or deemed ineligible for, solid-organ transplantation Patient/family/surrogate emotional, spiritual, or relational distress Patient/family/surrogate request for palliative care/hospice services Patient is a potential candidate for feeding tube placement, tracheostomy, initiation of renal replacement therapy, placement of left ventricular assist device or automated implantable cardioverter-defibrillator, bone marrow transplantation (high-risk patients)
*Primary criteria are the minimum indicators for screening patients at risk for unmet palliative care needs. †Secondary criteria are more specific indicators of a high likelihood of unmet palliative care needs.

Table 6

Source: [110] Reprinted, with permission, from Weissman DE, Meier DE. Identifying patients in need of a palliative care assessment in the hospital setting: a consensus report from the Center to Advance Palliative Care. J Palliat Med. 2011;14(1):17-23.

Knowledge and Attitudes of Patients, Families, and Physicians

Physicians have reported that they delay discussions of palliative care and hospice because they fear the reaction of the patient and/or family [31,32]. Negative reactions are grounded in a lack of accurate knowledge about palliative care and hospice. According to two polls conducted in 2011 (800 adults in one poll and 1,000 adults in the other), 70% to 92% of respondents were not "too" or "at all" familiar with the term palliative care [121,122].
Enhancing the public's knowledge can improve access to palliative care: the 2011 polls showed that once palliative care was appropriately defined, 92% said they were likely (63% "very likely" and 29% "somewhat likely") to consider palliative care for a loved one who had a serious illness [121] and 96% said that it was important for palliative (and end-of-life) care to be a top priority for the healthcare system [122].
Hospice is a more familiar concept to the general population. One of the 2011 polls showed that 86% of respondents were familiar with the term hospice care, and other studies have indicated that approximately half of patients with a life-limiting illness know what hospice is [122,123]. Although people may be familiar with the term, many believe several myths about hospice; for example, that hospice is only for old people, is only for people with cancer, is for people who do not need a high level of care, is used when there is no hope, and is expensive [124].
Several other factors contribute to negative feelings about hospice [77,85,125]:

• Denial or lack of awareness about the severity of the illness
• Not wanting to "give up"
• Fear of abandonment by the family physician
• Perception that the patient will not receive adequate medical services
• Interpretation of hospice referral as a cost-savings measure

When initiating a discussion about palliative care and hospice, clinicians should always first ask the patient if he or she has heard of either term and, if so, to describe his or her experience and knowledge [126]. Guidelines on communicating in the end-of-life setting note that clinicians must "clarify and correct misconceptions" about palliative care, especially emphasizing that such care is not limited to people who are imminently dying [114]. Clinicians should also address the factors that act as barriers to hospice by explaining that the goal of hospice is to die naturally—in the patient's own time, not sooner—and by ensuring that patients and families are fully informed about the prognosis, understand that the physician will be available for care, and know that routine care will continue [95,127].
Clinicians also need to evaluate their own attitudes about the use of curative therapies and hospice. Their interpretation of quality of life, a focus on longer survival rather than better quality of life, a fear of failure, and religious and cultural beliefs may influence their decision making about treatment options for patients near the end of life [128].

COMMUNICATION ISSUES

Communicating effectively about palliative care and hospice requires basic patient-physician communication skills as well as skills specific to the end-of-life setting. The importance of effective patient-clinician communication across all healthcare settings has received heightened attention over the past several years, as studies have shown a direct relationship between enhanced communication and better patient decision making, patient satisfaction, adherence to treatment, health-related quality of life, and survival [34,66].

Basic Patient-Clinician Communication

Among the most important factors for effective communication across all healthcare settings are knowledge of the language preference of the patient and family; an awareness of the patient's and family's health literacy levels; and an understanding of and respect for the patient's and family's cultural values, beliefs, and practices (referred to as cultural competency) [129,130,131]. These issues are significant, given the growing percentages of racial/ethnic populations. According to U.S. Census Bureau data from 2010, more than 59.5 million Americans speak a language other than English in the home, with more than 25.2 million of them (8.7% of the population) reporting that they speak English less than "very well" [132]. Clinicians should ask their patients what language is spoken at home and what language they prefer for their medical care information, as some patients prefer their native language even though they have said they can understand and discuss medical information in English [133].When the healthcare professional and the patient speak different languages, a professional interpreter should be used. Studies have demonstrated that the use of professional interpreters rather than "ad hoc" interpreters (untrained staff members, family members, friends) facilitates a broader understanding and leads to better outcomes [134,135]. Using a family member as a translator confuses the role of that member in the family, may involve confidentiality issues, and may lead to a modified message to protect the patient. In addition, individuals with limited English language skills have indicated a preference for professional interpreters rather than family members [136]. Professional interpreters have recommended that clinicians can further enhance the quality of care by meeting with interpreters before discussions of bad news and by explicitly discussing with the interpreter whether strict interpretation or cultural brokering is expected [137].
Knowledge of the family's health literacy is important for achieving treatment goals and good outcomes, yet most individuals lack adequate health literacy. Studies have indicated that as many as 26% of patients have inadequate health literacy, which means they lack the ability to understand health information and make informed health decisions; an additional 20% have marginal health literacy [138,139,140]. Health literacy varies widely according to race/ethnicity, level of education, and gender, and clinicians are often unaware of the literacy level of their patients and family [131,141].
Several instruments are available to test the health literacy level, and they vary in the amount of time needed to administer and the reliability in identifying low literacy. Among the most recent tools is the Newest Vital Sign (NVS), an instrument named to promote the assessment of health literacy as part of the overall routine patient evaluation [142]. The NVS takes fewer than 3 minutes to administer, has correlated well with more extensive literacy tests, and has performed moderately well at identifying limited literacy [131,141]. Two questions have also been found to perform moderately well in identifying patients with inadequate or marginal literacy: "How confident are you in filling out medical forms by yourself?" and "How often do you have someone help you read health information?" [131]. Clinicians should adapt their discussions and educational resources to the patient's and family's identified health literacy level and degree of language proficiency and should also provide culturally appropriate and translated educational materials when possible.
Cultural competency is essential for addressing healthcare disparities among minority groups [129]. Clinicians should ask the patient about his or her cultural beliefs, especial those related to health and dying and should be sensitive to those beliefs [143]. In addition, information sharing and the role of decision maker vary across cultures, and the healthcare team must understand the family dynamics with respect to decision making [114]. Clinicians should not make assumptions about the preferences of the patient or family on the basis of cultural beliefs. Even within a single culture or ethnicity, the level of information desired, preferences for treatment, role of other family members in decision making, and goals of care differ among patients and families [39,114]. Clinicians should ask their patients about these issues, as well as other family and social factors and religious or spiritual views [39].

Communication in End-of-Life Setting

Patients and families have noted that communication about end-of-life care is one of the most important skills for clinicians to have [144]. Experts in end-of-life communication note that physicians have an obligation to discuss medical, psychosocial, and spiritual needs with seriously ill patients in a timely and sensitive manner [145]. In addition, communication guidelines developed by an Australian and New Zealand Expert Advisory Group recommend that "all patients with advanced progressive life-limiting illnesses should be given the opportunity to discuss prognosis…and end-of-life issues" [114].
Although the topic is emotionally and intellectually overwhelming for patients and families, they want information. In a systematic review (46 studies), Parker et al. found that patients with advanced life-limiting illnesses and their families have a high level of information needs at all stages of disease [146]. That study and others have shown that the end-of-life issues of most importance to patients are [61,146]:

• Disease process
• Prognosis for survival for quality of life
• Likely symptoms and how they will be managed
• Treatment options and how they will affect quality of life and duration life
• What dying might be like
• Advance care planning

Most patients want some discussion of end-of-life issues (including hospice care) at the time a life-limiting illness is diagnosed or shortly thereafter [61,146].
Although many physicians say they avoid discussing end-of-life issues because they are afraid the conversation will destroy the patient's hope, the discussion actually offers many benefits: it makes patients fully informed and thus better able to make decisions about treatment options and care goals; provides patients with an opportunity to achieve closure on life and family issues; allows patients to handle practical matters; and enables patients to carry out advance care planning [34,78,145,147]. As such, the discussion empowers patients, giving them a sense of control over choices [145,147]. Patients who discuss end-of-life issues with their clinician also are more likely to receive care that is consistent with their preferences, to enroll in hospice, and to complete advance directives and are less likely to be admitted to an intensive care unit or be intubated [148,181].
Despite these benefits, studies have consistently shown that few clinicians and patients discuss end-of-life issues or discuss them in a timely manner. Overall, about 25% to 33% of physicians have noted that they did not discuss hospice or end-of-life care with their patients who have life-limiting diseases [125]. In a multiregional study of more than 1,500 people with stage IV lung cancer, 47% had not discussed hospice within 4 to 7 months after diagnosis [149]. Discussions are particularly lacking among people with nonmalignant life-limiting diseases, with 66% to more than 90% of patients or clinicians reporting that they had not discussed end-of-life issues [61,123,150,151].
Even among clinicians who discuss end-of-life care with their patients, the timing is not optimal. Approximately 24% of physicians have noted that they provide hospice information at the time of diagnosis, the point at which this discussion is recommended [125,152]. In a national survey of clinicians caring for people with cancer, most respondents said they would wait until treatment options had been exhausted or symptoms had occurred before discussing end-of-life issues, and many said they would have the discussion only if the patient or family raised the issue [153].
Patient and clinicians should talk about end-of-life issues early to avoid discussing the topic during the stress of exacerbated disease or imminent death. The topic can then be framed as a component of care for all patients with a life-limiting illness [61,114]. According to published guidelines and expert recommendations, end-of-life issues should be discussed when the clinician would not be surprised if the patient died within 6 months to 1 year [5,114,145]. As other markers, an end-of-life discussion is generally recommended in the presence of moderate or severe COPD, during evaluation for liver transplantation, and in the presence of stage 4 or 5 chronic kidney disease or end-stage renal disease [61,118,120]. ACCF/AHA guidelines for the diagnosis and management of heart failure note that end-of-life care options should be discussed when "severe symptoms in patients with refractory end-stage heart failure persist despite application of all recommended therapies" [154]. Other indications that should prompt a conversation about end-of-life care are a discussion of prognosis or of a treatment option with a low likelihood of success, a change in the patient's condition, patient and/or family requests or expectations that are inconsistent with the clinician's judgment, recent hospitalizations, and patient and/or family questions about hospice or palliative care [114,145].

Several patient-related and clinician-related factors contribute to the low rate of end-of-life discussions or their untimeliness. Most patients will not raise the issue for many reasons: they believe the physician should raise the topic without prompting, they do not want to take up clinical time with the conversation, they prefer to focus on living rather than death, and they are uncertain about continuity of care and fear abandonment [61,114,145,147]. Clinician-related factors include [78,144,145,155,156]:

• Lack of time for discussion and/or to address patient's emotional needs
• Uncertainty about prognosis
• Fear about the patient's reaction (anger, despair, fear)
• Lack of awareness and inability to elicit the concerns of patients and their families regarding prognosis
• Lack of strategies to cope with own emotions and those of patient and family
• Feeling of hopelessness or inadequacy about the lack of curative therapies (perceived as "giving up")

Perhaps the greatest barrier to end-of-life care discussions is clinicians' lack of confidence in their ability to talk about end-of-life issues, and research has confirmed a low rate of effective communication skills among clinicians, especially with respect to delivering "bad news" [61,78,151,157].
The Australian/New Zealand communication guidelines provide several evidence-based recommendations for discussing end-of-life issues, and other experts have offered practical guidance to help clinicians discuss bad news and end-of-life care more effectively [114,158,159,160]. These guidelines and expert recommendations emphasize communication behaviors that patients and families have noted to be most important, such as expression of empathy, acknowledgment and support of emotions, honesty, willingness to listen more than talk, and encouragement of questions [78,114,120,146,144,159].
The most commonly recommended communication approach is SPIKES, a six-step protocol that was developed for delivering bad news in the oncology setting and can be used in other settings [158,159]:

• S: Setting (context and listening skills)
• P: Patient's perception of condition and seriousness
• I: Invitation from patient to give information
• K: Knowledge—explaining medical facts
• E: Explore emotions and empathize as patient responds
• S: Strategy and summary

In establishing the setting, the clinician should ask the patient if he or she wishes to have a family member present for the conversation and should ensure that the discussion takes place in privacy [61,159]. The clinician should also introduce himself or herself to the patient and any others present [159]. With SPIKES, the setting also involves listening skills—the use of open-ended questions, clarification of points, and avoidance of distractions [159].
Bad news—even when delivered clearly and compassionately—can affect the ability of patients and family members to understand and retain information. To minimize misinterpretation, clinicians should use simple (jargon-free) language and open-ended questions and ask follow-up questions that include the patient's own words [114,159]. Clinicians should also check often to make sure the patient and/or family understands, as research has shown that clinicians tend to overestimate their patients' understanding of end-of-life issues [161]. The discussion should focus on the importance of relieving symptoms and enhancing the quality of life, to avoid having the patient and/or family think that the clinician is "giving up" or abandoning the patient [39,114]. Clinicians should also provide educational resources in a variety of formats (print, Web-based, video, etc) to address different learning styles.
It was once thought that the ability to communicate effectively was innate and thus could not be taught [159]. However, multiday communication skills training programs have enhanced the skills and behaviors of beginning and experienced physicians and nurses. These programs have improved clinicians' use of more focused questions and open questions, expression of empathy, and appropriate responses to cues [162,163]. Patient-related interventions have also helped to enhance end-of-life discussions. A structured list of questions and individualized feedback forms on end-of-life preferences have led more patients to ask their physicians about end-of-life care [164,165].

Discussing Prognosis

The vast majority of patients say that they want to know their prognosis, and most clinicians believe that patients and families should be told the truth about the prognosis [119,123,147]. However, discussions of prognosis are lacking among clinicians and patients with life-limiting diseases. Across studies and surveys, fewer than half of patients have had a truthful discussion of prognosis [78,105,147]. Many physicians have said they discuss prognosis only when asked by the patient or family [78].
In discussing prognosis, clinicians tend to be overly optimistic, and, although most clinicians believe that they should be truthful, they sometimes withhold the truth, often at the request of a family member [155]. Honesty about the prognosis, with acknowledgment of inherent uncertainty, is needed because patients who are aware of their prognosis are more likely to choose hospice rather than aggressive treatment and to carry out advance directives [30,78,166]. Conversely, patients who are not fully aware of their prognosis tend to overestimate their life expectancy, which can influence decision making about treatment options [126].
As with other end-of-life issues, the prognosis should be discussed when the clinician would not be surprised if the patient died within 6 months to 1 year [5,114,145]. For patients with cancer, it is recommended that the prognosis be discussed within 1 month after a new diagnosis of advanced cancer is made [156]. Guidelines from the Renal Physicians Association note that prognosis should be fully discussed with all patients who have stage 4 or 5 chronic kidney disease or end-stage renal disease [118]. A discussion about prognosis is also recommended before the initiation of such treatments as implantation of a left ventricular assist device, dialysis, and ventilator support [119,147,167,168,169].
Clinicians should carefully prepare for the discussion of prognosis by reviewing the patient's medical record and talking to other healthcare professionals involved in the care of the patient [114]. Because there is variation among patients with regard to their desire for information, clinicians should follow the "ask-tell-ask" approach: ask the patient if he or she is willing to discuss prognosis; if yes, discuss the prognosis and then ask the patient to confirm his or her understanding [61,159]. When discussing prognosis, quantitative estimates are more understandable for patients and family than qualitative ones (such as "poor"), and general timeframes for survival should be given [61,78,159,170]. In addition, clinicians should emphasize that prognosis is determined by looking at large groups of patients and that it is harder to predict survival for an individual [61,118,126,156]. The discussion of prognosis is often not documented in the patient's record but should be [114].

Discussing Treatment Options and Goals

Treatment options and goals of care are other topics that are often avoided in the end-of-life setting. A discussion of the survival benefit of palliative chemotherapy is frequently vague or absent from discussions of treatment options for patients with cancer [171]. In another example, approximately 60% to 95% of physicians involved with the care of patients with heart failure have two or fewer conversations about deactivation of implantable cardioverter defibrillators, and the discussions are usually within the last few days of life [86,172].

Deciding when curative therapy should end is difficult because of the advances made in treatment and life-prolonging technology and the unpredictable course of disease, especially for organ-failure diseases. These factors have led many patients, as well as some clinicians, to have unrealistic expectations for survival [51,173]. Unrealistic expectations are a major contributor to an increased use of aggressive treatment at the end of life. Among more than 900 patients with cancer, those who thought they would live for at least 6 months were more likely to choose curative therapy than "comfort care" compared with patients who thought there was at least a 10% chance they would not survive for 6 months [174].

Many studies have demonstrated high rates of aggressive treatment within the last months to weeks of life, with increased rates of hospital admissions, stays in an intensive care unit, use of medical resources, and use of chemotherapy. Goodman et al. found that patients with advanced chronic illness near the end of life spent more days in an intensive care unit and received more care from physicians; more than half of the patients saw 10 or more physicians within the last 6 months of life [54]. Similarly, Sheffield et al. found high rates of admission to the intensive care unit among nearly 23,000 patients with pancreatic cancer, and Unroe et al. found that 80% of more than 229,000 people with heart failure were hospitalized in the last 6 months of life [175,176]. In the cancer setting, several researchers have reported increased rates of chemotherapy in the last 2 to 4 weeks of life [175,177,178]. However, studies to evaluate the benefit of high-intensity treatment near the end of life have consistently found that such treatment offers no survival benefit, decreases the quality of life, and delays the use of hospice [54,77,179,180].
Before discussing treatment options, the clinician should talk to the patient to gauge his or her level of understanding of the disease and prognosis and to explore the quality-of-life factors that are most important [182]. The clinician should frame the conversation to focus on active interventions rather than the end of curative therapy; should focus on the overall care goals; and should discuss options within the context of these goals (that is, does the patient wish to enroll in hospice, enroll in a phase I trial, or be present at a family event?) [78,114]. The discussion should include an explanation of the likelihood of achieving the patient's goals with each option and a comparison of the risks, benefits, and costs of each option, noting the overall lack of benefit of aggressive treatment [183,184]. It is also important to allow the patient and family enough time to express emotion and concerns and to ask questions [114,159,185]. Because frequent exacerbations in organ-failure diseases are usually predictive of a more rapid decline, hospitalizations for disease exacerbation should prompt discussions about changes in prognosis and treatment goals and advance care planning [98,186,187]. Admission to the hospital or intensive care unit should also prompt a discussion of goals and preferences with patients with cancer; this conversation should be documented within 48 hours after admission [156].
When the patient, family, and/or healthcare team do not agree on the benefit/utility of interventions, the clinician should consider consulting with social workers or pastoral care services to help with conflict resolution [183]. In addition, the clinician should explain to patients that the likelihood of insurance coverage for a treatment is low if it is not medically indicated [184].
Clinical guidelines have begun to address the use of aggressive treatment at the end of life. The ACCF/AHA guidelines on the diagnosis and management of heart failure note that it is not appropriate to carry out aggressive procedures in the last several months of life if they do not contribute to recovery or improve quality of life (including intubation and implantation of a cardiac defibrillator) [105]. In addition, discussion of device deactivation for patients with heart failure is a class I recommendation in the guidelines [105]. The Renal Physicians Association recommends forgoing dialysis for patients with chronic kidney disease or end-stage renal disease who have "very poor prognosis" [118]. The increased use of chemotherapy near the end of life has led oncology experts to recommend more judicious use of chemotherapy. Oncologists have called for the discontinuation of chemotherapy when the chance of success is minimal, such as when disease progresses after three consecutive regimens [173,188].
Early discussion of preferences for life-sustaining measures is especially important. Nearly three-quarters of people will be unable to participate in some or all of the decisions about their care at the end of life [189,190]. Documentation of preferences help inform decision making by the physician and the patient's health care proxy (surrogate decision maker). Clinicians should encourage their patients to designate a healthcare proxy early in the course of a life-limiting disease [61,79,119]. Patients should be urged to clarify their wishes with their chosen health proxy, as a proxy often inaccurately predicts a patient's wishes or may have values that conflict with those of the patient [190].

Advance directives, designation of a healthcare proxy, do-not-resuscitate (DNR) orders, and living wills were developed as a way to ensure that patients received care that was consistent with their preferences and goals. Advance directives offer many benefits; they have been associated with a lower likelihood of in-hospital deaths, an increased use of hospice, and a significant reduction in costs [191]. Although early studies showed that advance directives did not always translate into patients receiving their preferred level of care, later studies have demonstrated that most patients with advance directives do receive care consistent with their preferences, especially if they want limited care (rather than "all possible" care) [190,192].

The American College of Physicians recommends that clinicians ensure that advance care planning, including completion of advance directives, occurs for all patients with serious illness.

(http://www.guideline.gov/content.aspx?id=12149 Last Accessed: May 24, 2012)

Strength of Recommendation/Level of Evidence: Strong recommendation based on low quality of evidence

The American College of Physicians recommends that clinicians ensure that patients with "serious illness" engage in advance care planning, including the completion of advance directives [46]. Clinicians must emphasize the value of advance directives because most patients have not completed them. An estimated 20% of the population have written advance directives, with higher rates among the older population and nursing home residents and lower rates among minority populations and those with nonmalignant life-limiting diseases (compared with people with cancer) [193,194,195,196,197]. Other guidelines recommend that advance care planning be done early in the course of disease, to help avoid potential compromise of decision-making capacity near the end of life [61,105,118,119].

In preparing for a discussion about advance directives, clinicians should ask the patient if he or she wishes to have other family members present during the conversation. This is especially important for patients of some cultural backgrounds, as healthcare decisions are the responsibility of family members in many cultures [196]. Increased efforts should be aimed at obtaining advance directives from patients of minority races/ethnicities. Although the rate of advance directives is higher in the gay and lesbian community than in the general population, clinicians should emphasize the importance of these documents to gay and lesbian patients to ensure that the patient's wishes are carried out and to avoid legal consequences for the patient's partner [198].

DNR orders and living wills have limitations and have been open to interpretation, which has led to the development of medical order forms based on patients' preferences. Developed at the Oregon Health & Science University, the Physicians Orders for Life-Sustaining Treatment (POLST) program is designed to ensure that a patient's preferences regarding cardiopulmonary resuscitation, scope of treatment, artificial nutrition by tube, and use of antibiotics (in some states) can be followed, regardless of where the patient receives care [199]. Nearly all states have an endorsed POLST program or one in development [199]. A POLST does not replace a traditional advance directive, and when available, an advance directive should accompany the POLST form [199]. Early studies have demonstrated that the use POLST has led to higher rates of meeting patients' preferences [200,201].
Legal issues related to advance directives and POLSTs vary according to state, and clinicians should be familiar with the law in the state in which they practice [193].

GUIDELINES FOR PALLIATIVE CARE

The ICSI updated its guidelines for palliative care in 2009 and presented an algorithm for overall care, with details on the management of several specific symptoms [110]. Other general guidelines for palliative care have been developed by the International Association for Hospice and Palliative Care, now in its second edition [202]. However, evidence-based guidelines on the treatment of specific symptoms in specific disease settings have been lacking. A systematic review published in 2004 noted that palliative care content was "minimal" in 64% of the clinical practice guidelines for nine chronic diseases (cancer [breast, colon, prostate, and lung], COPD, heart failure, dementia, end-stage renal disease, HIV/AIDS, end-stage liver disease, stroke, and amyotrophic lateral sclerosis) [203]. Ten percent of the guidelines had "significant" palliative content, and 36% had mention of palliation or hospice [203].
A major reason for the absence of guidelines is the under-recognition of symptoms among patients with life-limiting diseases other than cancer. As a way to heighten awareness of the need for improved palliative care across disease settings, researchers began to document the prevalence of symptoms among groups of patients as well as compare the prevalence and severity of symptoms with those found among patients with cancer. Studies have documented that the symptom burden at the end of life for patients with life-limiting diseases is often as high as—or higher than—that for patients with cancer, and the most common symptoms are similar across disease settings (Table 7) [119,197,204,205,206,207,208]

MOST COMMON SYMPTOMS AT THE END OF LIFE ACROSS LIFE-LIMITING DISEASE SETTINGS

Overall	Fatigue Pain Dyspnea Delirium Anorexia
Cancer	Pain Fatigue Anorexia Anxiety Depression
Heart failure	Dyspnea Fatigue Pain Anxiety Sleep disturbances
COPD	Dyspnea Fatigue Xerostomia Coughing Anxiety
Renal disease	Fatigue Sleep disturbances Pain Anxiety Constipation
End-stage liver disease	Depression Sleep disturbances Fatigue Muscle cramps Cachexia
HIV/AIDS	Diarrhea Fatigue Depression Pain Delirium

Table 7

Source: [119,197,204,205,206,207,208]

In the wake of such studies, the American College of Physicians published a clinical practice guideline on palliative care interventions for three symptoms with the overall strongest evidence—pain, dyspnea, and depression—and evidence-based guidelines and recommendations for palliative care have been developed for respiratory diseases, heart failure, and end-stage renal disease [46,105,118,119,210,209,211]. These guidelines represent an important step toward enhancing palliative care, but more work is needed in many disease settings to address all aspects of palliative care.