PMCCPMCCPMCC

Search tips
Search criteria 

Advanced

 
Logo of nihpaAbout Author manuscriptsSubmit a manuscriptNIH Public Access; Author Manuscript; Accepted for publication in peer reviewed journal;
 
JAMA. Author manuscript; available in PMC May 23, 2011.
Published in final edited form as:
PMCID: PMC3099412
NIHMSID: NIHMS289985
The Role of Chemotherapy at the End of Life
“When Is Enough, Enough?”
Sarah Elizabeth Harrington, MD and Thomas J. Smith, MD
Department of Internal Medicine and the Thomas Palliative Care Program of the Massey Cancer Center of Virginia Commonwealth University, Richmond
Corresponding Author: Thomas J. Smith, MD, Virginia Commonwealth University, Division of Hematology/Oncology and Palliative Care, MCV Box 980230, Richmond, VA 23298-0230 (tsmith/at/hsc.vcu.edu)
Patients face difficult decisions about chemotherapy near the end of life. Such treatment might prolong survival or reduce symptoms but cause adverse effects, prevent the patient from engaging in meaningful life review and preparing for death, and preclude entry into hospice. Palliative care and oncology clinicians should be logical partners in caring for patients with serious cancers for which symptom control, medically appropriate goal setting, and communication are paramount, but some studies have shown limited cooperation. We illustrate how clinicians involved in palliative care and oncology can more effectively work together with the story of Mr L, a previously healthy 56-year-old man, who wanted to survive his lung cancer at all costs. He lived 14 months with 3 types of chemotherapy, received chemotherapy just 6 days before his death, and resisted entering hospice until his prognosis and options were explicitly communicated. Approaches to communication about prognosis and treatment options and questions that patients may want to ask are discussed.
Mr L was a 56-year-old previously healthy businessman. He presented with progressive back pain in April 2005. Vertebral biopsy showed poorly differentiated non–small cell (squamous cell) lung cancer. His vertebral metastases and multiple asymptomatic brain metastases were treated with dexamethasone and radiation therapy.
After discussing prognosis and options with his oncologist, Dr O, he received chemotherapy with weekly gemcitabine and carboplatin. He tolerated treatment well, and for 4 months during this period his cancer did not grow. When the disease progressed, he switched to erlotinib orally. This prevented further cancer growth for almost 6 months, during which time he was asymptomatic, except for a mild rash and diarrhea. For a few months, he was able to travel and lead a normal life. However, in January 2006, Mr L’s cancer again progressed. His chemotherapy was switched to pemetrexed but the tumor continued to grow.
Mr L developed diplopia in February 2006, and meningeal carcinomatosis was confirmed in March 2006 when magnetic resonance imaging of the brain showed enhancement of the fifth, seventh, and eighth cranial nerves. In the few days Mr L took to discuss his care with his medical student son, he progressed from manageable double vision to needing a wheelchair and becoming incontinent. An Ommaya reservoir was placed, and Dr O started the patient on twice weekly intrathecal methotrexate. He improved slightly, then remained stable for 2 months, enough to return to work part time and to travel a bit. Soon progression of the leptomeningeal disease resulted in additional cranial neuropathies. The intrathecal therapy was changed to liposomal cytarabine. Mr L continued to want active therapy; he attempted to enter a clinical trial for an investigational central nervous system chemotherapeutic treatment but was not accepted due to his general debility.
Over the month prior to hospital admission, Mr L had a rapid decline with less appetite and reduced ability to walk. After several falls, he required a wheelchair for mobility. In July 2006, he was admitted to the hospital for aspiration pneumonia and hypoxemia. At the time of admission, Mr L was a “full code” and had appointed his wife as durable power of attorney for health care decisions. The patient and family had been considering hospice, as suggested by the oncologist, and had been visited at home by a hospice intake worker. However, the patient wanted to continue fighting the disease instead of entering hospice.
On examination, Mr L was a chronically ill–appearing man whose breathing was aided by nasal oxygen and who sat on a bedside “neuro” chair. He had a fourth cranial nerve palsy and disconjugate gaze, facial droop, hoarse voice, absent gag reflex, and coarse breath sounds. Chest x-ray showed multiple pulmonary nodules and a new patchy left lower-lobe infiltrate.
The medical house staff called a palliative care specialist, Dr A, who noted that the patient was receiving a dose of intrathecal liposomal cytarabine during his initial visit. Dr A discussed the patient with Dr O, who now estimated that the patient had “only a month to live.” Dr A estimated a prognosis that could be as short as 2 weeks.
The palliative care team initially conferred with the patient’s son and sister, outlined the likely prognosis, advised them to proceed with hospice enrollment, and outlined the requirement for a do-not-attempt resuscitation and do not intubate order for this hospice. After this meeting, all acknowledged that this was the end of beneficial palliative chemotherapy, which his oncologist was now no longer recommending. The family accepted these plans. Dr A then met Mr L and his wife, who agreed to these recommendations, and he met with the executor of the patient’s estate whom he urged to immediately complete a durable power of attorney for legal and financial transactions. Later, Dr A met with Mrs L and 2 sons to answer their questions (eg, likely time course, signs of impending death, eating for pleasure rather than nutrition, how to inform relatives at a distance), then talked with the hospice nurse to begin hospice enrollment. Finally, at Mrs L’s request, Dr A spoke with the patient’s mother and brother in England, who were displeased with the plan for hospice enrollment.
Mr L was transferred to his home with hospice care, where he remained alert and interactive for several days. On the sixth day at home, Mr L died peacefully with his wife and his children at his side and with his favorite music playing, some 14 months after the initial diagnosis. His mother and brother flew in from abroad but arrived only after Mr L had died.
Mrs L, Dr A, and Dr O were interviewed by a Perspectives editor in August and September 2006, 2 months after Mr L’s death.
Dr O (THE ONCOLOGIST): We discussed with Mr L and his wife that this [leptomeningeal carcinomatosis] was a very ominous turn of events and that without intervention, his prognosis was clearly going to be weeks to a couple of months or so. His choices were to just focus on his comfort or to try to see if we could reverse that and … do additional systemic therapy. Without hesitation, Mr L did not want … hospice care or [to] just focus on palliative care. He absolutely wanted to try….
Mrs L: I think our doctor in this case was amazing…. He obviously knew what the outcome was going to be, but you always pray for the miracle. I think the miracle we got was another year of his life…. you know my husband was extremely determined to remain positive, and he never was going to give in [to the fact] that this could eventually kill him…. It didn’t really dawn on my husband that he was going to die until he was in the hospital with pneumonia, which was 2 weeks before he passed away…. I think my husband lived very well at the end and he died well.
Dr A (THE PALLIATIVE CARE CONSULTANT): I was called by the primary medicine team, who were taking care of him for an aspiration pneumonia. They wanted me to talk to the patient about future options and hospice, but he was still getting chemotherapy. Before I saw the patient, I called the oncologist. He said he would talk to the patient about his prognosis and about his chemotherapy. I went by later that day and the patient was seeing a speech therapist. Instead of talking to him first, I talked to his son, who was a medical student, and his sister, who was visiting from abroad, separately. They were shocked about the prognosis that I offered … of days to weeks. They were still expecting more chemotherapy. Here I was, walking into the room and basically saying, “Okay, folks, it’s time for hospice.”
Seeking Balance: The Goals and Use of Chemotherapy Near the End of Life
The appropriate role of chemotherapy near the end of life is a complex issue.1 As chemotherapy is increasingly available, and better tolerated, its use at life’s end involves sophisticated oncological assessment, a focus on the patient’s goals of care, and a balancing of perspectives of the patient and treating oncologist. Ultimately, it may involve judgments about the use or restraint of use of costly resources despite little chance of benefit.2
In some respects, Mr L’s care proceeded appropriately from a cancer diagnosis to hospice care. But were there missed opportunities to improve Mr L’s care? How can clinicians help patients and families determine when further chemotherapy is no longer beneficial and when they have had enough? Using the case of Mr L as an example, we discuss how clinicians can help patients identify the goals of therapy, the ways that oncology and palliative care clinicians can work together, and strategies to improve communication when chemotherapy is being considered at the end of life.
From the viewpoint of oncologist Dr O, Mr L presented with stage IV lung cancer, with brain and bone metastases. His cancer initially responded to brain and spinal radiation and first-line chemotherapy but then progressed. It stabilized for several months on a second-line agent, but a third-line agent did not halt its growth. He died of leptomeningeal metastases that progressed despite 2 types of intrathecal chemotherapy. He lived 14 months, fairly typical for non–small cell lung cancer, but spent only 6 days in home hospice before death. At the time of the first visit by Dr A, the palliative care physician, Mr L was still a full code and had not made any financial transition plans, although he did have a designated power of attorney for health care, which may be more important,3 and Dr A believed that the family and patient were unprepared for the nearness of death. Dr A bore the brunt of some family anger when recommending hospice. He responded by stating that oncologists “need to be trained to involve palliative care folks earlier.” However, the oncologist had brought up hospice, and the patient initially declined it, only accepting palliative care involvement when death was imminent. The admitting house staff and palliative care consultant had a sense that this patient with brain metastases was not always making informed choices and had lost opportunities to do other important things with his remaining time while pursuing further chemotherapies and clinical trials. They had concerns about providing care (such as the final dose of intrathecal chemotherapy) that really could not help the patient.
Identifying the Appropriate Goals of Chemotherapy
Reasons for Late-Stage Chemotherapy
Patients may find it hard to get or accept truthful information about the benefits and harms of palliative chemotherapy. In the largest study of 95 consecutive patients receiving palliative chemotherapy, prognosis was discussed by only 39% of medical oncologists.4 In a longitudinal study of hospitalized patients for whom death was believed imminent, families reported that the attending physician never discussed the possibility of death 62% of the time and no one on the medical team discussed the possibility of death with cancer patients in 39% of cases.5 In other studies, at least one-third of patients and families reported they did not believe the information given them that treatment was not curative despite receiving such information.6,7 Another study showed that physicians may “collude” in this hopefulness by giving such a wide range of outcomes that people choose the most favorable.8
It is critical to understand that people looking death in the eye have a different perspective. Studies from the United States, England, Canada, Japan, Norway, and Italy consistently show that patients with cancer generally were willing to undergo aggressive treatment with major adverse effects for very small chance of benefit, different from what their well physicians or nurses would choose.9 Some patients with previously treated non–small cell lung cancer would accept chemotherapy for a survival benefit as short as 1 week, while others would not, even for a benefit of 2 years (the actual expected benefit was ~3 months).10 Highly educated and motivated patients enrolled in phase 1 studies at the National Cancer Institute said that they would be willing to take an experimental drug—with a 10% mortality rate—for an unknown small chance of benefit.11 Box 1 lists some of the difficulties in giving and receiving information about prognosis in advanced cancer.
Box 1. What Patients Know About Their Advanced Cancer and Its Prognosis
Patients Are Never Told or Are Not Told Well
Small Cell Lung Cancer
Thirty-five patients reported learning more about their prognosis from other patients in the waiting room than from their health care professionals. Physicians did not always want to pronounce a “death sentence,” and patients did not always want to hear it.12
High-Dose Chemotherapy (With Stem Cell Transplant)
Physicians prescribing high-dose chemotherapy overestimated survival, especially for patients with poor prognosis who might most need to balance toxicity with outcomes.13 The optimistic patients had no better survival than those who were more realistic.14
Terminally Ill With Cancer
Even if patients requested survival estimates, physicians said that they provided them only 37% of the time. Physicians reported that they would provide no estimate, conscious over-estimates, or conscious underestimates 63% of the time.15
Solid Tumors
In Belgium, only 39% of oncologists reported ever reviewing prognosis with patients. Most of the interview was spent on active treatment, not alternatives.4
Nearly all patients could name their diagnosis, but only 23% knew their stage, which is critical to appropriate goal setting.16
Oncologists consistently overestimated prognosis by at least 30%.17 In our own study, physicians’ estimate of survival could be divided by 3.5 for actual survival.18
Patients Don’t Believe Information About Benefits and Risks of Treatment
Metastatic Lung Cancer
One-third of patients thought they were receiving therapy with curative intent despite being told prognosis and goals of care.6
Head and Neck Cancer
Thirty-five percent of patients believed their palliative radiation was supposed to be curative.7
Phase 1: Overoptimistic
If told that a treatment helps 20% of people like them, patients reported a 44% chance of it helping them personally.19
Patients Change Their Mind About Communication
Metastatic Breast Cancer
Between first and second lines of chemotherapy, 59% of 729 patients with advanced cancer changed their preference about involvement in decision making; 37% wanted a less active role, and 22% wanted a more active role.20
Thirty-eight percent of women took an active role in decision making for first-line chemotherapy, and 43% for second-line chemotherapy. The reasons to take chemotherapy shifted from the possibility of controlling the tumor (50% for first chemotherapy, 38% for second) to providing hope (19% for first-line chemotherapy, 43% for second line); the proportion expecting to be cured fell from 10% to 0% with second-line chemotherapy.21
Patients Have Different Perspectives Than Their Well Health Care Professionals
Solid Tumors
England
Patients would have toxic treatment for a 1% chance of cure, 10% chance of symptom relief, or chance to prolong life 12 months. Their physicians and nurses would require a 50% chance of cure, 75% chance of symptom relief, and 24 to 60 months added survival.22
Patients accepted a lower chance of benefit from chemotherapy than their physicians or nurses, even when treatment involved great toxicity.23
Canada
Fifty-seven percent of patients would choose chemotherapy for a survival benefit of 10% at 1 year. Some chose more toxic treatments even if they offered no survival advantage while others declined chemotherapy regardless of perceived advantage of treatment. It was difficult to predict what individual patients would choose.24
Lung Cancer
Norway
Patients younger than 40 years would accept the toxic treatment with only a small benefit: chance of cure (median, 7%), life prolongation (3 months), and symptom relief (8%).25
Italy
Patients would be willing to undergo chemotherapy for small benefit, even if the physician presents the results pessimistically.26
United States
Patients who had undergone chemotherapy for lung cancer would take it again if it added survival of 4.5 months with mild toxicity or 9 months with severe toxicity. When given the choice between supportive care and chemotherapy, 22% chose chemotherapy for a survival benefit of 3 months, which was the actual expected benefit. Sixty-eight percent would choose chemotherapy if it substantially reduced symptoms without prolonging life. Only a quarter remembered hearing any options about treatment that did not involve chemotherapy, such as palliative care.4
Japan
If their lives would be prolonged by 3 months, 19% would choose to receive intensive treatment, and 21% would choose less intensive treatment. With a 70% chance of symptom relief, 73% of patients were willing to choose intensive chemotherapy.27
Palliative Chemotherapy, Belgium
Patients’ choice for chemotherapy or palliative care was most strongly predicted by their preconsultation treatment preference.28
Phase 1 Participants
Of 163 patients participating in a phase 1 study, for which by definition, the goal is to assess toxicity, only 7% considered no treatment at all; 81% were aware of hospice, but only 6% had seriously considered hospice for themselves.11 “More than 90% of patients said they would still participate in the study even if the experimental drug caused serious adverse effects, including a 10% chance of dying.”
Multiple studies document that palliative chemotherapy is increasingly given near death. More than 20% of patients receiving Medicare who had metastatic cancer started a new chemotherapy treatment regimen in the 2 weeks before death.29 In Italy, 23% of patients with incurable cancer received chemotherapy within 30 days of death.2 In a US community practice, chemotherapy for patients with lung cancer was given within 30 days of death for 43% and 14 days for 20% of patients.30 In 2008, a medical director of a large insurance company reported that 16% of its cancer patients receive chemotherapy within 14 days of death. Patients are unlikely to benefit from chemotherapy when they have already been failed by the standard regimens, have poor performance status, and otherwise have a poor prognosis. The largest study of matched patients who received hospice and no chemotherapy vs those who did not receive hospice care but had chemotherapy showed that survival was significantly longer for hospice patients with lung cancer and pancreatic cancer, marginally longer for colon cancer, but no different with breast or prostate cancer. The authors concluded that this was consistent with chemotherapy not prolonging and possibly shortening life for those eligible for hospice.31 Furthermore, chemotherapy produces adverse effects, precipitates hospitalization and emergency department visits, precludes entry into most hospices, and may require additional supportive care with erythropoietinlike drugs and colony-stimulating factors that are expensive and contribute little to the patient’s overall quality of life. For these reasons, the factors that go into patients’ decisions to undergo chemotherapy near the end of life bear examination.
Is Distinguishing Curative From Palliative Chemotherapy Important?
Chemotherapy for metastatic solid tumors such as lung, breast, colon, or prostate cancer rarely if ever cures patients. The indication for such chemotherapy is to improve disease-free or overall survival, relieve symptoms, and improve quality of life. Palliative chemotherapy accounts for most of the work of everyday oncology given the rarity of curable disease. The American Society of Clinical Oncology could not decide on a minimal benefit for which chemotherapy was indicated, only that some benefit must be demonstrable.32 Consensus panels that include cancer advocates make little distinction between curative treatment and palliative treatment that could extend life,33 since 6 months’ added survival could be as important as an increased rate of cure.
The increasing effectiveness and lessened toxicity of palliative chemotherapy is well supported by randomized trial data. First-line chemotherapy for patients with non–small cell lung cancer improves survival by 2 to 3 months, relieves symptoms, and improves quality of life compared with best supportive care.34 Second-line treatment of patients with non–small cell lung cancer with docetaxel vs best supportive care is associated with significantly longer survival (7.0 vs 4.6 months, or 10 weeks, and a difference in 1-year survival, 29% vs 19%)35; and improvements in pain and less deterioration in quality of life.36 Even third-line treatment may improve survival or symptoms, especially with novel, relatively nontoxic oral agents such as erlotinib, which, in 1 study, improved survival compared with best supportive care from 4.7 to 6.7 months with improved results for pain, dyspnea, and physical functioning.37 Palliative chemotherapy has also increased survival and quality of life in metastatic colorectal38 and prostate cancer39 (Table 1). Mr L benefited from receiving 3 separate types of palliative non–small cell lung cancer chemotherapy: gemcitabine and carboplatin, oral erlotinib, and pemetrexed. Although he never had dramatic responses to treatment, his disease stabilized for months while he received the first 2 treatments, and his central nervous system disease was stable for weeks because of intrathecal methotrexate.
Table 1
Table 1
Palliative Chemotherapy for Metastatic Disease for 4 Common Solid Tumors
How Can Clinicians Help Patients With Decision Making?
Mr L’s palliative care specialist noted that because patients are vulnerable to fastening on slim hopes, oncologists must improve their skills in helping patients think clearly about the appropriateness of chemotherapy.44,45 To help their patients make wise decisions, oncologists can start with a prompt list of questions, proven to enhance communication4648 and similar to one in use in several oncology practices,49,50 including ours (Box 2). This can be provided to the patient in the waiting room for discussion with his or her physician.
Box 2. Helpful Questions to Consider Asking About Palliative Chemotherapy
Treatment
  • What is my chance of cure?
  • What is the chance that this chemotherapy will make my cancer shrink? Stay stable? Grow?
  • If I cannot be cured, will I live longer with chemotherapy?
    • How much longer?
  • What are the main side effects of the chemotherapy?
  • Will I feel better or worse?
  • Are there other options, such as hospice or palliative care?
  • How do other people make these decisions?
  • Are there clinical trials available?
    • What are the benefits?
    • Am I eligible?
    • What is needed to enroll?
Prognosis
  • What are the likely things that will happen to me?
  • How long will I live? (Ask for a range, and the most likely scenario for the period ahead, and when death might be expected.)
  • Are there other things I should be doing?
    • Will?
    • Advance directives?
    • Durable power of attorney for health care who can speak for me, if I am unable?
    • Financial or family legal issues?
    • Durable power of attorney for financial affairs?
    • Trust?
    • Family issues
      • Will you help me talk with my children?
    • Spiritual and psychological issues
      • Who is available to help me cope with this situation?
    • Legacy and life review
      • What do I want to pass on to my family to tell them about my life?
    • Other concerns?
Another important communication is a straightforward discussion of the quality and quantity of life with or without chemotherapy. In most cases, there will not be a randomized trial of best supportive care vs best supportive care plus chemotherapy, but at least the important discussion points can be raised. There must be some definable benefit before chemotherapy can be recommended. Table 2 provides some examples of helpful communication strategies.
Table 2
Table 2
Things to Do or Say (and Not to Do or Say) About Chemotherapy for Advanced Cancer
Studies consistently document that patients want and use such information. Of 126 terminally ill patients, 98% said they wanted their oncologists to be realistic51 and patients want oncologists to be truthful and compassionate and to continue caring for them during their illness.52 A comprehensive review found that randomized trials of decision aids in oncology yielded increased patient knowledge and more involvement in decision making,53 and a decision aid for adjuvant therapy of breast cancer (http://www.adjuvantonline.org) improved medical decision making and helped low-risk patients avoid unnecessary chemotherapy.54,55 A preliminary study showed that directly giving patients information about prognosis and treatment to share with their oncologist is desired and helpful.56 We use decision aids in our own practice that address prognosis with and without chemotherapy in a question-and-answer format, using simple terms (ie, “10 in 100 people” instead of “10%”) and figures.
What Should the Clinician Do When the Patient Wants to Continue Chemotherapy at the Very End of Life?
Dr O: I couldn’t get him to stop thinking that he needed one more treatment. One more treatment was what he needed to spring him loose.
In the difficult situation faced by Dr O and Mr L, when the oncologist thinks further chemotherapy is not indicated, a number of strategies may be tried: holding family conferences to identify the decision makers in the family and getting the same information to all involved; informing people of and giving them access to the actual medical research studies and results; or writing the options down in concrete terms.57 Much of the time, patients and families may simply need more time to adjust to a difficult situation. Sometimes, they just have a different perspective that must be valued as much as the health care professional’s.
When Should Patients Stop Chemotherapy and Transition to Palliative or Hospice Care?
Mrs L: I think that he felt he was in control until the last 2 weeks of his life, and that was important. The kids were very involved. We had a lot of closure.
Dr O: [Within weeks of his death,] Mr L was still in a “I’ve got to do something” mode, but I was telling him …. “We’ve got to get hospice going so that you can relax and everyone [in your family] can get what they need and they can move on.” He was not having any of it, though.
Dr A: I was going in there to talk hospice, prognosis less than 6 months, and he was still full code. He had to be made no code. He was still expecting chemotherapy, [and] at least some of the members in his family were, and he was getting chemotherapy. When I went in on Saturday morning, it was a totally changed picture. The patient and his wife were now demanding to go home on hospice.
Making the transition to palliative care or hospice is difficult for both patients and oncologists. There are usually some treatment options, even for relapsed disease. The available lung cancer treatment data suggest that each 3.3% of response rate leads to better survival of 1 week and increases survival at 1 year by 1.6%, which might be important to some patients.58 The National Comprehensive Cancer Center Network guidelines recommend that after 2 chemotherapy regimens have failed to benefit the patient or if the patient’s performance status declines to 3 or more, such that chemotherapy will not be tolerated, a switch to palliative or hospice care be made (http://www.nccn.org/professionals/physician_gls/default.asp). The American Society of Clinical Oncology and other major professional societies have long recommended hospice as the best available care for dying patients.59
In our experience, many families and patients who choose, like Mr. L, to enroll in hospice wish they had done so sooner. The median length of stay on hospice has declined from 29 days in 1995 to 26 days in 2005, with one-third enrolling in the last week of life and 10% on the last day of life (http://www.nphco.org). Hospice care may help the family as well as the patient. One study showed that hospice care was associated with a 0.5% lower absolute risk of death for the Medicare-age surviving spouse.60 Families’ perception of late referral is associated with lower satisfaction with hospice care overall.61 In the most recent and largest study, among those with hospice stays of less than 30 days, 16% of families said they were referred too late.62 Of note, the perception of being referred too late, but not the actual length of stay, was associated with more unmet needs, lower satisfaction, and more concerns. One study found that patients would have liked palliative care consultation earlier in their course.63 It is unknown whether this view of “too-late” referrals to palliative care and hospice will change with the new relatively nontoxic chemotherapy treatments.
Improving Communication About Hospice and End of Life
Mrs L: He wanted to keep fighting. There was also a lot of animosity [from the overseas family members] toward Dr A, who is the most honest and incredible person on the planet. They felt that he had talked my husband into stopping treatment, and that was not the case at all. Dr A never really had anything to do with that. It was strictly between my husband and his oncologist.
Dr O suggested hospice enrollment to Mr L and he was even visited by a hospice intake worker, but he chose not to enroll until it was explicitly clarified that there were no further chemotherapy options. This is not unusual: Teno et al62 estimated that 23% to 61% of short-stay hospice patients could not have been referred earlier due to late diagnosis or patient refusal.
In our opinion, oncologists should note the availability of hospice from the beginning, as part of routine good care of the seriously ill patient. After all, in 2005 hospices enrolled more than 1.2 million patients, representing one-third of all deaths in the United States, with nearly half of the patients having cancer. Unfortunately, families often receive little information from physicians about hospice.64 In one study, physicians initiated the discussion about hospice about half the time, while patients or families initiated one-third of the discussions. Patients and families identified as important in deciding about hospice the frequency of visits, payment, and the practical help it provides.65 (A list of the resources that hospices can provide to patients is found in the online resources [http://www.getpalliativecare.org].) Barriers include physicians’ lack of knowledge of hospice philosophy, services, and patient eligibility requirements. Brickner et al66 found that 84% of physicians surveyed were unable to identify appropriate hospice diagnoses and that only 12% were aware of the National Hospice Organization Medical Guidelines for Determining Prognosis in Selected Non-Cancer Diagnoses. In a randomized trial of nursing home residents, a structured interview on admission—in essence bypassing physician reluctance and making the hospice benefit known to families and patients—increased appropriate hospice enrollment from 1% to 20%.67
In our opinion, patients and families should receive all of the necessary information about hospice and palliative care in order to permit the most informed decision about how to spend their last few weeks or months. We also recognize that even after the most earnest communication efforts, patients and families may continue to want chemotherapy.44 Communication about prognosis, what to expect with disease progression, and advanced directive and financial planning can all be done independently of a hospice decision and should remain a high priority for patients with advanced disease.
Dr O: I thought that it would help everybody for Mr L to hear that he couldn’t get into a clinical trial because physically he wasn’t up to the standards of the trial. That, I thought, would have allowed Mr L to accept palliative care sooner than he did.
Mrs L: I never thought “too much” was too much. You always hope that he can come out of this by some miracle. The “too much” was when he became ill in the hospital.
When the prognosis is predictable, as with Mr L, why do most oncologists not directly address it? One paradoxical explanation is that patients do not want to discuss such terrible issues with their oncologist. Of 101 inpatients with cancer admitted without advanced directives, only 23 wished to discuss the issue with their oncologists; however, 56% of those without advanced directives (44 of 78) supported discussing it with the admitting physician and not the oncologist.68
Another explanation is that such discussions are simply too difficult and painful. Even clinicians who are well trained and skilled at giving bad news can find it burdensome and emotionally difficult. Prior surveys documented “serious shortcomings in the training and current practices of oncologists” of palliative care and that only 25% of oncologists found end-of-life care highly satisfying.69 Given the incurability of some cancers, such as with Mr L, there is a need for these conversations and consideration of hospice care. At the very least, finding out how much a patient wants to know and then providing that information should be addressed by all clinicians.70
Shifting Goals of Care to Palliation: Why Is It So Difficult for Physicians?
Clinicians often struggle with initiating discussions about shifting treatment goals and in particular transitioning to palliative care. Patients may respond with denial, anger, or sadness. These are all normal responses to the associated loss of control, a fear of the immediate future, or an underlying fear of death. For the most part, patients and families will have their own unique timetable and method for processing this information.7 Clinicians should generally respond with patience, emphasizing support (non-abandonment) and assurance of aggressive symptom management71 (Table 2).
Not surprisingly, physicians may respond to their patients, particularly those with whom they share a long-term relationship, with powerful emotions of their own.72 These can include a personal and professional sense of failure and frustration, guilt, powerlessness against the illness, grief, a need to rescue the patient, or a desire to separate from and avoid patients to escape these feelings.73 Clinicians’ feelings of medical ineffectiveness can lead to failure to identify patient-specific and family-specific values influencing decisions, which may lead to a lack of clarity about care goals. Avoidance of the discussion altogether can lead to mistrust of the health care system and medical profession, inappropriate use of life-sustaining medical technologies, increased medical complications, and long hospital stays.74 Recognizing, accepting, and reflecting on the normalcy of such feelings allows the professional to make a conscious choice about how to proceed in the relationship with the patient. Finding a trusted colleague in whom to confide can be part of a plan to prevent isolation, improve objectivity, and avoid burnout.75
Doesn’t Honesty Take Away Hope?
No data are available that show hope can be taken from patients, as was once thought, or that patients are harmed by carefully provided information.76,77 As the Education Physicians End of Life Care for Oncologists (EPEC-O) curriculum78 states, “Information carefully shared is a gift to the patient and the family who want it and minimizes the risk that patients will distrust the cancer care team.” In pediatric oncology, full prognostic disclosure supported hope, even when the prognosis was poor.79
Ways That Oncologists and Palliative Care Specialists Can Work Together
Dr A: I think oncologists, in general, need to get more comfortable with palliative care. It’s not an “either, or” situation, it’s a “both, and.” I think physicians, in general, including people like this excellent oncologist, need to be bolder at offering more real prognoses.
Evidence, albeit far from conclusive, suggests that “concurrent” palliative or hospice care alongside routine oncology care improves health outcomes (Table 3). Project Safe Conduct was started to integrate hospice care into lung cancer care at the Ireland Cancer Center. Before the study, 13% of patients with advanced lung cancer were referred to hospice; afterward, 80% of such patients enrolled in hospices and the average length of stay in hospice increased from 10 days to 44 days.81 The one randomized trial of concurrent hospice care plus usual oncology care vs usual oncology care alone has been published only in abstract form.80 The group with concurrent care lived slightly longer (not statistically significant), had quality of life preserved longer, used less chemotherapy, and transitioned to hospice enrollment sooner. The clinical care differences were modestly in favor of the concurrent-care approach, but the hospice cost was substantial and much higher than the cost of hospitalizations avoided (oral communication, John Finn, MD, Ascension Health Systems, Detroit, Michigan, October 2004). Meyers and colleagues84 enrolled patients in a phase 1 and 2 cancer treatment study and into a simultaneous care program that emphasized symptom management and transition to hospice. The uptake of the program was excellent. Patients received as many cycles of chemotherapy as without simultaneous care and were referred to hospice more frequently and earlier. A study at the Dana Farber Cancer Institute showed that cancer patients will use a free palliative care service alongside their usual oncology care, but health outcomes are not yet available.1 The one large randomized controlled trial of usual care plus palliative care consultation, in which 27% to 34% of patients had cancer, showed no difference in symptoms or survival but did show a $4855-per- patient cost savings.85 Proof of symptom control or survival improvement at a cost society can afford will require rigorous testing, preferably in randomized clinical trials.
Table 3
Table 3
Studies of Concurrent Palliative Care With Oncology Care
One of the largest barriers to hospice in the United States is the way it is defined in the Medicare Hospice Benefit. Patients must have a life expectancy of 6 months or less and must forego curative treatment. Funding for chemotherapy and radiation is limited; thus, being enrolled in hospice can significantly limit very useful palliative treatment. Several hospice programs have begun to respond to these eligibility barriers and are providing a broader range of services.45 Some have changed to palliative care programs under home health care services, integrating palliative chemotherapy and radiation and related treatments (paid for by the patient’s insurance or Medicare drug benefit) with elements of traditional hospice care. Passik and colleagues86 at Hospice of the Bluegrass showed that patients who transition from acute care to palliative care then to the hospice benefit, compared with those who transition directly from acute care to the hospice benefit, may prove to be both financial and care burdens to the hospice. As noted above, a randomized trial showed palliative care consultation alongside usual medical care saved the insurer $4855 per patient with no decrement in survival or symptoms.85 Several larger insurance-sponsored trials are ongoing.
Experimental Chemotherapy
Dr O: We were continuing the current course of treatment because he wanted it, but it was quite appropriate to initiate palliative care. Then Mr L and his wife embarked on this idea that he needed to get into a clinical trial…. Dr A was able to help the family put aside their differences in order to allow Mr L to enter into palliative care and go home and stay home.
Patients on clinical trials have as good an understanding of the risks and benefits as we can give them—after all, they have read and signed informed consent documents—but this understanding is far from perfect. Despite written information, many will still overestimate their own particular chance of success.19 Mrs L expressed, as do many patients and families, that they hoped Mr L would survive long enough to receive a new treatment, or even a cure. And as we noted above, informed phase 1 patients are willing to undergo new treatments with a 10% mortality risk for an unknown but low chance of benefit.
Reimbursement and Economic Issues: Why Oncology is Different
Most palliative care is relatively inexpensive. However, palliative chemotherapy regimens have a huge price tag, at a cost of up to $100 000 a year per patient, and even insured patients can be burdened by a 20% co-payment requirement. The cost of palliative chemotherapy for colorectal cancer could easily be $50 000 a year, not counting supportive care drugs or imaging.87 Patients with cancer account for about 40% of all Medicare drug costs, totaling an estimated $5.3 billion in 2006, with $1.5 billion for erythropoietin-like drugs alone.88 Some drugs (oxaliplatin for metastatic colon cancer89 and docetaxol for metastatic prostate cancer42) have acceptable cost-effectiveness ratios in which treated patients gain several weeks or months of life, at a cost less than $100 000 per additional year of life saved, but for Medicare, these are new costs to pay. For Mr L, his last dose of intrathecal cytarabine given 6 days before his death would cost $3400 at our institution.
The manner in which oncologists are reimbursed may play a role in chemotherapy use. Over the past 10 years, oncologists have become some of the highest paid medical specialists.90 Some of oncologists’ practice income comes from administering and selling chemotherapeutic agents and supportive care drugs (eg, bisphosphonates, erythropoietin-like drugs and colony stimulating factors). As is the case in other medical specialties, oncologists are reimbursed more for their specialized treatment of chemotherapy than for lengthy discussions about prognosis and palliative care options.91 This potential for conflict of interest has been the subject of controversy. The only published study was conducted before Medicare chemotherapy reimbursement was reduced in 2003 and found that reimbursement did not affect the decision to give palliative chemotherapy but that oncologists tended to choose chemotherapy that gave the highest profit to the practice.92 Although hospice care and in-patient palliative care93 may save money during the last month of life, total disease costs are unchanged or increased,94 so hospices cannot save enough money to allow more chemotherapy. It is critical to improve reimbursement incentives. For example, in 1 study, more than 25% of oncologists reported insufficient reimbursement for time spent in discussion with patients and families as “the most troublesome” reimbursement barrier to providing better end-of-life-care.69
If societal resources become limited, and maximizing health benefit becomes more difficult, there are only a few ways to reduce the cost of oncology care:
  • Reduce the services provided (eg, “stopping rules,”95 in which no more than 3 lines of chemotherapy would be given for refractory metastatic breast cancer or no erythropoietinlike drug treatment for anemia would be given unless the hemoglobin is <10 g/dL):
  • Reduce requested services by increasing patient co-payments.
  • Reduce the amount that Medicare or insurers pay for chemotherapy and supportive care drugs, health care professional services, or hospitalizations.
  • Prevent or delay new drugs from entering the market, or delay reimbursement for them.
  • Reduce the payment to oncologists for administering chemotherapy and supportive care drugs, perhaps influencing the type of chemotherapy administered.
Ultimately, unless resources are unlimited, patients and families (or society at large) may be asked to balance individual patient needs against those of society.96
Given understandable patient, family, clinician, and societal goals and concerns, how can all individuals be educated and informed as to the appropriate use of chemotherapy and the value of palliative care and hospice? First, as suggested by hospice experts and oncologists,12 someone other than the oncologist might give information about the hospice option and provide specific prognosis and palliative treatment information. Second, palliative care specialists should be aware of the difficult decision making that cancer patients face near death, and how different their perspective is about benefit and toxicity.9 Decision aids may be used. Finally, regarding palliative care options, completion of studies integrating hospice and palliative care into usual oncology care will permit evidence-based decision making.
The conundrum for today’s oncologist is that moving on to third- or fourth-line chemotherapy may be easier than discussing hospice care, the patient and family may be less upset, and they may prefer to not discuss the issue with the oncologist.68 Adverse effects of chemotherapy may be minimal, discussions take more time, and chemotherapy intervention is better compensated than are discussions. However, without a clear goals-of-care discussion, patients like Mr L and their families may be unprepared for what the final few months, weeks, or even days may bring. Through honest and respectful communication about the last stages of cancer, physicians can give patients a genuine choice about how to spend their last phase of life.
Acknowledgments
Funding/Support: The Perspectives on Care at the Close of Life series is made possible by funding from the California Archstone Foundation. The authors are also supported in part by grant funding from the Justice, Equality, Human Dignity, and Tolerance ( JEHT) Foundation, New York; by grants 1G08LM009525-01 of the National Library of Medicine, National Institutes of Health, and R01CA116227-01 of the National Cancer Institute (NCI) to study outcomes of hospitalized cancer patients (Dr Meier, PI); and by the Palliative Care Leadership Program (http://www.capc.org/palliative-care-leadership-initiative).
Role of the Sponsors: None of the funding agencies had a role in the preparation, review, or approval of the manuscript.
Footnotes
Financial Disclosures: None reported.
Other Sources: For a list of relevant Web sites, see the article on the JAMA Web site at http://www.jama.com.
Additional Contributions: We would like to thank Karen Scott, BA, for administrative assistance, the Center to Advance Palliative Care, http://www.capc.org.
1. Temel JS, Jackson VA, Billings JA, et al. Phase II study: integrated palliative care in newly diagnosed advanced non-small-cell lung cancer patients. J Clin Oncol. 2007;25(17):2377–2382. [PubMed]
2. Martoni AA, Tanneberger S, Mutri V. Cancer chemotherapy near the end of life: the time has come to set guidelines for its appropriate use. Tumori. 2007;93(5):417–422. [PubMed]
3. Teno JM. Advance directives: time to move on. Ann Intern Med. 2004;141(2):159–160. [PubMed]
4. Koedoot CG, Oort FJ, de Haan RJ, Bakker PJ, de Graeff A, de Haes JC. The content and amount of information given by medical oncologists when telling patients with advanced cancer what their treatment options are: palliative chemotherapy and watchful-waiting. Eur J Cancer. 2004;40(2):225–235. [PubMed]
5. Sullivan AM, Lakoma MD, Matsuyama RK, Rosenblatt L, Arnold RM, Block SD. Diagnosing and discussing imminent death in the hospital: a secondary analysis of physician interviews. J Palliat Med. 2007;10(4):882–893. [PubMed]
6. Mackillop WJ, Stewart WE, Ginsburg AD, Stewart SS. Cancer patients’ perceptions of their disease and its treatment. Br J Cancer. 1988;58(3):355–358. [PMC free article] [PubMed]
7. Chow E, Andersson L, Wong R, et al. Patients with advanced cancer: a survey of the understanding of their illness and expectations from palliative radiotherapy for symptomatic metastases. Clin Oncol (R Coll Radiol) 2001;13(3):204–208. [PubMed]
8. Helft PR. Necessary collusion: prognostic communication with advanced cancer patients. J Clin Oncol. 2005;23(13):3146–3150. [PubMed]
9. Matsuyama R, Reddy S, Smith TJ. Why do patients choose chemotherapy near the end of life? a review of the perspective of those facing death from cancer. J Clin Oncol. 2006;24(21):3490–3496. [PubMed]
10. Silvestri G, Pritchard R, Welch HG. Preferences for chemotherapy in patients with advanced non-small cell lung cancer: descriptive study based on scripted interviews. BMJ. 1998;317(7161):771–775. [PMC free article] [PubMed]
11. Agrawal M, Grady C, Fairclough DL, Meropol NJ, Maynard K, Emanuel EJ. Patients’ decision-making process regarding participation in phase I oncology research. J Clin Oncol. 2006;24(27):4479–4484. [PubMed]
12. The AM, Hak T, Koeter G, van der Wal G. Collusion in doctor-patient communication about imminent death: an ethnographic study. West J Med. 2001;174(4):247–253. [PMC free article] [PubMed]
13. Lee SJ, Fairclough D, Antin JH, Weeks JC. Discrepancies between patient and physician estimates for the success of stem cell transplantation. JAMA. 2001;285(8):1034–1038. [PubMed]
14. Lee SJ, Loberiza FR, Rizzo JD, Soiffer RJ, Antin JH, Weeks JC. Optimistic expectations and survival after hematopoietic stem cell transplantation. Biol Blood Marrow Transplant. 2003;9(6):389–396. [PubMed]
15. Lamont EB, Christakis NA. Prognostic disclosure to patients with cancer near the end of life. Ann Intern Med. 2001;134(12):1096–1105. [PubMed]
16. Santoso JT, Engle DB, Schaffer L, Wan JY. Cancer diagnosis and treatment: communication accuracy between patients and their physicians. Cancer J. 2006;12(1):73–76. [PubMed]
17. Glare P, Virik K, Jones M, et al. A systematic review of physicians’ survival predictions in terminally ill cancer patients. BMJ. 2003;327(7408):195–198. [PMC free article] [PubMed]
18. Smith TJ, Staats PS, Deer T, et al. Randomized clinical trial of an implantable drug delivery system compared with comprehensive medical management for refractory cancer pain: impact on pain, drug-related toxicity, and survival. J Clin Oncol. 2002;20(19):4040–4049. [PubMed]
19. Meropol NJ, Weinfurt KP, Burnett CB, et al. Perceptions of patients and physicians regarding phase I cancer clinical trials: implications for physician-patient communication. J Clin Oncol. 2003;21(13):2589–2596. [PubMed]
20. Mallinger JB, Shields CG, Griggs JJ, et al. Stability of decisional role preference over the course of cancer therapy. Psychooncology. 2006;15(4):297–305. [PubMed]
21. Grunfeld EA, Maher EJ, Browne S, et al. Advanced breast cancer patients’ perceptions of decision making for palliative chemotherapy. J Clin Oncol. 2006;24(7):1090–1098. [PubMed]
22. Slevin ML, Stubbs L, Plant HJ, et al. Attitudes to chemotherapy: comparing views of patients with cancer with those of doctors, nurses, and general public. BMJ. 1990;300(6737):1458–1460. [PMC free article] [PubMed]
23. Balmer CE, Thomas P, Osborne RJ. Who wants second-line, palliative chemotherapy? Psychooncology. 2001;10(5):410–418. [PubMed]
24. Brundage MD, Feldman-Stewart D, Cosby R, et al. Cancer patients’ attitudes toward treatment options for advanced non-small cell lung cancer: implications for patient education and decision support. Patient Educ Couns. 2001;45(2):149–157. [PubMed]
25. Bremnes RM, Andersen K, Wist EA. Cancer patients, doctors and nurses vary in their willingness to undertake cancer chemotherapy. Eur J Cancer. 1995;31A(12):1955–1959. [PubMed]
26. Tamburini M, Buccheri G, Brunelli C, Ferrigno D. The difficult choice of chemotherapy in patients with unresectable non-small-cell lung cancer. Support Care Cancer. 2000;8(3):223–228. [PubMed]
27. Hirose T, Horichi N, Ohmori T, et al. Patients preferences in chemotherapy for advanced non-small-cell lung cancer. Intern Med. 2005;44(2):107–113. [PubMed]
28. Koedoot CG, de Haan RJ, Stiggelbout AM, et al. Palliative chemotherapy or best supportive care? a prospective study explaining patients’ treatment preference and choice. Br J Cancer. 2003;89(12):2219–2226. [PMC free article] [PubMed]
29. Earle CC, Neville BA, Landrum MB, Ayanian JZ, Block SD, Weeks JC. Trends in the aggressiveness of cancer care near the end of life. J Clin Oncol. 2004;22(2):315–321. [PubMed]
30. Murillo JR, Jr, Koeller J. Chemotherapy given near the end of life by community oncologists for advanced non-small cell lung cancer. Oncologist. 2006;11(10):1095–1099. [PubMed]
31. Connor SR, Pyenson B, Fitch K, Spence C, Iwasaki K. Comparing hospice and nonhospice patient survival among patients who die within a three-year window. J Pain Symptom Manage. 2007;33(3):238–246. [PubMed]
32. American Society of Clinical Oncology Outcomes Working Group. Outcomes of cancer treatment for technology assessment and cancer treatment guidelines. J Clin Oncol. 1996;14(2):671–679. [PubMed]
33. Smith TJ, Khatcheressian J, Lyman GH, et al. 2006 Update of recommendations for the use of white blood cell growth factors: an evidence-based clinical practice guideline. J Clin Oncol. 2006;24(19):3187–3205. [PubMed]
34. Pfister DG, Johnson DH, Azzoli CG, et al. American Society of Clinical Oncology treatment of unresectable non-small-cell lung cancer guideline: Update 2003. J Clin Oncol. 2004;22(2):330–353. [PubMed]
35. Shepherd FA, Dancey J, Ramlau R, et al. Prospective randomized trial of doce-taxel versus best supportive care in patients with non-small-cell lung cancer previously treated with platinum-based chemotherapy. J Clin Oncol. 2000;18 (10):2095–2103. [PubMed]
36. Dancey J, Shepherd FA, Gralla RJ, Kim YS. Quality of life assessment of second-line docetaxel versus best supportive care in patients with non-small-cell lung cancer previously treated with platinum-based chemotherapy: results of a prospective, randomized phase III trial. Lung Cancer. 2004;43(2):183–194. [PubMed]
37. Shepherd FA, Rodrigues Pereira J, Ciuleanu T, et al. Erlotinib in previously treated non-small-cell lung cancer. N Engl J Med. 2005;353(2):123–132. [PubMed]
38. Goldberg RM, Rothenberg ML, Van Cutsem E, et al. The continuum of care: a paradigm for the management of metastatic colorectal cancer. Oncologist. 2007;12(1):38–50. [PubMed]
39. Tannock IF, de Wit R, Berry WR, et al. Docetaxel plus prednisone or mitox-antrone plus prednisone for advanced prostate cancer. N Engl J Med. 2004;351(15):1502–1512. [PubMed]
40. Massarelli E, Andre F, Liu DD, et al. A retrospective analysis of the outcome of patients who have received two prior chemotherapy regimens including platinum and docetaxel for recurrent non-small-cell lung cancer. Lung Cancer. 2003;39(1):55–61. [PubMed]
41. Hayes DF. An overview of treatment for locally advanced recurrent, and metastatic breast cancer. In: Rose BF, editor. UptoDate. Waltham, MA: UpToDate; 2008.
42. Collins R, Fenwick E, Trowman R, et al. A systematic review and economic model of the clinical effectiveness and cost-effectiveness of docetaxel in combination with prednisone or prednisolone for the treatment of hormone-refractory metastatic prostate cancer. Health Technol Assess. 2007;11(2):iii–iv. xv–xviii, 1–179. [PubMed]
43. El Demery M, Pouessel D, Avances C, et al. What is the objective of second-line chemotherapy after failure of first-line chemotherapy in hormone-resistant metastatic prostate? Prog Urol. 2006;16(3):320–323. [PubMed]
44. Casarett DJ, Quill TE. “I’m not ready for hospice”: strategies for timely and effective hospice discussions. Ann Intern Med. 2007;146(6):443–449. [PubMed]
45. Wright AA, Katz IT. Letting go of the rope—aggressive treatment, hospice care, and open access. N Engl J Med. 2007;357(4):324–327. [PubMed]
46. Bruera E, Sweeney C, Willey J, et al. Breast cancer patient perception of the helpfulness of a prompt sheet versus a general information sheet during outpatient consultation: a randomized, controlled trial. J Pain Symptom Manage. 2003;25(5):412–419. [PubMed]
47. Brown RF, Butow PN, Dunn SM, Tattersall MH. Promoting patient participation and shortening cancer consultations: a randomised trial. Br J Cancer. 2001;85(9):1273–1279. [PMC free article] [PubMed]
48. Glynne-Jones R, Ostler P, Lumley-Graybow S, et al. Can I look at my list? an evaluation of a ’prompt sheet’ within an oncology outpatient clinic. Clin Oncol (R Coll Radiol) 2006;18(5):395–400. [PubMed]
49. Smith TJ. The art of oncology: when the tumor is not the target. tell it like it is. J Clin Oncol. 2000;18(19):3441–3445. [PubMed]
50. Eisenberg PD. Caring for patients at the end of life. Ann Intern Med. 2002;136(6) 1 paragraph. [PubMed]
51. Hagerty RG, Butow PN, Ellis PM, et al. Communicating with realism and hope: incurable cancer patients’ views on the disclosure of prognosis [published correction appears in J Clin Oncol. 2005;23(15):3652] J Clin Oncol. 2005;23(6):1278–1288. [PubMed]
52. Kirk P, Kirk I, Kristjanson LJ. What do patients receiving palliative care for cancer and their families want to be told? a Canadian and Australian qualitative study. BMJ. 2004;328(7452):1343. [PMC free article] [PubMed]
53. Whelan TM, O’Brien MA, Villasis-Keever M, et al. Impact of Cancer-Related Decision Aids. Rockville, MD: Agency for Healthcare Research and Quality; Jul, 2002. Evidence Report/Technology Assessment 46. AHRQ publication no 01-E004.
54. Peele PB, Siminoff LA, Xu Y, Ravdin PM. Decreased use of adjuvant breast cancer therapy in a randomized controlled trial of a decision aid with individualized risk information. Med Decis Making. 2005;25(3):301–307. [PubMed]
55. Siminoff LA, Gordon NH, Silverman P, Budd T, Ravdin PM. A decision aid to assist in adjuvant therapy choices for breast cancer. Psychooncology. 2006;15(11):1001–1013. [PubMed]
56. Leighl NB, Shepherd H, Butow P, et al. When the goal is not cure: a randomized trial of a patient decision aid in advanced colorectal cancer. J Clin Oncol. 2007;25(suppl 18):6509.
57. Neff P, Lyckholm L, Smith T. Truth or consequences: what to do when the patient doesn’t want to know. J Clin Oncol. 2002;20(13):3035–3037. [PubMed]
58. Shanafelt TD, Loprinzi C, Marks R, Novotny P, Sloan J. Are chemotherapy response rates related to treatment-induced survival prolongations in patients with advanced cancer? J Clin Oncol. 2004;22(10):1966–1974. [PubMed]
59. Smith TJ, Schnipper LJ. The American Society of Clinical Oncology program to improve end-of-life care. J Palliat Med. 1998;1(3):221–230. [PubMed]
60. Christakis NA, Iwashyna TJ. The health impact of health care on families: a matched cohort study of hospice use by decedents and mortality outcomes in surviving, widowed spouses. Soc Sci Med. 2003;57(3):465–475. [PubMed]
61. Schockett ER, Teno JM, Miller SC, Stuart B. Late referral to hospice and bereaved family member perception of quality of end-of-life care. J Pain Symptom Manage. 2005;30(5):400–407. [PubMed]
62. Teno JM, Shu JE, Casarett D, Spence C, Rhodes R, Connor S. Timing of referral to hospice and quality of care: length of stay and bereaved family members’ perceptions of the timing of hospice referral. J Pain Symptom Manage. 2007;34(2):120–125. [PubMed]
63. Rabow MW, Schanche K, Petersen J, Dibble SL, McPhee SJ. Patient perceptions of an outpatient palliative care intervention: “It had been on my mind before, but I did not know how to start talking about death … ” J Pain Symptom Manage. 2003;26(5):1010–1015. [PubMed]
64. Casarett D, Crowley R, Stevenson C, Xie S, Teno J. Making difficult decisions about hospice enrollment: what do patients and families want to know? J Am Geriatr Soc. 2005;53(2):249–254. [PubMed]
65. Casarett DJ, Crowley RL, Hirschman KB. How should clinicians describe hospice to patients and families? J Am Geriatr Soc. 2004;52(11):1923–1928. [PubMed]
66. Brickner L, Scannell K, Marquet S, Ackerson L. Barriers to hospice care and referrals: survey of physicians’ knowledge, attitudes, and perceptions in a health maintenance organization. J Palliat Med. 2004;7(3):411–418. [PubMed]
67. Casarett D, Karlawish J, Morales K, Crowley R, Mirsch T, Asch DA. Improving the use of hospice services in nursing homes: a randomized controlled trial. JAMA. 2005;294(2):211–217. [PubMed]
68. Lamont EB, Siegler M. Paradoxes in cancer patients’ advance care planning. J Palliat Med. 2000;3(1):27–35. [PubMed]
69. Foley K, Gellband H, editors. Improving Palliative Care for Cancer. Washington, DC: National Academy Press; 2001.
70. Back A. Patient-physician communication in oncology: what does the evidence show? Oncology (Williston Park) 2006;20(1):67–74. [PubMed]
71. Rabinowitz T, Peirson R. “Nothing is wrong, doctor”: understanding and managing denial in patients with cancer. Cancer Invest. 2006;24(1):68–76. [PubMed]
72. Quill TE, Williamson PR. Healthy approaches to physician stress. Arch Intern Med. 1990;150(9):1857–1861. [PubMed]
73. Meier DE, Back AL, Morrison RS. The inner life of physicians and care of the seriously ill. JAMA. 2001;286(23):3007–3014. [PubMed]
74. Smith RC, Zimny GH. Physicians’ emotional reactions to patients. Psychosomatics. 1988;29(4):392–397. [PubMed]
75. Creagan ET. Burnout and balance: how to go the distance in the 21st century. Cancer Control. 2004;11(4):266–268. [PubMed]
76. Tobias JS, Souhami RL. Fully informed consent can be needlessly cruel. BMJ. 1993;307(6913):1199–1201. [PMC free article] [PubMed]
77. Fallowfield L. Participation of patients in decisions about treatment for cancer. BMJ. 2001;323(7322):1144. [PMC free article] [PubMed]
78. Emanuel LL, Ferris FD, von Gunten CF, Von Roenn J. Education in Palliative and End of Life Care for Oncology [CD-ROM] Chicago, IL: EPEC-O; 2007. NIH publication 07–6114.
79. Mack JW, Wolfe J, Cook EF, Grier HE, Cleary PD, Weeks JC. Hope and prognostic disclosure. J Clin Oncol. 2007;25(35):5636–5642. [PubMed]
80. Finn J, Pienta K, Parzuchowski J. Palliative care project: bridging cancer treatment and hospice care. Proc Am Soc Clin Oncol. 2002;21:1452.
81. Pitorak EF, Armour M, Sivec HD. [Accessed May 12, 2008.];Project Safe Conduct integrates palliative goals into comprehensive cancer care: an interview with Elizabeth Ford Pitorak and Meri Armour. 2002 http://www2.edc.org/lastacts/archives/archivesjuly02/featureinn.asp. [PubMed]
82. Bakitas M, Stevens M, Ahles T, et al. Project ENABLE: a palliative care demonstration project for advanced cancer patients in three settings. J Palliat Med. 2004;7(2):363–372. [PubMed]
83. Elsayem A, Swint K, Fisch MJ, et al. Palliative care inpatient service in a comprehensive cancer center: clinical and financial outcomes. J Clin Oncol. 2004;22(10):2008–2014. [PubMed]
84. Meyers FJ, Linder J, Beckett L, Christensen S, Blais J, Gandara DR. Simultaneous care: a model approach to the perceived conflict between investigational therapy and palliative care. J Pain Symptom Manage. 2004;28(6):548–556. [PubMed]
85. Gade G, Venohr I, Conner D, et al. Impact of an inpatient palliative care team: a randomized control trial. J Palliat Med. 2008;11(2):180–190. [PubMed]
86. Passik SD, Ruggles C, Brown G, et al. Is there a model for demonstrating a beneficial financial impact of initiating a palliative care program by an existing hospice program? Palliat Support Care. 2004;2(4):419–423. [PubMed]
87. Schrag D. The price tag on progress–chemotherapy for colorectal cancer. N Engl J Med. 2004;351(4):317–319. [PubMed]
88. Meropol NJ, Schulman KA. Cost of cancer care: issues and implications. J Clin Oncol. 2007;25(2):180–186. [PubMed]
89. Hillner BE, Schrag D, Sargent DJ, Fuchs CS, Goldberg RM. Cost-effectiveness projections of oxaliplatin and infusional fluorouracil versus irinotecan and bolus fluorouracil in first-line therapy for metastatic colorectal carcinoma. Cancer. 2005;104(9):1871–1884. [PubMed]
90. Bodenheimer T, Berenson RA, Rudolf P. The primary care-specialty income gap: why it matters. Ann Intern Med. 2007;146(4):301–306. [PubMed]
91. Smith TJ, Girtman J, Riggins J. Why academic divisions of hematology/oncology are in trouble and some suggestions for resolution. J Clin Oncol. 2001;19(1):260–264. [PubMed]
92. Jacobson M, O’Malley AJ, Earle CC, Pakes J, Gaccione P, Newhouse JP. Does reimbursement influence chemotherapy treatment for cancer patients? Health Aff (Millwood) 2006;25(2):437–443. [PubMed]
93. Smith TJ, Coyne P, Cassel B, Penberthy L, Hopson A, Hager MA. A high-volume specialist palliative care unit and team may reduce in-hospital end-of-life care costs. J Palliat Med. 2003;6(5):699–705. [PubMed]
94. Campbell DE, Lynn J, Louis TA, Shugarman LR. Medicare program expenditures associated with hospice use. Ann Intern Med. 2004;140(4):269–277. [PubMed]
95. Benner SE, Fetting JH, Brenner MH. A stopping rule for standard chemotherapy for metastatic breast cancer: lessons from a survey of Maryland medical oncologists. Cancer Invest. 1994;12(5):451–455. [PubMed]
96. Smith TJ, Bodurtha JN. Ethical considerations in oncology: balancing the interests of patients, oncologists, and society. J Clin Oncol. 1995;13(9):2464–2470. [PubMed]