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- How to Avoid Late Chemotherapy. September 20, 2016
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DOI: 10.1200/JOP.2016.013995 Journal of Oncology Practice - published online before print September 20, 2016
PMID: 27650843
Paradox of Prescribing Late Chemotherapy: Oncologists Explain
See accompanying editorial on page
The value of chemotherapy for patients with cancer in the last weeks of life warrants examination. Late chemotherapy may not improve survival or quality of life but typically precludes hospice enrollment and may result in additional symptoms, increased use of other aggressive treatments, and worsening quality of life. Few studies have explored oncologists’ rationales for administering chemotherapy near death. This study examines the self-reported factors that influence oncologists’ decisions about late chemotherapy.
In-depth individual interviews were conducted with 17 oncologists through a semistructured interview guide. Interviews were audio recorded and transcribed verbatim. Transcripts were coded and analyzed using conventional content analysis, a qualitative method that allows the detection and analysis of patterns in the data.
Clinical factors take priority in determining late chemotherapy decisions when clear treatment choices exist. When clinical factors are ambiguous, emotion becomes a highly salient influence. Oncologists view late chemotherapy to be patient driven and use it to palliate emotional distress and maintain patient hope even when physical benefit is unexpected. Oncologists experience unique and difficult challenges when caring for dying patients, including emotionally draining communication, overwhelming responsibility for life/death, limitations of oncology to heal, and prognostic uncertainty. These challenges are also eased by offering late chemotherapy.
The findings reveal a nuanced understanding of why oncologists find it difficult to refuse chemotherapy treatment for patients near death. Optimal end-of-life treatment decisions require supportive interventions and system change, both of which must take into account the challenges oncologists face.
The value of cancer care, including the use of expensive drugs during the last weeks of life, warrants examination.1-3 Evidence suggests that late chemotherapy may not improve survival or quality of life and that the benefits of many newer therapies are marginal and may not outweigh the costs.4,5 Alternatively, ample evidence indicates that chemotherapy can result in a wide range and number of toxicities, each with the potential to necessitate additional treatments, worsen quality of life, and result in hospitalization or death.6-10 Late chemotherapy, defined as the practice of continuing an existing regimen within 14 days of death or beginning a new one within 30 days of death, has been named an indicator of quality of care and cited as a barrier to timely transition to hospice and other forms of palliative care.11-13 For these reasons, experts strongly discourage the routine practice of prescribing drugs with marginal benefits to patients with advanced cancer and recommend that treatment at the end of life (EOL) be limited to palliative care, including symptom palliation and psychological support.14-16 Further, ASCO named the practice of administering cancer-directed treatments likely to be ineffective as number one on its 2012 list of top five practices that are widespread, costly, and not supported by strong evidence.17
ASCO recommends full integration of palliative care across the cancer care continuum.18,19 Nevertheless, oncologists tend to delay transitions to hospice and palliative care and may precede these with late chemotherapy regimens.20,21 However, little evidence explains why oncologists administer chemotherapy to patients near EOL. We examine the self-reported factors that influence oncologists’ decisions about late chemotherapy. A related article that focuses on the impact of patient age in this decision-making process has been published elsewhere.22
Given the exploratory nature of the study, we chose a qualitative approach to data collection using in-depth individual interviews with oncologists. This approach is well suited to examine factors that influence chemotherapy decision making.23,24 The research team included experts in palliative medicine, oncology, qualitative research methods, gerontology, and public health. Oncologists were recruited from two separate health care settings; the institutional review boards of each setting approved the study. A more detailed description of study methods has been published elsewhere.22
We used purposive sampling to recruit oncologists from three types of practice settings in the Midwest: academic, private practice, and an oncology fellowship program. All participants routinely prescribed cytotoxic chemotherapy.
Key informants (physicians or administrators known to the study team) at each practice setting identified a total of 19 eligible oncologists. All received invitation packets in the mail; 17 agreed to participate. Interviews were arranged and confirmed by telephone or e-mail. Written informed consent was obtained before each interview. On average, the interviews lasted between 60 and 90 min. Participants were offered $100 as an incentive; four refused payment.
Author M.B. conducted individual face-to-face interviews with each participant using a semistructured interview guide (Data Supplement). Questions elicited detailed narratives of oncologists’ perceptions of and experiences with late chemotherapy decisions, including descriptions of the factors that influence those decisions. Interviews were digitally recorded, transcribed verbatim, and checked for accuracy; all transcripts were deidentified.
Data were coded and analyzed using qualitative content analysis, an analytic approach frequently employed in qualitative research on EOL issues. Specifically, we used conventional content analysis, which is one of three systematic approaches to qualitative content analysis.25,26 Unlike summative content analysis, conventional content analysis does not quantify words or content, and it differs from directed content analysis in that codes are generated post hoc and not determined a priori. Conventional content analysis is appropriate for studying phenomena about which little is known and for which little theory exists. Although many aspects of this approach overlap with a closely related method—thematic analysis27—our analytic process was specifically guided by the conventional content analysis outlined by Hsieh and Shannon.25 NVivo 8 software (www.qsrinternational.com) was used to organize and manage the data.
Authors M.B. and K.E.B. began the analysis by reading each transcript start to finish several times to get an overall sense of the data and to note their impressions. They next developed a coding scheme by reading the first three transcripts line by line and highlighting and labeling (with words from the text) all pieces of text that identified or described an idea related to factors that influence oncologists’ chemotherapy decisions. These labels were examined and grouped into coherent categories. For example, labels such as “chemo caused a fever,” “chemo can kill you,” and “chemo made her tired” were grouped into an analytic code category called adverse effects of chemotherapy. The first three transcripts were then recoded using the analytic code categories as a preliminary coding scheme.
To reduce the risk of systematic bias, coding differences were discussed and reconciled between M.B. and K.E.B. Independent coding continued with transcripts four to six until both coders agreed that the codes were used uniformly, which resulted in a final version of the coding scheme that included definitions for each code category and exemplars. This final coding scheme was then used by M.B. to code the remaining transcripts line by line. Participant enrollment was discontinued when new ideas were no longer presented in the interview data and informational redundancy was achieved.28 The coding scheme allowed us to identify patterns within and across interviews, including elements that appeared frequently or were particularly illustrative or unexpected. Quoted responses included in this article are those that best capture the themes in the data.
Nineteen physicians were invited to participate in the study. Seventeen consented, which yielded a response rate of 89%. More than 70% of the respondents were male, and 82% were white. The mean respondent age was 47 years, and mean number of years in practice was 18. Sample characteristics are provided in Table 1. Variations in practice setting and clinical experience were intentional to capture heterogeneity across respondents.
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Three key findings emerged from the data:
Clinical factors take priority in determining late chemotherapy decisions when clear treatment choices exist. When clinical factors are ambiguous, emotion becomes a highly salient influence.
Oncologists view late chemotherapy to be patient driven. It is used to palliate emotional distress and maintain patient hope, even when physical benefit is unexpected.
Oncologists experience unique and difficult challenges when caring for dying patients, including emotionally draining communication, overwhelming feelings of responsibility for life and death, limitations of oncology to heal, and prognostic uncertainty. These challenges also can be eased by offering late treatment.
Oncologists first consider clinical factors when making chemotherapy decisions. Specifically, they weigh the likelihood of clinical benefit, such as tumor shrinkage, relative to the likelihood of clinical burdens, such as adverse effects like nausea. In certain cases, medical factors make the decision clear. For example, respondents often reported that they would unlikely offer treatment to very sick elderly patients with nonresponsive advanced cancers because these patients would be too sick to tolerate the therapy and would not benefit from it. Alternatively, young adults with responsive cancers who are otherwise healthy would likely be treated because they are expected to tolerate it well and benefit from it. In cases of relative medical certainty, decision making was described as “obvious” and even “easy.” However, at times, medical factors are uncertain, benefits of chemotherapy may be unclear, or tolerability may be difficult to determine. In those cases, oncologists reported turning to nonmedical factors to decide about chemotherapy.
Patient wishes for treatment were the most frequently and emphatically reported factor to influence oncologists’ chemotherapy decisions. Nearly 80% of respondents said that patient wishes are either the first or the second most important factor in their decision to offer late chemotherapy. More than half of the respondents said that patient wishes were the most important factor. They noted that when desperate patients ask for anything that may give them a chance, it is difficult to refuse.
Oncologists offer late chemotherapy to patients with incurable cancer who want it, even when they do not expect it to help the cancer or other physical symptoms, because they believe that it eases patients’ emotional distress. Similarly, they believe that patients equate chemotherapy with hope. Thus, maintaining patient hope was reported as a rationale for treatment. Finally, nearly all respondents noted that offering chemotherapy to address emotional needs and to preserve hope is ubiquitous. When asked how common this practice is, a representative response was, “We all do it.”
Table 2 presents respondents’ detailed descriptions of the patient factors that influence oncologists’ late chemotherapy decisions.
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Respondents identified four types of experiences that make EOL care especially difficult: emotionally draining communication, overwhelming feelings of responsibility for life and death, limitations of oncology to heal, and prognostic uncertainty.
For most of the respondents, telling patients that they have no further treatment to offer is one of their most difficult tasks. They characterized the discussion about stopping chemotherapy as “stomach turning,” “emotionally draining,” and “horribly sad.” Moreover, they reported that it is easier on everyone to bypass “the talk” and to offer the next round of chemotherapy.
Several respondents described depersonalization as a coping response to their emotionally difficult work. For example, one oncologist reported that when he goes into the room where the patient and family are waiting and he must tell them that treatment will no longer be useful, he feels like he is out of his body or is watching himself.
Feeling responsible for life-and-death decisions was also reported as among the most difficult aspects of EOL care. One oncologist explained it in terms of feeling responsible for having to decide when it is time for someone to die and noted that this overwhelming responsibility is what makes the job so hard.
Many respondents explained that encountering the limitations of oncology to heal is a challenge. In short, they reported feeling badly when they have no effective treatments left to offer. In addition, they reported that they are trained to act or to do something for their patients. When effective treatments run out, they can no longer do what their patients expect of them or what they expect of themselves. Offering purely palliative care or emotional support at EOL is rejected as an opportunity to meet those expectations. As one respondent remarked, “I didn’t go into medicine to help people die.”
One participant raised the question, unsolicited, of whether offering treatment (when no effective treatments are left) is a way to palliate oncologists’ discomfort with their limitations to heal. He put it this way: “I certainly like to think that I don’t do it to treat myself; like, I have nothing else to offer, so I give them treatment [be]cause I can’t think of what else to do.”
Respondents grapple with late treatment decisions in the face of two types of prognostic uncertainty: the inability to predict time of death and to know, for certain, whether chemotherapy will help a particular patient. For many, prognostic uncertainty favors offering treatment. All oncologists seemed to be able to call to mind cases of the rare patient who improved against all odds after late chemotherapy. Cases of prognostic uncertainty were reported to play a big role in treatment decisions because, for example, “you think about that in the back of your mind. You see a case like that, you think, it’s this person’s life.”
Table 3 presents respondents’ detailed descriptions of the oncologist factors that influence their late chemotherapy decisions.
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Several important insights emerged in our in-depth qualitative study of oncologists’ experiences with chemotherapy administration near EOL. In particular, we found that when treatment choices are medically ambiguous, certain considerations become highly salient, such as easing patients’ emotional pain and maintaining their hope. In addition, oncologists identified four types of experiences that make EOL care particularly challenging and affect their decisions about late chemotherapy: emotionally draining communication, overwhelming feelings of responsibility for life and death, limits of oncology to heal, and prognostic uncertainty.
The findings are consistent with those from related work that suggest a complex array of factors may influence decisions about late chemotherapy, such as clinical factors, patient wishes, the need to preserve hope, and difficulty with EOL conversations.29-34 The current work confirms and extends previous findings and sheds more light on why these factors present challenges to oncologists’ decision making.
This study provides a rich and detailed description of US oncologists’ rationales and experiences about deciding whether to offer late chemotherapy. The reasons for prescribing it are complex and go beyond oncologists’ desires to be responsive to patient wishes, palliate emotional symptoms, and preserve hope. The context of this important decision making also includes the impact on oncologists themselves of caring for people who are dying. The findings illuminate the paradox of late chemotherapy by revealing a nuanced understanding of why it can be so difficult for oncologists to refuse to offer it. Such decisions generate significant burdens such as emotionally draining communication, overwhelming feelings of responsibility, role dissonance (ie, the gap between what oncologists want to do for their patients and what they can actually do), and discomfort with prognostic uncertainty. Thus, at times, oncologists prescribe late chemotherapy to simply help the patient, family members, and themselves to feel better, regardless of expected clinical benefits or costs. This practice can be palliative for oncologists as well as patients, and perhaps is never more needed by both than when treatments are no longer effective. And yet, late chemotherapy imposes costs to patients and society that cannot be ignored.
Intervention research to reduce the use of late chemotherapy has been limited. Related work has focused on instrumental support, such as clinical decision support tools,35,36 education to improve communication skills and survival estimates,37-39 and financial incentives.40-42 The current data suggest that these approaches, topics, and interventions are important but not sufficient to change practice patterns. Interventions aimed at easing the emotional burdens oncologists experience in caring for patients at EOL have received little attention but are also needed. Failing to address these burdens has been associated with declining physician well-being and suboptimal patient care practices.43 Indeed, the current findings indicate that prescribing chemotherapy instead of talking with patients about stopping it may have more to do with how badly it makes oncologists feel (and their belief that it upsets the patient/family) than with not knowing what to say or how to say it. This suggests that oncologists may need emotional support (at least as much as instrumental support) to more routinely engage with patients in difficult conversations that lead to optimal EOL treatment decisions.
At a recent palliative care symposium, a prominent palliative care physician underscored the need for and value of emotional support. An oncologist asked this physician to accompany her for “the talk” with a patient. When the visit was over, the palliative care physician asked the oncologist why she wanted the consult because she handled the talk perfectly. The oncologist said, “I know what to say, but without you in the room, I was afraid I’d look the patient in the eye and give another round of chemo.” Although anecdotal, this story is consistent with the study findings and illustrates a role for emotional support in EOL communication. Further, it suggests that palliative care physicians may be uniquely suited to provide it.
A model for supportive interventions may be found in workplace support groups that address oncologists’ grief over patient loss.44 Typically, these groups allow colleagues to not only exchange experiences related to patient loss and grief but also reflect on self-care strategies and remember patients who died. Although this format provides an opportunity for collegial support, oncologists’ needs for and interest in this type of process varies.45 In some cases, physician culture may discourage participation. Findings from a Canadian study suggest that as part of physician culture, an expression of emotion indicates weakness and that a culture of cure and broader societal norms of death denial are common.46 In that study, oncologists reported a reluctance to share grief over patient loss with colleagues because they perceived it as too risky. To the extent that a similar physician culture exists in the United States, it may represent a missed opportunity to facilitate difficult EOL care, including engagement in clear and compassionate EOL discussions. Research is needed to determine the extent and impact of physician culture on EOL practices in general and on late chemotherapy decisions in particular.
Meanwhile, modest interventions to support oncologists in the emotionally demanding aspects of their work may prove useful. Increased awareness of these demands among members of the entire cancer care team (oncologists, nurses, social workers, primary care providers, and palliative care specialists) may result in a more supportive team and a physician culture that fosters optimal treatment decisions. Senior oncologists and other leaders on the team can model behaviors that create a culture in which the expression of vulnerability is safe rather than risky. Finally, practices might elevate the priority assigned to oncologists’ needs for self-care by ensuring time and opportunity for strategies that maintain wellness, such as developing relationships, protecting private time, and attending to spiritual practices.47,48
The findings from this study suggest a need for future work to develop, implement, and evaluate interventions and system changes that take into account the impact of caring for dying patients on oncologists and, in particular, the emotional challenges they face when discussing stopping or not starting chemotherapy at EOL. Such studies might suggest new opportunities to achieve optimal, sustainable treatment regimens; enhance the experience of EOL care for patients and physicians; and develop more complete models of medical decision making.
These results are intended to provide insight into oncologists’ explanations of their decisions to offer late chemotherapy. However, they cannot be generalized beyond the study population. Larger-scale studies are necessary to build on these findings. And yet, despite the small sample, respondents were diverse and closely approximate the population of US oncologists with respect to sex, ethnicity, and age.49,50 Another potential limitation is that responses may have been biased toward social acceptability. Selection bias may have occurred because those who were nominated by key informants and agreed to participate may differ from the larger population of oncologists. Finally, the results reflect oncologist perceptions and thoughts and were not confirmed with other sources of data (eg, medical records, nurses and other clinical staff, patients and families).
In conclusion, the findings reveal a nuanced understanding of why it can be so difficult for oncologists to refuse chemotherapy to patients near death. Doing so generates significant burdens such as emotionally draining communication with patients and families, a sense of overwhelming responsibility for life and death, role dissonance (ie, the gap between what oncologists want to do for patients and what they can actually do), and discomfort with decisions that rest on prognostic uncertainty. Future work is needed to assist oncologists in making optimal EOL treatment decisions with patients and their loved ones. To be effective, such efforts, including the development of supportive interventions and the promotion of system change, must take into account the challenges oncologists face during this process.
Conception and design: Minnie Bluhm, Cathleen M. Connell, Maria J. Silveira
Administrative support: Minnie Bluhm, Cathleen M. Connell
Provision of study materials or patients: Maria J. Silveira
Collection and assembly of data: Minnie Bluhm, Cathleen M. Connell
Data analysis and interpretation: Minnie Bluhm, Cathleen M. Connell, Raymond G. De Vries, Nancy K. Janz, Kathleen E. Bickel
Manuscript writing: All authors
Final approval of manuscript: All authors
Accountable for all aspects of the work: All authors
The following represents disclosure information provided by authors of this manuscript. All relationships are considered compensated. Relationships are self-held unless noted. I = Immediate Family Member, Inst = My Institution. Relationships may not relate to the subject matter of this manuscript. For more information about ASCO's conflict of interest policy, please refer to www.asco.org/rwc or jop.ascopubs.org/site/misc/ifc.xhtml.
No relationship to disclose
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ACKNOWLEDGMENT
This research was initiated and completed while M.B. was a doctoral candidate at the University of Michigan School of Public Health and K.E.B. was an oncology fellow at the University of Michigan Medical School, with funding from the University of Michigan Rackham Graduate School. The article was initiated and completed while M.B. was at Eastern Michigan University and K.E.B. was at the White River Junction VA Medical Center and Geisel School of Medicine at Dartmouth. Portions of this work were presented at the 4th Annual Lown Institute Conference, Chicago, IL, April 15-17, 2016; University of Michigan Center for Bioethics and Social Sciences in Medicine Research Colloquium, Ann Arbor, MI, March 17, 2015; Palliative Care in Oncology Symposium, Boston, MA, October 9-10, 2015; Michigan State University Center for Ethics & Humanities in the Life Sciences Webinar, East Lansing, MI, October 28, 2015; National Hospice and Palliative Care Organization 14th Clinical Team Conference, Kansas City, MO, September 26-28, 2013; and online only in the ASCO Annual Meeting Abstracts, June 2015. We appreciate the helpful reviews of Reshma Jagsi, MD, DPhil; Beverly Moy, MD; and Susan Dorr Goold, MD. We also thank the oncologists and oncology fellows who participated in this study.
| 1. | Jagsi R, Sulmasy DP, Moy B: Value of cancer care: Ethical considerations for the practicing oncologist. Am Soc Clin Oncol Ed Book e146-e149, 2014 Google Scholar |
| 2. | Garrido MM, Prigerson HG, Bao Y, et al: Chemotherapy use in the months before death and estimated costs of care in the last week of life. J Pain Symptom Manage 51:875-881.e2, 2016 Crossref, Medline, Google Scholar |
| 3. | Lakdawalla D, Shafrin J, Lucarelli C, et al: Quality-adjusted cost of care: A meaningful way to measure growth in innovation cost versus the value of health gains. Health Aff (Millwood) 34:555-561, 2015 Crossref, Medline, Google Scholar |
| 4. | Fojo T, Mailankody S, Lo A: Unintended consequences of expensive cancer therapeutics—the pursuit of marginal indications and a me-too mentality that stifles innovation and creativity: The John Conley Lecture. JAMA Otolaryngol Head Neck Surg 140:1225-1236, 2014 Crossref, Medline, Google Scholar |
| 5. | Sorenson C: Valuing end-of-life care in the United States: The case of new cancer drugs. Health Econ Policy Law 7:411-430, 2012 Crossref, Medline, Google Scholar |
| 6. | National Cancer Institute: Side effects. http://www.cancer.gov/about-cancer/treatment/side-effects Google Scholar |
| 7. | Hassett MJ, O’Malley AJ, Pakes JR, et al: Frequency and cost of chemotherapy-related serious adverse effects in a population sample of women with breast cancer. J Natl Cancer Inst 98:1108-1117, 2006 Crossref, Medline, Google Scholar |
| 8. | Cardinale D, Biasillo G, Cipolla CM: Curing cancer, saving the heart: A challenge that cardioncology should not miss. Curr Cardiol Rep 18:51, 2016 Crossref, Medline, Google Scholar |
| 9. | Wright AA, Zhang B, Keating NL, et al: Associations between palliative chemotherapy and adult cancer patients’ end of life care and place of death: Prospective cohort study. BMJ 348:g1219, 2014 Google Scholar |
| 10. | Prigerson HG, Bao Y, Shah MA, et al: Chemotherapy use, performance status, and quality of life at the end of life. JAMA Oncol 1:778-784, 2015 Google Scholar |
| 11. | Earle CC, Park ER, Lai B, et al: Identifying potential indicators of the quality of end-of-life cancer care from administrative data. J Clin Oncol 21:1133-1138, 2003 Link, Google Scholar |
| 12. | Earle CC, Neville BA, Landrum MB, et al: Trends in the aggressiveness of cancer care near the end of life. J Clin Oncol 22:315-321, 2004 Link, Google Scholar |
| 13. | Harrington SE, Smith TJ: The role of chemotherapy at the end of life: “When is enough, enough?”. JAMA 299:2667-2678, 2008 Crossref, Medline, Google Scholar |
| 14. | Fojo T, Grady C: How much is life worth: Cetuximab, non-small cell lung cancer, and the $440 billion question. J Natl Cancer Inst 101:1044-1048, 2009 Crossref, Medline, Google Scholar |
| 15. | Zarrabi AJ, Huo R, Meier DE: High-value palliative care for cancer patients. AMA J Ethics 17:1064-1072, 2015 Google Scholar |
| 16. | Sanft TB, Von Roenn JH: Palliative care across the continuum of cancer care. J Natl Compr Canc Netw 7:481-487, 2009 Crossref, Medline, Google Scholar |
| 17. | Schnipper LE, Smith TJ, Raghavan D, et al: American Society of Clinical Oncology identifies five key opportunities to improve care and reduce costs: The top five list for oncology. J Clin Oncol 30:1715-1724, 2012 Link, Google Scholar |
| 18. | Smith TJ, Temin S, Alesi ER, et al: American Society of Clinical Oncology provisional clinical opinion: The integration of palliative care into standard oncology care. J Clin Oncol 30:880-887, 2012 Link, Google Scholar |
| 19. | Ferris FD, Bruera E, Cherny N, et al: Palliative cancer care a decade later: Accomplishments, the need, next steps—from the American Society of Clinical Oncology. J Clin Oncol 27:3052-3058, 2009 Google Scholar |
| 20. | Hui D, Kim S-H, Kwon JH, et al: Access to palliative care among patients treated at a comprehensive cancer center. Oncologist 17:1574-1580, 2012 Crossref, Medline, Google Scholar |
| 21. | Mintzer DM, Zagrabbe K: On how increasing numbers of newer cancer therapies further delay referral to hospice: The increasing palliative care imperative. Am J Hosp Palliat Care 24:126-130, 2007 Crossref, Medline, Google Scholar |
| 22. | Bluhm M, Connell CM, Janz N, et al: Oncologists’ end of life treatment decisions: How much does patient age matter? J Appl Gerontol 10.1177/0733464815595510 [epub ahead of print on July 21, 2015] Google Scholar |
| 23. | Sandelowski M: Whatever happened to qualitative description. Res Nurs Health 23:334-340, 2000 Crossref, Medline, Google Scholar |
| 24. | Sandelowski M: What’s in a name? Qualitative description revisited. Res Nurs Health 33:77-84, 2010 Crossref, Medline, Google Scholar |
| 25. | Hsieh HF, Shannon SE: Three approaches to qualitative content analysis. Qual Health Res 15:1277-1288, 2005 Crossref, Medline, Google Scholar |
| 26. | Miles MB, Huberman AM, Saldana J. Qualitative Data Analysis: A Methods Sourcebook (ed 3) Thousand Oaks, CA, Sage, 2013 Google Scholar |
| 27. | Braun V, Clarke V: Using thematic analysis in psychology. Qual Res Psych 3, 2006 Google Scholar |
| 28. | Sandelowski M: Sample size in qualitative research. Res Nurs Health 18:179-183, 1995 Crossref, Medline, Google Scholar |
| 29. | Clarke G, Johnston S, Corrie P, et al: Withdrawal of anticancer therapy in advanced disease: A systematic literature review. BMC Cancer 15:892, 2015 Crossref, Medline, Google Scholar |
| 30. | Schildmann J, Tan J, Salloch S, et al: “Well, I think there is great variation...”: A qualitative study of oncologists’ experiences and views regarding medical criteria and other factors relevant to treatment decisions in advanced cancer. Oncologist 18:90-96, 2013 Crossref, Medline, Google Scholar |
| 31. | Buiting HM, Rurup ML, Wijsbek H, et al: Understanding provision of chemotherapy to patients with end stage cancer: Qualitative interview study. BMJ Support Palliat Care 1:33-41, 2011 Crossref, Medline, Google Scholar |
| 32. | McCullough L, McKinlay E, Barthow C, et al: A model of treatment decision making when patients have advanced cancer: How do cancer treatment doctors and nurses contribute to the process. Eur J Cancer Care (Engl) 19:482-491, 2010 Crossref, Medline, Google Scholar |
| 33. | Granek L, Krzyzanowska MK, Tozer R, et al: Oncologists’ strategies and barriers to effective communication about the end of life. J Oncol Pract 9:e129-e135, 2013 Link, Google Scholar |
| 34. | Behl D, Jatoi A: What do oncologists say about chemotherapy at the very end of life? Results from a semiqualitative survey. J Palliat Med 13:831-835, 2010 Crossref, Medline, Google Scholar |
| 35. | Ng T, Chew L, Yap CW: A clinical decision support tool to predict survival in cancer patients beyond 120 days after palliative chemotherapy. J Palliat Med 15:863-869, 2012 Crossref, Medline, Google Scholar |
| 36. | Smith TJ, Dow LA, Virago EA, et al: A pilot trial of decision aids to give truthful prognostic and treatment information to chemotherapy patients with advanced cancer. J Support Oncol 9:79-86, 2011 Crossref, Medline, Google Scholar |
| 37. | Bernacki RE, Block SD: American College of Physicians High Value Care Task Force: Communication about serious illness care goals: A review and synthesis of best practices. JAMA Intern Med 10.1001/jamainternmed.2014.5271 Google Scholar |
| 38. | Back AL, Arnold RM, Baile WF, et al: Efficacy of communication skills training for giving bad news and discussing transitions to palliative care. Arch Intern Med 167:453-460, 2007 Crossref, Medline, Google Scholar |
| 39. | Jang RW, Caraiscos VB, Swami N, et al: Simple prognostic model for patients with advanced cancer based on performance status. J Oncol Pract 10:e335-341 Google Scholar |
| 40. | Malin JL, Weeks JC, Potosky AL, et al: Medical oncologists’ perceptions of financial incentives in cancer care. J Clin Oncol 31:530-535, 2013 Link, Google Scholar |
| 41. | Smith TJ, Hillner BE: Concrete options and ideas for increasing value in oncology care: The view from one trench. Oncologist 15:65-72, 2010 (suppl 1) Google Scholar |
| 42. | Wong YN: Are oncologists’ financial incentives aligned with quality care. J Clin Oncol 31:517-519, 2013 Link, Google Scholar |
| 43. | Wallace JE, Lemaire JB, Ghali WA: Physician wellness: A missing quality indicator. Lancet 374:1714-1721, 2009 Crossref, Medline, Google Scholar |
| 44. | Shayne M, Quill TE: Oncologists responding to grief. Arch Intern Med 172:966-967, 2012 Crossref, Medline, Google Scholar |
| 45. | Jackson VA, Mack J, Matsuyama R, et al: A qualitative study of oncologists’ approaches to end-of-life care. J Palliat Med 11:893-906, 2008 Crossref, Medline, Google Scholar |
| 46. | Granek L, Krzyzanowska MK, Tozer R, et al: Difficult patient loss and physician culture for oncologists grieving patient loss. J Palliat Med 15:1254-1260, 2012 Crossref, Medline, Google Scholar |
| 47. | Shanafelt TD: Finding meaning, balance, and personal satisfaction in the practice of oncology. J Support Oncol 3:157-162, 164, 2005 Google Scholar |
| 48. | Sanchez-Reilly S, Morrison LJ, Carey E, et al: Caring for oneself to care for others: Physicians and their self-care. J Support Oncol 11:75-81, 2013 Crossref, Medline, Google Scholar |
| 49. | Kirkwood MK, Bruinooge SS, Goldstein MA, et al: Enhancing the American Society of Clinical Oncology workforce information system with geographic distribution of oncologists and comparison of data sources for the number of practicing oncologists. J Oncol Pract 10:32-38, 2014 Link, Google Scholar |
| 50. | Deville C, Chapman CH, Burgos R, et al: Diversity by race, Hispanic ethnicity, and sex of the United States medical oncology physician workforce over the past quarter century. J Oncol Pract 10:e328-e334, 2014 Link, Google Scholar |



