ORIGINAL ARTICLE
Academic and Resident Radiation Oncologists’ Attitudes and Intentions Regarding Radiation Therapy near the End of Life Shane Lloyd, MD, Arie P. Dosoretz, MD, MBA, James B. Yu, MD, Suzanne B. Evans, MD, MPH, and Roy H. Decker, MD, PhD
Objectives: There has been increasing scrutiny about cancer treatment for patients very near the end of life (EoL), yet a substantial number receive palliative radiation therapy (RT) in this setting. Our aim was to document the attitudes and intentions of thought leaders and trainees in giving RT near the EoL. Methods: We distributed an anonymous survey to 473 radiation oncologists and residents. The survey examined the clinical and psychosocial factors considered as well as intentions and expectations in the delivery of RT near the EoL. Factors surrounding unfinished treatment courses, and the formative factors that shape opinions about RT at the EoL were also explored. Results: We received 139 responses (29%). Eighty-nine percent of respondents worked at academic institutions. The factors that respondents most often consider very or extremely important to offer RT near the EoL were the preference of the patient to be treated (94%), the ability to tolerate treatment (88%), and palliative intent (70%). After instances when their patients were unable to complete treatment near the EoL, 42% of respondents said they would prescribe a shorter treatment the next time they see a similar patient. Personal experience (71%) was most often listed as very or extremely important in shaping their opinions about RT near the EoL. Conclusions: Survey respondents, 89% of whom were academic radiation oncologists, have a positive view of palliative RT near the EoL. They favor shorter fractionation for patients near the EoL. Personal experience is most important in shaping practices and attitudes. Key Words: palliation, radiation therapy, end of life, survey
(Am J Clin Oncol 2016;39:85–89)
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adiation therapy (RT) is effective in the palliation of advanced cancer including bony metastatic pain, brain metastases, and spinal cord compression. However, daily treatment can be burdensome for patients very near the end of life (EoL),1 and a substantial number of patients spend a portion of their last days getting treatment.2 Radiation oncologists are responsible for weighing the expected benefits and risks of treatment, counseling patients about these issues, and designing a regimen best suited to the goals of care.3 Even in cases of palliative intent, there are complex and important From the Department of Therapeutic Radiology, Yale University School of Medicine, New Haven, CT. The authors declare no conflicts of interest. Reprints: Roy H. Decker, MD, PhD, Department of Therapeutic Radiology, Yale University School of Medicine, 33 Cedar Street, P.O. Box 208040, New Haven, CT 06520-8040. E-mail: [email protected]. Supplemental Digital Content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal’s Website, www. amjclinicaloncology.com. Copyright r 2014 Wolters Kluwer Health, Inc. All rights reserved. ISSN: 0277-3732/16/3901-0085 DOI: 10.1097/COC.0000000000000026
American Journal of Clinical Oncology
decisions to be made regarding the utility of radiation near death. Physicians have been shown to perform poorly at predicting survival in terminally ill cancer patients,4 and radiation oncologists’ estimates of survival are unreliable particularly for patients near death.5 Furthermore, when radiation oncologists overestimate survival time, they tend to give longer treatment regimens.6 There are little data to help radiation oncologists predict whether patients near the EoL will live long enough to derive benefit from treatment or whether the side effects of treatment will cause an overall negative impact on health-related quality of life. Although clinical practice guidelines can aide physicians in providing palliative care,7–9 no standard philosophy has been adapted, nor have formal decision aids been developed for use in making these particular EoL determinations. Because of the inherent difficulty of accurately characterizing the opinions of the radiation oncology profession as a whole, our primary goal was to summarize the decision-making considerations of thought leaders and trainees in radiation oncology about RT near the EoL. Understanding their experiences and expectations is an important step in improving the care of dying patients.
METHODS We developed a survey to enable respondents to provide anonymous answers to questions and to provide free-response comments about RT near the EoL (Supplemental material, Supplemental Digital Content 1, http://links.lww.com/AJCO/ A31). The questions were trialed on a focus group of 6 radiation oncologists for clarity. We divided the questions into 4 categories: (1) clinical and psychosocial factors considered when recommending RT near the EoL; (2) intentions and expectations in giving RT in the last 30 days of life; (3) attitudes about unfinished treatment courses near the EoL; and (4) formative factors that have shaped radiation oncologists’ opinions about RT near the EoL. We distributed the survey electronically in the winter of 2013 to 473 radiation oncologists and residents, including 335 thought leaders. The group of thought leaders is comprised of presenters at the 52nd Annual Meeting of the American Society of Radiation Oncology (ASTRO), chairpersons and residency program directors of United States academic radiation oncology departments, and ASTRO gold medal winners. An additional group of resident and attending physicians was drawn from 8 academic training programs (The Cleveland Clinic, Harvard, MD Anderson, Memorial Sloan Kettering, New York Methodist, Oregon Health Sciences, Robert Wood Johnson, Stanford, The University of Utah, and Yale). Reminder emails were sent approximately 1 and 2 weeks after the initial invitation. We collected demographic information including respondents’ sex, number of years in practice, and primary practice setting (academic, hospital-based private practice, and
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Sex (n = 133) Male Female Years since completion of residency (n = 135) Resident 0-10 11-20 21-30 30 + Practice setting (n = 131) Academic Hospital-based private practice Free-standing center private practice No. patients respondents treated over the last year who died within 30 d of receiving RT (n = 114) 0 1-3 4-9 10-14 15 + No. patients started on treatment last year (n = 85)
Total (%) 95 (71) 38 (29) 42 30 28 20 15
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and Brittish Columbia), and 3 European Countries (Denmark, Italy, and the United Kingdom). All of the respondents had experience in treating patients near the EoL. The median range of patients that respondents treated in the last year who died within 30 days of receiving RT was 4 to 9. Only 10 (9%) of respondents treated Z10 patients in the last year who died within 30 days of receiving RT. The factors that respondents most commonly consider very or extremely important to offer RT near the EoL were “preference of the patient to be treated after discussion of the options, risks, and benefits” 115/122 (94%), “ability of the patient to tolerate treatment” 107/122 (88%), and that “treatment [be] with palliative intent” 85/122 (70%) (Table 2). The factors that respondents least commonly consider very or extremely important were that the tumor be a “radiosensitive cancer type” 28/121 (13%), “preference of the referring physician to offer RT” 20/121 (17%), and “discussion of hospice care before initiating RT” 30/122 (32%). Seventy-four percent of respondents at least somewhat disagreed with the statement that palliative radiation in the last 30 days of life should be avoided. Free-response comments about this question mentioned using short courses and large fraction sizes in the EoL setting. Many comments endorsed the use of RT in cases where RT may offer better quality of life by reducing the need for large doses of sedating narcotic medications. Only 11/112 (10%) had at least a somewhat negative feeling about palliative RT near the EoL, yet 101/111 (91%) had at least a somewhat negative feeling about definitive radiation in the last 30 days of life. Respondents indicated that, over the last year, 27% (SD = 21%) of patients they treated in the last 30 days of life died sooner than they expected. To determine radiation oncologists’ understanding of the tradeoff between time on treatment and length of benefit, we asked them to estimate the length of effective palliation before death necessary to justify 1 or 10 days of treatment. If respondents were able to know exactly when a terminal patient would die, an average of 3.9 weeks (SD = 2.8) of effective palliation before death would be needed to recommend a 1-day course of palliative RT, and an average of 9.0 weeks (SD = 3.5) would be needed to recommend a 10-day course of palliative RT (comparison between 1 and 10-d course, P < 0.01). In cases when patients were treated within the last 30 days of life and were not able to complete the planned course of treatment, the most common reason was that the patient
TABLE 1. Survey Respondent Characteristics
Self-reported Demographics
(31) (22) (21) (15) (11)
117 (89) 9 (7) 5 (4) 0 42 (37) 62 (54) 8 (7) 2 (2) 161 (SD = 64)
free-standing private practice). We compared the answers of attending radiation oncologists with those of residents using the 2-sample t test and w2 analysis to determine whether attitudes and opinions differ by training level. We anticipated a response rate consistent with similar studies in the literature of around 25%.10,11 The order of question response choices was randomized. Survey data were collected and analyzed using Qualtrics Online Survey Software (Qualtrics, Provo, UT). Statistical analyses were conducted using Stata 12.0 (StataCorp, College Station, TX). This study was approved by an institutional review board.
RESULTS We received responses from 139 of the 473 (29%) radiation oncologists surveyed (Table 1). Seventy-three of the 335 (22%) radiation oncologists from the “thought leaders” group completed the survey. The remaining 66 responses came from the 138 (49%) additional resident and attending physicians surveyed. The geographic distribution of those who responded to the survey included 22 states, 2 Canadian provinces (Ontario
TABLE 2. The Importance of Survey Items in Influencing Radiation Oncologists to Treat Patients near the End of Life
1. Not Important Ability of the patient to tolerate treatment (n = 122) Discussion of hospice care before initiating RT (n = 122) Good performance status (n = 120) Other treatment options have been thoroughly considered (n = 120) Preference of the referring physician to offer RT (n = 121) Preference of the patient’s family for treatment after discussion of the options, risks, and benefits (n = 122) Preference of the patient to be treated after discussion of the options, risks, and benefits (n = 122) Radiosensitive cancer type (n = 121) Treatment is with palliative intent (not for cure) (n = 122)
0 9 4 1 12 0
(0) (7) (3) (1) (10) (0)
2. Somewhat Important 2 34 28 10 51 24
(2) (28) (23) (8) (42) (20)
3. 4. Very Important Important 13 39 38 31 38 32
(11) (32) (32) (26) (31) (26)
0 (0)
1 (1)
6 (5)
18 (15) 7 (6)
39 (32) 1 (1)
36 (30) 29 (24)
43 25 28 53 14 42
(35) (20) (23) (44) (12) (34)
37 (30)
5. Extremely Important 64 15 22 25 6 24
(52) (12) (18) (21) (5) (20)
78 (64)
21 (17) 7 (6) 39 (32) 46 (38) w2: P < 0.01
RT indicates radiation therapy.
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Radiation Therapy near the End of Life
TABLE 3. Attitudes About Instances of Unfinished Treatment Courses
If You Saw a Similar Patient in the Future, What Would You Do? Thinking of the Most Recent Time You Treated a Patient in the Last 30 d of Life Who was NOT Able to Complete the Planned Course of Treatment, What was the Reason? Total
The Same Thing
Encourage Other Options or Consult With More Doctors
Prescribe a Shorter Course
Not Offer Radiation Therapy
The patient The patient measures The patient Other Total
7 70
1 (14) 21 (30)
1 (14) 12 (17)
5 (71) 32 (46)
0 (0) 5 (7)
25 8 110
16 (64) 4 (50) 42 (38)
0 (0) 0 (0) 13 (12)
7 (28) 2 (8) 2 (25) 2 (25) 46 (42) 9 (8) w2: P = 0.02
didn’t tolerate treatment decided to pursue hospice care or comfort only died
For What Reason(s) Would You do the Same Thing? Mark all That Apply (n = 42) Because I acted on the best information available at the time Because the patient derived some benefit, even if they didn’t receive the originally prescribed dose Because it is worth giving radiation a chance to palliate symptoms Other
27 (69) 8 (21)
decided to pursue hospice care or comfort measures only (70/ 110, 64%) (Table 3). In 25 of 110 (23%) cases the patient’s death was the reason that treatment could not be completed. Forty-two percent of radiation oncologists would prescribe a shorter course if they saw a similar patient in the future, whereas 38% would do the same thing. The most common reasons for advocating for the same treatment for a similar patient in the future were that the radiation oncologist “acted on the best available information at the time” (69%) and that it is “worth giving the treatment a chance to palliate symptoms” (62%). The formative factors that respondents listed most commonly as very or extremely important in shaping their opinions about RT near the EoL were their “own clinical experience/ patients [they] have treated” in 77/108 (71%), “personal values and beliefs” in 44/107 (41%), and “instruction from mentors during training” in 43/107 (40%) (Table 4). The formative factors that respondents listed least commonly as very or extremely important in shaping their opinions about RT near the EoL were the “influence of referring physicians” in 19/107 (18%), “clinical guidelines” in 23/100 (23%), and “published literature” in 32/105 (31%). The clinical practice guidelines
respondents listed as influential in shaping their opinions about RT near the EoL included several ASTRO guidelines,7–9 the National Comprehensive Cancer Center Network clinical practice guidelines, and institutional unpublished data. Some respondents provided other influences in the free-answer section including, “patient and family values,” “the palliative care team,” “peer case discussions,” and fear that the “patients [will be] denied treatment [later] on hospice for seemingly financial reasons only.” Resident and attending responses differed on only 3 questions, all of them concerning formative factors shaping their practice and attitudes about RT near the EoL. Residents were more likely than attendings to list the influence of mentors (63% vs. 31%, P < 0.01), and peers (48% vs. 27%, P = 0.03) as very or extremely important. They were less likely than attendings to list their “own clinical experience/patients [they] have treated” as very or extremely important (55% vs. 79%, P = 0.01). The answers of residents and attendings did not differ significantly for the rest of the questions on the survey. There were no statistical differences between the responses of those in the “thought leader” group and the other respondents.
24 (62) 3 (7)
TABLE 4. Factors Shaping Practices and Attitudes about Radiation Therapy near the End of Life
Formal informational sources Clinical guidelines (n = 100) Instruction from mentors during training (n = 107) Published literature (n = 105)
1. Not Important
2. Somewhat Important
3. Important
4. Very Important
5. Extremely Important
16 (16) 7 (7)
28 (28) 21 (20)
33 (33) 36 (34)
21 (21) 27 (25)
2 (2) 16 (15)
8 (8)
26 (25)
39 (37)
27 (26)
5 (5) w2: P < 0.01
Subjective influences Influence of my radiation oncology peers (n = 106) Influence of referring physicians (n = 107) My own clinical experience/patients I’ve treated (n = 108) Personal values and beliefs (n = 107)
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7 (7)
26 (25)
37 (35)
33 (31)
3 (3)
11 (10) 0 (0)
43 (40) 5 (5)
34 (32) 26 (24)
15 (14) 50 (46)
4 (4) 27 (25)
6 (6)
15 (14)
42 (39)
27 (25)
17 (16) w2: P < 0.01
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DISCUSSION Surveyed radiation oncology thought leaders and trainees at academic centers have a positive view of palliative RT near the EoL and feel that many patients may benefit from properly designed treatment regimens. They indicated that they consider patients’ wishes, but it should be noted that the survey was not designed to accurately distinguish “patients’ wishes” from “patients’ consent” for treatment after discussion with a radiation oncologist. They also consider patients’ ability to tolerate treatment and short courses are favored when prognosis is limited. For some radiation oncologists, experiences of patients not being able to complete treatment have made them more likely to prescribe shorter treatment courses in the future. Practicing radiation oncologists are more likely to list personal experience as important in shaping their opinions about RT at the EoL, whereas residents are more likely to list the influence of mentors and peers. Cancer treatment at the EoL is increasing overall.12 Chemotherapy is given in the last month of life at rates of 20% to 24%12,13 and higher for patients who die in the hospital.14 Although some studies have indicated substantial use of RT at the EoL,2,15 those studies cannot distinguish between palliative and definitive RT. Our survey responses partially address this knowledge gap by confirming an endorsement of palliative and not definitive RT among radiation oncologists. Their belief in the usefulness of palliative RT is supported by data that demonstrates improved quality of life in advanced cancer,10,16 even in patients very near the EoL.17,18
Complexities in EoL Care Responses to this survey illustrate a number of complexities faced by radiation oncologists treating patients near the EoL. These include the time to pain relief in patients with limited time remaining, the uncertainty in predicting prognosis, and the problem of unfinished treatment courses. Although there is great variation among individual patients, the median time to pain relief may be 3 to 4 weeks for both single-fraction and multiple-fraction treatments.19,20 This means that palliative RT does benefit many of those patients with limited, but imprecise prognoses of weeks to months. However, to have maximal effect, palliative consults should not be delayed. Survey respondents reported overestimating prognosis 24% of the time and multiple previous studies demonstrate the difficulty of accurate prognosis.4–6 Although prediction scores for survival near the EoL have been validated,21,22 more research is needed to help radiation oncologists make determinations of life expectancy. In addition, in light of evidence that radiation oncologists may overestimate the prognosis of dying cancer patients,23 conversations about goals of care must occur even before the physician perceives the patient to be at or near the EoL.24,25 It is difficult to predict which patients will be unable to complete a prescribed course of treatment. In thinking of past situations of unfinished treatment, many respondents see the benefits of shorter palliative regimens. However, some radiation oncologists may prefer to offer the treatment they deem most likely to provide palliation and accept the fact that some patients will die or discontinue treatment. Many respondents endorsed shorter or single-fraction treatments that can reduce the number of patient visits, especially when simulation and treatment can be expedited and performed on the same day.26,27
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Formative Factors that Shape Providers’ Opinions About RT near the EoL EoL decisions can be very personal. Although some clinical practice guidelines were cited, only 23% of radiation oncologists felt that guidelines are very or extremely important in shaping their opinions about RT near the EoL. The formative importance of personal experience seen in the survey results may speak to the importance of nuance and flexibility in helping patients make EoL decisions. Nevertheless, there may be a void that could be filled by guidelines and texts that recognize the shifting goals and values of patients as they near death.28 Radiation oncologists early in their careers may benefit from more instruction and guidance in approaching EoL issues. This may be accomplished when mentors approach palliative care as any other subspecialty in radiation oncology. Residents in the survey were more likely to list the influence of both mentors and peers as being influential in shaping their views of RT near the EoL. Past clinical experience was understandably less important for this group. Resident responses did not differ significantly from attendings in other areas of the survey indicating some degree of unity in attitudes, intentions, and expectations across career levels. This study has important limitations. Twenty-nine percent of radiation oncologists surveyed responded, 89% of whom were academic physicians. Therefore, our results may not be generalizable to all radiation oncologists, and the low proportion of community radiation oncologists precludes meaningful comparison of academic and community practices and opinions in this study. Nevertheless, this response rate is comparable with other studies of patterns of care and physician attitudes,10,11 and respondents were from a wide and varied geographic distribution. Also, although there was minimal variation in the number of dying patients that respondents treated over the last year, survey responses may be different depending on the number or percentage of palliative patients radiation oncologists treat, and this was not ascertained. Likewise, the results may be subject to nonresponse bias, in which those interested in the subject of the survey are more likely to respond. Our survey results may also be subject to social desirability bias in which subjects may misrepresent their actions or attitudes in favor of what they think is desirable to the group. In this way, radiation oncologists’ reported attitudes may favor less treatment in thinking about theoretical patients who are “near the EoL” compared with the real, living patients they see in practice. The Likert scales we used in the survey are subject to acquiescence bias in which the subject agrees to the statement as presented. Responses may have also been subject to central tendency bias, in which extreme answers are avoided. Finally, the role of RT near the EoL is a complex issue, and the decision to offer treatment is based on societal values and patients’ interactions with a very complex medical system, which are difficult to capture in a single survey.
CONCLUSIONS Academic radiation oncology thought leaders and trainees have a positive view of palliative radiation near the EoL and believe palliative effect can often be achieved with short treatment regimens, especially in cases of very limited prognosis. Personal experience has shaped their opinions more than current clinical guidelines or literature, potentially pointing to the personal nature of EoL decisions and the importance of the art of medicine in radiation oncology. Complexities regarding
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RT near the EoL include the difficulty of accurately assessing prognosis and identifying patients who may not be able to complete treatment. More instruction and guidance may be warranted for radiation oncologists early in their careers who look to the influence of mentors in forming their attitudes about treatment near the EoL. REFERENCES 1. Brogaard T, Neergaard MA, Sokolowski I, et al. Congruence between preferred and actual place of care and death among Danish cancer patients. Palliat Med. 2013;27:155–164. 2. Guadagnolo BA, Liao K, Elting L, et al. Use of radiation therapy in the last 30 days of life among a large population-based cohort of elderly patients in the United States. J Clin Oncol. 2013;31:80–87. 3. Earle CC, Neville BA, Souza JM, et al. Aggressiveness of cancer care near the end of life: is it a quality-of-care issue? J Clin Oncol. 2008;26:3860–3866. 4. Glare P, Virik K, Jones M, et al. A systematic review of physicians’ survival predictions in terminally ill cancer patients. BMJ. 2003;327:195–200. 5. Gripp S, Moeller S, Bolke E, et al. Survival prediction in terminally ill cancer patients by clinical estimates, laboratory tests, and self-rated anxiety and depression. J Clin Oncol. 2007;25: 3313–3320. 6. Maher EJ, Coia L, Duncan G, et al. Treatment strategies in advanced and metastatic cancer: differences in attitude between the USA, Canada and Europe. Int J Radiat Oncol Biol Phys. 1992;23:239–244. 7. Lutz ST, Berk LB, Chang EL, et al. Palliative radiotherapy for bone metastases: an ASTRO evidence-based guideline. Int J Radiat Oncol Biol Phys. 2011;79:965–976. 8. Rodrigues G, Videtic GMM, Sur R, et al. Palliative thoracic radiotherapy in lung cancer: an American Society for Radiation Oncology evidence-based clinical practice guideline. Pract Radiat Oncol. 2011;1:60–71. 9. Tsao MN, Rades D, Wirth A, et al. Radiotherapeutic and surgical management for newly diagnosed brain metastasis(es): an American Society for Radiation Oncology evidence-based guideline. Pract Radiat Oncol. 2012;2:210–225. 10. Cleeland CS, Janjan NA, Scott CB, et al. Cancer pain management by radiotherapists: a survey of radiation therapy oncology group physicians. Int J Radiat Oncol Biol Phys. 2000;47:203–208. 11. Behl D, Jatoi A. What do oncologists say about chemotherapy at the very end of life? Results from a semiqualitative survey. J Palliat Med. 2010;13:831–835. 12. Earle CC, Neville BA, Landrum MB, et al. Trends in the aggressiveness of cancer care near the end of life. J Clin Oncol. 2004;22:315–321.
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13. Frigeri M, De Dosso S, Castillo-Fernandez O, et al. Chemotherapy in patients with advanced pancreatic cancer: too close to death? Support Care Cancer. 2013;21:157–163. 14. Sanz Ortiz J. Chemotherapy at the end of life: up until when? Clin Transl Oncol. 2012;14:667–674. 15. Kapadia NS, Mamet R, Zornosa C, et al. Radiation therapy at the end of life in patients with incurable nonsmall cell lung cancer. Cancer. 2012;118:4339–4345. 16. Lorenz KA, Lynn J, Dy SM, et al. Evidence for improving palliative care at the end of life: a systematic review. Ann Intern Med. 2008;148:147–159. 17. Dennis K, Wong K, Zhang L, et al. Palliative radiotherapy for bone metastases in the last 3 months of life: worthwhile or futile? Clin Oncol. 2001;23:709–715. 18. Meeuse JJ, van der Linden YM, van Tienhoven G, et al. Dutch Bone Metastasis Study Group. Efficacy of radiotherapy for painful bone metastases during the last 12 weeks of life: results from the Dutch Bone Metastasis Study. Cancer. 2010;116:2716–2725. 19. Steenland E, Leer JW, van Houwelingen H, et al. The effect of a single fraction compared to multiple fractions on painful bone metastases: a global analysis of the Dutch Bone Metastasis Study. Radiother Oncol. 1999;52:101–109. 20. Wu JS, Wong R, Johnston M, et al. Meta-analysis of dosefractionation radiotherapy trials for the palliation of painful bone metastases. Int J Radiat Oncol Biol Phys. 2003;55:594–605. 21. Chow E, Abdolell M, Panzarella T, et al. Validation of a predictive model for survival in metastatic cancer patients attending an outpatient palliative radiotherapy clinic. Int J Radiat Oncol Biol Phys. 2009;73:280–287. 22. Wilner SL, Arnold R. The Palliative Performance Scale (PPS). End of Life/Palliative Education Resource Center; 2012. Available at: http:// www.eperc.mcw.edu/EPERC/FastFactsIndex/ff_125.htm. Accessed October 11, 2013. 23. Gripp S, Mjartan S, Boelke E, et al. Palliative radiotherapy tailored to life expectancy in end-stage cancer patients: reality or myth? Cancer. 2010;116:3251–3256. 24. Lynn J, Harrell F Jr, Cohn F, et al. Prognoses of seriously ill hospitalized patients on the days before death: implications for patient care and public policy. New Horiz. 1997;5:56–61. 25. Mack JW, Cronin A, Keating NL, et al. Associations between endof-life discussion characteristics and care received near death: a prospective cohort study. J Clin Oncol. 2012;30:4387–4395. 26. Samant R, Gerig L, Montgomery L, et al. Rapid palliative radiotherapy: comparing IG-IMRT with more conventional approaches. J Radiother Pract. 2010;9:143–148. 27. MacPherson M, Montgomery L, Fox G, et al. On-line rapid palliation using helical tomotherapy: a prospective feasibility study. Radiother Oncol. 2008;87:116–118. 28. Rabow MW, Hardie GE, Fair JM, et al. End-of-life care content in 50 textbooks from multiple specialties. JAMA. 2000;283:771–778.
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Academic and Resident Radiation Oncologists’ Attitudes and Intentions Regarding Radiation Therapy near the End of Life Shane Lloyd, MD, Arie P. Dosoretz, MD, MBA, James B. Yu, MD, Suzanne B. Evans, MD, MPH, and Roy H. Decker, MD, PhD
Objectives: There has been increasing scrutiny about cancer treatment for patients very near the end of life (EoL), yet a substantial number receive palliative radiation therapy (RT) in this setting. Our aim was to document the attitudes and intentions of thought leaders and trainees in giving RT near the EoL. Methods: We distributed an anonymous survey to 473 radiation oncologists and residents. The survey examined the clinical and psychosocial factors considered as well as intentions and expectations in the delivery of RT near the EoL. Factors surrounding unfinished treatment courses, and the formative factors that shape opinions about RT at the EoL were also explored. Results: We received 139 responses (29%). Eighty-nine percent of respondents worked at academic institutions. The factors that respondents most often consider very or extremely important to offer RT near the EoL were the preference of the patient to be treated (94%), the ability to tolerate treatment (88%), and palliative intent (70%). After instances when their patients were unable to complete treatment near the EoL, 42% of respondents said they would prescribe a shorter treatment the next time they see a similar patient. Personal experience (71%) was most often listed as very or extremely important in shaping their opinions about RT near the EoL. Conclusions: Survey respondents, 89% of whom were academic radiation oncologists, have a positive view of palliative RT near the EoL. They favor shorter fractionation for patients near the EoL. Personal experience is most important in shaping practices and attitudes. Key Words: palliation, radiation therapy, end of life, survey
(Am J Clin Oncol 2016;39:85–89)
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adiation therapy (RT) is effective in the palliation of advanced cancer including bony metastatic pain, brain metastases, and spinal cord compression. However, daily treatment can be burdensome for patients very near the end of life (EoL),1 and a substantial number of patients spend a portion of their last days getting treatment.2 Radiation oncologists are responsible for weighing the expected benefits and risks of treatment, counseling patients about these issues, and designing a regimen best suited to the goals of care.3 Even in cases of palliative intent, there are complex and important From the Department of Therapeutic Radiology, Yale University School of Medicine, New Haven, CT. The authors declare no conflicts of interest. Reprints: Roy H. Decker, MD, PhD, Department of Therapeutic Radiology, Yale University School of Medicine, 33 Cedar Street, P.O. Box 208040, New Haven, CT 06520-8040. E-mail: [email protected]. Supplemental Digital Content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal’s Website, www. amjclinicaloncology.com. Copyright r 2014 Wolters Kluwer Health, Inc. All rights reserved. ISSN: 0277-3732/16/3901-0085 DOI: 10.1097/COC.0000000000000026
American Journal of Clinical Oncology
decisions to be made regarding the utility of radiation near death. Physicians have been shown to perform poorly at predicting survival in terminally ill cancer patients,4 and radiation oncologists’ estimates of survival are unreliable particularly for patients near death.5 Furthermore, when radiation oncologists overestimate survival time, they tend to give longer treatment regimens.6 There are little data to help radiation oncologists predict whether patients near the EoL will live long enough to derive benefit from treatment or whether the side effects of treatment will cause an overall negative impact on health-related quality of life. Although clinical practice guidelines can aide physicians in providing palliative care,7–9 no standard philosophy has been adapted, nor have formal decision aids been developed for use in making these particular EoL determinations. Because of the inherent difficulty of accurately characterizing the opinions of the radiation oncology profession as a whole, our primary goal was to summarize the decision-making considerations of thought leaders and trainees in radiation oncology about RT near the EoL. Understanding their experiences and expectations is an important step in improving the care of dying patients.
METHODS We developed a survey to enable respondents to provide anonymous answers to questions and to provide free-response comments about RT near the EoL (Supplemental material, Supplemental Digital Content 1, http://links.lww.com/AJCO/ A31). The questions were trialed on a focus group of 6 radiation oncologists for clarity. We divided the questions into 4 categories: (1) clinical and psychosocial factors considered when recommending RT near the EoL; (2) intentions and expectations in giving RT in the last 30 days of life; (3) attitudes about unfinished treatment courses near the EoL; and (4) formative factors that have shaped radiation oncologists’ opinions about RT near the EoL. We distributed the survey electronically in the winter of 2013 to 473 radiation oncologists and residents, including 335 thought leaders. The group of thought leaders is comprised of presenters at the 52nd Annual Meeting of the American Society of Radiation Oncology (ASTRO), chairpersons and residency program directors of United States academic radiation oncology departments, and ASTRO gold medal winners. An additional group of resident and attending physicians was drawn from 8 academic training programs (The Cleveland Clinic, Harvard, MD Anderson, Memorial Sloan Kettering, New York Methodist, Oregon Health Sciences, Robert Wood Johnson, Stanford, The University of Utah, and Yale). Reminder emails were sent approximately 1 and 2 weeks after the initial invitation. We collected demographic information including respondents’ sex, number of years in practice, and primary practice setting (academic, hospital-based private practice, and
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Sex (n = 133) Male Female Years since completion of residency (n = 135) Resident 0-10 11-20 21-30 30 + Practice setting (n = 131) Academic Hospital-based private practice Free-standing center private practice No. patients respondents treated over the last year who died within 30 d of receiving RT (n = 114) 0 1-3 4-9 10-14 15 + No. patients started on treatment last year (n = 85)
Total (%) 95 (71) 38 (29) 42 30 28 20 15
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and Brittish Columbia), and 3 European Countries (Denmark, Italy, and the United Kingdom). All of the respondents had experience in treating patients near the EoL. The median range of patients that respondents treated in the last year who died within 30 days of receiving RT was 4 to 9. Only 10 (9%) of respondents treated Z10 patients in the last year who died within 30 days of receiving RT. The factors that respondents most commonly consider very or extremely important to offer RT near the EoL were “preference of the patient to be treated after discussion of the options, risks, and benefits” 115/122 (94%), “ability of the patient to tolerate treatment” 107/122 (88%), and that “treatment [be] with palliative intent” 85/122 (70%) (Table 2). The factors that respondents least commonly consider very or extremely important were that the tumor be a “radiosensitive cancer type” 28/121 (13%), “preference of the referring physician to offer RT” 20/121 (17%), and “discussion of hospice care before initiating RT” 30/122 (32%). Seventy-four percent of respondents at least somewhat disagreed with the statement that palliative radiation in the last 30 days of life should be avoided. Free-response comments about this question mentioned using short courses and large fraction sizes in the EoL setting. Many comments endorsed the use of RT in cases where RT may offer better quality of life by reducing the need for large doses of sedating narcotic medications. Only 11/112 (10%) had at least a somewhat negative feeling about palliative RT near the EoL, yet 101/111 (91%) had at least a somewhat negative feeling about definitive radiation in the last 30 days of life. Respondents indicated that, over the last year, 27% (SD = 21%) of patients they treated in the last 30 days of life died sooner than they expected. To determine radiation oncologists’ understanding of the tradeoff between time on treatment and length of benefit, we asked them to estimate the length of effective palliation before death necessary to justify 1 or 10 days of treatment. If respondents were able to know exactly when a terminal patient would die, an average of 3.9 weeks (SD = 2.8) of effective palliation before death would be needed to recommend a 1-day course of palliative RT, and an average of 9.0 weeks (SD = 3.5) would be needed to recommend a 10-day course of palliative RT (comparison between 1 and 10-d course, P < 0.01). In cases when patients were treated within the last 30 days of life and were not able to complete the planned course of treatment, the most common reason was that the patient
TABLE 1. Survey Respondent Characteristics
Self-reported Demographics
(31) (22) (21) (15) (11)
117 (89) 9 (7) 5 (4) 0 42 (37) 62 (54) 8 (7) 2 (2) 161 (SD = 64)
free-standing private practice). We compared the answers of attending radiation oncologists with those of residents using the 2-sample t test and w2 analysis to determine whether attitudes and opinions differ by training level. We anticipated a response rate consistent with similar studies in the literature of around 25%.10,11 The order of question response choices was randomized. Survey data were collected and analyzed using Qualtrics Online Survey Software (Qualtrics, Provo, UT). Statistical analyses were conducted using Stata 12.0 (StataCorp, College Station, TX). This study was approved by an institutional review board.
RESULTS We received responses from 139 of the 473 (29%) radiation oncologists surveyed (Table 1). Seventy-three of the 335 (22%) radiation oncologists from the “thought leaders” group completed the survey. The remaining 66 responses came from the 138 (49%) additional resident and attending physicians surveyed. The geographic distribution of those who responded to the survey included 22 states, 2 Canadian provinces (Ontario
TABLE 2. The Importance of Survey Items in Influencing Radiation Oncologists to Treat Patients near the End of Life
1. Not Important Ability of the patient to tolerate treatment (n = 122) Discussion of hospice care before initiating RT (n = 122) Good performance status (n = 120) Other treatment options have been thoroughly considered (n = 120) Preference of the referring physician to offer RT (n = 121) Preference of the patient’s family for treatment after discussion of the options, risks, and benefits (n = 122) Preference of the patient to be treated after discussion of the options, risks, and benefits (n = 122) Radiosensitive cancer type (n = 121) Treatment is with palliative intent (not for cure) (n = 122)
0 9 4 1 12 0
(0) (7) (3) (1) (10) (0)
2. Somewhat Important 2 34 28 10 51 24
(2) (28) (23) (8) (42) (20)
3. 4. Very Important Important 13 39 38 31 38 32
(11) (32) (32) (26) (31) (26)
0 (0)
1 (1)
6 (5)
18 (15) 7 (6)
39 (32) 1 (1)
36 (30) 29 (24)
43 25 28 53 14 42
(35) (20) (23) (44) (12) (34)
37 (30)
5. Extremely Important 64 15 22 25 6 24
(52) (12) (18) (21) (5) (20)
78 (64)
21 (17) 7 (6) 39 (32) 46 (38) w2: P < 0.01
RT indicates radiation therapy.
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Radiation Therapy near the End of Life
TABLE 3. Attitudes About Instances of Unfinished Treatment Courses
If You Saw a Similar Patient in the Future, What Would You Do? Thinking of the Most Recent Time You Treated a Patient in the Last 30 d of Life Who was NOT Able to Complete the Planned Course of Treatment, What was the Reason? Total
The Same Thing
Encourage Other Options or Consult With More Doctors
Prescribe a Shorter Course
Not Offer Radiation Therapy
The patient The patient measures The patient Other Total
7 70
1 (14) 21 (30)
1 (14) 12 (17)
5 (71) 32 (46)
0 (0) 5 (7)
25 8 110
16 (64) 4 (50) 42 (38)
0 (0) 0 (0) 13 (12)
7 (28) 2 (8) 2 (25) 2 (25) 46 (42) 9 (8) w2: P = 0.02
didn’t tolerate treatment decided to pursue hospice care or comfort only died
For What Reason(s) Would You do the Same Thing? Mark all That Apply (n = 42) Because I acted on the best information available at the time Because the patient derived some benefit, even if they didn’t receive the originally prescribed dose Because it is worth giving radiation a chance to palliate symptoms Other
27 (69) 8 (21)
decided to pursue hospice care or comfort measures only (70/ 110, 64%) (Table 3). In 25 of 110 (23%) cases the patient’s death was the reason that treatment could not be completed. Forty-two percent of radiation oncologists would prescribe a shorter course if they saw a similar patient in the future, whereas 38% would do the same thing. The most common reasons for advocating for the same treatment for a similar patient in the future were that the radiation oncologist “acted on the best available information at the time” (69%) and that it is “worth giving the treatment a chance to palliate symptoms” (62%). The formative factors that respondents listed most commonly as very or extremely important in shaping their opinions about RT near the EoL were their “own clinical experience/ patients [they] have treated” in 77/108 (71%), “personal values and beliefs” in 44/107 (41%), and “instruction from mentors during training” in 43/107 (40%) (Table 4). The formative factors that respondents listed least commonly as very or extremely important in shaping their opinions about RT near the EoL were the “influence of referring physicians” in 19/107 (18%), “clinical guidelines” in 23/100 (23%), and “published literature” in 32/105 (31%). The clinical practice guidelines
respondents listed as influential in shaping their opinions about RT near the EoL included several ASTRO guidelines,7–9 the National Comprehensive Cancer Center Network clinical practice guidelines, and institutional unpublished data. Some respondents provided other influences in the free-answer section including, “patient and family values,” “the palliative care team,” “peer case discussions,” and fear that the “patients [will be] denied treatment [later] on hospice for seemingly financial reasons only.” Resident and attending responses differed on only 3 questions, all of them concerning formative factors shaping their practice and attitudes about RT near the EoL. Residents were more likely than attendings to list the influence of mentors (63% vs. 31%, P < 0.01), and peers (48% vs. 27%, P = 0.03) as very or extremely important. They were less likely than attendings to list their “own clinical experience/patients [they] have treated” as very or extremely important (55% vs. 79%, P = 0.01). The answers of residents and attendings did not differ significantly for the rest of the questions on the survey. There were no statistical differences between the responses of those in the “thought leader” group and the other respondents.
24 (62) 3 (7)
TABLE 4. Factors Shaping Practices and Attitudes about Radiation Therapy near the End of Life
Formal informational sources Clinical guidelines (n = 100) Instruction from mentors during training (n = 107) Published literature (n = 105)
1. Not Important
2. Somewhat Important
3. Important
4. Very Important
5. Extremely Important
16 (16) 7 (7)
28 (28) 21 (20)
33 (33) 36 (34)
21 (21) 27 (25)
2 (2) 16 (15)
8 (8)
26 (25)
39 (37)
27 (26)
5 (5) w2: P < 0.01
Subjective influences Influence of my radiation oncology peers (n = 106) Influence of referring physicians (n = 107) My own clinical experience/patients I’ve treated (n = 108) Personal values and beliefs (n = 107)
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7 (7)
26 (25)
37 (35)
33 (31)
3 (3)
11 (10) 0 (0)
43 (40) 5 (5)
34 (32) 26 (24)
15 (14) 50 (46)
4 (4) 27 (25)
6 (6)
15 (14)
42 (39)
27 (25)
17 (16) w2: P < 0.01
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DISCUSSION Surveyed radiation oncology thought leaders and trainees at academic centers have a positive view of palliative RT near the EoL and feel that many patients may benefit from properly designed treatment regimens. They indicated that they consider patients’ wishes, but it should be noted that the survey was not designed to accurately distinguish “patients’ wishes” from “patients’ consent” for treatment after discussion with a radiation oncologist. They also consider patients’ ability to tolerate treatment and short courses are favored when prognosis is limited. For some radiation oncologists, experiences of patients not being able to complete treatment have made them more likely to prescribe shorter treatment courses in the future. Practicing radiation oncologists are more likely to list personal experience as important in shaping their opinions about RT at the EoL, whereas residents are more likely to list the influence of mentors and peers. Cancer treatment at the EoL is increasing overall.12 Chemotherapy is given in the last month of life at rates of 20% to 24%12,13 and higher for patients who die in the hospital.14 Although some studies have indicated substantial use of RT at the EoL,2,15 those studies cannot distinguish between palliative and definitive RT. Our survey responses partially address this knowledge gap by confirming an endorsement of palliative and not definitive RT among radiation oncologists. Their belief in the usefulness of palliative RT is supported by data that demonstrates improved quality of life in advanced cancer,10,16 even in patients very near the EoL.17,18
Complexities in EoL Care Responses to this survey illustrate a number of complexities faced by radiation oncologists treating patients near the EoL. These include the time to pain relief in patients with limited time remaining, the uncertainty in predicting prognosis, and the problem of unfinished treatment courses. Although there is great variation among individual patients, the median time to pain relief may be 3 to 4 weeks for both single-fraction and multiple-fraction treatments.19,20 This means that palliative RT does benefit many of those patients with limited, but imprecise prognoses of weeks to months. However, to have maximal effect, palliative consults should not be delayed. Survey respondents reported overestimating prognosis 24% of the time and multiple previous studies demonstrate the difficulty of accurate prognosis.4–6 Although prediction scores for survival near the EoL have been validated,21,22 more research is needed to help radiation oncologists make determinations of life expectancy. In addition, in light of evidence that radiation oncologists may overestimate the prognosis of dying cancer patients,23 conversations about goals of care must occur even before the physician perceives the patient to be at or near the EoL.24,25 It is difficult to predict which patients will be unable to complete a prescribed course of treatment. In thinking of past situations of unfinished treatment, many respondents see the benefits of shorter palliative regimens. However, some radiation oncologists may prefer to offer the treatment they deem most likely to provide palliation and accept the fact that some patients will die or discontinue treatment. Many respondents endorsed shorter or single-fraction treatments that can reduce the number of patient visits, especially when simulation and treatment can be expedited and performed on the same day.26,27
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Formative Factors that Shape Providers’ Opinions About RT near the EoL EoL decisions can be very personal. Although some clinical practice guidelines were cited, only 23% of radiation oncologists felt that guidelines are very or extremely important in shaping their opinions about RT near the EoL. The formative importance of personal experience seen in the survey results may speak to the importance of nuance and flexibility in helping patients make EoL decisions. Nevertheless, there may be a void that could be filled by guidelines and texts that recognize the shifting goals and values of patients as they near death.28 Radiation oncologists early in their careers may benefit from more instruction and guidance in approaching EoL issues. This may be accomplished when mentors approach palliative care as any other subspecialty in radiation oncology. Residents in the survey were more likely to list the influence of both mentors and peers as being influential in shaping their views of RT near the EoL. Past clinical experience was understandably less important for this group. Resident responses did not differ significantly from attendings in other areas of the survey indicating some degree of unity in attitudes, intentions, and expectations across career levels. This study has important limitations. Twenty-nine percent of radiation oncologists surveyed responded, 89% of whom were academic physicians. Therefore, our results may not be generalizable to all radiation oncologists, and the low proportion of community radiation oncologists precludes meaningful comparison of academic and community practices and opinions in this study. Nevertheless, this response rate is comparable with other studies of patterns of care and physician attitudes,10,11 and respondents were from a wide and varied geographic distribution. Also, although there was minimal variation in the number of dying patients that respondents treated over the last year, survey responses may be different depending on the number or percentage of palliative patients radiation oncologists treat, and this was not ascertained. Likewise, the results may be subject to nonresponse bias, in which those interested in the subject of the survey are more likely to respond. Our survey results may also be subject to social desirability bias in which subjects may misrepresent their actions or attitudes in favor of what they think is desirable to the group. In this way, radiation oncologists’ reported attitudes may favor less treatment in thinking about theoretical patients who are “near the EoL” compared with the real, living patients they see in practice. The Likert scales we used in the survey are subject to acquiescence bias in which the subject agrees to the statement as presented. Responses may have also been subject to central tendency bias, in which extreme answers are avoided. Finally, the role of RT near the EoL is a complex issue, and the decision to offer treatment is based on societal values and patients’ interactions with a very complex medical system, which are difficult to capture in a single survey.
CONCLUSIONS Academic radiation oncology thought leaders and trainees have a positive view of palliative radiation near the EoL and believe palliative effect can often be achieved with short treatment regimens, especially in cases of very limited prognosis. Personal experience has shaped their opinions more than current clinical guidelines or literature, potentially pointing to the personal nature of EoL decisions and the importance of the art of medicine in radiation oncology. Complexities regarding
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RT near the EoL include the difficulty of accurately assessing prognosis and identifying patients who may not be able to complete treatment. More instruction and guidance may be warranted for radiation oncologists early in their careers who look to the influence of mentors in forming their attitudes about treatment near the EoL. REFERENCES 1. Brogaard T, Neergaard MA, Sokolowski I, et al. Congruence between preferred and actual place of care and death among Danish cancer patients. Palliat Med. 2013;27:155–164. 2. Guadagnolo BA, Liao K, Elting L, et al. Use of radiation therapy in the last 30 days of life among a large population-based cohort of elderly patients in the United States. J Clin Oncol. 2013;31:80–87. 3. Earle CC, Neville BA, Souza JM, et al. Aggressiveness of cancer care near the end of life: is it a quality-of-care issue? J Clin Oncol. 2008;26:3860–3866. 4. Glare P, Virik K, Jones M, et al. A systematic review of physicians’ survival predictions in terminally ill cancer patients. BMJ. 2003;327:195–200. 5. Gripp S, Moeller S, Bolke E, et al. Survival prediction in terminally ill cancer patients by clinical estimates, laboratory tests, and self-rated anxiety and depression. J Clin Oncol. 2007;25: 3313–3320. 6. Maher EJ, Coia L, Duncan G, et al. Treatment strategies in advanced and metastatic cancer: differences in attitude between the USA, Canada and Europe. Int J Radiat Oncol Biol Phys. 1992;23:239–244. 7. Lutz ST, Berk LB, Chang EL, et al. Palliative radiotherapy for bone metastases: an ASTRO evidence-based guideline. Int J Radiat Oncol Biol Phys. 2011;79:965–976. 8. Rodrigues G, Videtic GMM, Sur R, et al. Palliative thoracic radiotherapy in lung cancer: an American Society for Radiation Oncology evidence-based clinical practice guideline. Pract Radiat Oncol. 2011;1:60–71. 9. Tsao MN, Rades D, Wirth A, et al. Radiotherapeutic and surgical management for newly diagnosed brain metastasis(es): an American Society for Radiation Oncology evidence-based guideline. Pract Radiat Oncol. 2012;2:210–225. 10. Cleeland CS, Janjan NA, Scott CB, et al. Cancer pain management by radiotherapists: a survey of radiation therapy oncology group physicians. Int J Radiat Oncol Biol Phys. 2000;47:203–208. 11. Behl D, Jatoi A. What do oncologists say about chemotherapy at the very end of life? Results from a semiqualitative survey. J Palliat Med. 2010;13:831–835. 12. Earle CC, Neville BA, Landrum MB, et al. Trends in the aggressiveness of cancer care near the end of life. J Clin Oncol. 2004;22:315–321.
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