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Patterns of Care Among Patients Receiving Radiation Therapy for Bone Metastases at a Large Academic Institution
International Journal of
Radiation Oncology biology
physics
www.redjournal.org
Clinical Investigation
Patterns of Care Among Patients Receiving Radiation Therapy for Bone Metastases at a Large Academic Institution Susannah G. Ellsworth, MD,* Sara R. Alcorn, MD, MPH,* Russell K. Hales, MD,* Todd R. McNutt, PhD,* Theodore L. DeWeese, MD,* and Thomas J. Smith, MDy *Departments of Radiation Oncology and Molecular Radiation Sciences and yMedical Oncology and Harry J. Duffey Family Program in Palliative Care, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine, Baltimore, Maryland Received Jan 17, 2014, and in revised form Apr 13, 2014. Accepted for publication Apr 16, 2014.
Summary To evaluate outcomes and patterns of care among patients receiving radiation therapy (RT) for bone metastases, we reviewed records of 339 patients at a highvolume academic institution. The majority of patients had a documented goal of care discussion and were referred to hospice (52% and 56% of patients, respectively). Although single-fraction RT remained relatively uncommon (prescribed to 8% of patients), 83% of patients received palliative bone RT with 10 fractions. Implications for clinical practice and
Purpose: This study evaluates outcomes and patterns of care among patients receiving radiation therapy (RT) for bone metastases at a high-volume academic institution. Methods and Materials: Records of all patients whose final RT course was for bone metastases from April 2007 to July 2012 were identified from electronic medical records. Chart review yielded demographic and clinical data. Rates of complicated versus uncomplicated bone metastases were not analyzed. Results: We identified 339 patients whose final RT course was for bone metastases. Of these, 52.2% were male; median age was 65 years old. The most common primary was non-small-cell lung cancer (29%). Most patients (83%) were prescribed 10 fractions; 8% received single-fraction RT. Most patients (52%) had a documented goals of care (GOC) discussion with their radiation oncologist; hospice referral rates were higher when patients had such discussions (66% with vs 50% without GOC discussion, PZ.004). Median life expectancy after RT was 96 days. Median survival after RT was shorter based on inpatient as opposed to outpatient status at the time of consultation (35 vs 136 days, respectively, P<.001). Hospice referrals occurred for 56% of patients, with a median interval between completion of RT and hospice referral of 29 days and a median hospice stay of 22 days. Conclusions: These data document excellent adherence to American Society for Radiation Oncolology Choosing Wisely recommendation to avoid routinely using >10 fractions of palliative RT for bone metastasis. Nonetheless, single-fraction RT remains
Reprint requests to: Sara Alcorn, MD, MPH, 401 N. Broadway, Ste. 1440, Baltimore, MD 21287. Tel: (410) 955-6980; E-mail: salcorn2@ jhmi.edu Int J Radiation Oncol Biol Phys, Vol. 89, No. 5, pp. 1100e1105, 2014 0360-3016/$ - see front matter Ó 2014 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ijrobp.2014.04.028
Drs. Ellsworth and Alcorn are co-first authors who contributed equally to design, data collection, and manuscript preparation for this work. Conflict of interest: none.
Volume 89 Number 5 2014
medical education are discussed.
Patterns of care in palliative bone radiation 1101
relatively uncommon. Participating in GOC discussions with a radiation oncologist is associated with higher rates of hospice referral. Inpatient status at consultation is associated with short survival. Ó 2014 Elsevier Inc.
Introduction Pain due to bone metastasis is common and often associated with significant morbidity. The International Atomic Energy Agency (IAEA) estimates that approximately 100,000 cases of bone metastases occur annually in the United States (1). Such lesions can be painful and increase the risk of pathologic fracture or spinal cord compression. Radiation therapy is an effective treatment option for patients with painful bony metastases, with an overall pain response rate approaching 60%, and is therefore commonly recommended as a palliative intervention (2). Current practice patterns for palliative radiation in the United States have recently come under scrutiny because of concerns for excessively long treatment courses with major implications for patient quality of life, including travel time and costs (3). Single-fraction radiation is recommended by a recent consensus guideline published by the American Society for Radiation Oncology (ASTRO) for uncomplicated bone metastases, defined as a) lesions without spinal cord compression, cauda equina compression, radicular bone pain, or extensive involvement (>3 cm) of the femoral cortex, b) lesions not requiring surgical stabilization, c) spinal lesions that have not been previously irradiated, and d) lesions for which retreatment would not be excessively problematic (4). However, only 3% of Medicare-age patients with prostate cancer received single-fraction RT for bone metastases, and half received 10 fractions (5), contrary to ASTRO’s Choosing Wisely recommendations (6). However, few investigators have comprehensively evaluated practice patterns among patients receiving palliative RT for bone metastases. Specifically, data are lacking for hospice use, compliance with national best practice guidelines, and factors predictive of survival after RT. In this study, we seek to describe patterns of care for patients with bone metastasis at a large US academic hospital.
Methods and Materials Electronic medical records were used to identify all patients 18 years old whose last RT course was for bone metastasis from any primary tumor, treated between April 2007 and July 2012. Patients whose last course of radiation was for bone metastasis were chosen in order to enrich the sample for patients who received treatment near the end of life. Charts were independently reviewed by 2 authors to gather demographic and clinical data. Data for rates of complicated versus uncomplicated bone metastases was not collected as part of this analysis. Patient fractionation patterns were also analyzed relative to the date of publication of ASTRO’s consensus guidelines for single-fraction
palliative radiation therapy (RT) for bone metastasis (March 15, 2011) (4). Patients were considered to have had a documented goals of care (GOC) discussion with the radiation oncologist at consultation if (1) there was any discussion of specific symptoms that the RT was directed at relieving; (2) the RT course was clearly described as “palliative,” that is, focused on relieving the symptoms described and not directed at affecting the overall course of disease; and (3) the discussion was documented in the consultation notes. For patients who underwent multiple courses of palliative RT, time since completion of RT was calculated from the end date of the final RT course. For patients who were prescribed but never began a course of palliative RT, the date of consultation was used except for the estimation of survival. Only patients receiving at least 1 fraction of RT were included in survival modeling. Patients alive at the completion of the study period but with less than 1 month between last follow-up and the study end date were excluded from the survival analysis. Descriptive statistics were used to summarize the data. Analysis by c2 and t-tests evaluated differences between groups. Kaplan-Meier curves and log-rank tests were applied to estimate the effects of factors on survival following palliative bone RT. All P values for statistical significance were set at <.05.
Results Patient demographic and clinical data Approximately 8000 patients were treated at our institution during the studied time frame. Of these patients, medical record review identified 339 patients whose last course of RT was for bone metastasis. Median age was 65 years old (range 22-94 years), and 52% of patients were male. Seventy-three percent of patients were white, 22% black, and 4% other. The most common primary histology was non-small-cell lung cancer (29%), followed by breast (18%) and prostate cancer (13%). Median baseline Karnofsky performance status (KPS) was 70 (range 30-100), and 29% of patients were admitted to the hospital at the time of radiation oncology consultation. Table 1 summarizes the patients’ baseline clinical characteristics.
Radiation treatment The spine was the most common body site treated (55%), followed by pelvis (17%), extremities (17%), and chest wall (8%). Stereotactic body RT techniques were used in <5% of patients. Nineteen patients (6%) did not start a prescribed course of RT, and another 56 patients (17%) did
International Journal of Radiation Oncology Biology Physics
1102 Ellsworth et al. Table 1
Patient demographics
Demographic
Number
Sex Male 177 Female 162 Race White 248 Black 75 Asian 8 Hispanic 3 Other/unspecified 5 Primary tumor histology Lung (non-small-cell) 97 Breast 60 Prostate 43 Other 139 Admission status at consultation Inpatient 99 Outpatient 240 Age Median 65 Range 22 e 94 Karnofsky performance status Median 70 Range 30 e 100
Percent 52.2 47.8 73 22 2 1 1 29 18 13 41 29 71 -
not complete their scheduled course of RT. Mean baseline KPS was lower in patients who did not complete RT (59.3 among patients who did not complete RT vs 69.3 among patients who finished RT; t-test P<.001), and the most common reason for discontinuing treatment was declining KPS (46%). Twelve patients (4% of the entire cohort, 21% of patients not completing treatment) received RT on the date of their death. The most frequently prescribed radiation dose was 30 Gy in 10 fractions, received by 51% of patients. Figure 1
Percent of treatments
100% 80% 56%
60% 40%
17%
19%
20% 8%
0% 1
2 to 5
6 to 10
>10
Number of fractions Fig. 1. Percent of palliative bone RT treatments by number of fractions prescribed. The most common fractionation scheme was 30 Gy in 10 fractions, comprising 51% of prescribed treatments.
details fractionation schemes prescribed. Eight percent of patients were prescribed single-fraction treatment, and 17% of patients were prescribed more than 10 fractions. Rates of single-fraction RT were relatively low regardless of which body site was targeted (Table 2). Ninety-one patients (27%) were treated after the ASTRO consensus guidelines were published on March 15, 2011; there were no significant differences between rates of single-fraction RT (8% both before and after March 15, 2011, c2 PZ.992) or >10 fraction RT (17% before and 19% after March 15, 2011, c2 PZ.641) prescribed relative to this publication date.
Hospice utilization rates and GOC discussions Fifty-six percent of patients had documented referral to hospice, with a median time to hospice referral after RT of 29 days (range 0-365 days); for 9% of patients, referral status was considered to be unknown due to >3 months between their last follow-up and death or the study end date. There were no differences in baseline mean KPS scores between patients who were versus were not referred to hospice (67.2 vs 68.3, respectively, t-test PZ.576). Median length of time between hospice referral and death was 22 days (range 0-180 days). The radiation oncologist conducted a documented GOC discussion in 52% of cases. Patients who had a documented GOC discussion were significantly more likely to be referred to hospice than those who did not have a GOC discussion (66% vs 50%, respectively, c2 PZ.004).
Survival Median survival for the entire cohort of patients was 111 days (range 0-2212 days) from consultation and 96 days (range 0-2194 days) from completion of RT for those who received at least 1 fraction. Eighty-nine patients (26%) died within 30 days of completing RT. Among these, 64% were referred to hospice. There was no significant difference in mean age between patients who lived for 30 days versus those who lived >30 days after RT (60.8 vs 63.1 years, respectively). However, patients with shorter survival had a lower mean KPS (60 vs 70, respectively, t-test P<.001) and were significantly more likely to be inpatients at the time of initial radiation oncology evaluation than those living >30 days after RT (53% vs 21%, respectively, c2 P<.001). In the group of patients who survived 30 days after completing RT, the rate of single-fraction treatment was 8%, identical to the rate of single-fraction treatment in patients surviving >30 days after completing RT. Median survival after RT was 35 days among people who were inpatients at the time of radiation oncology consultation and 136 days among those evaluated as outpatients (log-rank P<.001), as shown in Figure 2. In the group of patients surviving 30 days after completing RT, the rate of single-fraction treatment was 8%, identical to the
Volume 89 Number 5 2014 Table 2
Patterns of care in palliative bone radiation 1103
Prescribed fractionation patterns by treated site
Treated site
Total no. of patients
% Of entire cohort
No. of patients treated with single-fraction RT
% Of patients treated with single-fraction RT
Spine Pelvis Extremity Chest wall Skull Total
187 56 57 26 13 339
55 17 17 8 4 100
12 4 8 2 0 26
6.4 7.1 14 7.7 0 7.6
rate of single-fraction treatment in patients surviving >30 days after completing RT.
Discussion This report summarizes patterns of care and survival outcomes for patients receiving palliative RT at a large US academic institution and highlights significant implications for both practice guidelines and academic teaching. We present several novel findings.
Hospice utilization rates and GOC discussions First, our data suggest that patients managed with palliative RT near the end of life may have equal if not somewhat higher hospice referral rates than average. Compared to the national hospice utilization rate of 43% reported among Medicare decedents with cancer, 56% of our patients had documented referrals to hospice (7). Given the role of hospice in improving care and reducing costs (8), these data emphasize the important function that radiation oncologists can and do play in improving end-of-life care. At least half of our patients had a documented GOC discussion with a radiation oncologist, and among patients who had such discussions, there were higher rates of hospice utilization. This could be partly due to the fact that
patients who have already considered hospice care may be more likely to initiate GOC conversations with their physicians. Alternatively, open discussions with the radiation oncologist about the palliative nature of a treatment plan may facilitate discussions about hospice care with patients, families, and other providers. Recent data have shown that 64% of patients receiving palliative RT did not understand that RT was unlikely to cure them, reinforcing the importance of honest discussions about prognosis and GOC with all members of the cancer treatment team, including radiation oncologists (9, 10). It should be noted that the rate of GOC discussions reported here may underestimate the actual frequency at which such discussions occur in clinical practice, as this analysis was limited to discussions that were both documented and occurred at consultation.
Hospitalization status at consultation We also observed significantly shorter survival among patients who were hospital inpatients at the time of initial radiation oncology consultation than for those who were evaluated as outpatients, a finding which has not previously been reported. It should be noted that because these data originate from a high-volume tertiary care center, the percentage of patients admitted at the time of radiation oncology consultation is likely higher than is typical in community practice. Nevertheless, differences in survival
Survival Functions Proportion surviving
1.0
Admission status Inpatient Outpatient Inpatient-censored Outpatient-censored
0.8 0.6 0.4 0.2 0.0 0
10
20
30
40
50
60
70
Time to death (months) Fig. 2. Kaplan-Meier death-censored survival after RT by admission status at the time of radiation oncology consultation for bone metastases. Survival curves demonstrate longer survival after RT among patients who were outpatients at the time of radiation oncology consultation (log-rank test, P<.001). Solid line Z survival after RT among outpatients; dashed line Z survival after RT among inpatients; crosses Z censored cases.
1104 Ellsworth et al.
International Journal of Radiation Oncology Biology Physics
between outpatients and inpatients is striking, with a median survival of just over 1 month among those who were hospital inpatients at the time of radiation oncology consultation, compared to more than 4 months among outpatients. These numbers are consistent with a recent study reporting a short median survival (3.4 months) among patients with advanced cancer who had an unplanned inpatient admission for symptom management (11). Moreover, these data suggest that abbreviated courses of RT as well as hospice referral should be strongly considered in hospitalized patients referred for palliative RT and that inpatient RT is a good “trigger” for a full palliative care consultation.
relative paucity of evidence supporting the use of singlefraction RT for complicated bone metastases; of note, there are some data to suggest that single-fraction radiation can provide effective symptom control for patients with spinal cord compression and poor performance status (16). As such, increasing the appropriate use of single-fraction RT represents a promising target for research and quality improvement initiatives in radiation oncology, as emphasized in the ASTRO consensus guideline regarding palliative RT for bone metastases (4). Important future directions include evaluation of outcomes for single-fraction RT in complicated bone metastases and further validation of predictors of survival following palliative RT to aid in clinical decision-making.
End-of-life fractionation patterns
Implications for medical training
The delivery of chemotherapy within the last 2 weeks of life is considered an indication of suboptimal cancer care (12). Conversely, palliative RT within the last weeks of life should not necessarily be deemed as an indicator of poor cancer care; radiation can be highly effective for the management of distressing symptoms such as pain, bleeding, superior vena cava (SVC) syndrome, and airway obstruction, often with relatively fewer side effects than many chemotherapeutic agents. The present survey documents excellent adherence to the ASTRO Choosing Wisely recommendation to avoid routinely using >10 fractions of RT for palliative treatment of bone metastasis. These data also document the fact that there may still be room for improvement in RT delivery at or near end of life by using even shorter fractionation regimens. Among patients who lived for less than 1 month after RT, rates of single-fraction treatment remained low. These results are consistent with previous data reporting infrequent use of single-fraction palliative RT for bone metastases in terminally ill patients, despite national guidelines reinforcing single-fraction treatment as the standard of care for uncomplicated bone metastasis (4). A recent Surveillance, Epidemiology, and End Results analysis reported on more than 15,000 Medicare patients who received RT for any indication during the last 30 days of life and similarly found that fewer than 10% of patients received single-fraction RT, whereas 17.8% received more than 10 days of RT (13). An analysis of Medicare patients with prostate cancer treated for painful bone metastases showed that only 3.3% received single-fraction RT, with multiple-fraction RT costing Medicare an average of $3094 more per patient than single-fraction treatment (5). Although likely multifactorial, the low frequency of single-fraction RT use is probably influenced by deeply rooted and historical practice patterns in the United States favoring multi-fraction courses, despite data from multiple randomized controlled trials showing that single-fraction treatment is as effective for relieving pain as more prolonged courses (14, 15). Additional contributing factors may include fraction-based reimbursement schemes and the
Our study also has implications for medical education in radiation oncology. Administering palliative radiation, particularly among patients with short life expectancy, requires not only training in hypofractionation but in symptom management and communication about GOC and the role of hospice. There is ample evidence that these skills can be learned at the resident and practicing oncologist level, either in person, at courses such as Oncotalk, or with computerized distance learning (17-19).
Limitations This study is inherently limited by its retrospective design. These data were collected from a single academic institution with a patient population that may be more skewed toward advanced and refractory disease than is common in the community, which may limit the generalizability of our findings. Referral patterns at our institution may result in a disproportionately high number of complicated bone metastases, which could sway physicians away from prescribing single-fraction RT due to a relative lack of data regarding its efficacy in this setting. Nonetheless, our results provide a framework for evaluating radiation practice patterns in the context of established national quality guidelines and support our future goal of developing predictive models to help guide decision-making regarding RT for patients with metastatic disease.
Conclusions Palliative RT is a mainstay of management for patients with bone metastases. In patients offered palliative RT for bone metastases, a GOC discussion with a radiation oncologist is associated with higher rates of hospice referrals. Inpatients as well as patients with poor KPS have worse survival outcomes, and hypofractionated RT courses as well as hospice referral should be strongly considered in such cases. The use of palliative RT strategies using 10 fractions is quite high, but single-fraction RT remains relatively
Volume 89 Number 5 2014
low. This is consistent with national practice patterns in the United States, but a more complete analysis is needed to determine the degree to which these data are influenced by rates of complicated versus uncomplicated bone metastases. Further research is required to improve our ability to predict survival among patients offered palliative RT and to increase the appropriate use of palliative single-fraction or hypofractionated RT in patients with metastatic cancer.
References 1. International Atomic Energy Agency. Criteria for Palliation of Bone MetastasesdClinical Applications. Vienna, Austria: International Atomic Energy Agency; 2007. 2. Chow E, Harris K, Fan G, et al. Palliative radiotherapy trials for bone metastases: a systematic review. J Clin Oncol 2007;25:1423-1436. 3. Fischberg D, Bull J, Casarett D, et al. Five things physicians and patients should question in hospice and palliative medicine. J Pain Symptom Manage 2013;45:595-605. 4. Lutz S, Berk L, Chang E, et al. Palliative radiotherapy for bone metastases: an ASTRO evidence-based guideline. Available at: https:// www.astro.org/uploadedFiles/Main_Site/Clinical_Practice/Guidelines/ ASTRO_bone_mets_guideline_full_version.pdf. Accessed April 11, 2014. 5. Bekelman JE, Epstein AJ, Emanuel EJ. Single- vs. multiple-fraction radiotherapy for bone metastases from prostate cancer. JAMA 2013; 310:1501-1502. 6. ASTRO releases list of five radiation oncology treatments to question as part of national choosing wisely campaign. Available at: http:// www.choosingwisely.org/astro-releases-list-of-five-radiation-oncologytreatments-to-question-as-part-of-national-choosing-wisely-campaign/. Accessed January 10, 2013. 7. National Hospice and Palliative Care Organization. NHPCO’s Facts and Figures: Hospice Care in America. Alexandria, VA: NHPCO; 2013.
Patterns of care in palliative bone radiation 1105 8. Kelley AS, Deb P, Du Q, et al. Hospice enrollment saves money for Medicare and improves care quality across a number of different lengths-of-stay. Health Aff (Millwood) 2013;32:552-561. 9. Chen AB, Cronin A, Weeks JC, et al. Expectations about the effectiveness of radiation therapy among patients with incurable lung cancer. J Clin Oncol 2013;31:2730-2735. 10. Smith TJ, Longo DL. Talking with patients about dying. N Engl J Med 2013;368:481. 11. Rocque GB, Barnett AE, Illig LC, et al. Inpatient hospitalization of oncology patients: Are we missing an opportunity for end-of-life care? J Oncol Pract 2013;9:51-54. 12. Campion FX, Larson LR, Kadlubek PJ, et al. Advancing performance measurement in oncology: quality oncology practice initiative participation and quality outcomes. J Oncol Pract 2011;7(Suppl. 3): 31s-35s. 13. Guadagnolo BA, Liao KP, 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. 14. Sze WM, Shelley M, Held I, et al. Palliation of metastatic bone pain: single fraction versus multifraction radiotherapyda systematic review of the randomised trials. Cochrane Database Sys Rev 2004; CD004721. 15. Wu JS-Y, 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. 16. Maranzano E, Trippa F, Casale M, et al. 8Gy single-dose radiotherapy is effective in metastatic spinal cord compression: results of a phase III randomized multicentre Italian trial. Radiother Oncol 2009;93: 174-179. 17. Pham AK, Bauer MT, Balan S. Closing the patient-oncologist communication gap: a review of historic and current efforts. J Cancer Educ 2014;29:106-113. 18. 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 2007;167:453-460. 19. Tulsky JA, Arnold RM, Alexander SC, et al. Enhancing communication between oncologists and patients with a computer-based training program: a randomized trial. Ann Intern Med 2011;155:593-601.
Radiation Oncology biology
physics
www.redjournal.org
Clinical Investigation
Patterns of Care Among Patients Receiving Radiation Therapy for Bone Metastases at a Large Academic Institution Susannah G. Ellsworth, MD,* Sara R. Alcorn, MD, MPH,* Russell K. Hales, MD,* Todd R. McNutt, PhD,* Theodore L. DeWeese, MD,* and Thomas J. Smith, MDy *Departments of Radiation Oncology and Molecular Radiation Sciences and yMedical Oncology and Harry J. Duffey Family Program in Palliative Care, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine, Baltimore, Maryland Received Jan 17, 2014, and in revised form Apr 13, 2014. Accepted for publication Apr 16, 2014.
Summary To evaluate outcomes and patterns of care among patients receiving radiation therapy (RT) for bone metastases, we reviewed records of 339 patients at a highvolume academic institution. The majority of patients had a documented goal of care discussion and were referred to hospice (52% and 56% of patients, respectively). Although single-fraction RT remained relatively uncommon (prescribed to 8% of patients), 83% of patients received palliative bone RT with 10 fractions. Implications for clinical practice and
Purpose: This study evaluates outcomes and patterns of care among patients receiving radiation therapy (RT) for bone metastases at a high-volume academic institution. Methods and Materials: Records of all patients whose final RT course was for bone metastases from April 2007 to July 2012 were identified from electronic medical records. Chart review yielded demographic and clinical data. Rates of complicated versus uncomplicated bone metastases were not analyzed. Results: We identified 339 patients whose final RT course was for bone metastases. Of these, 52.2% were male; median age was 65 years old. The most common primary was non-small-cell lung cancer (29%). Most patients (83%) were prescribed 10 fractions; 8% received single-fraction RT. Most patients (52%) had a documented goals of care (GOC) discussion with their radiation oncologist; hospice referral rates were higher when patients had such discussions (66% with vs 50% without GOC discussion, PZ.004). Median life expectancy after RT was 96 days. Median survival after RT was shorter based on inpatient as opposed to outpatient status at the time of consultation (35 vs 136 days, respectively, P<.001). Hospice referrals occurred for 56% of patients, with a median interval between completion of RT and hospice referral of 29 days and a median hospice stay of 22 days. Conclusions: These data document excellent adherence to American Society for Radiation Oncolology Choosing Wisely recommendation to avoid routinely using >10 fractions of palliative RT for bone metastasis. Nonetheless, single-fraction RT remains
Reprint requests to: Sara Alcorn, MD, MPH, 401 N. Broadway, Ste. 1440, Baltimore, MD 21287. Tel: (410) 955-6980; E-mail: salcorn2@ jhmi.edu Int J Radiation Oncol Biol Phys, Vol. 89, No. 5, pp. 1100e1105, 2014 0360-3016/$ - see front matter Ó 2014 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ijrobp.2014.04.028
Drs. Ellsworth and Alcorn are co-first authors who contributed equally to design, data collection, and manuscript preparation for this work. Conflict of interest: none.
Volume 89 Number 5 2014
medical education are discussed.
Patterns of care in palliative bone radiation 1101
relatively uncommon. Participating in GOC discussions with a radiation oncologist is associated with higher rates of hospice referral. Inpatient status at consultation is associated with short survival. Ó 2014 Elsevier Inc.
Introduction Pain due to bone metastasis is common and often associated with significant morbidity. The International Atomic Energy Agency (IAEA) estimates that approximately 100,000 cases of bone metastases occur annually in the United States (1). Such lesions can be painful and increase the risk of pathologic fracture or spinal cord compression. Radiation therapy is an effective treatment option for patients with painful bony metastases, with an overall pain response rate approaching 60%, and is therefore commonly recommended as a palliative intervention (2). Current practice patterns for palliative radiation in the United States have recently come under scrutiny because of concerns for excessively long treatment courses with major implications for patient quality of life, including travel time and costs (3). Single-fraction radiation is recommended by a recent consensus guideline published by the American Society for Radiation Oncology (ASTRO) for uncomplicated bone metastases, defined as a) lesions without spinal cord compression, cauda equina compression, radicular bone pain, or extensive involvement (>3 cm) of the femoral cortex, b) lesions not requiring surgical stabilization, c) spinal lesions that have not been previously irradiated, and d) lesions for which retreatment would not be excessively problematic (4). However, only 3% of Medicare-age patients with prostate cancer received single-fraction RT for bone metastases, and half received 10 fractions (5), contrary to ASTRO’s Choosing Wisely recommendations (6). However, few investigators have comprehensively evaluated practice patterns among patients receiving palliative RT for bone metastases. Specifically, data are lacking for hospice use, compliance with national best practice guidelines, and factors predictive of survival after RT. In this study, we seek to describe patterns of care for patients with bone metastasis at a large US academic hospital.
Methods and Materials Electronic medical records were used to identify all patients 18 years old whose last RT course was for bone metastasis from any primary tumor, treated between April 2007 and July 2012. Patients whose last course of radiation was for bone metastasis were chosen in order to enrich the sample for patients who received treatment near the end of life. Charts were independently reviewed by 2 authors to gather demographic and clinical data. Data for rates of complicated versus uncomplicated bone metastases was not collected as part of this analysis. Patient fractionation patterns were also analyzed relative to the date of publication of ASTRO’s consensus guidelines for single-fraction
palliative radiation therapy (RT) for bone metastasis (March 15, 2011) (4). Patients were considered to have had a documented goals of care (GOC) discussion with the radiation oncologist at consultation if (1) there was any discussion of specific symptoms that the RT was directed at relieving; (2) the RT course was clearly described as “palliative,” that is, focused on relieving the symptoms described and not directed at affecting the overall course of disease; and (3) the discussion was documented in the consultation notes. For patients who underwent multiple courses of palliative RT, time since completion of RT was calculated from the end date of the final RT course. For patients who were prescribed but never began a course of palliative RT, the date of consultation was used except for the estimation of survival. Only patients receiving at least 1 fraction of RT were included in survival modeling. Patients alive at the completion of the study period but with less than 1 month between last follow-up and the study end date were excluded from the survival analysis. Descriptive statistics were used to summarize the data. Analysis by c2 and t-tests evaluated differences between groups. Kaplan-Meier curves and log-rank tests were applied to estimate the effects of factors on survival following palliative bone RT. All P values for statistical significance were set at <.05.
Results Patient demographic and clinical data Approximately 8000 patients were treated at our institution during the studied time frame. Of these patients, medical record review identified 339 patients whose last course of RT was for bone metastasis. Median age was 65 years old (range 22-94 years), and 52% of patients were male. Seventy-three percent of patients were white, 22% black, and 4% other. The most common primary histology was non-small-cell lung cancer (29%), followed by breast (18%) and prostate cancer (13%). Median baseline Karnofsky performance status (KPS) was 70 (range 30-100), and 29% of patients were admitted to the hospital at the time of radiation oncology consultation. Table 1 summarizes the patients’ baseline clinical characteristics.
Radiation treatment The spine was the most common body site treated (55%), followed by pelvis (17%), extremities (17%), and chest wall (8%). Stereotactic body RT techniques were used in <5% of patients. Nineteen patients (6%) did not start a prescribed course of RT, and another 56 patients (17%) did
International Journal of Radiation Oncology Biology Physics
1102 Ellsworth et al. Table 1
Patient demographics
Demographic
Number
Sex Male 177 Female 162 Race White 248 Black 75 Asian 8 Hispanic 3 Other/unspecified 5 Primary tumor histology Lung (non-small-cell) 97 Breast 60 Prostate 43 Other 139 Admission status at consultation Inpatient 99 Outpatient 240 Age Median 65 Range 22 e 94 Karnofsky performance status Median 70 Range 30 e 100
Percent 52.2 47.8 73 22 2 1 1 29 18 13 41 29 71 -
not complete their scheduled course of RT. Mean baseline KPS was lower in patients who did not complete RT (59.3 among patients who did not complete RT vs 69.3 among patients who finished RT; t-test P<.001), and the most common reason for discontinuing treatment was declining KPS (46%). Twelve patients (4% of the entire cohort, 21% of patients not completing treatment) received RT on the date of their death. The most frequently prescribed radiation dose was 30 Gy in 10 fractions, received by 51% of patients. Figure 1
Percent of treatments
100% 80% 56%
60% 40%
17%
19%
20% 8%
0% 1
2 to 5
6 to 10
>10
Number of fractions Fig. 1. Percent of palliative bone RT treatments by number of fractions prescribed. The most common fractionation scheme was 30 Gy in 10 fractions, comprising 51% of prescribed treatments.
details fractionation schemes prescribed. Eight percent of patients were prescribed single-fraction treatment, and 17% of patients were prescribed more than 10 fractions. Rates of single-fraction RT were relatively low regardless of which body site was targeted (Table 2). Ninety-one patients (27%) were treated after the ASTRO consensus guidelines were published on March 15, 2011; there were no significant differences between rates of single-fraction RT (8% both before and after March 15, 2011, c2 PZ.992) or >10 fraction RT (17% before and 19% after March 15, 2011, c2 PZ.641) prescribed relative to this publication date.
Hospice utilization rates and GOC discussions Fifty-six percent of patients had documented referral to hospice, with a median time to hospice referral after RT of 29 days (range 0-365 days); for 9% of patients, referral status was considered to be unknown due to >3 months between their last follow-up and death or the study end date. There were no differences in baseline mean KPS scores between patients who were versus were not referred to hospice (67.2 vs 68.3, respectively, t-test PZ.576). Median length of time between hospice referral and death was 22 days (range 0-180 days). The radiation oncologist conducted a documented GOC discussion in 52% of cases. Patients who had a documented GOC discussion were significantly more likely to be referred to hospice than those who did not have a GOC discussion (66% vs 50%, respectively, c2 PZ.004).
Survival Median survival for the entire cohort of patients was 111 days (range 0-2212 days) from consultation and 96 days (range 0-2194 days) from completion of RT for those who received at least 1 fraction. Eighty-nine patients (26%) died within 30 days of completing RT. Among these, 64% were referred to hospice. There was no significant difference in mean age between patients who lived for 30 days versus those who lived >30 days after RT (60.8 vs 63.1 years, respectively). However, patients with shorter survival had a lower mean KPS (60 vs 70, respectively, t-test P<.001) and were significantly more likely to be inpatients at the time of initial radiation oncology evaluation than those living >30 days after RT (53% vs 21%, respectively, c2 P<.001). In the group of patients who survived 30 days after completing RT, the rate of single-fraction treatment was 8%, identical to the rate of single-fraction treatment in patients surviving >30 days after completing RT. Median survival after RT was 35 days among people who were inpatients at the time of radiation oncology consultation and 136 days among those evaluated as outpatients (log-rank P<.001), as shown in Figure 2. In the group of patients surviving 30 days after completing RT, the rate of single-fraction treatment was 8%, identical to the
Volume 89 Number 5 2014 Table 2
Patterns of care in palliative bone radiation 1103
Prescribed fractionation patterns by treated site
Treated site
Total no. of patients
% Of entire cohort
No. of patients treated with single-fraction RT
% Of patients treated with single-fraction RT
Spine Pelvis Extremity Chest wall Skull Total
187 56 57 26 13 339
55 17 17 8 4 100
12 4 8 2 0 26
6.4 7.1 14 7.7 0 7.6
rate of single-fraction treatment in patients surviving >30 days after completing RT.
Discussion This report summarizes patterns of care and survival outcomes for patients receiving palliative RT at a large US academic institution and highlights significant implications for both practice guidelines and academic teaching. We present several novel findings.
Hospice utilization rates and GOC discussions First, our data suggest that patients managed with palliative RT near the end of life may have equal if not somewhat higher hospice referral rates than average. Compared to the national hospice utilization rate of 43% reported among Medicare decedents with cancer, 56% of our patients had documented referrals to hospice (7). Given the role of hospice in improving care and reducing costs (8), these data emphasize the important function that radiation oncologists can and do play in improving end-of-life care. At least half of our patients had a documented GOC discussion with a radiation oncologist, and among patients who had such discussions, there were higher rates of hospice utilization. This could be partly due to the fact that
patients who have already considered hospice care may be more likely to initiate GOC conversations with their physicians. Alternatively, open discussions with the radiation oncologist about the palliative nature of a treatment plan may facilitate discussions about hospice care with patients, families, and other providers. Recent data have shown that 64% of patients receiving palliative RT did not understand that RT was unlikely to cure them, reinforcing the importance of honest discussions about prognosis and GOC with all members of the cancer treatment team, including radiation oncologists (9, 10). It should be noted that the rate of GOC discussions reported here may underestimate the actual frequency at which such discussions occur in clinical practice, as this analysis was limited to discussions that were both documented and occurred at consultation.
Hospitalization status at consultation We also observed significantly shorter survival among patients who were hospital inpatients at the time of initial radiation oncology consultation than for those who were evaluated as outpatients, a finding which has not previously been reported. It should be noted that because these data originate from a high-volume tertiary care center, the percentage of patients admitted at the time of radiation oncology consultation is likely higher than is typical in community practice. Nevertheless, differences in survival
Survival Functions Proportion surviving
1.0
Admission status Inpatient Outpatient Inpatient-censored Outpatient-censored
0.8 0.6 0.4 0.2 0.0 0
10
20
30
40
50
60
70
Time to death (months) Fig. 2. Kaplan-Meier death-censored survival after RT by admission status at the time of radiation oncology consultation for bone metastases. Survival curves demonstrate longer survival after RT among patients who were outpatients at the time of radiation oncology consultation (log-rank test, P<.001). Solid line Z survival after RT among outpatients; dashed line Z survival after RT among inpatients; crosses Z censored cases.
1104 Ellsworth et al.
International Journal of Radiation Oncology Biology Physics
between outpatients and inpatients is striking, with a median survival of just over 1 month among those who were hospital inpatients at the time of radiation oncology consultation, compared to more than 4 months among outpatients. These numbers are consistent with a recent study reporting a short median survival (3.4 months) among patients with advanced cancer who had an unplanned inpatient admission for symptom management (11). Moreover, these data suggest that abbreviated courses of RT as well as hospice referral should be strongly considered in hospitalized patients referred for palliative RT and that inpatient RT is a good “trigger” for a full palliative care consultation.
relative paucity of evidence supporting the use of singlefraction RT for complicated bone metastases; of note, there are some data to suggest that single-fraction radiation can provide effective symptom control for patients with spinal cord compression and poor performance status (16). As such, increasing the appropriate use of single-fraction RT represents a promising target for research and quality improvement initiatives in radiation oncology, as emphasized in the ASTRO consensus guideline regarding palliative RT for bone metastases (4). Important future directions include evaluation of outcomes for single-fraction RT in complicated bone metastases and further validation of predictors of survival following palliative RT to aid in clinical decision-making.
End-of-life fractionation patterns
Implications for medical training
The delivery of chemotherapy within the last 2 weeks of life is considered an indication of suboptimal cancer care (12). Conversely, palliative RT within the last weeks of life should not necessarily be deemed as an indicator of poor cancer care; radiation can be highly effective for the management of distressing symptoms such as pain, bleeding, superior vena cava (SVC) syndrome, and airway obstruction, often with relatively fewer side effects than many chemotherapeutic agents. The present survey documents excellent adherence to the ASTRO Choosing Wisely recommendation to avoid routinely using >10 fractions of RT for palliative treatment of bone metastasis. These data also document the fact that there may still be room for improvement in RT delivery at or near end of life by using even shorter fractionation regimens. Among patients who lived for less than 1 month after RT, rates of single-fraction treatment remained low. These results are consistent with previous data reporting infrequent use of single-fraction palliative RT for bone metastases in terminally ill patients, despite national guidelines reinforcing single-fraction treatment as the standard of care for uncomplicated bone metastasis (4). A recent Surveillance, Epidemiology, and End Results analysis reported on more than 15,000 Medicare patients who received RT for any indication during the last 30 days of life and similarly found that fewer than 10% of patients received single-fraction RT, whereas 17.8% received more than 10 days of RT (13). An analysis of Medicare patients with prostate cancer treated for painful bone metastases showed that only 3.3% received single-fraction RT, with multiple-fraction RT costing Medicare an average of $3094 more per patient than single-fraction treatment (5). Although likely multifactorial, the low frequency of single-fraction RT use is probably influenced by deeply rooted and historical practice patterns in the United States favoring multi-fraction courses, despite data from multiple randomized controlled trials showing that single-fraction treatment is as effective for relieving pain as more prolonged courses (14, 15). Additional contributing factors may include fraction-based reimbursement schemes and the
Our study also has implications for medical education in radiation oncology. Administering palliative radiation, particularly among patients with short life expectancy, requires not only training in hypofractionation but in symptom management and communication about GOC and the role of hospice. There is ample evidence that these skills can be learned at the resident and practicing oncologist level, either in person, at courses such as Oncotalk, or with computerized distance learning (17-19).
Limitations This study is inherently limited by its retrospective design. These data were collected from a single academic institution with a patient population that may be more skewed toward advanced and refractory disease than is common in the community, which may limit the generalizability of our findings. Referral patterns at our institution may result in a disproportionately high number of complicated bone metastases, which could sway physicians away from prescribing single-fraction RT due to a relative lack of data regarding its efficacy in this setting. Nonetheless, our results provide a framework for evaluating radiation practice patterns in the context of established national quality guidelines and support our future goal of developing predictive models to help guide decision-making regarding RT for patients with metastatic disease.
Conclusions Palliative RT is a mainstay of management for patients with bone metastases. In patients offered palliative RT for bone metastases, a GOC discussion with a radiation oncologist is associated with higher rates of hospice referrals. Inpatients as well as patients with poor KPS have worse survival outcomes, and hypofractionated RT courses as well as hospice referral should be strongly considered in such cases. The use of palliative RT strategies using 10 fractions is quite high, but single-fraction RT remains relatively
Volume 89 Number 5 2014
low. This is consistent with national practice patterns in the United States, but a more complete analysis is needed to determine the degree to which these data are influenced by rates of complicated versus uncomplicated bone metastases. Further research is required to improve our ability to predict survival among patients offered palliative RT and to increase the appropriate use of palliative single-fraction or hypofractionated RT in patients with metastatic cancer.
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