- Email: [email protected]
Lung cancer physicians’ referral practices for palliative care consultation
original articles
Annals of Oncology
Lung cancer physicians’ referral practices for palliative care consultation C. B. Smith1,2*, J. E. Nelson2,3, A. R. Berman4, C. A. Powell5, J. Fleischman6, J. Salazar-Schicchi7 & J. P. Wisnivesky3,8 1 Division of Hematology/Oncology, Tisch Cancer Institute; 2Hertzberg Palliative Care Institute of the Brookdale Department of Geriatrics and Palliative Medicine; 3Division of Pulmonary, Critical Care and Sleep Medicine, Department of Medicine, Mount Sinai School of Medicine, New York; 4Division of Pulmonary and Critical Care Medicine, Montefiore Medical Center, Bronx; 5Division of Pulmonary and Critical Care Medicine, New York-Presbyterian Hospital, New York; 6Division of Pulmonary and Critical Care Medicine, Queens Hospital Center, Jamaica; 7Division of Pulmonary and Critical Care Medicine, Harlem Hospital Center, Harlem; 8Division of General Internal Medicine, Department of Medicine, Mount Sinai School of Medicine, New York USA
Received 23 March 2011; revised 14 June 2011; accepted 15 June 2011
Background: Integration of palliative care with standard oncologic care improves quality of life and survival of lung cancer patients. We surveyed physicians to identify factors influencing their decisions for referral to palliative care.
Methods: We provided a self-administered questionnaire to physicians caring for lung cancer patients at five medical centers. The questionnaire asked about practices and views with respect to palliative care referral. We used multiple regression analysis to identify predictors of low referral rates (<25%). Results: Of 155 physicians who returned survey responses, 75 (48%) reported referring <25% of patients for palliative care consultation. Multivariate analysis, controlling for provider characteristics, found that low referral
*Correspondence to: Dr C. B. Smith, One Gustave L. Levy Place, Box 1079, New York, NY 10029, USA. Tel: +1-212-241-8149; Fax: +1-212-659-5599; E-mail: [email protected]
ª The Author 2011. Published by Oxford University Press on behalf of the European Society for Medical Oncology. All rights reserved. For permissions, please email: [email protected]
Downloaded from http://annonc.oxfordjournals.org/ at Robertson Library University of prince Edward Island on July 12, 2015
Annals of Oncology 23: 382–387, 2012 doi:10.1093/annonc/mdr345 Published online 29 July 2011
original articles
Annals of Oncology
rates were associated with physicians’ concerns that palliative care referral would alarm patients and families [odds ratio (OR) 0.45, 95% confidence interval (CI) 0.21–0.98], while the belief that palliative care specialists have more time to discuss complex issues (OR 3.07, 95% CI 1.56–6.02) was associated with higher rates of referral. Conclusions: Although palliative care consultation is increasingly available and recommended throughout the trajectory of lung cancer, our data indicate it is underutilized. Understanding factors influencing decisions to refer can be used to improve integration of palliative care as part of lung cancer management. Key words: lung cancer, palliative care, physician, survey
methods
Lung cancer patients across all stages, including those pursuing aggressive disease-directed therapies, face substantial rates of morbidity and mortality. The risk of death from disease progression exceeds 30% for patients with early-stage disease and is >90% for those diagnosed with advanced disease [1, 2]. Symptom burden from standard treatments such as surgical resection, chemotherapy, and radiation therapy, as well as from the disease itself, is often significant. In a systematic review of the literature, patients with lung cancer were found to have multiple physical and psychological symptoms throughout the trajectory of the disease [3]. The literature also suggests that lung cancer patients have more distressing symptoms than other cancer patients of similar stage [3] and that significant stresses are experienced by their families [4]. The value of integrating expert palliative care, including symptom management, psychosocial support, communication, complex decision making, and transition planning, in oncologic management of lung cancer patients and their families is well documented. Benefits of consultation by palliative care specialists include improved symptom control [5], clearer understanding of diagnosis and prognosis [5], more efficient utilization of health care resources [6], and greater patient and family satisfaction [5–8]. In a recent randomized controlled trial, early integration of palliative care with standard oncologic care for ambulatory patients with stage IV lung cancer was associated not only with improvements in quality of life and mood but also with longer survival [9]. Based on these data, clinical guidelines recommend routine integration of palliative care as part of comprehensive lung cancer care from the time of diagnosis, even for patients pursuing cure-oriented or life-prolonging therapies [10–13]. Over the past decade, the availability of palliative care consultation services has increased dramatically in developed countries. However, existing evidence indicates that referral of patients with lung cancer and other malignancies for palliative care is infrequent and delayed until after discontinuation of disease-directed treatment [14, 15]. This pattern of referral undermines access to and effectiveness of palliative care for lung cancer patients and their families. There is limited information about factors influencing palliative care referral decisions by physicians, who make the vast majority of these referrals. In this study, conducted at five hospitals with established palliative care consultation services, we sought a better understanding of the factors influencing lung cancer physicians’ decisions to refer their patients to experts in palliative care.
physician sample and survey administration
Volume 23 | No. 2 | February 2012
The study population consisted of attending physicians and fellows caring for lung cancer patients at five hospitals located in New York City. From the hospitals’ staff lists, we identified physicians in pulmonary disease; hospital medicine; and medical, surgical, and/or radiation oncology who were known to care regularly for lung cancer patients. Following informed consent, physicians were given a self-administered survey. Physicians who did not respond to an initial contact to discuss study participation or who agreed to participate but did not return the completed survey were recontacted up to two more times, after which they were deemed to be nonresponders.
study sites The study hospitals were the following: Mount Sinai Hospital, Montefiore Hospital, New York-Presbyterian Hospital, Harlem Hospital, and Queens Hospital. Mount Sinai, Montefiore, and New York-Presbyterian are large, not-for-profit, teaching hospitals with 1100, 1200, and 740 beds, respectively. Harlem Hospital and Queens Hospital are city hospitals with 286 and 200 beds, respectively. These hospitals provide medical and surgical care for patients with lung cancer in inpatient and ambulatory settings. All sites have established interdisciplinary palliative care consultation services that include physicians; advanced practice nurses; and social work, mental health, and pastoral care professionals.
survey instrument To identify potential domains of interest for our survey, we conducted a review of literature examining clinicians’ attitudes toward ‘palliative care’, ‘supportive care’, and ‘end-of-life care’. We also obtained input on content from five nationally recognized experts in oncology, cancer health services research, and/ or palliative medicine. After pilot testing with 10 lung cancer physicians, we refined the survey to clarify items and minimize respondent burden. The final survey assessed physicians’ beliefs and attitudes toward palliative care in the following categories: (i) level of care in relation to disease status and prognosis; (ii) communication with patients and families; (iii) patient management; and (iv) the role of the primary physician and availability of palliative care. Physicians were asked to indicate their level of agreement on a 4-point scale (strongly agree, agree, disagree, strongly disagree) with statements about why they are inclined, hesitant, or don’t need to refer lung cancer patients to a palliative care specialist; for analyses, we collapsed into two categories the ‘agree’ and ‘strongly agree’ responses and ‘disagree’ and ‘strongly disagree’ responses. In addition, the survey asked physicians to report the percentage of lung cancer patients referred for palliative care consultation during the prior year (<25%, 25%–50%, 51%–75%, or 76%– 100%); we classified physicians who reported referring <25% of their patients for such consultation as having a ‘low referral’ pattern. The survey also collected information about the physician’s sociodemographic characteristics (age, gender, race/ethnicity), religious preference, year of graduation from medical school, and current level of training.
doi:10.1093/annonc/mdr345 | 383
Downloaded from http://annonc.oxfordjournals.org/ at Robertson Library University of prince Edward Island on July 12, 2015
introduction
original articles statistical analysis
results Of 198 eligible physicians who were offered participation at the five institutions, 155 (78%) returned completed surveys. Overall, 75 (48%) providers reported referring <25% of their lung cancer patients for palliative care consultation. Baseline characteristics of physicians in the two groups based on referral rates (<25% or ‡25%) are reported in Table 1. There was no difference between these groups in age distribution (P = 0.58), religious affiliation (P = 0.88), or physician specialty (P = 0.62). Those who referred <25% of lung cancer patients for palliative care consultation were more likely to be male (P < 0.0001) and white (P = 0.04) and to be attending physicians (P = 0.02) rather than trainees. As shown in Table 2, univariate analysis revealed that low referral rates were associated with physicians’ beliefs that patients and families would be alarmed by the mention of palliative care (P = 0.02), that patients prefer to focus on curative rather than palliative therapies (P = 0.05), and that patients do not want to discuss prognosis (P = 0.04). Conversely, physicians referring more frequently were more likely to believe that palliative care specialists can spend more time discussing complex issues (P < 0.0001) and are helpful in establishing goals of care (P = 0.049). In multiple regression analysis (Table 3), adjusting for sociodemographic characteristics, physicians’ belief that referral for palliative care consultation would alarm patients and families was a significant predictor of low referral (OR 0.45, 95% CI 0.21–0.98), while the belief that palliative care specialists spend more time discussing complex issues was a significant predictor (OR 3.07, 95% CI 1.56–6.02) of more frequent referral.
discussion In this survey of a diverse group of >150 physicians who regularly provide lung cancer care at five New York City hospitals with well-established palliative care programs, half of the respondents reported referring <25% of their lung cancer patients for palliative care consultation. Among these physicians, reluctance to refer was explained mainly by their
384 | Smith et al.
concern that involvement of a palliative care specialist would alarm patients and families posed a significant barrier to referral for palliative care consultation. Conversely, physicians valuing the time devoted by palliative care specialists to discussion of complex issues were more likely to engage these specialists for expert assistance in caring for their patients with lung cancer. Our study contributes new evidence that can help target efforts to achieve wider and more timely access for lung cancer patients and their families to expert palliative care. Previous surveys conducted in other countries have examined physician practices and attitudes with respect to palliative care consultation among patients with cancer in general or other chronic conditions [16, 17]. A survey in Australia focused on medical oncologists, who reported frequent collaboration with palliative care specialists in management of cancer patients, even though the vast majority of these oncologists viewed their own training in palliative care as adequate [16]. Although many of the respondents believed that patients and families were reluctant to involve palliative care specialists, few saw this as a major barrier for referral of their patients. A survey of physicians in the European Society of Medical Oncology revealed that most physicians felt confident about their own knowledge and skills for meeting patients’ palliative care needs, while 35% of the respondents reported frequent collaboration with palliative care specialists [17]. In the United States, Snow et al. [18] surveyed 74 physicians in selected divisions within the department of medicine of a single tertiary-care hospital about barriers to referral of patients with any advanced disease (including but not limited to cancer) to the hospital’s inpatient palliative care service. Most physicians acknowledged a lack of expertise in management of distressing symptoms and agreed that a multidisciplinary approach might benefit patients with advanced disease; the most important barriers to referral were unrealistic expectations on the part of patients and families and lack of familiarity with this service. Our study extends prior research by surveying physicians across multiple institutions and specifically focusing lung cancer patients, who are known to benefit from early integration of palliative care. Among physicians we surveyed, reluctance to refer for palliative care consultation was significantly associated with the belief that referral would alarm lung cancer patients and their families. While it is possible that physicians in our study or others have anecdotally met with this response in clinical practice, no convincing evidence exists in the literature that patients or families typically respond with anxiety, fear, or other negative emotions or resistance to the suggestion that they might benefit from the input of a palliative care expert. Physicians have similarly been concerned that discussions of unfavorable prognosis and of preferences for end-of-life care would be harmful to patients and families. Yet research continues to show that such communication does not increase psychological distress but instead promotes acceptance of the gravity of the illness, preference for realistic goals of care, better quality of life as death approaches, and more successful coping for informal caregivers [19, 20]. Wider dissemination of this evidence may help to allay physician concerns that appear to serve as a barrier for delivery of expert palliative care to lung cancer patients and their families.
Volume 23 | No. 2 | February 2012
Downloaded from http://annonc.oxfordjournals.org/ at Robertson Library University of prince Edward Island on July 12, 2015
We compared the baseline characteristics and the perspectives of physicians who reported referring <25% versus ‡25% of their lung cancer patients for specialist palliative care using the chi-square test. We used logistic regression analysis, adjusting for gender, race/ethnicity, religious affiliation, specialty, and level of training, to identify factors associated with low referral rates. Potential predictors within the same domain of the questionnaire were assessed for colinearity. The best candidate predictors from each domain were carried forward into the multiple regression model. The selection of these variables was based on the distribution of physician responses, prior knowledge of the importance of the variable as a predictor of palliative care referrals, and the results of the correlation and the univariate analysis. The multiple regression model was built manually to determine odds ratios (ORs) for low referral rates with 95% confidence intervals (CIs). All analyses were carried out with SPSS statistical package (IBM, Chicago, IL). The institutional review boards (GCO#05-08343) at each site approved all components of this study and all subjects provided informed consent before research participation.
Annals of Oncology
original articles
Annals of Oncology
Table 1. Characteristics of lung cancer physicians by reported rate of referral to palliative care Reported percentage of lung cancer patients referred to palliative care <25% (N = 75), n (%) ‡25% (N = 80), n (%)
Age (mean 6 SD), years Sex Male Female Race/ethnicitya White African–American Hispanic Asian Other race Religious affiliationb Yes No Provider training status Attending Fellow Physician specialty Oncologyc Pulmonary Internists
40 6 11
41 6 12
0.58
49 (65) 26 (35)
33 (41) 47 (59)
<0.0001
43 1 5 17 4
32 4 14 18 3
(61) (2) (7) (24) (6)
P value
(45) (6) (20) (25) (4)
0.04
46 (61) 29 (39)
50 (62) 30 (38)
0.88
48 (64) 27 (36)
36 (45) 44 (55)
0.02
27 (36) 25 (33) 23 (31)
19 (24) 26 (32) 35 (44)
0.62
a
N = 70. Includes physicians reporting Protestant, Catholic, Jewish, Buddhist, Hindu, or Muslim religious affiliation. c Oncology specialists include medical (70%), surgical (17%), and radiation (13%) oncologists. SD, standard deviation. b
Whereas physicians may be concerned that involvement of palliative care consultants would engender fear that death is approaching, recent research suggests that early integration of palliative care in lung cancer management is actually associated with longer survival as well as a range of other favorable outcomes. Temel et al. [9] found that ambulatory patients with advanced-stage lung cancer who were randomly assigned to receive early palliative care had improved quality of life and lower rates of depressive symptoms, as compared with those receiving standard oncologic care. In addition, although patients in the early palliative care group had reduced chemotherapy and longer hospice care, they survived longer. These findings add to a growing body of evidence establishing the value of specialized palliative care throughout the trajectory of lung cancer, other malignancies, and other serious and complex illnesses. They also demonstrate the feasibility and effectiveness of concurrent delivery of palliative care with disease-directed treatment [21, 22]. The early integration of palliative care for patients with lung cancer is particularly important given the heavy symptom burden that is associated with this disease [3]. Even those with curable lung cancer often experience distressing symptoms and both they and their families have a range of important palliative care needs [23]. Several limitations of this study deserve mention. First, all the physicians we surveyed were affiliated with large medical centers in New York City that have well-established palliative care programs. Our results may not be generalizable to other regions or to physicians who care primarily for outpatients in
Volume 23 | No. 2 | February 2012
community settings, although we included a diverse group of physicians across different hospitals including voluntary physicians who spend more time in office-based practice than in the hospital. Secondly, we relied on the respondents’ selfreports of their referral practices rather than directly observing them or verifying referrals by other methods. Since almost half of the physicians in our study reported low rates, however, it is unlikely that they overestimated their referrals, which would be the expected direction of self-reporting bias in this context. Thirdly, this study focused specifically on palliative care referral for patients with lung cancer and may not reflect physicians’ practices and perspectives on integration of specialist palliative care in the treatment of patients with other cancers or nonmalignant diseases. Of all respondents, eight were surgeons. While surgeons typically see primarily patients with early-stage lung cancer, palliative care should be offered throughout the trajectory of illness including those with potentially curable disease. Palliative care is not limited to end-of-life or hospice care and is appropriate for all patients with serious and complex illness.
conclusions Integration of specialized palliative care in comprehensive lung cancer care throughout the continuum of this disease is supported by compelling evidence and consensus of professional opinion for all patients, including those pursuing disease-modifying and life-prolonging treatments. As the number of palliative care programs and specialists continues to
doi:10.1093/annonc/mdr345 | 385
Downloaded from http://annonc.oxfordjournals.org/ at Robertson Library University of prince Edward Island on July 12, 2015
Characteristic
original articles
Annals of Oncology
Table 2. Univariate predictors of palliative care referral Domain
386 | Smith et al.
P value
16 84
11 89
0.39
9 91
9 91
0.90
25 75
14 86
0.05
24 76
16 84
0.23
79 21
81 19
0.69
56 44
84 16
<0.0001
77 23
89 11
0.05
15 85
5 95
0.04
36 65
18 82
0.02
77 23
88 12
0.09
84 16
79 21
0.40
80 20
86 14
0.30
82 18
89 11
0.39
71 29
59 41
0.10
13 87
5 95
0.07
15 85
14 86
0.87
43 57
34 66
0.25
Volume 23 | No. 2 | February 2012
Downloaded from http://annonc.oxfordjournals.org/ at Robertson Library University of prince Edward Island on July 12, 2015
Level of care in relation to disease status and prognosis Hesitate to refer as patient will be less likely to get disease-modifying treatment Agree Disagree Hesitate to refer unless death is imminent Agree Disagree Hesitate to refer because patients want to focus on curative therapies Agree Disagree Hesitate to refer because there is so much uncertainty about prognosis Agree Disagree Inclined to refer patients with more advanced disease Agree Disagree Communication with patients and families Inclined to refer as palliative care has more time to discuss complex issues Agree Disagree Inclined to refer because palliative care is helpful establishing goals of care Agree Disagree Hesitate to refer because patients do not want to discuss prognosis Agree Disagree Hesitate as patients and families are alarmed by the mention of palliative care Agree Disagree Patient management Inclined to refer as palliative care helps manage patients’ physical symptoms Agree Disagree Inclined to refer as palliative care is helpful in managing analgesic side-effects Agree Disagree Inclined to refer as palliative care can help with emotional symptoms Agree Disagree Inclined to refer because palliative care can help address spiritual concerns Agree Disagree Incline to refer because palliative care can decrease hospital length of stay Agree Disagree Role of the primary physician and availability of palliative care Hesitate to refer because the primary physician becomes less important Agree Disagree I don’t need to refer as I am able to address palliative needs on my own Agree Disagree Hesitate to refer because palliative care is not routinely available Agree Disagree
Reported percentage of lung cancer patients referred to palliative care <25% ‡25%
original articles
Annals of Oncology
Table 3. Multivariate predictors of palliative care referral Variable
1.09 1.84 0.48 0.75
0.50–2.37 0.86–3.94 0.22–1.05 0.31–1.86
1.59
0.74–3.42
1.30
0.37–2.13
0.45
0.21–0.98
3.07
1.56–6.02
a
Odds for low rates of referral to palliative care consultation.
increase, it will be important to ensure timely access to this care for lung cancer patients, their families, and others facing serious and complex illness. Insights about perspectives of referring physicians, who largely control access to palliative care, can inform ongoing efforts to achieve this goal.
funding American Cancer Society (PEP2-114269 to JEN, RSGT-07-16201-CPHPS to JPW); National Institute on Aging (AG034234 to JEN); National Cancer Institute (R01CA131348 to CBS); GlaxoSmithKline to JPW.
disclosure JPW is a member of the research board of EHC International and has received lecture fees from Novartis Pharmaceuticals. The remaining authors have no relevant relationships to disclose. The funder had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; and preparation, review, or approval of the manuscript.
references 1. Nesbitt JC, Putnam JB Jr, Walsh GL et al. Survival in early-stage non-small cell lung cancer. Ann Thorac Surg 1995; 60: 466–472. 2. Williams DE, Pairolero PC, Davis CS et al. Survival of patients surgically treated for stage I lung cancer. J Thorac Cardiovasc Surg 1981; 82: 70–76. 3. Cooley ME. Symptoms in adults with lung cancer. A systematic research review. J Pain Symptom Manage 2000; 19: 137–153.
Volume 23 | No. 2 | February 2012
doi:10.1093/annonc/mdr345 | 387
Downloaded from http://annonc.oxfordjournals.org/ at Robertson Library University of prince Edward Island on July 12, 2015
Physician characteristics White Female Attending Oncology providers Physicians attitudes toward palliative care Patients want to focus on curative therapies Patients do not want to discuss prognosis Patients and families are alarmed by the mention of palliative care Palliative care has more time to discuss complex issues
Odds ratioa 95% confidence interval
4. Murray SA, Kendall M, Boyd K et al. Archetypal trajectories of social, psychological, and spiritual wellbeing and distress in family care givers of patients with lung cancer: secondary analysis of serial qualitative interviews. BMJ 2010; 340: c2581. 5. Ellershaw JE, Peat SJ, Boys LC. Assessing the effectiveness of a hospital palliative care team. Palliat Med 1995; 9: 145–152. 6. Morrison RS, Penrod JD, Cassel JB et al. Cost savings associated with US hospital palliative care consultation programs. Arch Intern Med 2008; 168: 1783–1790. 7. Ringdal GI, Jordhoy MS, Kaasa S. Family satisfaction with end-of-life care for cancer patients in a cluster randomized trial. J Pain Symptom Manage 2002; 24: 53–63. 8. Manfredi PL, Morrison RS, Morris J et al. Palliative care consultations: how do they impact the care of hospitalized patients? J Pain Symptom Manage 2000; 20: 166–173. 9. Temel JS, Greer JA, Muzikansky A et al. Early palliative care for patients with metastatic non-small-cell lung cancer. N Engl J Med 2010; 363: 733–742. 10. Ferris FD, Bruera E, Cherny N et al. Palliative cancer care a decade later: accomplishments, the need, next steps—from the American Society of Clinical Oncology. J Clin Oncol 2009; 27: 3052–3058. 11. Levy MH, Back A, Benedetti C et al. NCCN clinical practice guidelines in oncology: palliative care. J Natl Compr Canc Netw 2009; 7: 436–473. 12. Foley KM, Gelband H. Improving Palliative Care for Cancer: Summary and Recommendations. Washington, DC: Institute of Medicine 2001. 13. World Health Organization. Pain relief and palliative care. In National Cancer Control Programmes: Policies and Managerial Guidelines, 2nd edition. Geneva, Switzerland: World Health Organization 2002; 83–91. 14. Osta BE, Palmer JL, Paraskevopoulos T et al. Interval between first palliative care consult and death in patients diagnosed with advanced cancer at a comprehensive cancer center. J Palliat Med 2008; 11: 51–57. 15. Reville B, Miller MN, Toner RW, Reifsnyder J. End-of-life care for hospitalized patients with lung cancer: utilization of a palliative care service. J Palliat Med 2010; 13: 1261–1266. 16. Ward AM, Agar M, Koczwara B. Collaborating or co-existing: a survey of attitudes of medical oncologists toward specialist palliative care. Palliat Med 2009; 23: 698–707. 17. Cherny NI, Catane R. Attitudes of medical oncologists toward palliative care for patients with advanced and incurable cancer: report on a survey by the European Society of Medical Oncology Taskforce on Palliative and Supportive Care. Cancer 2003; 98: 2502–2510. 18. Snow CE, Varela BR, Pardi DA et al. Identifying factors affecting utilization of an inpatient palliative care service: a physician survey. J Palliat Med 2009; 12: 231–237. 19. Wright AA, Zhang B, Ray A et al. Associations between end-of-life discussions, patient mental health, medical care near death, and caregiver bereavement adjustment. JAMA 2008; 300: 1665–1673. 20. Apatira L, Boyd EA, Malvar G et al. Hope, truth, and preparing for death: perspectives of surrogate decision makers. Ann Intern Med 2008; 149: 861–868. 21. Bakitas M, Lyons KD, Hegel MT et al. Effects of a palliative care intervention on clinical outcomes in patients with advanced cancer: the Project ENABLE II randomized controlled trial. JAMA 2009; 302: 741–749. 22. Stephen RC, Bruce P, Kathryn F et al. Comparing hospice and nonhospice patient survival among patients who die within a three-year window. J Pain Symptom Manage 2007; 33: 238–246. 23. Nelson JE, Gay EB, Berman AR et al. Patients rate physician communication about lung cancer. Cancer 2011; April 14 [Epub ahead of print].
Annals of Oncology
Lung cancer physicians’ referral practices for palliative care consultation C. B. Smith1,2*, J. E. Nelson2,3, A. R. Berman4, C. A. Powell5, J. Fleischman6, J. Salazar-Schicchi7 & J. P. Wisnivesky3,8 1 Division of Hematology/Oncology, Tisch Cancer Institute; 2Hertzberg Palliative Care Institute of the Brookdale Department of Geriatrics and Palliative Medicine; 3Division of Pulmonary, Critical Care and Sleep Medicine, Department of Medicine, Mount Sinai School of Medicine, New York; 4Division of Pulmonary and Critical Care Medicine, Montefiore Medical Center, Bronx; 5Division of Pulmonary and Critical Care Medicine, New York-Presbyterian Hospital, New York; 6Division of Pulmonary and Critical Care Medicine, Queens Hospital Center, Jamaica; 7Division of Pulmonary and Critical Care Medicine, Harlem Hospital Center, Harlem; 8Division of General Internal Medicine, Department of Medicine, Mount Sinai School of Medicine, New York USA
Received 23 March 2011; revised 14 June 2011; accepted 15 June 2011
Background: Integration of palliative care with standard oncologic care improves quality of life and survival of lung cancer patients. We surveyed physicians to identify factors influencing their decisions for referral to palliative care.
Methods: We provided a self-administered questionnaire to physicians caring for lung cancer patients at five medical centers. The questionnaire asked about practices and views with respect to palliative care referral. We used multiple regression analysis to identify predictors of low referral rates (<25%). Results: Of 155 physicians who returned survey responses, 75 (48%) reported referring <25% of patients for palliative care consultation. Multivariate analysis, controlling for provider characteristics, found that low referral
*Correspondence to: Dr C. B. Smith, One Gustave L. Levy Place, Box 1079, New York, NY 10029, USA. Tel: +1-212-241-8149; Fax: +1-212-659-5599; E-mail: [email protected]
ª The Author 2011. Published by Oxford University Press on behalf of the European Society for Medical Oncology. All rights reserved. For permissions, please email: [email protected]
Downloaded from http://annonc.oxfordjournals.org/ at Robertson Library University of prince Edward Island on July 12, 2015
Annals of Oncology 23: 382–387, 2012 doi:10.1093/annonc/mdr345 Published online 29 July 2011
original articles
Annals of Oncology
rates were associated with physicians’ concerns that palliative care referral would alarm patients and families [odds ratio (OR) 0.45, 95% confidence interval (CI) 0.21–0.98], while the belief that palliative care specialists have more time to discuss complex issues (OR 3.07, 95% CI 1.56–6.02) was associated with higher rates of referral. Conclusions: Although palliative care consultation is increasingly available and recommended throughout the trajectory of lung cancer, our data indicate it is underutilized. Understanding factors influencing decisions to refer can be used to improve integration of palliative care as part of lung cancer management. Key words: lung cancer, palliative care, physician, survey
methods
Lung cancer patients across all stages, including those pursuing aggressive disease-directed therapies, face substantial rates of morbidity and mortality. The risk of death from disease progression exceeds 30% for patients with early-stage disease and is >90% for those diagnosed with advanced disease [1, 2]. Symptom burden from standard treatments such as surgical resection, chemotherapy, and radiation therapy, as well as from the disease itself, is often significant. In a systematic review of the literature, patients with lung cancer were found to have multiple physical and psychological symptoms throughout the trajectory of the disease [3]. The literature also suggests that lung cancer patients have more distressing symptoms than other cancer patients of similar stage [3] and that significant stresses are experienced by their families [4]. The value of integrating expert palliative care, including symptom management, psychosocial support, communication, complex decision making, and transition planning, in oncologic management of lung cancer patients and their families is well documented. Benefits of consultation by palliative care specialists include improved symptom control [5], clearer understanding of diagnosis and prognosis [5], more efficient utilization of health care resources [6], and greater patient and family satisfaction [5–8]. In a recent randomized controlled trial, early integration of palliative care with standard oncologic care for ambulatory patients with stage IV lung cancer was associated not only with improvements in quality of life and mood but also with longer survival [9]. Based on these data, clinical guidelines recommend routine integration of palliative care as part of comprehensive lung cancer care from the time of diagnosis, even for patients pursuing cure-oriented or life-prolonging therapies [10–13]. Over the past decade, the availability of palliative care consultation services has increased dramatically in developed countries. However, existing evidence indicates that referral of patients with lung cancer and other malignancies for palliative care is infrequent and delayed until after discontinuation of disease-directed treatment [14, 15]. This pattern of referral undermines access to and effectiveness of palliative care for lung cancer patients and their families. There is limited information about factors influencing palliative care referral decisions by physicians, who make the vast majority of these referrals. In this study, conducted at five hospitals with established palliative care consultation services, we sought a better understanding of the factors influencing lung cancer physicians’ decisions to refer their patients to experts in palliative care.
physician sample and survey administration
Volume 23 | No. 2 | February 2012
The study population consisted of attending physicians and fellows caring for lung cancer patients at five hospitals located in New York City. From the hospitals’ staff lists, we identified physicians in pulmonary disease; hospital medicine; and medical, surgical, and/or radiation oncology who were known to care regularly for lung cancer patients. Following informed consent, physicians were given a self-administered survey. Physicians who did not respond to an initial contact to discuss study participation or who agreed to participate but did not return the completed survey were recontacted up to two more times, after which they were deemed to be nonresponders.
study sites The study hospitals were the following: Mount Sinai Hospital, Montefiore Hospital, New York-Presbyterian Hospital, Harlem Hospital, and Queens Hospital. Mount Sinai, Montefiore, and New York-Presbyterian are large, not-for-profit, teaching hospitals with 1100, 1200, and 740 beds, respectively. Harlem Hospital and Queens Hospital are city hospitals with 286 and 200 beds, respectively. These hospitals provide medical and surgical care for patients with lung cancer in inpatient and ambulatory settings. All sites have established interdisciplinary palliative care consultation services that include physicians; advanced practice nurses; and social work, mental health, and pastoral care professionals.
survey instrument To identify potential domains of interest for our survey, we conducted a review of literature examining clinicians’ attitudes toward ‘palliative care’, ‘supportive care’, and ‘end-of-life care’. We also obtained input on content from five nationally recognized experts in oncology, cancer health services research, and/ or palliative medicine. After pilot testing with 10 lung cancer physicians, we refined the survey to clarify items and minimize respondent burden. The final survey assessed physicians’ beliefs and attitudes toward palliative care in the following categories: (i) level of care in relation to disease status and prognosis; (ii) communication with patients and families; (iii) patient management; and (iv) the role of the primary physician and availability of palliative care. Physicians were asked to indicate their level of agreement on a 4-point scale (strongly agree, agree, disagree, strongly disagree) with statements about why they are inclined, hesitant, or don’t need to refer lung cancer patients to a palliative care specialist; for analyses, we collapsed into two categories the ‘agree’ and ‘strongly agree’ responses and ‘disagree’ and ‘strongly disagree’ responses. In addition, the survey asked physicians to report the percentage of lung cancer patients referred for palliative care consultation during the prior year (<25%, 25%–50%, 51%–75%, or 76%– 100%); we classified physicians who reported referring <25% of their patients for such consultation as having a ‘low referral’ pattern. The survey also collected information about the physician’s sociodemographic characteristics (age, gender, race/ethnicity), religious preference, year of graduation from medical school, and current level of training.
doi:10.1093/annonc/mdr345 | 383
Downloaded from http://annonc.oxfordjournals.org/ at Robertson Library University of prince Edward Island on July 12, 2015
introduction
original articles statistical analysis
results Of 198 eligible physicians who were offered participation at the five institutions, 155 (78%) returned completed surveys. Overall, 75 (48%) providers reported referring <25% of their lung cancer patients for palliative care consultation. Baseline characteristics of physicians in the two groups based on referral rates (<25% or ‡25%) are reported in Table 1. There was no difference between these groups in age distribution (P = 0.58), religious affiliation (P = 0.88), or physician specialty (P = 0.62). Those who referred <25% of lung cancer patients for palliative care consultation were more likely to be male (P < 0.0001) and white (P = 0.04) and to be attending physicians (P = 0.02) rather than trainees. As shown in Table 2, univariate analysis revealed that low referral rates were associated with physicians’ beliefs that patients and families would be alarmed by the mention of palliative care (P = 0.02), that patients prefer to focus on curative rather than palliative therapies (P = 0.05), and that patients do not want to discuss prognosis (P = 0.04). Conversely, physicians referring more frequently were more likely to believe that palliative care specialists can spend more time discussing complex issues (P < 0.0001) and are helpful in establishing goals of care (P = 0.049). In multiple regression analysis (Table 3), adjusting for sociodemographic characteristics, physicians’ belief that referral for palliative care consultation would alarm patients and families was a significant predictor of low referral (OR 0.45, 95% CI 0.21–0.98), while the belief that palliative care specialists spend more time discussing complex issues was a significant predictor (OR 3.07, 95% CI 1.56–6.02) of more frequent referral.
discussion In this survey of a diverse group of >150 physicians who regularly provide lung cancer care at five New York City hospitals with well-established palliative care programs, half of the respondents reported referring <25% of their lung cancer patients for palliative care consultation. Among these physicians, reluctance to refer was explained mainly by their
384 | Smith et al.
concern that involvement of a palliative care specialist would alarm patients and families posed a significant barrier to referral for palliative care consultation. Conversely, physicians valuing the time devoted by palliative care specialists to discussion of complex issues were more likely to engage these specialists for expert assistance in caring for their patients with lung cancer. Our study contributes new evidence that can help target efforts to achieve wider and more timely access for lung cancer patients and their families to expert palliative care. Previous surveys conducted in other countries have examined physician practices and attitudes with respect to palliative care consultation among patients with cancer in general or other chronic conditions [16, 17]. A survey in Australia focused on medical oncologists, who reported frequent collaboration with palliative care specialists in management of cancer patients, even though the vast majority of these oncologists viewed their own training in palliative care as adequate [16]. Although many of the respondents believed that patients and families were reluctant to involve palliative care specialists, few saw this as a major barrier for referral of their patients. A survey of physicians in the European Society of Medical Oncology revealed that most physicians felt confident about their own knowledge and skills for meeting patients’ palliative care needs, while 35% of the respondents reported frequent collaboration with palliative care specialists [17]. In the United States, Snow et al. [18] surveyed 74 physicians in selected divisions within the department of medicine of a single tertiary-care hospital about barriers to referral of patients with any advanced disease (including but not limited to cancer) to the hospital’s inpatient palliative care service. Most physicians acknowledged a lack of expertise in management of distressing symptoms and agreed that a multidisciplinary approach might benefit patients with advanced disease; the most important barriers to referral were unrealistic expectations on the part of patients and families and lack of familiarity with this service. Our study extends prior research by surveying physicians across multiple institutions and specifically focusing lung cancer patients, who are known to benefit from early integration of palliative care. Among physicians we surveyed, reluctance to refer for palliative care consultation was significantly associated with the belief that referral would alarm lung cancer patients and their families. While it is possible that physicians in our study or others have anecdotally met with this response in clinical practice, no convincing evidence exists in the literature that patients or families typically respond with anxiety, fear, or other negative emotions or resistance to the suggestion that they might benefit from the input of a palliative care expert. Physicians have similarly been concerned that discussions of unfavorable prognosis and of preferences for end-of-life care would be harmful to patients and families. Yet research continues to show that such communication does not increase psychological distress but instead promotes acceptance of the gravity of the illness, preference for realistic goals of care, better quality of life as death approaches, and more successful coping for informal caregivers [19, 20]. Wider dissemination of this evidence may help to allay physician concerns that appear to serve as a barrier for delivery of expert palliative care to lung cancer patients and their families.
Volume 23 | No. 2 | February 2012
Downloaded from http://annonc.oxfordjournals.org/ at Robertson Library University of prince Edward Island on July 12, 2015
We compared the baseline characteristics and the perspectives of physicians who reported referring <25% versus ‡25% of their lung cancer patients for specialist palliative care using the chi-square test. We used logistic regression analysis, adjusting for gender, race/ethnicity, religious affiliation, specialty, and level of training, to identify factors associated with low referral rates. Potential predictors within the same domain of the questionnaire were assessed for colinearity. The best candidate predictors from each domain were carried forward into the multiple regression model. The selection of these variables was based on the distribution of physician responses, prior knowledge of the importance of the variable as a predictor of palliative care referrals, and the results of the correlation and the univariate analysis. The multiple regression model was built manually to determine odds ratios (ORs) for low referral rates with 95% confidence intervals (CIs). All analyses were carried out with SPSS statistical package (IBM, Chicago, IL). The institutional review boards (GCO#05-08343) at each site approved all components of this study and all subjects provided informed consent before research participation.
Annals of Oncology
original articles
Annals of Oncology
Table 1. Characteristics of lung cancer physicians by reported rate of referral to palliative care Reported percentage of lung cancer patients referred to palliative care <25% (N = 75), n (%) ‡25% (N = 80), n (%)
Age (mean 6 SD), years Sex Male Female Race/ethnicitya White African–American Hispanic Asian Other race Religious affiliationb Yes No Provider training status Attending Fellow Physician specialty Oncologyc Pulmonary Internists
40 6 11
41 6 12
0.58
49 (65) 26 (35)
33 (41) 47 (59)
<0.0001
43 1 5 17 4
32 4 14 18 3
(61) (2) (7) (24) (6)
P value
(45) (6) (20) (25) (4)
0.04
46 (61) 29 (39)
50 (62) 30 (38)
0.88
48 (64) 27 (36)
36 (45) 44 (55)
0.02
27 (36) 25 (33) 23 (31)
19 (24) 26 (32) 35 (44)
0.62
a
N = 70. Includes physicians reporting Protestant, Catholic, Jewish, Buddhist, Hindu, or Muslim religious affiliation. c Oncology specialists include medical (70%), surgical (17%), and radiation (13%) oncologists. SD, standard deviation. b
Whereas physicians may be concerned that involvement of palliative care consultants would engender fear that death is approaching, recent research suggests that early integration of palliative care in lung cancer management is actually associated with longer survival as well as a range of other favorable outcomes. Temel et al. [9] found that ambulatory patients with advanced-stage lung cancer who were randomly assigned to receive early palliative care had improved quality of life and lower rates of depressive symptoms, as compared with those receiving standard oncologic care. In addition, although patients in the early palliative care group had reduced chemotherapy and longer hospice care, they survived longer. These findings add to a growing body of evidence establishing the value of specialized palliative care throughout the trajectory of lung cancer, other malignancies, and other serious and complex illnesses. They also demonstrate the feasibility and effectiveness of concurrent delivery of palliative care with disease-directed treatment [21, 22]. The early integration of palliative care for patients with lung cancer is particularly important given the heavy symptom burden that is associated with this disease [3]. Even those with curable lung cancer often experience distressing symptoms and both they and their families have a range of important palliative care needs [23]. Several limitations of this study deserve mention. First, all the physicians we surveyed were affiliated with large medical centers in New York City that have well-established palliative care programs. Our results may not be generalizable to other regions or to physicians who care primarily for outpatients in
Volume 23 | No. 2 | February 2012
community settings, although we included a diverse group of physicians across different hospitals including voluntary physicians who spend more time in office-based practice than in the hospital. Secondly, we relied on the respondents’ selfreports of their referral practices rather than directly observing them or verifying referrals by other methods. Since almost half of the physicians in our study reported low rates, however, it is unlikely that they overestimated their referrals, which would be the expected direction of self-reporting bias in this context. Thirdly, this study focused specifically on palliative care referral for patients with lung cancer and may not reflect physicians’ practices and perspectives on integration of specialist palliative care in the treatment of patients with other cancers or nonmalignant diseases. Of all respondents, eight were surgeons. While surgeons typically see primarily patients with early-stage lung cancer, palliative care should be offered throughout the trajectory of illness including those with potentially curable disease. Palliative care is not limited to end-of-life or hospice care and is appropriate for all patients with serious and complex illness.
conclusions Integration of specialized palliative care in comprehensive lung cancer care throughout the continuum of this disease is supported by compelling evidence and consensus of professional opinion for all patients, including those pursuing disease-modifying and life-prolonging treatments. As the number of palliative care programs and specialists continues to
doi:10.1093/annonc/mdr345 | 385
Downloaded from http://annonc.oxfordjournals.org/ at Robertson Library University of prince Edward Island on July 12, 2015
Characteristic
original articles
Annals of Oncology
Table 2. Univariate predictors of palliative care referral Domain
386 | Smith et al.
P value
16 84
11 89
0.39
9 91
9 91
0.90
25 75
14 86
0.05
24 76
16 84
0.23
79 21
81 19
0.69
56 44
84 16
<0.0001
77 23
89 11
0.05
15 85
5 95
0.04
36 65
18 82
0.02
77 23
88 12
0.09
84 16
79 21
0.40
80 20
86 14
0.30
82 18
89 11
0.39
71 29
59 41
0.10
13 87
5 95
0.07
15 85
14 86
0.87
43 57
34 66
0.25
Volume 23 | No. 2 | February 2012
Downloaded from http://annonc.oxfordjournals.org/ at Robertson Library University of prince Edward Island on July 12, 2015
Level of care in relation to disease status and prognosis Hesitate to refer as patient will be less likely to get disease-modifying treatment Agree Disagree Hesitate to refer unless death is imminent Agree Disagree Hesitate to refer because patients want to focus on curative therapies Agree Disagree Hesitate to refer because there is so much uncertainty about prognosis Agree Disagree Inclined to refer patients with more advanced disease Agree Disagree Communication with patients and families Inclined to refer as palliative care has more time to discuss complex issues Agree Disagree Inclined to refer because palliative care is helpful establishing goals of care Agree Disagree Hesitate to refer because patients do not want to discuss prognosis Agree Disagree Hesitate as patients and families are alarmed by the mention of palliative care Agree Disagree Patient management Inclined to refer as palliative care helps manage patients’ physical symptoms Agree Disagree Inclined to refer as palliative care is helpful in managing analgesic side-effects Agree Disagree Inclined to refer as palliative care can help with emotional symptoms Agree Disagree Inclined to refer because palliative care can help address spiritual concerns Agree Disagree Incline to refer because palliative care can decrease hospital length of stay Agree Disagree Role of the primary physician and availability of palliative care Hesitate to refer because the primary physician becomes less important Agree Disagree I don’t need to refer as I am able to address palliative needs on my own Agree Disagree Hesitate to refer because palliative care is not routinely available Agree Disagree
Reported percentage of lung cancer patients referred to palliative care <25% ‡25%
original articles
Annals of Oncology
Table 3. Multivariate predictors of palliative care referral Variable
1.09 1.84 0.48 0.75
0.50–2.37 0.86–3.94 0.22–1.05 0.31–1.86
1.59
0.74–3.42
1.30
0.37–2.13
0.45
0.21–0.98
3.07
1.56–6.02
a
Odds for low rates of referral to palliative care consultation.
increase, it will be important to ensure timely access to this care for lung cancer patients, their families, and others facing serious and complex illness. Insights about perspectives of referring physicians, who largely control access to palliative care, can inform ongoing efforts to achieve this goal.
funding American Cancer Society (PEP2-114269 to JEN, RSGT-07-16201-CPHPS to JPW); National Institute on Aging (AG034234 to JEN); National Cancer Institute (R01CA131348 to CBS); GlaxoSmithKline to JPW.
disclosure JPW is a member of the research board of EHC International and has received lecture fees from Novartis Pharmaceuticals. The remaining authors have no relevant relationships to disclose. The funder had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; and preparation, review, or approval of the manuscript.
references 1. Nesbitt JC, Putnam JB Jr, Walsh GL et al. Survival in early-stage non-small cell lung cancer. Ann Thorac Surg 1995; 60: 466–472. 2. Williams DE, Pairolero PC, Davis CS et al. Survival of patients surgically treated for stage I lung cancer. J Thorac Cardiovasc Surg 1981; 82: 70–76. 3. Cooley ME. Symptoms in adults with lung cancer. A systematic research review. J Pain Symptom Manage 2000; 19: 137–153.
Volume 23 | No. 2 | February 2012
doi:10.1093/annonc/mdr345 | 387
Downloaded from http://annonc.oxfordjournals.org/ at Robertson Library University of prince Edward Island on July 12, 2015
Physician characteristics White Female Attending Oncology providers Physicians attitudes toward palliative care Patients want to focus on curative therapies Patients do not want to discuss prognosis Patients and families are alarmed by the mention of palliative care Palliative care has more time to discuss complex issues
Odds ratioa 95% confidence interval
4. Murray SA, Kendall M, Boyd K et al. Archetypal trajectories of social, psychological, and spiritual wellbeing and distress in family care givers of patients with lung cancer: secondary analysis of serial qualitative interviews. BMJ 2010; 340: c2581. 5. Ellershaw JE, Peat SJ, Boys LC. Assessing the effectiveness of a hospital palliative care team. Palliat Med 1995; 9: 145–152. 6. Morrison RS, Penrod JD, Cassel JB et al. Cost savings associated with US hospital palliative care consultation programs. Arch Intern Med 2008; 168: 1783–1790. 7. Ringdal GI, Jordhoy MS, Kaasa S. Family satisfaction with end-of-life care for cancer patients in a cluster randomized trial. J Pain Symptom Manage 2002; 24: 53–63. 8. Manfredi PL, Morrison RS, Morris J et al. Palliative care consultations: how do they impact the care of hospitalized patients? J Pain Symptom Manage 2000; 20: 166–173. 9. Temel JS, Greer JA, Muzikansky A et al. Early palliative care for patients with metastatic non-small-cell lung cancer. N Engl J Med 2010; 363: 733–742. 10. Ferris FD, Bruera E, Cherny N et al. Palliative cancer care a decade later: accomplishments, the need, next steps—from the American Society of Clinical Oncology. J Clin Oncol 2009; 27: 3052–3058. 11. Levy MH, Back A, Benedetti C et al. NCCN clinical practice guidelines in oncology: palliative care. J Natl Compr Canc Netw 2009; 7: 436–473. 12. Foley KM, Gelband H. Improving Palliative Care for Cancer: Summary and Recommendations. Washington, DC: Institute of Medicine 2001. 13. World Health Organization. Pain relief and palliative care. In National Cancer Control Programmes: Policies and Managerial Guidelines, 2nd edition. Geneva, Switzerland: World Health Organization 2002; 83–91. 14. Osta BE, Palmer JL, Paraskevopoulos T et al. Interval between first palliative care consult and death in patients diagnosed with advanced cancer at a comprehensive cancer center. J Palliat Med 2008; 11: 51–57. 15. Reville B, Miller MN, Toner RW, Reifsnyder J. End-of-life care for hospitalized patients with lung cancer: utilization of a palliative care service. J Palliat Med 2010; 13: 1261–1266. 16. Ward AM, Agar M, Koczwara B. Collaborating or co-existing: a survey of attitudes of medical oncologists toward specialist palliative care. Palliat Med 2009; 23: 698–707. 17. Cherny NI, Catane R. Attitudes of medical oncologists toward palliative care for patients with advanced and incurable cancer: report on a survey by the European Society of Medical Oncology Taskforce on Palliative and Supportive Care. Cancer 2003; 98: 2502–2510. 18. Snow CE, Varela BR, Pardi DA et al. Identifying factors affecting utilization of an inpatient palliative care service: a physician survey. J Palliat Med 2009; 12: 231–237. 19. Wright AA, Zhang B, Ray A et al. Associations between end-of-life discussions, patient mental health, medical care near death, and caregiver bereavement adjustment. JAMA 2008; 300: 1665–1673. 20. Apatira L, Boyd EA, Malvar G et al. Hope, truth, and preparing for death: perspectives of surrogate decision makers. Ann Intern Med 2008; 149: 861–868. 21. Bakitas M, Lyons KD, Hegel MT et al. Effects of a palliative care intervention on clinical outcomes in patients with advanced cancer: the Project ENABLE II randomized controlled trial. JAMA 2009; 302: 741–749. 22. Stephen RC, Bruce P, Kathryn F et al. Comparing hospice and nonhospice patient survival among patients who die within a three-year window. J Pain Symptom Manage 2007; 33: 238–246. 23. Nelson JE, Gay EB, Berman AR et al. Patients rate physician communication about lung cancer. Cancer 2011; April 14 [Epub ahead of print].