|
Advertisement |
|
|
||
 |
|
|||||
|
|||||
|
 |
||||||
|
||||||
|
||||||
|
© 2003 American Society for Clinical Oncology Are Older Cancer Patients Being Referred to Oncologists? A Mail Questionnaire of Ontario Primary Care Practitioners to Evaluate Their Referral Patterns
From the Princess Margaret Hospital and Toronto General Hospital, University Health Network, University of Toronto, Toronto, Canada. Address reprint requests to Lillian L. Siu, MD, Princess Margaret Hospital, University Health Network, Department of Medical Oncology and Hematology, 610 University Ave, Suite 5-210, Toronto, Ontario M5G 2M9, Canada; e-mail: lillian.siu{at}uhn.on.ca.
Purpose: Understanding why older patients are frequently underrepresented in cancer services use and clinical research may help to increase their participation in clinical trials and eventually result in better cancer care for this vulnerable population. Methods: To identify potential barriers that may prevent older cancer patients from being referred from a primary care physician (PCP) to an oncology specialist, a self-administered questionnaire was mailed to 9,312 PCPs throughout Ontario. Results: With a one-time mailing, 2,240 questionnaires were returned (response rate, 24%) of which 2,089 (93%) were assessable. Although 86% of respondents would refer most older patients with early-stage, potentially curable cancers to oncologists, only 65% would refer those with advanced-stage, potentially incurable cancers. The factors that most influence referral decisions of PCPs are patient’s desire to be referred (69%), type (54%) and stage (49%) of cancer, and severity of cancer symptoms (49%). Other factors including age do not seem to influence the referral decision. Approximately 9% of respondents found it difficult to refer older cancer patients to oncology specialists, with the most commonly cited barriers being the length of waiting lists, mandatory tissue diagnosis before referral, and the belief that oncologists seldom relate to PCPs. Conclusion: Most PCPs stated that they would refer all elderly patients with cancer to oncologists and that referral decisions were based mainly on patients’ wishes. Continued efforts are needed to overcome barriers in the referral process and to understand the perspectives of elderly patients to enhance their cancer care.
CANCER IS a disease primarily of the elderly and a major determinant of future cancer burden is the demographic phenomenon of the increasing proportion of elderly in our population. Within the next 30 years in the United States, the absolute number of cancers occurring in persons  65 years old is expected to double, and the number of cancer patients in the United States 85 years old is expected to increase by more than four-fold between 2000 and 2050.1 In Canada, 60,900 (45%) of new cases and 38,500 (59%) of cancer deaths occur in elderly patients 70 years or older.2 Despite these statistics, older patients are disproportionately underrepresented in many areas of cancer services use. Population-based studies in the United States, Europe, and Canada have consistently identified old age as a barrier to access for therapy, including surgery, radiotherapy, and chemotherapy in cancer patients.3–10 Interestingly, in an Ontario study, most of the decline in radiotherapy use observed with increasing age was explained by a decline in referral to cancer centers.5 Conversely, in a retrospective cohort study of the Surveillance, Epidemiology, and End Results data in the United States, age did not significantly influence the referral of lung cancer patients to oncologists. However, after patients were seen by oncologists, increasing age was associated with a lower likelihood of subsequently receiving chemotherapy.8
Examination of accrual rates to cancer treatment trials sponsored by the National Cancer Institute has consistently demonstrated an age-dependent phenomenon in the last decade.11–13 For almost all disease sites a striking imbalance was seen between the proportion of patients enrolled onto studies and the Surveillance, Epidemiology, and End Results incidence data for those patients Older patients with cancer are vulnerable to being inappropriately managed because of misconceptions about the safety and feasibility of potentially toxic therapy. They may or may not require interventions different from their younger counterparts and clinical trials can help elucidate this. For example, some studies suggest that for breast and lung cancers, given the same treatment regimen and dose-intensity, older patients have no increased toxicity and have similar survivals compared with those of younger patients.16–20 In contrast, other studies of patients with acute myeloid leukemia and non-Hodgkin’s lymphoma have shown increased toxicity, with poorer overall survivals in older patients versus younger patients.21–23 Not surprisingly, the toxicities and differences in overall survival are likely to be dependent on the type and dose-intensity of therapy, the type and stage of cancer, the underlying biology of the cancer, and differences in functional reserve of the different organ systems. Many treatment decisions can only be made appropriately when clinical trials addressing therapeutic dilemmas have been performed. Unfortunately, there is a lack of published clinical trial data in the older patient population. Given the exponential growth of the elderly population, the prevalence of cancer in older patients, and the need to optimize their disease control and quality of life, it is important to identify the barriers that may lead to a disparity in their health care. Potential barriers that may exist include attitudes of primary care physicians (PCPs) and specialists toward older patients, and the level of care they provide these patients; attitudes of the patients and their families toward cancer treatment; and the lack of clinical trials to provide good evidence-based information guiding treatment of older cancer patients. As the initial decision-making step in the healthcare process, PCPs play a vital role in the management algorithm. This questionnaire was therefore designed to evaluate their attitudes toward referring older patients with cancer throughout Ontario.
A self-administered questionnaire to identify existent and potential barriers to access for the diagnosis and management of cancer in older patients was mailed to 9,312 family doctors and general practitioners (PCPs collectively) in Ontario between June and August 2002. To encourage response, a stamped, self-addressed envelope and a brief letter describing the goals of the questionnaire were included with every questionnaire package. Respondents were offered the chance to enter into a drawing for a gift certificate in an attempt to maximize the response rate. The questionnaire was developed by completing an extensive literature review to identify factors that could influence access to cancer care by older patients. Using a modified Delphi approach, this list of items was reduced to a group of items that were included in the final questionnaire. Before administration, the questionnaire was pilot tested with a group of four family physicians to ensure the questionnaire was clear and had appropriate face validity, and to identify any additional items for inclusion. The questionnaire contained a total of 21 questions. Nineteen questions were multiple choice; three questions included a description of a clinical scenario and asked the clinicians to outline their management of these patients and what factors influenced their decisions (Appendix). Three central domains were addressed in the questionnaire including physician demographics, approach to selected clinical scenarios, and attitudes toward managing older patients with cancer. The questionnaire addressed possible barriers that may prevent the referral of older patients with cancer to an oncology specialist including a patient’s, family member’s, and/or physician’s attitudes toward cancer and cancer management; resources availability to facilitate referrals; and awareness of such referral resources. In particular, potential determinants of referral by PCPs of older cancer patients to cancer specialists were examined using three relevant clinical scenarios. Potential participants were identified using a comprehensive list (Southam Inc, Toronto, Ontario, Canada) of both family physicians and general practitioners registered with the College of Physicians and Surgeons of Ontario. There was no possible method to determine what proportion of clinicians was actively practicing primary care in the province. Two members of the research team independently entered the results of the questionnaire into a database. Data entry was manually checked for accuracy by random selection of 100 questionnaires to be verified between the source document and the database. Completion of the questionnaire was anonymous and no unique identifying features were included in the study database.
Summary statistics, such as the median, interquartile range, percentage, and frequency, were used to describe the participating physicians. Potential associations between demographics, approach to referral, and attitudes were investigated using Ethics approval for this project was obtained from the University Health Network Research Ethics Board.
With a single mailing, 2,240 surveys were returned (response rate, 24%), and 2,089 surveys (93%) were assessable. Many of the inassessable surveys returned were from physicians who were not in active clinical practice, had retired, or were working in a specialist field, in private insurance companies, or in governmental agencies. The number of actively practicing PCPs is unknown; it is hypothesized that many of the physicians who did not return surveys would be similarly inassessable, thus the true response rate as a proportion of actively practicing physicians is likely to be much higher than the stated 24%. Of the 100 random surveys reviewed by two investigators, the data entry error rate was found to be 0.352%.
The demographics of respondents are listed in Table 1
Beliefs and attitudes of PCPs are listed in Table 2  . Although 86% of respondents would refer most older patients with early-stage, potentially curable cancers to oncologists, only 65% would refer most older patients with advanced-stage, potentially incurable cancers. The factors that most influenced referral decisions of PCPs are patient’s desire to be referred (69%), type (54%) and stage (49%) of cancer, severity of cancer symptoms (49%), and level of comorbid factors (28%). Factors such as age (7.4%), accessibility of specialists (7.2%), social support (2.7%), socioeconomic status of the patient (0.3%), and education level (0.2%) do not seem to influence the referral decision. More than 90% of PCPs stated that they would be more influenced by patients’ well-being than their chronologic age when deciding whether to refer older patients with cancer to oncology specialists. Responses to the three example clinical scenarios to evaluate the potential determinants of referral by PCPs of older cancer patients to oncology specialists are described in the Appendix.
Most PCPs (59%) found it easy to refer older patients to oncology specialists, but 9% believed that oncology specialists are reluctant to accept such referrals (Table 3 ). The most commonly cited difficulties in making referrals included the length of waiting lists, oncologists’ desire to have a tissue diagnosis before referral, and the belief that oncologists seldom relate to PCPs. It was also believed by many specialists that older patients might be put on a lengthier waiting list by specialists if treatment benefit is believed to be minimal, and that PCPs do not want to "swamp the system with cases that may be only palliative." The most commonly described difficulty expressed by PCPs was that inadequate educational resources are available to help manage older cancer patients in Ontario. Many respondents believed that additional improvements to cancer therapy can be achieved by increasing continuing medical education among the PCPs to enhance their knowledge and comfort level in managing older patients with cancer.
Physicians practicing in rural or mixed areas were less likely to refer late-stage, potentially incurable cancer patients (57.0% v 72.1%; P < .001) than those practicing in urban areas (Table 4 ). These physicians were also more likely than physicians practicing in urban areas to use the patient’s wishes as the primary factor in deriving their referral decisions, along with logistics reasons and accessibility of specialists. Similarly, physicians practicing greater than 3 hours from a teaching hospital were less likely to refer late-stage, potentially incurable cancer patients (54.0% v 67.0%; P = .001), and were more likely to consider logistics and the availability of specialists in their referral decisions than those whose practices were within 3 hours from a teaching hospital. Physicians with an extra year of geriatric training were less likely to refer cancer patients to oncology specialists regardless of stage (77.3% v 87.1%, P = .015 for early stage; 43.2% v 66.9%, P < .001 for late stage), and also were more likely to base their referral decisions on the cancer type rather than patient’s desire, compared with those clinicians without additional training in geriatrics. Physicians who have been practicing longer were slightly less likely to refer cancer patients to oncology specialists regardless of stage (85.1% v 88.3%, P = .033 for early stage; 62.2% v 69.8%, P < .001 for late stage), and were less likely to base their referral decisions on patient’s desire or logistics than those who have been in practice for a shorter duration.
Characteristics of the respondents, including type of practice, additional training in geriatrics, length of time in clinical practice, and referral attitudes (Table 4  ), were entered in a multivariate logistic regression model to determine which factors were most predictive of decisions by PCPs to refer older cancer patients to oncologists (Table 5).
An effort was also made to identify if there were groups of physicians who found it most difficult to refer cancer patients (Table 6 ). Physicians who have been practicing for less than the median practice duration of respondents were more likely to indicate difficulties in referring older cancer patients (P = .004) than physicians who have been practicing beyond the median duration. Paradoxically, physicians practicing less than 3 hours away from a teaching hospital were more likely to indicate difficulties in referring older oncology patients (P = .025) than those practicing further away from a teaching hospital.
We completed the first province-wide questionnaire to address relevant issues and barriers implicated in the referral process of older patients with cancer from PCPs to oncology specialists. Factors that were considered as most relevant to this process by PCPs included patient’s desire to be referred, the type and stage of the cancer, the potential curability of the cancer, patient’s symptoms or overall well-being, and level of comorbid factors. Age, accessibility of specialists, social support, socioeconomic status, and education level did not seem to play a role in the decision process. The subgroup analyses conducted are speculative and hypothesis generating. Physicians practicing in rural or mixed areas, or those at a distance from a teaching hospital, were less likely to refer late-stage, potentially incurable cancer patients, and more likely than those practicing in urban areas to consider patient’s desire, logistics, and availability of oncology specialists in their referral decisions. Once the referral decision has been made, physicians practicing far away from a teaching hospital actually indicated greater ease in obtaining the referrals, suggesting that perhaps oncology specialists are more willing to accept these referrals given the geographic circumstances, or that the referral procedures are more efficient for the PCPs from more remote areas. Another possibility is that because of the more remote geographic location, PCPs practicing in rural or mixed areas are more selective in the patients whom they chose to refer, to prevent long travel for a consult that may not be necessary. Additional evaluation is needed to ensure that older patients who live in the more remote areas but who are interested in pursuing treatments, even among those with late-stage and potentially incurable malignancies, are offered the referral opportunities despite a possible geographic or logistical barrier. Improvements in physician and patient education regarding the existent therapeutic options and available resources, and creation of more outreach cancer treatment clinics to provide adequate care to those residing in remote areas are two examples of possible solutions to overcome this barrier. Physicians with extra training in geriatrics and those who have been in practice longer were also less likely than their counterparts to refer cancer patients regardless of tumor stage. These physicians were less likely to base their referral decisions on patient’s desire or logistics, but placed greater emphasis on the type of cancer than did their counterparts. One may hypothesize that both physicians who have been in practice for longer and those with extra geriatric training may feel more comfortable with their knowledge of cancer care and thereby base their referral decisions more on what they perceive treatment options to be. This triage process by PCPs with greater levels of comfort or experience may represent a useful screening to ensure appropriate referrals are made to oncology specialists. However, to maintain appropriate referral strategies, continued efforts are necessary to provide PCPs with evidence-based educational activities highlighting management of cancer. For the subgroups of PCPs that indicated difficulties in coordinating referrals of older patients to cancer specialists, such as those who have been in practice for less time and those whose practices are paradoxically closer to a teaching hospital, a more detailed exploration of existent barriers to the referral process is warranted. Comments from the respondents of our survey suggest that issues such as long waiting lists, difficulties in communication with oncologists, and oncologists’ reluctance to accept referrals without a tissue diagnosis can deter the referral process. Additional evaluation of these barriers may provide potential solutions to facilitate the referral procedures, such that the interactions between these PCPs and oncology specialists can be more effective. It is clear that there are many strengths to this study. First, although the true response rate is not known because some of the questionnaires were mailed to physicians no longer in clinical practice, on the basis of the demographics it seems that the respondents of our study are reflective of the views of a wide range of PCPs. Almost one fourth of the respondents had rural practices, the range of practice duration varied from less than 1 year to 58 years, and 40% of the respondents were female. These results suggest that the respondents represent diverse primary care practice conditions throughout Ontario, and are typical of those from a large Canadian province. Second, this study is the first survey reported in the literature identifying the potential barriers that influence referrals of older cancer patients by PCPs to oncology specialists. Results of our survey should complement other published studies addressing the underrepresentation of older patients in cancer services use and clinical research activity.11–15 Third, after identifying the main issues that are important to PCPs when referring older patients with cancer to oncology specialists, we can take steps to further define these barriers and ultimately propose interventions to overcome them. Practical examples of such next steps include establishing focus groups among PCPs from different practice settings to obtain a more complete understanding of the findings in this study, and conducting personalized interviews of older patients with and without cancer to gain insights into their perspectives. One of the weaknesses in the current study is the response rate of 24%. Because of the inability to determine the exact number of actively practicing PCPs in Ontario, the reported response rate is undoubtedly an underestimate. Other studies that involved large physician surveys in the United States and Canada have obtained response rates between 30% and 70%, with the studies conducted in the United States generally obtaining greater response rates than those conducted in Canada.24–29 Although the response rates of physician mail surveys published in the literature were higher than that obtained in our study, they were typically conducted among much smaller groups of physicians that possibly were selected using mailing lists of actively practicing physicians. In addition, the majority of the published studies performed multiple mailings to maximize their response rates. Only a single mailing was performed in our study because of the large sample size of our mailing list and the substantial absolute number of respondents (ie, 2,240).
Physicians who completed the questionnaires are likely to have interest in the subject, and therefore volunteer bias should be considered in the interpretation of the results. In addition, because this is a self-reported questionnaire, the results may not accurately reflect real-life decisions made by PCPs in their practices. For instance, most physicians reported that patient preference was the dominant factor driving their referral decisions. This may be the physicians’ idealistic intention but it is likely that in individualized cases, other factors may play an influential role, such as the difficulties of referral procedures or their own perceptions of available effective treatment options, among other factors. Lastly, the small differences in characteristics of PCPs that were found in some of the analyses, such as the referral patterns of early-stage patients by PCPs at variable distances from teaching hospitals (87% v 88%; Table 4 The main finding from this study is that patient preference is a major determinant in the referral decisions of PCPs. Hence, a better understanding of the attitudes of older patients toward cancer care and clinical trials will lead to more effective strategies about how best to remove barriers that result in the inequity of their cancer management. Older cancer patients are encouraged to ask their doctors about the standard of care for their type and stage of cancer, regardless of their age, and inquiries should be made about their eligibility for standard treatments or for clinical trials. In addition, PCPs need more information about making appropriate referrals to oncologists, given that one of the potential referral barriers is that PCPs might not have been aware of available treatment options (including clinical trials) to offer older cancer patients. By enhancing the decision-making abilities of both the PCPs and the older cancer patients, the goals of providing appropriate cancer care to this vulnerable population and increasing their accrual to clinical trials will ultimately be achieved.
The authors indicated no potential conflicts of interest.
Presented in part at the 39th Annual Meeting of the American Society of Clinical Oncology, Chicago, IL, May 31 to June 3, 2003. Support for S.E.S. is funded by a Career Scientist Award from the Ontario Ministry of Health and Long-Term Care, and by a Career Award from the Knowledge Translation Program at the University of Toronto.
1. Kornblith AB, Kemeny M, Peterson BL, et al: Survey of oncologists’ perceptions of barriers to accrual of older patients with breast carcinoma to clinical trials. Cancer 95:989–996, 2002[CrossRef][Medline] 2. National Cancer Institute of Canada: Canadian Cancer Statistics, 2001, Toronto, Canada 3. Mor V, Masterson-Allen S, Goldberg RJ, et al: Relationship between age at diagnosis and treatments received by cancer patients. J Am Geriatr Soc 33:585–589, 1985[Medline] 4. Greemberg ER, Chute CG, Stukel T, et al: Social and economic factors in the choice of lung cancer treatment. N Engl J Med 318:612–617, 1988[Abstract] 5. Tyldesley S, Zhang-Salomons J, Groom PA, et al: Association between age and the utilization of radiotherapy in Ontario. Int J Radiat Oncol Biol Phys 47:469–480, 2000[CrossRef][Medline] 6. Huang J, Zhou S, Groome P, et al: Factors affecting the use of palliative radiotherapy in Ontario. J Clin Oncol 19:137–144, 2001 7. Paszat L, Laperriere N, Groome P, et al: A population-based study of glioblastoma multiforme. Int J Radiat Oncol Biol Phys 51:100–107, 2001[Medline] 8. Earle CC, Neumann PJ, Gelber RD, et al: Impact of referral patterns on the use of chemotherapy for lung cancer. J Clin Oncol 20:1786–1792, 2002 9. Easson AM, Cotterchio M, Crosby JA, et al: A population-based study of the extent of surgical resection of potentially curable colon cancer. Ann Surg Oncol 9:380–387, 2002 10. Vercelli M, Quaglia A, Casella C, et al: Relative survival in elderly cancer patients in Europe. Eur J Cancer 34:2264–2270, 1998[CrossRef][Medline] 11. Tejeda HA, Green SB, Trimble EL, et al: Representation of African-Americans, Hispanics, and whites in National Cancer Institute cancer treatment trials. J Natl Cancer Inst 88:812–816, 1996 12. Trimble EL, Carter CL, Cain D, et al: Representation of older patients in cancer treatment trials. Cancer 74:2208–2214, 1994 (suppl)[CrossRef][Medline] 13. Lewis JH, Kilgore ML, Goldman DP, et al: Participation of patients 65 years of age or older in cancer clinical trials. J Clin Oncol 21:1383–1389, 2003 14. Hutchins LF, Unger JM, Crowley JJ, et al: Underrepresentation of patients 65 years of age or older in cancer-treatment trials. N Engl J Med 341:2061–2067, 1999 15. Yee K, Pater JL, Pho L, et al: Enrollment of elderly patients in cancer treatment trials in Canada: Why is age a barrier? J Clin Oncol 21:1618–1623, 2003 16. Begg CB, Cohen JL, Ellerton J: Are the elderly predisposed to toxicity from cancer chemotherapy? An investigation using data from the Eastern Cooperative Oncology Group. Cancer Clin Trials 3:369–374, 1980[Medline] 17. Christman K, Muss HB, Case LD, et al: Chemotherapy of metastatic breast cancer in the elderly: The Piedmont Oncology Association experience. JAMA 268:57–62, 1992[Abstract] 18. Giovanazzi-Banon S, Rademaker A, Lai G, et al: Treatment tolerance of elderly cancer patients entered onto phase II clinical trials: An Illinois Cancer Center study. J Clin Oncol 12:2447–2452, 1994 19. Siu LL, Shepherd FA, Murray N, et al: Influence of age on the treatment of limited-stage small-cell lung cancer. J Clin Oncol 14:821–828, 1996 20. Chen H, Cantor A, Meyer J, et al: Can older patient’s tolerate chemotherapy? A prospective pilot study. Cancer 97:1107–1114, 2003[CrossRef][Medline] 21. Johnson PRE: Acute myeloid leukemia in the elderly: Biology and treatment. Br J Haematol 83:1–6, 1993[Medline] 22. Weick JK, Kopecky KJ, Appelbaum FR, et al: A randomized investigation of high-dose versus standard-dose cytosine arabinoside with daunorubicin in patients with previously untreated acute myeloid leukemia: A Southwest Oncology Group Study. Blood 88:2841–2851, 1996 23. Shipp MA, Harrington DP, Anderson JR, et al: A predictive model for aggressive non-Hodgkin’s lymphoma: The International Non-Hodgkin’s Lymphoma Prognostic Factors Project. N Engl J Med 329:987–994, 1993 24. Klabunde CN, Frame PS, Meadow A, et al: A national survey of primary care physicians’ colorectal cancer screening recommendations and practices. Prev Med 36:352–356, 2003[CrossRef][Medline] 25. Ubel PA, Jepson C, Baron J, et al: The influence of cost-effectiveness information on physicians’ cancer screening recommendations. Soc Sci Med 56:1727–1736, 2003[CrossRef][Medline] 26. Gramling R, Nash J, Siren K, et al: Predictive genetics in primary care: Expectations for the motivational impact of genetic testing affects the importance family physicians place on screening for familial cancer risk. Genet Med 5:172–175, 2003[Medline] 27. Carroll GRE, Goel VV, Orr VV, et al: Canadian family physicians and prostate cancer: A national survey. Can J Urol 6:892–897, 1999[Medline] 28. Wilson R, Godwin M, Seguin R, et al: End-stage renal disease: Factors affecting referral decisions by family physicians in Canada, the United States and Britain. Am J Kidney Dis 38:42–48, 2001[Medline] 29. Del Giudice ME, Sawka CA, Pritchard KI, et al: Hormone replacement therapy after breast cancer: Physicians’ attitudes towards randomized clinical trials. Breast Cancer Res Treat 79:213–223, 2003[CrossRef][Medline] Submitted June 17, 2003; accepted October 8, 2003. This article has been cited by other articles:
|
||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
|
|
|||||||||||
|
|||||||||||
|
|
Copyright © 2003 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
|
TOP
ABSTRACT
INTRODUCTION
2 tests and the Cochran-Armitage test for trend. Grouping of variables was performed for statistical purposes. A multivariate logistic regression model was constructed using a backward stepwise selection procedure to investigate which PCP characteristics and referral attitudes were predictive of the decision to refer. Because this was a descriptive analysis, no P value adjustments were done and P values of 
.05 were considered to be statistically significant. 
