Perceptions of Active Surveillance and Treatment Recommendations for Low-risk Prostate Cancer: Results from a National Survey of Radiation Oncologists and Urologists
Kim, Simon P. MD, MPH*; Gross, Cary P. MD†; Nguyen, Paul L. MD‡; Smaldone, Marc C. MD, MSPH§; Shah, Nilay D. PhD∥; Karnes, R. Jeffrey MD¶; Thompson, R. Houston MD¶; Han, Leona C. MBA#; Yu, James B. MD**; Trinh, Quoc D. MD††; Ziegenfuss, Jeanette Y. PhD‡‡; Sun, Maxine PhD§§; Tilburt, Jon C. MD, MPH∥∥
Departments of *Urology
†Internal Medicine, Cancer Outcomes, Public Policy and Effectiveness Research (COPPER) Center Yale University, New Haven, CT
‡Department of Radiation Oncology, Harvard Medical School, Brigham and Women’s Hospital, Boston, MA
§Department of Surgery, Fox Chase Cancer Center-Temple University Health System, Philadelphia, PA
∥Division of Health Care Policy & Research, Knowledge and Evaluation Research Unit
¶Department of Urology, Mayo Clinic, Rochester
#Division of Health Care Policy & Research, Mayo Clinic, Rochester, MN
**Department of Radiation Oncology, Cancer Outcomes, Public Policy, and Effectiveness Research Center (COPPER), Yale University, New Haven, CT
††Division of Urology, Harvard Medical School, Brigham and Women’s Hospital, Boston, MA
‡‡HealthPartners Institute for Education and Research, Minneapolis, MN
§§Cancer Prognostics and Health Outcomes, University of Montreal Health Center, Montreal, QC, Canada
∥∥Bioethics Research Unit, Knowledge and Evaluation Research Unit, Division of General Medicine, Mayo Clinic, Rochester, MN
Supplemental Digital Content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal's Website, www.lww-medicalcare.com.
Supported by the Robert Derzon Award from the Medical Decision Foundations, Boston, MA.
Presented at the 2012 Annual Meeting of the American Society of Clinical Oncology (ASCO), Chicago, IL.
C.P.G. reports being member of a scientific advisory board for FAIR Health Inc. and receiving research support from Medtronic Inc. to develop methods of clinical trial data sharing. The remaining authors declare no conflict of interest.
Reprints: Simon P. Kim, MD, MPH, Department of Urology, Cancer Outcomes, Public Policy, and Effectiveness Research Center (COPPER), Yale University, P.O. Box 208058, New Haven, CT 06519. E-mail: email@example.com.
Background: With the growing concerns about overtreatment in prostate cancer, the extent to which radiation oncologists and urologists perceive active surveillance (AS) as effective and recommend it to patients are unknown.
Objective: To assess opinions of radiation oncologists and urologists about their perceptions of AS and treatment recommendations for low-risk prostate cancer.
Research Design: National survey of specialists.
Participants: Radiation oncologists and urologists practicing in the United States.
Measures: A total of 1366 respondents were asked whether AS was effective and whether it was underused nationally, whether their patients were interested in AS, and treatment recommendations for low-risk prostate cancer. Pearson’s χ2 test and multivariate logistic regression were used to test for differences in physician perceptions on AS and treatment recommendations.
Results: Overall, 717 (52.5%) of physicians completed the survey with minimal differences between specialties (P=0.92). Although most physicians reported that AS is effective (71.9%) and underused in the United States (80.0%), 71.0% stated that their patients were not interested in AS. For low-risk prostate cancer, more physicians recommended radical prostatectomy (44.9%) or brachytherapy (35.4%); fewer endorsed AS (22.1%). On multivariable analysis, urologists were more likely to recommend surgery [odds ratio (OR): 4.19; P<0.001] and AS (OR: 2.55; P<0.001), but less likely to recommend brachytherapy (OR: 0.13; P<0.001) and external beam radiation therapy (OR: 0.11; P<0.001) compared with radiation oncologists.
Conclusions and Relevance: Most prostate cancer specialists in the United States believe AS effective and underused for low-risk prostate cancer, yet continue to recommend the primary treatments their specialties deliver.
Among the approximately 230,000 patients diagnosed with prostate cancer each year, most men present with clinically localized disease and can achieve long-term survival with radiation therapy or surgery.1–3 However, active surveillance (AS) has become an emerging disease management strategy for this common malignancy.4 Clinical guidelines recommend AS, which involves close monitoring for disease progression by serial prostate-specific antigen (PSA) testing, digital rectal examinations and prostate biopsies, as 1 treatment alternative for patients with low-risk disease (T1c, PSA: 4–10 ng/mL and Gleason 6).5,6 To address the growing concern of overtreatment, a recent NIH consensus statement on the role of AS for prostate cancer concluded that it should be offered to eligible patients with low-risk disease and that approximately 100,000 patients are eligible for such an approach annually.7 Yet, most patients are treated with radiation therapy or surgery with approximately 10% undergoing AS, despite the current guidelines and existing evidence.8–11 A recent Veterans Affairs study also reported that a majority of men with low-risk prostate cancer and multiple comorbidities were being overtreated with brachytherapy, radiation therapy, or surgery.12 Indeed, advanced treatment technology—intensity-modulated radiation therapy and robotic surgery—are being increasingly used among men who are least likely to benefit due to low-risk prostate cancer or limited life expectancy.13 As a consequence, treatment recommendations of radiation oncologists and urologists for low-risk prostate cancer bear particular relevance on the national use of AS.
Current perceptions of radiation oncologists and urologists on whether AS is effective and the degree to which it is recommended may represent key barriers to its greater adoption in clinical practice. Attitudes toward this conservative disease management approach from specialists who treat prostate cancer may contextualize the relatively low adoption of AS in the United States. Therefore, we performed a national survey of radiation oncologists and urologists to assess their perceptions regarding the effectiveness of AS, comfort with routinely recommending it to patients, and typical treatment recommendations for low-risk PC. We also aimed to ascertain the physician-reported rates of patients who choose AS in clinical practice, whether their patients are interested in it, and their perceptions about the appropriate national utilization of different primary treatments for localized prostate cancer in the United States.
Upon Institutional Review Board approval, we acquired a random sample of radiation oncologists and urologists from the American Medical Association (AMA) Physician Masterfile in June 2011. The survey sample was restricted to physicians who had completed their residency training, aged less than 65 years, primarily involved in patient care, and practicing in the United States.
Survey Questionnaire and Administration
A pilot questionnaire was developed to assess the perceptions and beliefs of radiation oncologists and urologists on emerging issues in the treatment of localized prostate cancer. The pilot survey instrument was initially tested in a random sample of 50 radiation oncologists and 50 urologists from a single mailing in July 2011. Items were then revised according to the responses in the pilot survey.
To assess for possible barriers in clinical practice, we conceptualized case presentations where AS would be considered an acceptable treatment option based on clinical guidelines.5,6 For the first clinical scenario, we presented a healthy 65-year-old patient diagnosed with low-risk prostate cancer based on the following clinical features: PSA 4–10 ng/mL, T1c, and Gleason 6. Respondents were queried about whether AS was effective as a disease management strategy and whether they felt comfortable routinely recommending AS in the clinical scenario (Appendix I, Supplemental Digital Content 1, http://links.lww.com/MLR/A728). Respondents could select from a 4-point Likert scale for each item, which was then dichotomized for the analysis.
The survey instrument also included items assessing physicians’ perceptions regarding the patterns of care for men with localized prostate cancer. Considering a clinical scenario similar to the initial case presentations, respondents were asked to report the percentage of patients (<5%; 5%–10%; 11%–15%; or >15%) who choose AS in their clinical practice (Appendix II, Supplemental Digital Content 2, http://links.lww.com/MLR/A729). In addition, the survey included items that assessed whether the national rates of AS, brachytherapy, external beam radiation therapy, and radical prostatectomy were being “overused,” “used at the right rate,” or “underused” in United States (Appendix III, Supplemental Digital Content 3, http://links.lww.com/MLR/A730).
The survey included a second case presentation of a healthy 60-year-old patient diagnosed with localized prostate cancer with normal functional outcomes and greater than 10-year life expectancy (Appendix IV, Supplemental Digital Content 4, http://links.lww.com/MLR/A731). Physicians were asked to select a treatment recommendation of AS, brachytherapy, external beam radiation therapy, radical prostatectomy, or primary androgen deprivation for this case presentation.
Study Implementation Process
From November 2011 to April 2012, the survey was mailed to a random sample of 1366 physicians (n=686 for radiation oncology; n=680 for urology) in the United States. Each eligible respondent was mailed a cover letter, survey, and a token cash incentive. Nonresponders were mailed a reminder letter and another copy of the survey questionnaire for 3 successive waves approximately every 6 weeks. Framing variables obtained from the survey and AMA Masterfile included physician demographics, practice setting (academic or community), compensation structure (billing or salary with/without bonus), number of physicians in practice and prostate cancer patients seen each week, and geographic region (northeast, midwest, south, or west).
Pearson’s χ2 test was used to assess for bivariate associations between physician specialty and perceptions of AS and treatment recommendations. We constructed multivariable logistic regression models to test for differences in treatment recommendations from the case presentation of a 60-year-old man with PSA 4–10 ng/mL, Gleason 6, and T1c prostate cancer, adjusting for physician characteristics, practice settings, compensation structure, geographic region, and specialty. A 2-sided P-value of ≤0.05 was used to determine statistical significance. Stata MP version 11.0 (College Station, TX) was used to perform all statistical analyses.
Characteristics of the respondents by physician specialty are shown in Table 1. Overall, 717 physicians returned the survey from the 1,366 eligible respondents (52.5%). Response rates were similar among radiation oncologists and urologists in our survey sample (52.6% vs. 52.3%; P=0.92). Relative to urologists, radiation oncologists differed in having a higher proportion who were younger, female, practicing in academic medical centers and larger physician groups, and reimbursed by a salaried compensation structure (all P<0.05). Radiation oncologists also tended to see a greater number of new prostate cancer patients per week than urologists (P=0.06).
Overall, 71.9% of physicians in the survey responded that AS was effective and 68.6% reported feeling comfortable routinely recommending it as a disease management strategy from the case presentation of 65-year-old diagnosed with low-risk prostate cancer. However, 71.0% of physicians responded that their patients were not interested in AS. Responses to these items differed markedly by physician specialty (Fig. 1A). For example, urologists were more likely to agree than radiation oncologists that AS is effective (75.5% vs. 65.7%; P<0.001), and to report comfort recommending it (75.8% vs. 61.7%; P<0.001) to low-risk prostate cancer patients. Conversely, more radiation oncologists stated that patients were not interested in AS as a treatment option compared with urologists (82.3% vs. 59.1%; P<0.001). Not surprisingly, these perceptions were accompanied by differences in reported management strategies: approximately a quarter of radiation oncologists stated that >10% of their patients are managed with AS compared with 40% of urologists in the survey sample (P<0.001; Fig. 1B).
Radiation oncologists and urologists also disagreed in their assessment of population-level underuse or overuse of different primary treatments (Fig. 2). Approximately 80% of physicians in each specialty stated that AS is underused in the United States. However, a higher proportion of radiation oncologists viewed that radical prostatectomy is overused in the United States than urologists (70.3% vs. 45.6%; P<0.001), whereas a higher proportion of urologists believed that brachytherapy (37.1% vs. 17.8%; P<0.001) and external beam radiation therapy (48.2% vs. 32.4%; P<0.001) are both overused nationally compared with radiation oncologists. Interestingly, a small percentage from both specialties viewed that most primary therapies for localized prostate cancer are underused. However, 43.4% and 20.6% of radiation oncologists believed that there is a national underuse of brachytherapy and external beam radiation therapy, respectively.
Despite a majority of physicians viewing AS as effective and underused, radiation oncologists and urologists consistently selected brachytherapy or surgery from the case presentation inquiring for treatment recommendations of a 60-year-old man diagnosed with low-risk prostate cancer (Fig. 3). Although a small minority of urologists endorsed brachytherapy (8.4%) or external beam radiation therapy (2.0%), radiation oncologists preferred brachytherapy (42.8%) as the treatment recommendation. Conversely, a markedly higher percentage of urologists chose radical prostatectomy compared with radiation oncologists (61.5% vs. 28.0%; P<0.001). More urologists also recommended AS relative to radiation oncologists from the case presentation (27.8% vs. 16.2%; P<0.001). On multivariable analysis adjusting for physician demographics, practice setting, compensation structure, and number of prostate cancer patients seen, urologists were more likely to recommend surgery [odds ratio (OR): 4.19; 95% confidence interval (CI), 2.99–5.89; P<0.001] and AS (OR: 2.55; 95% CI, 1.72–3.88; P<0.001), but less likely to recommend brachytherapy (OR: 0.13; 95% CI, 0.05–0.27; P<0.001) and external beam radiation therapy (OR: 0.11; 95% CI, 0.08–0.24; P<0.001) relative to radiation oncologists (Table 2). In addition, we also found that physicians practicing in academic medical centers had higher adjusted ORs for recommending AS compared with those practicing in the community setting (OR: 2.35; 95% CI, 1.42–3.89; P<0.001). The remaining physician characteristics were not associated across all treatment recommendations.
This national survey of prostate cancer specialists builds upon prior work in several ways. At a time when there is increasing concern about overtreatment, we found that a vast majority of radiation oncologists and urologists considered AS effective and felt comfortable recommending it to patients. However, our study suggests that both specialties may not be routinely recommending AS in favor of radiation therapy or surgery. This bears particular relevance as the use of AS has been associated with physician recommendations and the use of multidisciplinary care. For instance, Davison et al14 demonstrated that physician treatment recommendations strongly influenced whether appropriately selected patients received AS. Similarly, patients who were treated by physicians IN multidisciplinary clinics for prostate cancer were more likely to undergo AS.15
Our study evaluated if perceptions about AS for-low-risk prostate cancer may represent key barriers to its greater adoption in the United States. Our findings suggest that beliefs in the effectiveness of AS are not the main barrier to their use. These clinician perceptions are consistent with a growing amount of evidence that AS is reasonable approach in delaying treatment for those patients who progress and warrant treatment while minimizing the risk of overtreatment for those patients who have competing risks from other comorbidities greater than prostate cancer.4,10,11,16–23
Our study also provides important information about the perceptions of specialists about the state of prostate cancer treatment. The patterns of self-reported recommendations in this study mirror national trends documenting that most patients receive some form of primary therapy.2,24–26 Our respondents also recognized the underuse of AS, yet recommended treatments with which they are most familiar. In our study, most radiation oncologists and urologists were concerned about overtreatment with radical prostatectomy and radiation therapy, but their perceptions of what treatments were the culprit in overtreatment varied by physician specialty. In this regard, radiation oncologists and urologists concluded that primary treatment provided by the other specialty as being overused. Fowler et al27 performed a similar national survey of radiation oncologists and urologists about treatment recommendations for localized prostate cancer. In this study, each specialty viewed their primary therapy treatment more favorably in regards to providing better survival benefit and less loss of sexual function and urinary incontinence from radiation therapy. Furthermore, specialists similarly recognize that brachytherapy, radiation therapy, and surgery were being overused in 2000, but respondents were somewhat biased in viewing the other treatments provided by the other specialty as being more responsible for overtreatment. Therefore, our study suggests that little has changed in that both specialties continue to acknowledge the growing concerns about the overtreatment of localized prostate cancer even if that has not consistently translated into their self-reported patterns of treatment recommendations.28,29
So why are so many men with low-risk prostate cancer being treated, if clinicians feel that AS is underused? Our study also sheds light on this question. In our survey study, radiation oncologists and urologist appeared biased in favor of treatments from their particular specialty. Two thirds of urologists recommended surgery, whereas half of radiation oncologists endorsed either brachytherapy or radiation therapy. Furthermore, only a small fraction of physicians chose AS for the primary treatment recommendation of low-risk disease (22.1%). There also appeared to be key differences in responses on whether prostate cancer patients are interested in AS that also raise concern about its broader use in the United States. Although a majority of both specialties stated that patients were not interested in this disease management option, more radiation oncologists responded this way compared with urologists. Furthermore, a greater number of radiation oncologists had reported fewer patients undergoing AS in their clinical practice. This difference may be attributable to the clinical aspects of AS (serial digital rectal examinations, PSA testing, and biopsies) that are traditionally part of the clinical practice for urologists than radiation oncologists. Nonetheless, our study suggests that there remain some key attitudinal barriers to AS among prostate cancer specialists, especially considering radiation oncologists and urologists may view their treatment as superior. It is also concerning that a large percentage of respondents from both specialties reported that most prostate cancer patients are not interested in AS. Increased attention to education at the time of the diagnosis may help alleviate distressed patients who are concerned about risks of progression and the intensity of diagnostic testing from undergoing AS.
We acknowledge that several limitations exist in this study. Although the response rate in this study may limit the results due to possible bias, it is on par with previous studies, especially among specialists.30,31 Furthermore, the demographic characteristics (age and sex) from the AMA Masterfile were similar between responders and nonresponders. However, response rates were higher among physicians practicing in academic hospitals or reimbursed by a billing compensation structure. Therefore, this difference in practice settings may possibly explain some of our findings. We also recognize that physicians were asked for perceptions about AS and treatment recommendations for low-risk prostate cancer in the setting of case presentations. It is feasible that attitudes about AS and treatment recommendations would have changed due to differing clinical characteristics such as advanced age, poor existing health-related quality of life, or limited life expectancy. Survey data on self-reported behavior and attitudes are also more limited THAN directly observed behavior. Finally, we recognize that the preferences of prostate cancer patients for treatment may have influenced the responses of both the specialties. For instance, Jang et al32 recently reported that approximately 40% of Medicare beneficiaries visited with both a radiation oncologist and urologist and were then more likely to receive radiation therapy. It is possible that radiation oncologists may be seeing more patients who prefer radiation therapy, thereby potentially biasing the survey responses.
In summary, our study is the first to gauge the attitudes and perceptions of AS and the relative merits of different treatment options for low-risk prostate cancer from a national survey of radiation oncologists and urologists. We highlight the apparent disconnect between the perceptions of specialists that AS is effective and yet it does not translate into treatment recommendations for low-risk disease. Furthermore, our results suggest that both radiation oncologists and urologists agree with the growing concerns of overtreatment with prostate cancer. Possible explanations of these findings may be the belief from both specialties that most patients are not interested in pursuing AS and possible specialty biases regarding better survival from their primary therapy. To overcome this disconnect of AS and treatment recommendations in favor of radiation therapy and surgery, efforts to improve the clinical encounter between patients and physicians at the time of diagnosis and treatment decisions by bringing the evidence-based benefits for improved survival and treatment-related quality of life issues into the discussion has the potential to improve the role of AS in the United States. Decision aids, which incorporate the principles of shared decision making, have been shown to improve patient knowledge about prostate cancer and incorporate patient preferences into treatment decisions.33,34 This is particularly concerning as only a third of Medicare beneficiaries reported that conservative management was discussed in a recent national survey.35 Furthermore, the use of multidisciplinary care in a coordinated manner with radiation oncologists, urologists, and primary care providers may afford the opportunity to better balance treatment decisions regarding the possible benefits and risks of primary therapy in the context of life expectancy and competing comorbidities.15,32,36 However, our previous study demonstrated that radiation oncologists and urologists do not routinely make use of instruments that objectively measure prostate cancer severity, life expectancy, and quality of life.37 Therefore, increased attention is needed to ensure that patient preferences are incorporated into treatment decisions and decision aids and tools are more easily implemented into clinical practice. By doing so, AS may then become a more acceptable disease management strategy for low-risk prostate cancer among newly diagnosed patients and specialists.
1. Siegel R, Naishadham D, Jemal A.Cancer statistics, 2013.CA Cancer J Clin.2013;63:11–30.
2. Welch HG, Albertsen PC.Prostate cancer diagnosis and treatment after the introduction of prostate-specific antigen screening: 1986-2005.J Natl Cancer Inst.2009;101:1325–1329.
3. Wilt TJ, MacDonald R, Rutks I, et al..Systematic review: comparative effectiveness and harms of treatments for clinically localized prostate cancer.Ann Intern Med.2008;148:435–448.
4. Klotz L, Zhang L, Lam A, et al..Clinical results of long-term follow-up of a large, active surveillance cohort with localized prostate cancer.J Clin Oncol.2010;28:126–131.
5. Mohler J, Bahnson RR, Boston B, et al..NCCN clinical practice guidelines in oncology: prostate cancer.J Natl Compr Canc Netw.2010;8:162–200.
6. Thompson I, Thrasher JB, Aus G, et al..Guideline for the management of clinically localized prostate cancer: 2007 update.J Urol.2007;177:2106–2131.
8. Cooperberg MR, Broering JM, Carroll PR.Time trends and local variation in primary treatment of localized prostate cancer.J Clin Oncol.2010;28:1117–1123.
9. Cooperberg MR, Broering JM, Kantoff PW, et al..Contemporary trends in low risk prostate cancer: risk assessment and treatment.J Urol.2007;1783 pt 2S14–S19.
10. van den Bergh RC, Albertsen PC, Bangma CH, et al..Timing of curative treatment for prostate cancer: a systematic review.Eur Urol.2013;64:204–215.
11. Dall’Era MA, Albertsen PC, Bangma C, et al..Active surveillance for prostate cancer: a systematic review of the literature.Eur Urol.2012;62:976–983.
12. Daskivich TJ, Chamie K, Kwan L, et al..Overtreatment of men with low-risk prostate cancer and significant comorbidity.Cancer.2011;117:2058–2066.
13. Jacobs BL, Zhang Y, Schroeck FR, et al..Use of advanced treatment technologies among men at low risk of dying from prostate cancer.JAMA.2013;309:2587–2595.
14. Davison BJ, Oliffe JL, Pickles T, et al..Factors influencing men undertaking active surveillance for the management of low-risk prostate cancer.Oncol Nurs Forum.2009;36:89–96.
15. Aizer AA, Paly JJ, Zietman AL, et al..Multidisciplinary care and pursuit of active surveillance in low-risk prostate cancer.J Clin Oncol.2012;30:3071–3076.
16. Bul M, Zhu X, Rannikko A, et al..Radical prostatectomy for low-risk prostate cancer following initial active surveillance: results from a prospective observational study.Eur Urol.2012;62:195–200.
17. Bul M, Zhu X, Valdagni R, et al..Active surveillance for low-risk prostate cancer worldwide: the PRIAS study.Eur Urol.2013;63:597–603.
18. Bill-Axelson A, Holmberg L, Filen F, et al..Radical prostatectomy versus watchful waiting in localized prostate cancer: the Scandinavian prostate cancer group-4 randomized trial.J Natl Cancer Inst.2008;100:1144–1154.
19. Bill-Axelson A, Holmberg L, Ruutu M, et al..Radical prostatectomy versus watchful waiting in early prostate cancer.N Engl J Med.2011;364:1708–1717.
20. Bill-Axelson A, Holmberg L, Ruutu M, et al..Radical prostatectomy versus watchful waiting in early prostate cancer.N Engl J Med.2005;352:1977–1984.
21. Wilt TJ, Brawer MK, Jones KM, et al..Radical prostatectomy versus observation for localized prostate cancer.N Engl J Med.2012;367:203–213.
22. Daskivich TJ, Fan KH, Koyama T, et al..Effect of age, tumor risk, and comorbidity on competing risks for survival in a US population-based cohort of men with prostate cancer.Ann Intern Med.2013;158:709–717.
23. Raldow AC, Presley CJ, Yu JB, et al..The relationship between clinical benefit and receipt of curative therapy for prostate cancer.Arch Intern Med.2012;172:362–363.
24. Cooperberg MR, Broering JM, Litwin MS, et al..The contemporary management of prostate cancer in the United States: lessons from the cancer of the prostate strategic urologic research endeavor (CapSURE), a national disease registry.J Urol.2004;171:1393–1401.
25. Cooperberg MR, Lubeck DP, Mehta SS, et al..Time trends in clinical risk stratification for prostate cancer: implications for outcomes (data from CaPSURE).J Urol.2003;1706 pt 2S21–S25discussion S26-27.
26. Cooperberg MR, Lubeck DP, Meng MV, et al..The changing face of low-risk prostate cancer: trends in clinical presentation and primary management.J Clin Oncol.2004;22:2141–2149.
27. Fowler FJ Jr, McNaughton Collins M, Albertsen PC, et al..Comparison of recommendations by urologists and radiation oncologists for treatment of clinically localized prostate cancer.JAMA.2000;283:3217–3222.
28. Carter HB.Active surveillance for prostate cancer: an underutilized opportunity for reducing harm.J Natl Cancer Inst Monogr.2012;2012:175–183.
29. Sandhu GS, Andriole GL.Overdiagnosis of prostate cancer.J Natl Cancer Inst Monogr.2012;2012:146–151.
30. Asch DA, Jedrziewski MK, Christakis NA.Response rates to mail surveys published in medical journals.J Clin Epidemiol.1997;50:1129–1136.
31. Cummings SM, Savitz LA, Konrad TR.Reported response rates to mailed physician questionnaires.Health Serv Res.2001;35:1347–1355.
32. Jang TL, Bekelman JE, Liu Y, et al..Physician visits prior to treatment for clinically localized prostate cancer.Arch Intern Med.2010;170:440–450.
33. Lin GA, Aaronson DS, Knight SJ, et al..Patient decision aids for prostate cancer treatment: a systematic review of the literature.CA Cancer J Clin.2009;59:379–390.
34. O’Brien MA, Whelan TJ, Villasis-Keever M, et al..Are cancer-related decision aids effective? A systematic review and meta-analysis.J Clin Oncol.2009;27:974–985.
35. Fowler FJ Jr, Gallagher PM, Bynum JP, et al..Decision-making process reported by Medicare patients who had coronary artery stenting or surgery for prostate cancer.J Gen Intern Med.2012;27:911–916.
36. Albertsen PC, Moore DF, Shih W, et al..Impact of comorbidity on survival among men with localized prostate cancer.J Clin Oncol.2011;29:1335–1341.
37. Kim SP, Karnes RJ, Nguyen PL, et al..Clinical implementation of quality of life instruments and prediction tools for localized prostate cancer: results from a national survey of radiation oncologists and urologists.J Urol.2013;189:2092–2098.
active surveillance; outcomes; prostate cancer; recommendations; survey
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