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© 2001 American Society for Clinical Oncology Quality-of-Life Outcomes After Primary Androgen Deprivation Therapy: Results From the Prostate Cancer Outcomes StudyByFrom the Division of Cancer Control and Population Sciences, National Cancer Institute, Bethesda, MD; Division of Urology, University of Connecticut Health Center, Farmington, CT; Fred Hutchinson Cancer Research Center, Seattle, WA; University of Southern California, Keck School of Medicine, Department of Preventive Medicine, Los Angeles, CA; New Mexico Tumor Registry, University of New Mexico Health Sciences Center, and Medical Service, Department of Veterans Affairs Medical Center, Albuquerque, NM; Georgia Center for Cancer Statistics, Rollins School of Public Health, Emory University, Atlanta, GA; and Division of Urology, Department of Surgery, University of Utah, Salt Lake City, UT. Address reprint requests to Arnold L. Potosky, PhD, Applied Research Branch, National Cancer Institute, Executive Plaza North Rm 4005, 6130 Executive Blvd, MSC 7344, Bethesda, MD 20892-7344; email: potosky{at}nih.gov
PURPOSE: To compare health-related quality-of-life outcomes after primary androgen deprivation (AD) therapy with orchiectomy versus luteinizing hormone-releasing hormone (LHRH) agonists for patients with prostate cancer. PATIENTS AND METHODS: Men (n = 431) newly diagnosed with all stages of prostate cancer from six geographic regions who participated in the Prostate Cancer Outcomes Study and who received primary AD therapy but no other treatments within 12 months of initial diagnosis were included in a study of health outcomes. Comparisons were statistically adjusted for patient sociodemographic and clinical characteristics, timing of therapy, and use of combined androgen blockade. RESULTS: More than half of the patients receiving primary AD therapy had been initially diagnosed with clinically localized prostate cancer. Among these patients, almost two thirds were at high risk of progression on the basis of prognostic factors. Sexual function outcomes were similar by treatment group both before and after implementation of AD therapy. LHRH patients reported more breast swelling than did orchiectomy patients (24.9% v 9.7%, P < .01). LHRH patients reported more physical discomfort and worry because of cancer or its treatment than did orchiectomy patients. LHRH patients assessed their overall health as fair or poor more frequently than did orchiectomy patients (35.4% v 28.1%, P = .01) and also were less likely to consider themselves free of prostate cancer after treatment. CONCLUSION: Most endocrine-related health outcomes are similar after surgical versus medical primary hormonal therapy. Stage at diagnosis had little effect on outcomes. These results provide representative information comparing surgical and medical AD therapy that may be used by physicians and patients to inform treatment decisions.
ANTIANDROGENIC AGENTS and surgical orchiectomy have been the standard initial treatment for metastatic prostate cancers. Randomized studies from the 1970s comparing the oral hormone diethylstilbestrol with orchiectomy for advanced disease demonstrated equivalent survival but an excess in cardiovascular mortality with hormone therapy.1 Newer antiandrogenic agents have replaced diethylstilbestrol, particularly injections of luteinizing hormone-releasing hormone (LHRH) agonists. The LHRH agonists are physiologically equivalent to orchiectomy in suppressing testicular androgen production,2,3 and a meta-analysis found no statistically significant differences in survival for men treated with an LHRH agonist versus orchiectomy.4 The role for combined androgen blockade (CAB) with or without oral antiandrogenic agents has been more controversial.5-7 Given similar efficacy between LHRH agonists and orchiectomy, quality-of-life outcomes, costs, and body image perception may predominate in treatment decisions. The availability of more acceptable nonsurgical androgen deprivation (AD) therapies may be stimulating a renewed interest in such therapies as an alternative to surgery or radiation, particularly for those patients with clinically localized prostate cancer at high risk for progression. AD therapy has also been proposed as an alternative to watchful waiting for men electing to undergo less aggressive treatments,8 and community urologists now include AD therapy as a viable treatment option for some men with localized prostate cancer.9 However, little is known about the use of AD therapy for clinically localized prostate cancer in the community setting. AD therapy for prostate cancer is known to adversely affect quality of life, leading to increased fatigue, erectile difficulties, and declines in sexual interest and enjoyment.10-12 Equivalent quality of life and urinary, bowel, and sexual function have been reported for patients receiving orchiectomy versus LHRH agonists.13 However, these results are limited by small sample size, inclusion of patients with metastatic disease only, no baseline information, and the failure to account for multiple confounding factors. Because most prior studies have usually enrolled patients treated at academic institutions, estimates of chronic treatment complications may not apply in more diverse community settings. Using data from the Prostate Cancer Outcomes Study (PCOS), we compared sexual function outcomes and general perceptions and satisfaction among newly diagnosed men who were treated with either orchiectomy or LHRH agonists alone as primary therapy within 12 months of initial diagnosis, adjusting for disease and sociodemographic characteristics.
Study Subjects In 1994, the PCOS was initiated within the National Cancer Institute (NCI)’s Surveillance, Epidemiology, and End Results (SEER) Program to investigate variations in the initial treatment of prostate cancer, and to describe health outcomes in a socioeconomically heterogeneous cohort of newly diagnosed prostate cancer patients treated primarily in community medical practices.14 SEER is a set of geographically defined, population-based, central cancer registries in the United States, operated by local nonprofit organizations under contract to the NCI. Registry data are submitted electronically to the NCI on a biannual basis, and the NCI makes the data available to the public for scientific research (http://www.seer.cancer.gov/). The PCOS enrolled men diagnosed as having primary invasive prostate cancer between October 1, 1994, and October 31, 1995, and who were residents of areas covered by six population-based registries participating in the SEER Program (the states Connecticut, Utah, and New Mexico, and the metropolitan areas Atlanta, Los Angeles, and Seattle/Puget Sound). The PCOS sampled a total of 5,672 men from 11,137 eligible men residing in these areas, of whom 3,486 (62%) participated by completing a 6-month and/or a 12-month self-administered questionnaire and consented to medical record reviews. Responders to the PCOS were similar to nonresponders with respect to mean age (66 and 67 years, respectively), tumor stage, and grade. Nonresponders were slightly more likely to be nonwhite and from geographic areas having lower median incomes.14 For this study of AD therapy, the following exclusions were made from the total PCOS sample of 3,486 men: 2,350 men who received no AD therapy and 714 men who had received radical prostatectomy or radiotherapy in addition to AD therapy. Of the remaining 476 men, 45 men taking oral monotherapy but not receiving an orchiectomy or LHRH agonists were excluded because they were too small a group to be included in a separate category for analysis. The final study sample of 431 men either underwent orchiectomy or initiated LHRH agonists (leuprolide or goserelin injections) as primary therapy within 12 months after initial diagnosis, with no evidence from medical record reviews or surveys of receiving any other prostate cancer therapy.
Data Collection The survey instrument obtained information on demographics, satisfaction with treatment, comorbidity, and both general and disease-specific measures of health-related quality of life (HRQOL). Disease-specific HRQOL was measured using a newly adapted prostate cancer–specific instrument that is based on items from three existing instruments.15-17 The disease-specific component of the instrument contained six scales using 18 items covering urinary, bowel, and sexual domains and is reprinted elsewhere.14 The sexual function scale analyzed in this study consists of four items pertaining to sexual interest, frequency of activity, and the ability to achieve and maintain an erection. Other items asked respondents about overall physical discomfort, worry, limitations in daily activities, and bother as a result of prostate cancer or treatments. Because surveying all cases before initial treatment was impractical, respondents were asked on the 6-month survey about urinary, bowel, and sexual function just before prostate cancer was diagnosed, and about their function during the past month. Of the sample of 431 men, 401 completed the initial survey 6 months after diagnosis and provided retrospective assessments of pretreatment sexual function. The accuracy of the 6-month retrospective recall of urinary, bowel, and sexual function was assessed in a separate validation study.18 Over 70% of the men reported prediagnostic functioning at the highest level on 12 of 17 survey items. For each of these items, recall at 6 months was identical to the baseline survey response for 69% or more of the men. The values of the weighted kappas for changes computed using baseline reports (prospective) and changes computed using 6-month recall (retrospective) ranged from 0.42 to 0.67 for the four individual items regarding sexual libido, frequency, and achieving and maintaining erections. Only the item regarding maintenance of erections revealed a systematic recall bias, since men tended to more often overestimate (v underestimate) their ability to maintain an erection at baseline 6 months later. On the other three items, the disagreements between baseline and retrospective reports balanced out. We assessed general health-related quality of life by selecting five scales (bodily pain, depression/anxiety, vitality, role limitations related to physical health, and role limitations related to emotional health) and a global item on overall health status from the Medical Outcomes Study (MOS) short form 36-item generic health status questionnaire (SF-36). This instrument, which has excellent reliability and validity, has been used in numerous studies to measure general HRQOL.19 Centrally trained, experienced abstractors from each registry abstracted medical records from hospitals, free-standing radiologic or surgical centers, Veterans Affairs medical centers, health maintenance organizations, and private physician offices, which were usually the treating urologist or radiation oncologist. The outpatient medical record abstractions obtained information not routinely collected by SEER registries, such as Gleason grade, baseline prostate-specific antigen (PSA) levels, baseline symptoms, and type and dates of specific hormonal agents given.
Statistical Analysis We did not present outcomes from the 24-month follow-up survey for three reasons. First, outcomes at 24 months after diagnosis were essentially similar to those observed at 12 months. Second, the ascertainment of clinical status (recurrence and progression) and the use of secondary treatments between the 12-month and 24-month surveys was incomplete, thus potentially confounding the assessment of outcomes at 24 months. Finally, it is possible that a substantial proportion of men in the LHRH group may have discontinued therapy at the time of the 24-month survey. Unadjusted estimates of outcomes in the two AD therapy groups were calculated to assess cross-sectional differences before and after treatment. We determined whether the relationship between type of AD therapy and outcomes remained after adjusting for other variables by using a series of logistic or ordinal polychotomous regression models, depending on the number of response categories. The following baseline variables were included as covariates: age at diagnosis, race/ethnicity, educational attainment, annual household income, geographic region, clinical stage, Gleason score, pretreatment PSA value, lymph node status, comorbidity score, pretreatment metastatic symptoms (bone pain, anorexia, or fatigue), the presence of pretreatment urinary obstructive symptoms, and the timing of initiating therapy (or date of orchiectomy). The use of oral hormonal agents for CAB was also added to models to account for the potential confounding effects of the use of these therapies on outcomes. P values corresponding to the regression parameters for the treatment effects are shown in all tables and figures. Similar regression models were also used to assess differences by AD therapy group in terms of general perceptions regarding prostate cancer or its treatment, and satisfaction and regret with treatment decision. A series of ordinary least squares linear regression models using the same independent variables were used to compare the two treatment groups with respect to continuous SF-36 scale scores (on a 0 to 100 scale, with 100 indicating best health) in the five domains included in the PCOS survey. Interactions of treatment type with age group, clinical stage (localized v advanced or metastatic), and education were systematically examined in all regression models. All analyses were implemented using the Survey Data Analysis statistical software.20 The Horvitz-Thompson weight, which is the inverse of the sampling proportion for each sampling stratum (defined by age/race/study area), was used to obtain unbiased estimates for all eligible prostate cancer patients in the PCOS study areas. Wald-type tests using the robust sandwich estimator were used to assess statistical significance of estimated regression coefficients. All P values were two-sided.
Table 1 shows the distribution of demographic and clinical characteristics for the 431 PCOS study participants who received either orchiectomy or LHRH agonists as their only therapy within 12 months of initial diagnosis. Although similar with respect to age at diagnosis and race/ethnicity, the orchiectomy group had a lower educational attainment and household income compared with the LHRH patients. There were significant geographic variations observed, with men residing in residing in Atlanta and Connecticut more likely to receive LHRH agonists. The largest percentage of men receiving AD therapy within the first year of diagnosis were those with clinically localized (T1 or T2) disease. A small percentage of cases had positive lymph nodes, with no differences by type of therapy. (Only 10% of the entire sample had lymph nodes examined, presumably via laparotomy or laparoscopy.) Patients receiving orchiectomy were more often diagnosed with metastatic (included as clinical stage T4) disease than were LHRH patients (43.1% v 24.7%, P < .01), mainly because of the presence of bone metastases. Orchiectomy patients had slightly worse prognoses in terms of Gleason score, baseline PSA, and positive lymph nodes, none of which were statistically different from the LHRH group. Among clinically localized patients, 68% of orchiectomy and 58% of LHRH patients had high-risk disease as defined by the presence of a baseline PSA over 20 ng/mL, Gleason score of 8 to 10, positive nodes, or symptoms such as bone pain, anorexia, or weight loss. More patients in the orchiectomy group had pretreatment urinary obstructive symptoms, but the frequency of symptoms associated with metastatic disease was similar in both groups. More than 90% of all cases were given AD therapy before completing the first PCOS survey 6 months after diagnosis. The median interval between initiating therapy to completing the 12-month survey was similar in the two groups, 11 and 10 months for orchiectomy and LHRH patients, respectively.
We examined postbaseline differences using other treatments that might confound observed outcome comparisons of the two AD therapy groups. The use of CAB was greater in the LHRH group (27.4% v 14.3%, P < .01). Therefore, adjustments in regression models that compared orchiectomy and LHRH outcomes included the baseline variables in Table 1, the timing of initial therapy, and the use of CAB. In a multivariate model assessing all the factors in Table 1, only registry area, clinical stage, obstructive symptoms, and CAB use remained significantly associated with type of AD therapy.
Sexual Function
We assessed change in function by calculating the percentage of men with normal pretreatment function who reported dysfunction after treatment (data not shown). Among men with some interest in sex before treatment, 51% reported no interest after treatment. Approximately 73% of men ceased engaging in sexual activity after treatment, and 69% of men who were potent before treatment were impotent after treatment. No differences were observed by type of AD therapy. A larger percentage of LHRH patients (38.4%) than orchiectomy patients (25.6%) reported a big or moderate problem with their overall sexual function (Table 2). This difference, which remained statistically significant after adjusting for baseline covariates, is likely a result of a higher percentage of LHRH patients who reported a big or moderate problem with sexual function before treatment. There was no difference by type of therapy in change on this measure, with 23% of all patients who reported no problems before treatment later reporting they had some problem with their sexual function after treatment. We also examined the prevalence of breast swelling and hot flashes after treatment (no baseline reports were obtained for these outcomes). The prevalence of breast swelling after treatment was 24.9% in LHRH patients, compared with 9.7% in orchiectomy patients, even after adjustment for all the covariates in Table 1 (P < .01). Hot flashes were similar in both AD therapy groups (56.5% v 67.9%, adjusted P = .38). All of these hormone-related outcomes were assessed by stage grouping to examine whether there were differences in clinically localized versus clinically advanced or metastatic cases. There was no evidence of an interaction between stage at diagnosis and type of AD therapy with respect to these outcomes.
General Perceptions and Satisfaction
Figure 1 compares the two treatment groups on five scales of the MOS SF-36. There were no differences in emotional role, pain, mental health, or vitality, even after adjustment for the variables in Table 1. In multivariate regression analyses, comorbidity was the single factor consistently inversely related to these general health outcomes. There was no significant independent effect of stage on these outcomes, nor were there any interaction effects observed between stage and AD therapy.
Our study provides the first comprehensive population-based assessment of patient-oriented health outcomes for the two current alternatives to block androgen exposure, LHRH agonists and orchiectomy, in men with newly diagnosed prostate cancer. Although we initiated this investigation of outcomes among men with metastatic prostate cancer, we found a surprisingly large number of patients with clinically localized disease who received primary AD therapy. The men included in our study represented approximately 12.5% of the entire PCOS cohort of 3,486 men. Extrapolating this prevalence to the estimated number of new cases diagnosed each year in the United States population yields an approximate conservative estimate of 22,000 men each year who are treated with primary hormonal therapy, which assumes the use of therapies by stage has remained constant since 1995, when our patients were first diagnosed and enrolled. It is likely that such use of hormonal therapy has increased since 1995. Among men in our sample with clinically localized disease, almost two thirds had possible signs of advanced-stage cancer, characterized mainly by baseline PSA over 20 ng/mL and Gleason scores of 8 to 10. The majority had no lymph nodes examined and had negative bone scans. For these men, who are generally considered unlikely to benefit from surgery, the use of AD therapy may represent an alternative treatment approach designed to treat the likely underlying metastatic disease, thereby delaying progression to symptomatic disease. For other men with clinically localized disease but who have more favorable prognostic factors, the use of AD therapy is more controversial. These men tended to be older than men with metastatic disease, with more comorbid conditions. To some extent, AD therapy for such cases may reflect the patient’s preference to do something about their cancer versus watching and waiting with regular PSA tests and to avoid the more serious complications after surgery or radiotherapy. Given the lack of evidence regarding the efficacy of hormonal therapy for localized cancer, even for high-risk patients, information about costs and other health effects of AD therapies may be paramount in defining policies and for aiding clinical decision making. The costs of LHRH agonists are substantially higher than orchiectomy. At one institution, surgically treated patients with metastatic prostate cancer incurred one third the cost of patients treated with leuprolide over a 30-month period.21 These authors extrapolated a cost to the country of $100 million for medical versus surgical hormonal treatment for metastatic disease over a 10-year period. This estimate did not, however, account for the prevalence of AD therapy in clinically localized disease. A recent analysis suggested that, for men who accept it, orchiectomy is likely to be the most cost-effective AD therapy for advanced disease.22 Other studies of outcomes after hormonal therapy have demonstrated a decline in sexual function and sexual satisfaction among men with metastatic prostate cancer.10,11,13 Our results in a large population-based sample of patients confirmed that AD therapy is associated with considerable declines in sexual function, independent of initial stage at diagnosis. We also extend previous findings by showing that LHRH agonists and orchiectomy seem to have similar effects on sexual function, as might be expected. A new finding is that, after treatment, LHRH patients reported having a bigger problem than did orchiectomy patients with their overall sexual functioning despite similar function and bother before treatment. It is possible that this baseline difference may have been associated with treatment choice. For men who are less bothered by their level of sexual function, choosing a surgical therapy that cannot be discontinued or reversed may be less difficult than for men who are more concerned with sexual function, who may wish to reserve the option to discontinue AD therapy at a later time. We found that sexual function and bother associated with sexual function were not closely correlated, consistent with observations in other assessments of prostate cancer patients.15,17 The decline in interest, frequency of activity, and erectile function was much larger than the increase in the percentage of men who reported being bothered by their sexual function. This finding may be a result of the expectation by some men of a loss of sexual function that accompanies treatment for their cancer. Because of the different prognosis faced by men with advanced versus localized cancer, we assessed whether treatment outcomes were independently effected by clinical stage or other prognostic factors such as Gleason score. We found that stage and other prognostic factors had no significant effects on sexual function, general health status, or perceptions after adjusting for other baseline characteristics. This may indicate that many men with advanced disease had few or possibly no symptoms and were likely similar in most respects to men with localized cancer during the first year after diagnosis. We also observed no interaction between stage at diagnosis and type of AD therapy with respect to any of the outcomes measured, though our power to statistically detect such differences was limited by the sample size. Overall discomfort and worry about prostate cancer or its treatment was higher among LHRH patients, who also were less likely than orchiectomy patients to perceive themselves as free of cancer. These differences may be partly related to the regular injections that serve as constant reminders of the presence of disease. In a subgroup analysis, we found that men who had discontinued their LHRH injections had better erectile function and less worry than men still receiving them did. However, these outcomes in LHRH patients must be balanced against other unmeasured concerns about orchiectomy that may influence patient preferences for LHRH agonists. Preference for injections versus surgery may be associated with fear of permanent mutilation, loss of masculine self-image, and the ability to discontinue injections. Previous reports comparing CAB with orchiectomy alone revealed significantly more diarrhea and worse emotional functioning in patients receiving CAB at 6 months after therapy.23 We examined these outcomes in our cohort. The use of CAB, which includes orchiectomy or injections plus oral medication, was not associated with differences in sexual function, frequency of diarrhea, or generic health domains, including emotional function. There are several caveats to this analysis. First, the PCOS relied on 6-month retrospective recall for baseline sexual function. In a separate validation of recall accuracy, we found no consistent, significant recall bias over 6 months for the majority of the disease-specific items, primarily because most men had good baseline function and report this reasonably accurately 6 months later.18 No evidence supports any differential recall bias by type of hormonal therapy, so this was unlikely to have substantially influenced our comparisons. Second, the response rate to the overall PCOS study was approximately 62%, and nonresponders differed somewhat from responders on age and socioeconomic status.14 Although we adjusted for these characteristics, our results may have been biased under the assumption that responders systematically differed from nonresponders regarding measured outcomes. Third, statistical adjustments for the confounding factors cannot definitively account for the selection bias introduced by nonrandomized treatment groups. In summary, this study demonstrates that sexual function is significantly impaired after AD therapy, and that these effects are similar for surgical versus medical AD therapy. Stage at diagnosis had no effect on these comparisons of outcomes within 1 year of diagnosis. However, men receiving LHRH agonists reported more worry and discomfort and somewhat poorer overall health and were less likely to believe themselves free of cancer compared with orchiectomy patients. Our results reflect treatment delivered to a heterogeneous group of patients in diverse health care settings and provide representative information about the effects of hormonal therapy to help inform treatment decisions.
Supported by grant nos. N01-PC-67007, N01-CN-67009, N01-PC-67010, N01-PC-67006, N01-PC-67005, and N01-PC-67000 from the National Cancer Institute, National Institutes of Health, Bethesda, MD. We thank the men who, by their participation in the PCOS, have contributed to a better understanding of the effects of prostate cancer on men’s lives. Jonathan M. Liff from the Atlanta registry and Dennis Deapen from the Los Angeles registry contributed significantly to the conception, design, and data collection as senior PCOS coinvestigators. We thank the physicians from the six SEER areas who assisted in the collection of data from their patients and from medical records. We thank Jennifer Stevens, Information Management Services, Inc, Silver Spring, MD, who serves as the Data Coordinator for the PCOS and Ming Sheu, of Information Management Services, who assisted with the data processing.
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Copyright © 2001 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
