Original Article
Results of Conservative Management of Clinically Localized Prostate Cancer
N Engl J Med 1994; 330:242-248January 27, 1994
- Abstract
Background
The selection of treatment for patients with localized prostate cancer requires reliable information about the outcome of conservative management. Previous studies of this question are generally considered unreliable because they were uncontrolled and nonrandomized.
Methods
We performed a pooled analysis of 828 case records from six nonrandomized studies, published since 1985, of men treated conservatively (with observation and delayed hormone therapy but no radical surgery or irradiation) for clinically localized prostate cancer. A Cox regression analysis was performed to determine which factors influenced survival among patients who did not die of causes other than prostate cancer (disease-specific survival). Kaplan-Meier curves for overall and metastasis-free survival among such patients were compared with use of the log-rank method and the Mantel-Haenszel test.
Results
Factors that had a significant effect on disease-specific survival were grade 3 tumors (risk ratio, 10.04), residence in Israel (risk ratio, 2.48) or New York (risk ratio, 0.37), and age under 61 years (risk ratio, 0.32). Ten years after diagnosis, disease-specific survival (with data on men who died from causes other than prostate cancer censored) was 87 percent for men with grade 1 or 2 tumors and 34 percent for those with grade 3 tumors; metastasis-free survival among men who had not died of other causes was 81 percent for grade 1, 58 percent for grade 2, and 26 percent for grade 3 disease. These findings were not affected by the inclusion of men who had early-stage cancer, were older, had worse-than-average health, or underwent delayed radiation therapy or radical prostatectomy.
Conclusions
The strategy of initial conservative management and delayed hormone therapy is a reasonable choice for some men with grade 1 or 2 clinically localized prostate cancer, particularly for those who have an average life expectancy of 10 years or less. New treatment strategies are needed for men with grade 3 prostate cancer.
Media in This Article
Figure 1
Disease-Specific Survival among Untreated Patients with Localized Prostate Cancer, According to Tumor Grade.Figure 2
Metastasis-free Survival among Untreated Patients with Localized Prostate Cancer, According to Tumor Grade.Article Activity
- Article
Prostate cancer is now the most common cancer and the second most common cause of death from cancer among men in the United States1. Both the incidence and the mortality rate have continued to rise, with no reduction projected over the next several years2. Since a large percentage of patients have advanced disease at the time of diagnosis,3 routine screening of asymptomatic men, which increases early detection,4 has been recommended, but we do not know whether early detection will reduce mortality5.
After diagnosis, counseling patients about management is difficult. The relative benefit of different forms of treatment has never been properly determined. To date, only one randomized trial has compared the results of radical surgery with those of conservative management6. Although the rate of mortality from prostate cancer was similar in the two groups, methodologic flaws make the conclusions of this study suspect. The lack of a clearly superior therapy has contributed to marked differences in treatment recommendations in different regions of the United States and in Europe7.
The variable natural history of the disease contributes to this problem. At least 30 percent of men over 50 years of age have histologic evidence of prostate cancer,8,9 yet only a small fraction of these cancers are newly detected each year or cause death10. Prognostic factors have been recognized, but reliable methods for identifying potentially life-threatening tumors are lacking, and aggressive treatment of some patients may be unnecessary.
Specifically, information is needed about the outcome of clinically localized tumors treated conservatively. Since 1985, such information has been reported from 10 nonrandomized studies,11-21 but these studies have all been criticized because of factors that could have biased the results.
Recently, Stewart and Parmar showed that meta-analyses will be least biased and most reliable if data on individual patients are pooled rather than if only published summary data are combined22. To obtain a reliable but conservative estimate of the outcome of nonaggressive management, we performed a pooled analysis using data on individual patients from six nonrandomized studies of patients with clinically localized prostate cancer that was managed conservatively with observation and delayed hormone therapy but without irradiation or radical surgery11-17.
Methods
Sources of Data
We performed a MEDLINE search to identify studies of patients with clinically localized prostate cancer treated with observation and delayed hormone therapy that were published from January 1985 through July 1992. The bibliographies in published literature reviews on this subject were used to identify other appropriate studies. Authors of studies that reported only on patients with stage A1 disease (one to three prostate chips containing cancer) or stage T0a disease16 (less than 25 percent of the prostate sample containing cancer) were not contacted. A letter was sent to the principal author of each of the papers that met our criteria, inviting him or her to participate by providing original data on patients. The authors' cooperation was needed because insufficient information was contained in the published reports.
Inclusion of Patients
The information requested about each patient included his age, the clinical stage and tumor grade at the time of diagnosis, the method and timing of delayed treatment, the length of time to death from prostate cancer or from other causes, the length of time to the identification of distant metastases (metastasis-free survival), and the length of time to the most recent follow-up, if the patient was still alive. No attempt was made to review the pathological or cytologic findings. Some men eventually received local therapy, but all such patients continued to be included in our analyses. Patients in whom hormone therapy was administered for symptomatic progression or metastases were included but not specifically identified.
Subgroups of Patients
Because of differences among the patient cohorts in age distribution, country of origin, ethnic background, methods of patient selection, and methods of determining the grade and stage of cancer, a preliminary analysis was performed to determine which patients could be combined and analyzed together without favorably biasing the outcome.
The disease-specific survival (i.e., survival with censorship of patients who died from causes other than prostate cancer) of patients with cytologic23 grade 1 cancers was compared with that of patients with well-differentiated tumors on histologic examination24 or tumors with a Gleason sum25 of 2 through 4 (combined classification, grade 1), cytologic grade 2 cancers were compared with tumors that were moderately differentiated on histologic examination or tumors with a Gleason sum of 5 through 7 (grade 2), and cytologic grade 3 cancers were compared with histologically poorly differentiated cancers or tumors with a Gleason sum of 8 through 10 (grade 3).
Although four systems were used to determine patients' cancer stages, comparable stages were easily identified except for stages A1, “focal,” T0l, and T0a tumors. Stages T0a and T0l modified11,16 from the TNM system26,27 include cancers that would be classified as either stage A1 or A2 disease in the Jewett-Whitmore system28 and “focal” or “diffuse” disease in the Chisholm system12. Disease-specific survival was compared by Cox regression for patients with the following stages of disease: A1, T0a, T0l, and “focal”; A2, T0d (>25 percent cancer in the total specimen),26 T0b, and “diffuse”; B1 and T1; and B2, B3, and T2.
Age-Specific Life Expectancy
The expected survival in the general male populations of the United States and Sweden was determined from standard life tables for the years 1980 (in the United States) and 1980 through 1984 (in Sweden),29,30 since these dates reflected years or partial years of accrual for the studies from these two countries. After verifying the appropriateness of the proportional-hazards assumption, Sweden's published life table for the age of 70 years was compared with the observed survival in the Swedish series (cohorts 415 and 516,17) by adjusting the latter to the age of 70 by means of Cox regression. The U.S. patients (cohorts 313 and 614) were compared with U.S. life tables in the same manner. Observed and expected life expectancy was not compared in Scotland or Israel.
Statistical Analysis
The goal of this study was to calculate conservative estimates of the effect of nonaggressive treatment on disease-specific survival, overall survival, survival among patients who did not die of prostate cancer (noncancer survival), and metastasis-free survival among men with clinically localized prostate cancer. For disease-specific survival, data were censored at the time of death from other causes. Metastasis-free survival was defined as survival without metastasis. For patients who died of prostate cancer without a previous diagnosis of metastasis, the time to metastasis was considered to be the time to death. Factors affecting outcome were assessed with the Cox proportional-hazards regression model,31 which is incorporated into the statistical program STATA32. Survival curves were generated from this program by the Kaplan-Meier method33. Direct comparisons of survival curves were performed with the log-rank test or the Mantel-Haenszel test34.
Results
We identified 10 studies11-21 that met our criteria and contacted their authors. Six groups of investigators were able to provide data on 828 patients in the format requested, including one from Israel (cohort 111), one from Scotland (cohort 212), two from the United States (cohorts 313 and 614), and two from Sweden (cohorts 415 and 516,17) (Table 1Table 1
Distribution of Tumor Grade and Stage among the 828 Patients.). Demographic characteristics of these cohorts are shown in Table 2Table 2
Demographic Characteristics of 828 Patients with Untreated Prostate Cancer..After adjustment for tumor stage, a comparison of the patients from each cohort with tumors classified as grade 1 revealed no significant differences in disease-specific survival according to the log-rank test (P = 0.18). The results for grade 2 tumors were similar (P = 0.92). Therefore, we analyzed together the patients from the different cohorts who had similarly graded tumors. For tumors classified as grade 3, however, patients from Sweden (cohorts 4 and 5) and Israel (cohort 1) had a significantly lower disease-specific survival than patients with grade 3 tumors from the United States (cohorts 3 and 6) (P = 0.03 and P = 0.08, respectively). Nevertheless, all patients with grade 3 tumors were grouped together for analysis because we wished to determine the most conservative estimate of outcome for U.S. patients with this management strategy. Our preliminary analysis also showed no significant differences in disease-specific survival among patients with disease classified as stage T0a, T0l, A1, and local; T0b, T0d, A2, and diffuse; T1 and B1; and T2, B2, and B3 after we controlled for tumor grade. Therefore, the patients with cancers of similar stages were combined and analyzed together.
The Cox proportional-hazards regression model was used to determine the combined effects of the patient's age at diagnosis, the tumor grade, the disease stage, and the origin of the patient cohort on disease-specific survival. Patients were classified into four age groups: less than 61, 61 through 70, 71 through 80, and more than 80 years of age. A multivariate analysis showed that having grade 3 cancer (P<0.001) and belonging to the cohort from Israel (cohort 1) (P<0.02) had a significant negative effect on cancer-specific survival (i.e., mortality due to cancer); conversely, age of less than 61 years (P = 0.014) and membership in the cohort from New York (cohort 6) (P = 0.046) had a significant positive effect (Table 3Table 3
Effect of Age, Tumor Grade, Disease Stage, and Cohort on Mortality Due to Prostate Cancer, as Assessed by the Cox Proportional-Hazards Model.). Since the risk ratio for grade 3 disease was substantially higher than all other risk ratios, the subsequent data analyses were stratified only according to tumor grade.Disease-Specific and Metastasis-free Survival
Disease-specific survival (i.e., survival among only those patients who did not die of causes other than prostate cancer) and metastasis-free survival for grades 1, 2, and 3 tumors are shown in Figure 1Figure 1
Disease-Specific Survival among Untreated Patients with Localized Prostate Cancer, According to Tumor Grade. and Figure 2Figure 2Metastasis-free Survival among Untreated Patients with Localized Prostate Cancer, According to Tumor Grade.. Table 4Table 4
Outcomes of Conservative Management of Localized Prostate Cancer. shows the number of events after 5 and 10 years, and Table 5Table 5
Disease-Specific and Metastasis-free Survival 5 and 10 Years after Conservative Management of Localized Prostate Cancer. shows 5-year and 10-year survival in subgroups of patients. Patients with grade 3 cancer had a significantly lower cancer-specific rate of survival than those with either grade 1 disease (P<0.001) or grade 2 disease (P<0.001). Men with grade 2 cancer had a lower disease-specific survival rate than men with grade 1 disease, but the difference was not significant (P = 0.075 by Cox regression) because of the small number of events (Table 4). The rate of progression to metastasis differed significantly among the three tumor grades (P<0.001 for the comparisons of grade 1 with grade 2 tumors and of grade 2 with grade 3 tumors, by the log-rank test). The median length of time from the detection of metastasis to death from prostate cancer was 36 months.Evaluation of Bias
The data were analyzed for factors that might have biased the results favorably in the previously published reports. One potential source of bias was the inclusion of men who were less healthy than the usual patient with prostate cancer and were therefore more likely to die of other causes before the natural history of their cancer was expressed. For the patients from the United States (cohorts 3 and 6) and Sweden (cohorts 4 and 5), both the noncancer survival and overall survival curves were very similar to the expected survival from the country in question (Figure 3Figure 3
Comparison of Age-Adjusted Survival with Normal Life Expectancy.).We also investigated this source of bias by determining whether the severity of the cancer might have contributed to death from other causes. Despite the progression of disease with increasing tumor grade, however, the noncancer survival curves (i.e., survival among men who did not die of prostate cancer) did not differ significantly among men with grade 1, 2, or 3 cancer (P = 0.77). The differences remained nonsignificant when we adjusted for age using Cox regression analysis. Thus, the relatively favorable outcome associated with conservative management cannot be explained by the inclusion of men with shorter-than-average life expectancies.
Another factor that could have biased the results favorably was the use of delayed local treatment with external-beam radiation (in 18 patients), interstitial radiation (in 46 patients), or radical prostatectomy (in 6 patients) in three of the six studies13-15. For this analysis, men with grade 1 and grade 2 tumors were combined because the 10-year disease-specific survival for these two groups did not differ significantly. The Mantel-Haenszel test comparing two survival curves for equality showed that survival was not significantly higher among the patients who underwent delayed irradiation or radical prostatectomy than among those who received either delayed hormone therapy or no therapy at all (P = 0.53). Too few cases were available to permit us to assess delayed treatment in men with grade 3 disease.
The effect of delayed local treatment on the length of time to the development of metastasis was also assessed. For grade 1 cancers, metastasis-free survival was significantly higher (P<0.001) among the patients treated by observation than among those who underwent delayed surgery or radiation. For grade 2 tumors, metastasis-free survival was higher among the men treated by observation, but the difference was not significant (P<0.07). As before, metastasis-free survival was not assessed among men with grade 3 tumors, because of the small sample size. Thus, the outcomes in this pooled analysis of patients with grade 1 or grade 2 tumors were not favorably biased by the inclusion of men who underwent delayed irradiation or surgery.
The final potential source of bias we evaluated was the inclusion of patients with stage A1, focal, T0a, or T0l cancer (n = 155), because these groups are thought to have a more favorable outcome than patients with other stages of localized disease. A Cox regression analysis comparing men with any of these early disease stages with men with any of the other stages showed that disease-specific survival was not significantly better for men with grade 1 cancer (P = 0.11) or grade 2 cancer (P = 0.32). However, the odds ratio for metastasis-free survival was 2.5 for men with grade 1 or grade 2, stage T0l, T0a, A1, or focal disease, as compared with those with the remaining stages of localized disease. Similarly, metastasis-free survival among patients with stage T0l, T0a, A1, or focal grade 1 or grade 2 cancer was not significantly different (P = 0.09 and P = 0.63, respectively) from that among men with any of the other disease stages. Thus, the overall rates of disease-specific survival reported for the entire population of patients in this study have not been favorably biased by the inclusion of men with disease at the earliest stages (Table 5).
Discussion
Although mortality due to prostate cancer among men with grade 1 or grade 2 disease was only 13 percent at 10 years, as compared with 66 percent among men with grade 3 disease (Table 5), metastatic disease developed significantly more often with increasing tumor grade. By 10 years after diagnosis, metastases had occurred in 19 percent, 42 percent, and 74 percent of the men with grade 1, 2, and 3 cancer, respectively. These results clearly demonstrate that prostate cancer is a progressive disease when managed conservatively.
This analysis shows that previous reports on conservative management were not favorably biased by the inclusion of men who were older or less healthy than the general population, men who were treated with delayed radiation therapy or radical prostatectomy, or men who had stage A1, focal, T0a, or T0l disease.
One other potential source of bias was the method of patient selection, since the data used in our analysis were derived from nonrandomized studies. However, such bias appears relatively unimportant, because five of the six study samples had statistically similar survival, and because the bias applies equally when our results are compared grade by grade with all published reports involving surgery or radiation therapy.
It is possible that some patients were included who did not truly have prostate cancer, since no central pathological review was performed. Many men were considered to have cytologic grade 1 cancer, which in some cases may have been an overdiagnosis. However, disease-specific survival for men with grade 1 cancer diagnosed by cytologic study in Sweden (cohorts 4 and 5) was not significantly higher than that for men with grade 1 cancer diagnosed by histologic examination in the United States (cohorts 3 and 6) (data not shown); moreover, the outcomes were similar for five of the cohorts when analyzed according to tumor grade alone.
In the absence of randomized trials, these data probably provide a reliable estimate of outcome for patients treated with observation and delayed hormone therapy, against which the effect of aggressive therapy can be judged. Unfortunately, the results of aggressive therapy are difficult to determine, because data on disease-specific and metastasis-free survival according to tumor grade have not generally been reported7 and because no similar pooled analysis based on original patient data has been performed. Aggressive treatment may result in a lower mortality from cancer at 10 years among men with grade 1 or grade 2 cancer,35 but the differences appear to be small. Furthermore, aggressive treatment may have a substantial adverse effect on the quality of life. The relative benefit of aggressive treatment for grade 3 cancer is less clear36,37.
Grade-specific metastasis-free survival is also difficult to deduce from the literature. Hanks38 reported eight-year metastasis-free survival rates of approximately 90 percent, 65 percent, and 25 percent for men with grade 1, 2, and 3 localized cancers, respectively, after external-beam radiotherapy, rates that are similar to our findings. Grade-specific data on the results of surgery are not readily available. A recent study comparing outcomes after radiation therapy, surgery, or “watchful waiting” also concluded that the differences at 10 years were small39.
An argument for aggressive therapy36,37,40,41 is that overall survival after treatment closely approximates the expected survival among men of similar ages in the general population. Our data indicate, however, that essentially the same outcome can be achieved for at least 10 years with initially conservative management of grade 1 or grade 2 prostate cancer.
These results have several clinical implications. Despite the 35,000 deaths from prostate cancer expected this year in the United States, our results justify watchful waiting as a reasonable option for men with grade 1 or grade 2 clinically localized prostate cancer, especially if their life expectancy is 10 years or less. For men with a substantially longer life expectancy, however, this approach is associated with a higher probability of living with metastatic disease and of dying from prostate cancer than is aggressive therapy. Whether a higher 10-year disease-specific and metastasis-free survival rate for grade 1 or grade 2 cancer is worth the risk of complications associated with irradiation or surgery should ultimately be the patient's decision38,39. A randomized trial comparing aggressive local therapy with observation or delayed therapy for men with grade 1 or grade 2 cancer is clearly in order to assess the relative benefit of aggressive management as compared with watchful waiting. Finally, new management strategies are needed for men with grade 3 cancer, because neither radical surgery nor radiation therapy substantially lowers the high rates of metastasis and mortality when these patients are treated conservatively36,37.
Supported in part by a grant (1-RO3-HS07230-01) from the Public Health Service, by a Cancer Center Support Grant (P30 CA 14599) from the National Cancer Institute, and by the Cancer and Urology Research Fund at the University of Chicago.
We are indebted to Dr. Ashok Rana of the University of Edinburgh and Dr. S. Nitecki of Rambam Medical Center for their help in obtaining data from their centers, to Dr. Samuel Hellman, Dr. Harry Schoenberg, and Dr. Harvey Golomb of the University of Chicago and Dr. John Wasson of Dartmouth Medical Center for their helpful comments on the manuscript, and to Mr. Duane Corpis for assistance in data entry.
Source Information
From the Departments of Surgery (G.W.C., G.S.G.), Statistics (R.A.T.), Anesthesia and Critical Care (R.A.T.), and the Cancer Research Center (R.A.T.), University of Chicago-Pritzker School of Medicine, Chicago; the Department of Urology, Orebro Medical Center Hospital, and the Cancer Epidemiology Unit, Uppsala University Hospital, Uppsala, Sweden (J.-E.J.); the Department of Urology, Karolinska Hospital, Karolinska, Sweden (J.A.); the Division of Urology, Howard University Hospital, Washington, D.C. (G.W.J.); the Department of Surgery-Urology, University of Edinburgh-Western General Hospital, Edinburgh, Scotland (G.D.C.); the Department of Urology, Rambam Medical Center and Technion-Israel Institute of Technology, Haifa, Israel (B.M., P.M.L.); and the Urology Service, Memorial Sloan-Kettering Institute, New York (J.W.).
Address reprint requests to Dr. Chodak at the University of Chicago Hospitals, Weiss Memorial Hospital, Prostate and Urology Center, 4646 N. Marine Dr., Chicago, IL 60640.
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