Results of Conservative Management of Clinically Localized Prostate Cancer
Gerald W. Chodak, Ronald A. Thisted, Glenn S. Gerber, Jan-Erik Johansson, Jan Adolfsson, George W. Jones, Geoff D. Chisholm, Boaz Moskovitz, Pinhas M. Livne, and John Warner
Background The selection of treatment for patients with localizedprostate cancer requires reliable information about the outcomeof conservative management. Previous studies of this questionare generally considered unreliable because they were uncontrolledand nonrandomized.
Methods We performed a pooled analysis of 828 case records fromsix nonrandomized studies, published since 1985, of men treatedconservatively (with observation and delayed hormone therapybut no radical surgery or irradiation) for clinically localizedprostate cancer. A Cox regression analysis was performed todetermine which factors influenced survival among patients whodid not die of causes other than prostate cancer (disease-specificsurvival). Kaplan-Meier curves for overall and metastasis-freesurvival among such patients were compared with use of the log-rankmethod and the Mantel-Haenszel test.
Results Factors that had a significant effect on disease-specificsurvival were grade 3 tumors (risk ratio, 10.04), residencein 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 causesother than prostate cancer censored) was 87 percent for menwith grade 1 or 2 tumors and 34 percent for those with grade3 tumors; metastasis-free survival among men who had not diedof other causes was 81 percent for grade 1, 58 percent for grade2, and 26 percent for grade 3 disease. These findings were notaffected by the inclusion of men who had early-stage cancer,were older, had worse-than-average health, or underwent delayedradiation therapy or radical prostatectomy.
Conclusions The strategy of initial conservative managementand delayed hormone therapy is a reasonable choice for somemen with grade 1 or 2 clinically localized prostate cancer,particularly for those who have an average life expectancy of10 years or less. New treatment strategies are needed for menwith grade 3 prostate cancer.
Prostate cancer is now the most common cancer and the secondmost common cause of death from cancer among men in the UnitedStates1. Both the incidence and the mortality rate have continuedto rise, with no reduction projected over the next several years2.Since a large percentage of patients have advanced disease atthe time of diagnosis,3 routine screening of asymptomatic men,which increases early detection,4 has been recommended, butwe 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 neverbeen properly determined. To date, only one randomized trialhas compared the results of radical surgery with those of conservativemanagement6. Although the rate of mortality from prostate cancerwas similar in the two groups, methodologic flaws make the conclusionsof this study suspect. The lack of a clearly superior therapyhas contributed to marked differences in treatment recommendationsin different regions of the United States and in Europe7.
The variable natural history of the disease contributes to thisproblem. At least 30 percent of men over 50 years of age havehistologic evidence of prostate cancer,8,9 yet only a smallfraction of these cancers are newly detected each year or causedeath10. Prognostic factors have been recognized, but reliablemethods for identifying potentially life-threatening tumorsare lacking, and aggressive treatment of some patients may beunnecessary.
Specifically, information is needed about the outcome of clinicallylocalized tumors treated conservatively. Since 1985, such informationhas been reported from 10 nonrandomized studies,11,12,13,14,15,16,17,18,19,20,21but these studies have all been criticized because of factorsthat could have biased the results.
Recently, Stewart and Parmar showed that meta-analyses willbe least biased and most reliable if data on individual patientsare pooled rather than if only published summary data are combined22.To obtain a reliable but conservative estimate of the outcomeof nonaggressive management, we performed a pooled analysisusing data on individual patients from six nonrandomized studiesof patients with clinically localized prostate cancer that wasmanaged conservatively with observation and delayed hormonetherapy but without irradiation or radical surgery11,12,13,14,15,16,17.
Methods
Sources of Data
We performed a MEDLINE search to identify studies of patientswith clinically localized prostate cancer treated with observationand delayed hormone therapy that were published from January1985 through July 1992. The bibliographies in published literaturereviews on this subject were used to identify other appropriatestudies. Authors of studies that reported only on patients withstage A1 disease (one to three prostate chips containing cancer)or stage T0a disease16 (less than 25 percent of the prostatesample containing cancer) were not contacted. A letter was sentto the principal author of each of the papers that met our criteria,inviting him or her to participate by providing original dataon patients. The authors' cooperation was needed because insufficientinformation 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 timeto death from prostate cancer or from other causes, the lengthof time to the identification of distant metastases (metastasis-freesurvival), and the length of time to the most recent follow-up,if the patient was still alive. No attempt was made to reviewthe pathological or cytologic findings. Some men eventuallyreceived local therapy, but all such patients continued to beincluded in our analyses. Patients in whom hormone therapy wasadministered for symptomatic progression or metastases wereincluded 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, apreliminary analysis was performed to determine which patientscould be combined and analyzed together without favorably biasingthe outcome.
The disease-specific survival (i.e., survival with censorshipof patients who died from causes other than prostate cancer)of patients with cytologic23 grade 1 cancers was compared withthat of patients with well-differentiated tumors on histologicexamination24 or tumors with a Gleason sum25 of 2 through 4(combined classification, grade 1), cytologic grade 2 cancerswere compared with tumors that were moderately differentiatedon histologic examination or tumors with a Gleason sum of 5through 7 (grade 2), and cytologic grade 3 cancers were comparedwith histologically poorly differentiated cancers or tumorswith a Gleason sum of 8 through 10 (grade 3).
Although four systems were used to determine patients' cancerstages, comparable stages were easily identified except forstages A1, "focal," T0l, and T0a tumors. Stages T0a and T0lmodified11,16 from the TNM system26,27 include cancers thatwould be classified as either stage A1 or A2 disease in theJewett-Whitmore system28 and "focal" or "diffuse" disease inthe Chisholm system12. Disease-specific survival was comparedby Cox regression for patients with the following stages ofdisease: A1, T0a, T0l, and "focal"; A2, T0d (>25 percentcancer in the total specimen),26 T0b, and "diffuse"; B1 andT1; and B2, B3, and T2.
Age-Specific Life Expectancy
The expected survival in the general male populations of theUnited States and Sweden was determined from standard life tablesfor the years 1980 (in the United States) and 1980 through 1984(in Sweden),29,30 since these dates reflected years or partialyears of accrual for the studies from these two countries. Afterverifying the appropriateness of the proportional-hazards assumption,Sweden's published life table for the age of 70 years was comparedwith the observed survival in the Swedish series (cohorts 415and 516,17) by adjusting the latter to the age of 70 by meansof Cox regression. The U.S. patients (cohorts 313 and 614) werecompared with U.S. life tables in the same manner. Observedand expected life expectancy was not compared in Scotland orIsrael.
Statistical Analysis
The goal of this study was to calculate conservative estimatesof the effect of nonaggressive treatment on disease-specificsurvival, overall survival, survival among patients who didnot die of prostate cancer (noncancer survival), and metastasis-freesurvival among men with clinically localized prostate cancer.For disease-specific survival, data were censored at the timeof death from other causes. Metastasis-free survival was definedas survival without metastasis. For patients who died of prostatecancer without a previous diagnosis of metastasis, the timeto metastasis was considered to be the time to death. Factorsaffecting outcome were assessed with the Cox proportional-hazardsregression model,31 which is incorporated into the statisticalprogram STATA32. Survival curves were generated from this programby the Kaplan-Meier method33. Direct comparisons of survivalcurves were performed with the log-rank test or the Mantel-Haenszeltest34.
Results
We identified 10 studies11,12,13,14,15,16,17,18,19,20,21 thatmet our criteria and contacted their authors. Six groups ofinvestigators were able to provide data on 828 patients in theformat requested, including one from Israel (cohort 111), onefrom Scotland (cohort 212), two from the United States (cohorts313 and 614), and two from Sweden (cohorts 415 and 516,17) (Table 1).Demographic characteristics of these cohorts are shown inTable 2.
Table 2. Demographic Characteristics of 828 Patients with Untreated Prostate Cancer.
After adjustment for tumor stage, a comparison of the patientsfrom each cohort with tumors classified as grade 1 revealedno significant differences in disease-specific survival accordingto the log-rank test (P = 0.18). The results for grade 2 tumorswere similar (P = 0.92). Therefore, we analyzed together thepatients from the different cohorts who had similarly gradedtumors. For tumors classified as grade 3, however, patientsfrom Sweden (cohorts 4 and 5) and Israel (cohort 1) had a significantlylower disease-specific survival than patients with grade 3 tumorsfrom the United States (cohorts 3 and 6) (P = 0.03 and P = 0.08,respectively). Nevertheless, all patients with grade 3 tumorswere grouped together for analysis because we wished to determinethe most conservative estimate of outcome for U.S. patientswith this management strategy. Our preliminary analysis alsoshowed no significant differences in disease-specific survivalamong 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 patientswith cancers of similar stages were combined and analyzed together.
The Cox proportional-hazards regression model was used to determinethe combined effects of the patient's age at diagnosis, thetumor grade, the disease stage, and the origin of the patientcohort on disease-specific survival. Patients were classifiedinto four age groups: less than 61, 61 through 70, 71 through80, and more than 80 years of age. A multivariate analysis showedthat having grade 3 cancer (P<0.001) and belonging to thecohort from Israel (cohort 1) (P<0.02) had a significantnegative effect on cancer-specific survival (i.e., mortalitydue 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 3). Since the riskratio for grade 3 disease was substantially higher than allother risk ratios, the subsequent data analyses were stratifiedonly according to tumor grade.
Table 3. Effect of Age, Tumor Grade, Disease Stage, and Cohort on Mortality Due to Prostate Cancer, as Assessed by the Cox Proportional-Hazards Model.
Disease-Specific and Metastasis-free Survival
Disease-specific survival (i.e., survival among only those patientswho did not die of causes other than prostate cancer) and metastasis-freesurvival for grades 1, 2, and 3 tumors are shown in Figure 1and Figure 2. Table 4 shows the number of events after 5 and10 years, and Table 5 shows 5-year and 10-year survival in subgroupsof patients. Patients with grade 3 cancer had a significantlylower cancer-specific rate of survival than those with eithergrade 1 disease (P<0.001) or grade 2 disease (P<0.001).Men with grade 2 cancer had a lower disease-specific survivalrate than men with grade 1 disease, but the difference was notsignificant (P = 0.075 by Cox regression) because of the smallnumber of events (Table 4). The rate of progression to metastasisdiffered significantly among the three tumor grades (P<0.001for the comparisons of grade 1 with grade 2 tumors and of grade2 with grade 3 tumors, by the log-rank test). The median lengthof time from the detection of metastasis to death from prostatecancer was 36 months.
Table 5. Disease-Specific and Metastasis-free Survival 5 and 10 Years after Conservative Management of Localized Prostate Cancer.
Evaluation of Bias
The data were analyzed for factors that might have biased theresults favorably in the previously published reports. One potentialsource of bias was the inclusion of men who were less healthythan the usual patient with prostate cancer and were thereforemore likely to die of other causes before the natural historyof their cancer was expressed. For the patients from the UnitedStates (cohorts 3 and 6) and Sweden (cohorts 4 and 5), boththe noncancer survival and overall survival curves were verysimilar to the expected survival from the country in question(Figure 3).
Figure 3. Comparison of Age-Adjusted Survival with Normal Life Expectancy.
Panel A shows normal life expectancy for 70-year-old men in Sweden in 1980 (solid line) and survival among patients from the two Swedish series (cohorts 4 and 5) who did not die of prostate cancer, adjusted to the age of 70 years (dashed line). Panel B shows the same life-table curve for 70-year-old men in Sweden (solid line) and overall survival for men in the Swedish cohorts, adjusted to the age of 70 years (dashed line). Panel C shows the normal life expectancy for 70-year-old men in the United States in 1980 through 1984 (solid line) and survival among patients from the two U.S. series (cohorts 3 and 6) who did not die of prostate cancer, adjusted to the age of 70 years (dashed line). Panel D shows the same life-table curve for 70-year-old men in the United States (solid line) and overall survival for men in the U.S. cohorts, adjusted to the age of 70 years (dashed line). Survival curves for the study cohorts were derived by Cox regression analysis.
We also investigated this source of bias by determining whetherthe severity of the cancer might have contributed to death fromother causes. Despite the progression of disease with increasingtumor grade, however, the noncancer survival curves (i.e., survivalamong men who did not die of prostate cancer) did not differsignificantly among men with grade 1, 2, or 3 cancer (P = 0.77).The differences remained nonsignificant when we adjusted forage using Cox regression analysis. Thus, the relatively favorableoutcome associated with conservative management cannot be explainedby the inclusion of men with shorter-than-average life expectancies.
Another factor that could have biased the results favorablywas the use of delayed local treatment with external-beam radiation(in 18 patients), interstitial radiation (in 46 patients), orradical prostatectomy (in 6 patients) in three of the six studies13,14,15.For this analysis, men with grade 1 and grade 2 tumors werecombined because the 10-year disease-specific survival for thesetwo groups did not differ significantly. The Mantel-Haenszeltest comparing two survival curves for equality showed thatsurvival was not significantly higher among the patients whounderwent delayed irradiation or radical prostatectomy thanamong those who received either delayed hormone therapy or notherapy at all (P = 0.53). Too few cases were available to permitus to assess delayed treatment in men with grade 3 disease.
The effect of delayed local treatment on the length of timeto the development of metastasis was also assessed. For grade1 cancers, metastasis-free survival was significantly higher(P<0.001) among the patients treated by observation thanamong those who underwent delayed surgery or radiation. Forgrade 2 tumors, metastasis-free survival was higher among themen treated by observation, but the difference was not significant(P<0.07). As before, metastasis-free survival was not assessedamong men with grade 3 tumors, because of the small sample size.Thus, the outcomes in this pooled analysis of patients withgrade 1 or grade 2 tumors were not favorably biased by the inclusionof men who underwent delayed irradiation or surgery.
The final potential source of bias we evaluated was the inclusionof patients with stage A1, focal, T0a, or T0l cancer (n = 155),because these groups are thought to have a more favorable outcomethan patients with other stages of localized disease. A Coxregression analysis comparing men with any of these early diseasestages with men with any of the other stages showed that disease-specificsurvival was not significantly better for men with grade 1 cancer(P = 0.11) or grade 2 cancer (P = 0.32). However, the odds ratiofor metastasis-free survival was 2.5 for men with grade 1 orgrade 2, stage T0l, T0a, A1, or focal disease, as compared withthose 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 significantlydifferent (P = 0.09 and P = 0.63, respectively) from that amongmen with any of the other disease stages. Thus, the overallrates of disease-specific survival reported for the entire populationof patients in this study have not been favorably biased bythe inclusion of men with disease at the earliest stages (Table 5).
Discussion
Although mortality due to prostate cancer among men with grade1 or grade 2 disease was only 13 percent at 10 years, as comparedwith 66 percent among men with grade 3 disease (Table 5), metastaticdisease developed significantly more often with increasing tumorgrade. By 10 years after diagnosis, metastases had occurredin 19 percent, 42 percent, and 74 percent of the men with grade1, 2, and 3 cancer, respectively. These results clearly demonstratethat prostate cancer is a progressive disease when managed conservatively.
This analysis shows that previous reports on conservative managementwere not favorably biased by the inclusion of men who were olderor less healthy than the general population, men who were treatedwith delayed radiation therapy or radical prostatectomy, ormen who had stage A1, focal, T0a, or T0l disease.
One other potential source of bias was the method of patientselection, since the data used in our analysis were derivedfrom nonrandomized studies. However, such bias appears relativelyunimportant, because five of the six study samples had statisticallysimilar survival, and because the bias applies equally whenour results are compared grade by grade with all published reportsinvolving surgery or radiation therapy.
It is possible that some patients were included who did nottruly have prostate cancer, since no central pathological reviewwas performed. Many men were considered to have cytologic grade1 cancer, which in some cases may have been an overdiagnosis.However, disease-specific survival for men with grade 1 cancerdiagnosed by cytologic study in Sweden (cohorts 4 and 5) wasnot significantly higher than that for men with grade 1 cancerdiagnosed by histologic examination in the United States (cohorts3 and 6) (data not shown); moreover, the outcomes were similarfor five of the cohorts when analyzed according to tumor gradealone.
In the absence of randomized trials, these data probably providea reliable estimate of outcome for patients treated with observationand delayed hormone therapy, against which the effect of aggressivetherapy can be judged. Unfortunately, the results of aggressivetherapy are difficult to determine, because data on disease-specificand metastasis-free survival according to tumor grade have notgenerally been reported7 and because no similar pooled analysisbased on original patient data has been performed. Aggressivetreatment may result in a lower mortality from cancer at 10years among men with grade 1 or grade 2 cancer,35 but the differencesappear to be small. Furthermore, aggressive treatment may havea substantial adverse effect on the quality of life. The relativebenefit of aggressive treatment for grade 3 cancer is less clear36,37.
Grade-specific metastasis-free survival is also difficult todeduce from the literature. Hanks38 reported eight-year metastasis-freesurvival rates of approximately 90 percent, 65 percent, and25 percent for men with grade 1, 2, and 3 localized cancers,respectively, after external-beam radiotherapy, rates that aresimilar to our findings. Grade-specific data on the resultsof surgery are not readily available. A recent study comparingoutcomes 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 overallsurvival after treatment closely approximates the expected survivalamong men of similar ages in the general population. Our dataindicate, however, that essentially the same outcome can beachieved for at least 10 years with initially conservative managementof grade 1 or grade 2 prostate cancer.
These results have several clinical implications. Despite the35,000 deaths from prostate cancer expected this year in theUnited States, our results justify watchful waiting as a reasonableoption for men with grade 1 or grade 2 clinically localizedprostate cancer, especially if their life expectancy is 10 yearsor less. For men with a substantially longer life expectancy,however, this approach is associated with a higher probabilityof living with metastatic disease and of dying from prostatecancer than is aggressive therapy. Whether a higher 10-yeardisease-specific and metastasis-free survival rate for grade1 or grade 2 cancer is worth the risk of complications associatedwith irradiation or surgery should ultimately be the patient'sdecision38,39. A randomized trial comparing aggressive localtherapy with observation or delayed therapy for men with grade1 or grade 2 cancer is clearly in order to assess the relativebenefit of aggressive management as compared with watchful waiting.Finally, new management strategies are needed for men with grade3 cancer, because neither radical surgery nor radiation therapysubstantially lowers the high rates of metastasis and mortalitywhen these patients are treated conservatively36,37.
Supported in part by a grant (1-RO3-HS07230-01) from the PublicHealth Service, by a Cancer Center Support Grant (P30 CA 14599)from the National Cancer Institute, and by the Cancer and UrologyResearch Fund at the University of Chicago.
We are indebted to Dr. Ashok Rana of the University of Edinburghand Dr. S. Nitecki of Rambam Medical Center for their help inobtaining data from their centers, to Dr. Samuel Hellman, Dr.Harry Schoenberg, and Dr. Harvey Golomb of the University ofChicago and Dr. John Wasson of Dartmouth Medical Center fortheir helpful comments on the manuscript, and to Mr. Duane Corpisfor 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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