Radical Prostatectomy versus Watchful Waiting in Early Prostate Cancer
Anna Bill-Axelson, M.D., Lars Holmberg, M.D., Ph.D., Mirja Ruutu, M.D., Ph.D., Michael Häggman, M.D., Ph.D., Swen-Olof Andersson, M.D., Ph.D., Stefan Bratell, M.D., Ph.D., Anders Spångberg, M.D., Ph.D., Christer Busch, M.D., Ph.D., Stig Nordling, M.D., Ph.D., Hans Garmo, Ph.D., Juni Palmgren, Ph.D., Hans-Olov Adami, M.D., Ph.D., Bo Johan Norlén, M.D., Ph.D., Jan-Erik Johansson, M.D., Ph.D., for the Scandinavian Prostate Cancer Group Study No. 4
Background In 2002, we reported the initial results of a trialcomparing radical prostatectomy with watchful waiting in themanagement of early prostate cancer. After three more yearsof follow-up, we report estimated 10-year results.
Methods From October 1989 through February 1999, 695 men withearly prostate cancer (mean age, 64.7 years) were randomly assignedto radical prostatectomy (347 men) or watchful waiting (348men). The follow-up was complete through 2003, with blindedevaluation of the causes of death. The primary end point wasdeath due to prostate cancer; the secondary end points weredeath from any cause, metastasis, and local progression.
Results During a median of 8.2 years of follow-up, 83 men inthe surgery group and 106 men in the watchful-waiting groupdied (P=0.04). In 30 of the 347 men assigned to surgery (8.6percent) and 50 of the 348 men assigned to watchful waiting(14.4 percent), death was due to prostate cancer. The differencein the cumulative incidence of death due to prostate cancerincreased from 2.0 percentage points after 5 years to 5.3 percentagepoints after 10 years, for a relative risk of 0.56 (95 percentconfidence interval, 0.36 to 0.88; P=0.01 by Gray's test). Fordistant metastasis, the corresponding increase was from 1.7to 10.2 percentage points, for a relative risk in the surgerygroup of 0.60 (95 percent confidence interval, 0.42 to 0.86;P=0.004 by Gray's test), and for local progression, the increasewas from 19.1 to 25.1 percentage points, for a relative riskof 0.33 (95 percent confidence interval, 0.25 to 0.44; P<0.001by Gray's test).
Conclusions Radical prostatectomy reduces disease-specific mortality,overall mortality, and the risks of metastasis and local progression.The absolute reduction in the risk of death after 10 years issmall, but the reductions in the risks of metastasis and localtumor progression are substantial.
Radical prostatectomy is becoming one of the most common majorsurgical procedures in many Western countries. In the UnitedStates alone, an estimated 60,000 men undergo this operationeach year. However, to our knowledge, only one randomized trialquantified the benefit of radical prostatectomy.1
In 2002, we presented the results of a clinical trial in whichradical prostatectomy was compared with watchful waiting inthe management of early prostate cancer.1 Our analysis was basedon a mean follow-up time of 6.2 years, a relatively short periodin relation to the often long natural history of early prostatecancer.2 We found that, as compared with watchful waiting, radicalprostatectomy reduced the risk of death due to prostate cancerby 50 percent and the risk of distant metastasis by 37 percent,but there was no statistically significant reduction in overallmortality.
We now present a second analysis after an additional three yearsof follow-up, in accordance with the study protocol. Our mainpurpose was to analyze two hypotheses: first, that the relativereduction in the risk of death due to prostate cancer aftersurgery increases over time because removal of the primary tumorprevents metastasis and, second, that radical prostatectomysignificantly improves overall survival.
Methods
Study Design
Details concerning study design and methods have been publishedpreviously.1 The protocol, defined in 1988, is available withthe full text of this article at www.nejm.org.
From 1989 to 1999, 695 men from 14 centers in Sweden, Finland,and Iceland were enrolled. The eligibility criteria includedan age under 75 years; the presence of newly diagnosed, untreated,localized prostate cancer, as verified by cytologic or histologicexamination, with a tumor stage of T0d (later changed to T1b),T1, or T2 (T1c was included in 1994)3,4 (Table 1); a healthstatus that would permit radical prostatectomy; and a life expectancyof more than 10 years. The tumor had to be well differentiatedto moderately well differentiated, according to the definitionestablished by the World Health Organization.5 Patients hadto have a bone scan that showed no abnormalities and a prostate-specificantigen (PSA) level of less than 50 ng per milliliter. If thediagnosis had been established after transurethral resection,at least six blocks of prostate tissue should have been examined.After oral informed consent was received from eligible patients,they were randomly assigned to undergo either radical prostatectomyor watchful waiting through a telephone service outside theclinics. Stratification was made according to tumor grade andrandomization center.
Table 1. Baseline Characteristics of the 695 Men Enrolled in the Study.
For men assigned to the radical-prostatectomy group, surgerystarted with dissection of the pelvic lymph nodes.6 If therewere no signs of metastasis in frozen sections, the operationwas continued with retropubic radical prostatectomy.7 The menin the watchful-waiting group received no initial treatmentother than the transurethral resection some of them had alreadyundergone.
Hormonal treatment was recommended for men with symptomaticlocal progression in the radical-prostatectomy group and forthose with disseminated disease in both groups. Transurethralresection was recommended as the initial treatment for men withurinary obstruction in the watchful-waiting group. In January2003, an amendment to the protocol allowed men in both groupsto begin hormonal therapy if their physicians advised it.
Follow-up and Definition of Clinical Events
The participants were seen every six months during the firsttwo years and then annually for a clinical examination and bloodtests (to evaluate hemoglobin, PSA, alkaline phosphatase, andcreatinine levels). A bone scan and a chest radiograph wereobtained annually until 1997; thereafter, chest radiographswere obtained only once a year for the first two years afterrandomization. The clinical follow-up continued for all patientsexcept nine, who underwent blood tests (including tests forPSA levels) and bone scanning when possible but who did nothave clinical visits owing to old age and coexisting illnesses.Beginning in 2003, bone scans were allowed every second yearif the patient had no biochemical or clinical signs of progression.In 2001, a pathological review of cytologic and histologic datathat were available at inclusion was carried out. For the purposeof this analysis, all patient records were retrieved and individuallyreviewed for new events.
An independent end-point committee determined the cause of deathon the basis of standardized extractions from the patient files;for this determination, the treatment group was not revealed.The committee used six categories of cause of death: prostatecancer; another main cause but with distant metastases, regardlessof local status; another main cause but with local progression,without distant metastases; another main cause, but with localprogression and unknown status concerning distant metastases;another main cause, with no evidence of tumor recurrence, tumorprogression, or metastases; and another main cause within thefirst month after randomization.
In the radical-prostatectomy group, local progression was definedas the presence of a histologically confirmed local tumor. Inthe watchful-waiting group, men with palpable transcapsulartumor growth or with symptoms of urinary obstruction that necessitatedintervention were classified as having local progression. Distantmetastases were considered present when bone scans, skeletalradiographs, computed tomographic scans, or chest radiographsrevealed metastases or if lymph nodes at sites other than theregional sites showed cytologic or histologic evidence of prostatecancer.
Statistical Analysis
There were four main end points: disease-specific death, withdeath due to prostate cancer (the first cause-of-death category)considered the event and death from other causes treated asa competing risk; distant metastasis, with its diagnosis consideredthe event and death from other causes treated as a competingrisk; local progression, with death treated as a competing risk;and death from any cause.
All analyses were carried out in accordance with the intention-to-treatprinciple. Relative risks (with 95 percent confidence intervals)and differences in cumulative incidence (with 95 percent confidenceintervals) were used as measures of effect for each end point.Gray's test8 was used to test the hypothesis that there wasno difference between the treatment groups; a P value of lessthan 0.05 (two-sided) was considered to indicate statisticalsignificance. The relative risks were estimated from the Coxproportional-hazards model. Cumulative incidence (calculatedin terms of integrated subdensity) rather than cumulative hazard(integrated subhazard) was used in the acknowledgment that theend points constitute competing events.9 The results presentedhere and in the previous report1 involved low absolute risksfor disease-specific death and death from any cause, with nosensitivity to whether cumulative incidence rates or cumulativehazard rates were used.
Effect modification was first investigated through simple stratifiedanalyses. For all end points, three prespecified subgroup analyseswere carried out: analysis according to age at diagnosis —less than 65 years of age as compared with 65 years of age orolder; analysis according to PSA level at diagnosis —10 ng per milliliter or lower as compared with more than 10ng per milliliter; and analysis according to the Gleason scoreof the prerandomization biopsy specimen — lower than 7as compared with 7 or more (on a scale of 2 to 10, with 10 indicatingthe most poorly differentiated tumors). Any modification ofthe effect of radical prostatectomy according to subgroup wastested by a Cox proportional-hazards model, which included aninteraction term between subgroup category and randomizationgroup. In a second step, we further explored the interactionby including the possible effect modifier (age, PSA level atdiagnosis, or Gleason score) as a continuous variable. Whenthere was an indication of effect modification, we further controlledfor the PSA level at diagnosis, the tumor stage, the Gleasonscore, and the year at inclusion by adding these as additionalcovariates in the Cox proportional-hazards model.
Results
We randomly assigned 347 men to radical prostatectomy and 348to watchful waiting. Relevant characteristics at the time ofinclusion were similar in the two groups. Most patients (76percent) had stage T2 tumors (i.e., the tumor was confined withinthe prostate), and in only 12 percent were T1c (nonpalpable)tumors detected by means of PSA testing (Table 1). At the endof 2003, 21 men assigned to radical prostatectomy had not undergonesurgery, and 43 assigned to watchful waiting had undergone curativetreatment. Lymph-node metastases, which precluded surgery, werefound in frozen sections from 23 men in the radical-prostatectomygroup.
During follow-up, fewer men in the radical-prostatectomy groupthan in the watchful-waiting group died of prostate cancer (30vs. 50, P=0.01). As for causes of death other than prostatecancer, the numbers were similar in the two groups (53 and 56,respectively). However, among men who died from causes otherthan prostate cancer, a larger number in the watchful-waitinggroup had metastases or local progression. In terms of deathfrom any cause, 23 more men in the watchful-waiting group thanin the radical-prostatectomy group died (106 vs. 83, P=0.04)(Table 2).
Table 2. Causes of Death, According to the Final Consensus of the End-Point Committee.
Disease-Specific Mortality
The difference between the two groups in the cumulative incidenceof death from prostate cancer increased over time, from 2 percentagepoints (95 percent confidence interval, –0.6 to 4.7) afterfive years of follow-up to 5.3 percentage points (95 percentconfidence interval, –0.3 to 11.0) after 10 years, infavor of radical prostatectomy. The relative risk among menassigned to radical prostatectomy, as compared with those assignedto watchful waiting, was 0.56 (95 percent confidence interval,0.36 to 0.88) (Figure 1A and Table 3).
Table 3. Cumulative Incidence of the Main End Points and Corresponding Relative Risks.
Distant Metastases
The cumulative incidence of distant metastases was similar inthe two groups during the first five years (8.1 percent in theradical-prostatectomy group and 9.8 percent in the watchful-waitinggroup, P=0.42). However, a difference emerged after that time:at the second follow-up, 50 of the 347 men in the radical-prostatectomygroup had distant metastases, as compared with 79 of the 348men in the watchful-waiting group. In the radical-prostatectomygroup, the absolute risk reduction at 10 years was 10.2 percentagepoints (95 percent confidence interval, 3.1 to 17.2), correspondingto a relative risk of 0.60 (95 percent confidence interval,0.42 to 0.86) (Figure 2A and Table 3).
Figure 2. Cumulative Incidence of Distant Metastasis (Panel A) and of Death from Any Cause (Panel B).
Local Progression
The difference between the two groups in the cumulative incidenceof local progression was statistically significant after fiveyears of follow-up (8.1 percent in the radical-prostatectomygroup vs. 27.2 percent in the watchful-waiting group, P<0.01);the difference increased over time, to 64 men with local progressionamong the 347 in the prostatectomy group, as compared with 149men among the 348 in the watchful-waiting group, at the secondfollow-up. The difference in the absolute risk reduction after10 years was 25.1 percentage points (19.2 percent vs. 44.3 percent),corresponding to a relative risk in the radical-prostatectomygroup of 0.33 (95 percent confidence interval, 0.25 to 0.44)(Table 3).
Overall Mortality
The cumulative incidence of death from any cause was similarin the two groups during the first five years (7.8 percent forradical prostatectomy vs. 9.8 percent for watchful waiting).At the last follow-up, 83 of 347 men in the radical-prostatectomygroup and 106 of 348 in the watchful-waiting group had died.After randomization to radical prostatectomy, the absolute reductionin the risk of death from any cause after 10 years was 5.0 percentagepoints, corresponding to a relative risk of 0.74 (95 percentconfidence interval, 0.56 to 0.99; P=0.04 by Gray's test) (Figure 2Band Table 3).
Other Treatments
Hormonal treatment was administered less often in the radical-prostatectomygroup than in the watchful-waiting group (110 of 347 patientsvs. 177 of 348, P<0.01). The mean time to hormonal treatmentwas 4.5 years in the radical-prostatectomy group and 4.8 yearsin the watchful-waiting group. Palliative radiation was alsoadministered less often in the radical-prostatectomy group thanin the watchful-waiting group (29 patients vs. 38 patients,P=0.30), as was laminectomy (4 patients vs.11 patients, P=0.04).
Subgroup Analyses
In planned, simple stratified analyses, we found that the benefitof radical prostatectomy in terms of disease-specific mortalitydiffered according to age group but not according to the PSAlevel at diagnosis or the Gleason score. A further investigationof disease-specific mortality with the use of a Cox proportional-hazardsmodel that included the randomization group, the patient's ageas a continuous variable, and an interaction term showed thatthe interaction term was statistically significant (P=0.03).When the same model was augmented with the PSA level at diagnosis,the tumor stage, the Gleason score, and the year at inclusion,the P value for the interaction term shifted to 0.08. For overallmortality, the P value for the interaction term in the correspondingtwo analyses shifted only marginally and remained less than0.01. The cumulative incidence of death from prostate cancerin men under 65 years of age in the watchful-waiting group was19.2 percent at 10 years. This was markedly higher than thecumulative incidence of death in the other subgroups definedaccording to randomization group and age, for which the incidencevaried from 8.5 percent to 11.5 percent (Figure 1B).
Discussion
In this comparison of radical prostatectomy with watchful waitingfor patients with prostate cancer, the 10-year absolute differencesin disease-specific and overall mortality were statisticallysignificant, by 5.3 (P=0.01) and 5.0 (P=0.04) percentage points,respectively, in favor of radical prostatectomy. In addition,the cumulative incidence of distant metastasis was 10.2 percentagepoints lower in the surgery group than in the watchful-waitinggroup. Because clinical manifestations of disseminated diseasevirtually always precede death,2 this finding might herald afurther lowering of the risk of death due to prostate cancerin the radical-prostatectomy group after a longer period offollow-up. We found no evidence that the benefit of radicalprostatectomy was exaggerated by more frequent administrationof hormonal treatment, since hormonal therapy was given lessoften in the radical-prostatectomy group than in the watchful-waitinggroup (110 patients vs. 177 patients).
We found that the reduction in disease-specific mortality asa result of radical prostatectomy was greatest among, or evenlimited to, patients younger than 65 years. The multivariateanalyses indicated that this finding was attributable, onlyto a limited extent, to differences between younger and oldermen in the distribution of PSA levels or Gleason scores; however,there may have been other differences in characteristics betweenyounger and older men at the time of inclusion. These resultshave limited interpretability for two additional reasons: theywere based on small numbers, since the study was not poweredto analyze subgroups, and the analysis was exploratory ratherthan based on any a priori biologic hypothesis. Therefore, theresults of the subgroup analyses should be an incentive to conductfurther research rather than to introduce an immediate changein clinical practice.
Observational cohort studies have analyzed survival rates amongpatients whose cancer was managed by watchful waiting. After10 years of follow-up, such studies yielded disease-specificsurvival rates of 87 percent,10 86 percent,11 and 83 percent.12In our trial, the corresponding 10-year figure was 85 percent.The similar prognosis among patients randomly assigned to watchfulwaiting in our trial and those analyzed in observational studiesindicates that our findings are generalizable to patients insimilar settings. If watchful waiting with curative interventionin patients with rising PSA levels (as detected with activemonitoring) yields better survival than does traditional watchfulwaiting, the difference between watchful waiting and primarysurgery should diminish. As yet, however, there is no evidencefrom a randomized trial that the monitoring of PSA levels withaccompanying curative intervention will yield better resultsthan will watchful waiting as used in this trial and in theobservational studies.
In this follow-up period, we found a substantial absolute differencebetween the two groups in terms of local progression (whichcan cause problems with the micturition, pain, and anxiety).Moreover, the need for hormonal treatment increased in frequencyin the watchful-waiting group, as did the need for palliativeradiation; both types of treatment were associated with sideeffects that influenced patients' quality of life and well-being.Thus, the more immediate, though stable, side effects associatedwith surgery13 (predominantly, impotence and incontinence) andreported previously for this study,14 should be weighed againstthe increasing incidence of symptoms and use of treatments afterthe progression of disease in the watchful-waiting group. However,for several reasons, a reevaluation of the costs and benefitsof radical prostatectomy in the era of widespread screeningis necessary: the number of patients needed to treat may behigh, and the lead time to the onset of symptoms and treatmentmay be long in those undergoing monitoring, but the removalof small tumors may facilitate surgery and result in fewer sideeffects.
Our 10-year estimates show that radical prostatectomy is associatedwith a statistically significant reduction in all the end pointsthat we investigated, with a relative reduction of 44 percentin mortality due to prostate cancer, of 26 percent in overallmortality, of 40 percent in the risk of distant metastasis,and of 67 percent in local progression. Since, in absolute terms,the reduction in mortality is moderate, clinical decision makingand patient counseling will remain difficult. The additionalfinding that radical prostatectomy substantially reduces therisk of metastasis and symptomatic local tumor growth may, however,be of some help in guiding therapy, and we expect that the benefitsof this surgery will increase during longer periods of follow-up.
Supported by the Swedish Cancer Society.
* The participants in the Scandinavian Prostate Cancer Group StudyNo. 4 are listed in the Appendix.
Source Information
From the Department of Urology (A.B.-A., M.H., B.J.N.), the Regional Oncologic Center (L.H., H.G.), and the Department of Pathology (C.B.), University Hospital, Uppsala, Sweden; the Departments of Urology (M.R.) and Pathology (S.N.), University of Helsinki and University Hospital of Helsinki, Helsinki; the Department of Urology (S.-O.A., J.-E.J.) and the Center for Assessment of Medical Technology (J.-E.J.), Örebro University Hospital, Örebro, Sweden; the Department of Urology, Borås Hospital, Borås, Sweden (S.B.); the Department of Urology, Linköping University Hospital, Linköping, Sweden (A.S.); the Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm (J.P., H.-O.A.); and the Department of Epidemiology, Harvard School of Public Health, Boston (H.-O.A.). Drs. Bill-Axelson and Holmberg contributed equally to the article.
Address reprint requests to Dr. Bill-Axelson at the Department of Urology, University Hospital, SE-751 85 Uppsala, Sweden, or at anna.bill.axelson{at}akademiska.se.
References
Holmberg L, Bill-Axelson A, Helgesen F, et al. A randomized trial comparing radical prostatectomy with watchful waiting in early prostate cancer. N Engl J Med 2002;347:781-789. [Free Full Text]
Johansson JE, Andren O, Andersson SO, et al. Natural history of early, localized prostate cancer. JAMA 2004;291:2713-2719. [Free Full Text]
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Appendix
The participants in the Scandinavian Prostate Cancer Group StudyNo. 4 were as follows: Protocol Committee — H.-O. Adamiand J.-E. Johansson; Steering Committee — H.-O. Adami,A. Bill-Axelson, L. Holmberg, J.-E. Johansson (principal investigator),and B.-J. Norlén; Statistical Analysis — L. Holmberg,H. Garmo, and J. Palmgren; Manuscript Preparation — H.-O.Adami, A. Bill-Axelson, and L. Holmberg; Monitoring —A. Bill-Axelson and B. Gobén; Study Group, Recruitment,and Data Collection: Borås, Sweden — S. Bratell;Eskilstuna, Sweden — T. Lindeborg; Helsinki — M.Ruutu and J. Salo; Linköping, Sweden — A. Spångberg;Lund, Sweden — P. Elfving; Reykjavik, Iceland —G. Einarsson; Stockholm — J. Adolfsson, P. Ekman, P. -O.Hedlund, and H. Wikström; Uleåborg, Finland —O. Lukkarinen; Uppsala, Sweden — A. Bill-Axelson, M. Häggman,and B.-J. Norlén; Västerås, Sweden —L. Karlberg; Växjö, Sweden — G. Hagberg; Örebro,Sweden — S.-O. Andersson and J. -E. Johansson; ReferencePathologists — C. Busch (chair), M. de la Torre, A. Lindgren,and S. Nordling; End Point Committee — J.-E. Damber, Departmentof Urology, University Hospital, Göteborg, Sweden; A. Lindgren,Department of Pathology, University Hospital, Uppsala, Sweden;E. Varenhorst (chair), Department of Urology, University Hospital,Linköping, Sweden; External Review Committee — P.F.Schellhammer, Department of Urology, Eastern Virginia MedicalSchool, Norfolk, Va.; U.E. Studer, Department of Urology, Universityof Bern, Bern, Switzerland; and R. Sylvester, European Organizationfor Research and Treatment of Cancer, Brussels.
Radical Prostatectomy versus Watchful Waiting
Stuart M. E., Strite S. A., Marantz P. R., Hall C. B., Derby C. A., Liss H. K., Elmore J. G., Sonpavde G., Bill-Axelson A., Holmberg L., Johansson J.-E.
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353:1298-1300, Sep 22, 2005.
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