Original Article
The Influence of Finasteride on the Development of Prostate Cancer
N Engl J Med 2003; 349:215-224July 17, 2003
- Abstract
Background
Androgens are involved in the development of prostate cancer. Finasteride, an inhibitor of 5α-reductase, inhibits the conversion of testosterone to dihydrotestosterone, the primary androgen in the prostate, and may reduce the risk of prostate cancer.
Methods
In the Prostate Cancer Prevention Trial, we randomly assigned 18,882 men 55 years of age or older with a normal digital rectal examination and a prostate-specific antigen (PSA) level of 3.0 ng per milliliter or lower to treatment with finasteride (5 mg per day) or placebo for seven years. Prostate biopsy was recommended if the annual PSA level, adjusted for the effect of finasteride, exceeded 4.0 ng per milliliter or if the digital rectal examination was abnormal. It was anticipated that 60 percent of participants would have prostate cancer diagnosed during the study or would undergo biopsy at the end of the study. The primary end point was the prevalence of prostate cancer during the seven years of the study.
Results
Prostate cancer was detected in 803 of the 4368 men in the finasteride group who had data for the final analysis (18.4 percent) and 1147 of the 4692 men in the placebo group who had such data (24.4 percent), for a 24.8 percent reduction in prevalence over the seven-year period (95 percent confidence interval, 18.6 to 30.6 percent; P<0.001). Tumors of Gleason grade 7, 8, 9, or 10 were more common in the finasteride group (280 of 757 tumors [37.0 percent], or 6.4 percent of the 4368 men included in the final analysis) than in the placebo group (237 of 1068 tumors [22.2 percent], P<0.001 for the comparison between groups; or 5.1 percent of the 4692 men included in the final analysis, P=0.005 for the comparison between groups). Sexual side effects were more common in finasteride-treated men, whereas urinary symptoms were more common in men receiving placebo.
Conclusions
Finasteride prevents or delays the appearance of prostate cancer, but this possible benefit and a reduced risk of urinary problems must be weighed against sexual side effects and the increased risk of high-grade prostate cancer.
Media in This Article
Figure 1
Cumulative Incidence of Prostate Cancer Diagnosed in a Biopsy Performed for Cause or after an Interim Procedure.Table 1
Status of Men at the Time of the Analysis.Article Activity
- Article
To date, the management of prostate cancer, the most common nondermatologic neoplasm in men in the United States, has focused on early diagnosis and treatment. Given that the development of prostate cancer is a long-term process involving multiple steps, however, prevention may be a more effective approach.
There is abundant evidence that androgens influence the development of prostate cancer.1-3 The development of finasteride, an inhibitor of steroid 5α-reductase, the enzyme that converts testosterone to the more potent androgen dihydrotestosterone, created an opportunity to test the possibility that lowering the androgen levels in the prostate would reduce the risk of prostate cancer. We undertook a study to determine whether finasteride can reduce the prevalence of prostate cancer among initially healthy men during a seven-year study period.
Methods
Study Design
Men 55 years of age or older with a normal digital rectal examination, no clinically significant coexisting conditions, and an American Urological Association symptom score4 of less than 20 were recruited. The study was approved by institutional review boards at all sites. After the men had given written informed consent, blood was drawn to determine the level of prostate-specific antigen (PSA), and the men were issued a three-month supply of placebo tablets for the run-in phase of the trial. If, after this three-month period, the PSA level was 3.0 ng per milliliter or lower, adherence was within 20 percent of the expected rate of placebo use, and there were no clinically significant toxic effects, the men were randomly assigned to finasteride (5 mg per day) or placebo. The planned duration of treatment was seven years. A dynamic allocation scheme was used for randomization to ensure that the treatment groups were balanced within each of the 221 study sites.
The men underwent annual digital rectal examinations and measurements of PSA. Biannually, they were seen for reissuing of medication, counts of pills, and recording of clinically significant medical conditions and side effects. Every three months, the men were contacted by telephone for the collection of data on interim medical events.
Because of the effect of finasteride on the PSA level, the measure of which is the primary method of detection of prostate cancer, an end-of-study biopsy was planned. At the end of seven years, all men who had not been given a diagnosis of prostate cancer were offered an end-of-study prostate biopsy. This biopsy was to be performed within 7 years ±90 days after the date of randomization.
Prostate Biopsy
Measurements of PSA were performed in a central laboratory (with the use of the Tandem E assay [Hybritech] until 2000 and the Access assay [Beckman Coulter] thereafter). After the measurement of PSA at enrollment, all PSA measurements for men in the finasteride group were adjusted before being reported, because finasteride causes a decrease in the PSA level.5 A centralized adjustment, overseen by an independent data and safety monitoring committee, ensured that the men in the finasteride group had a rate of recommendation for prostate biopsy approximately equal to that among men in the placebo group. Initially, the adjustment consisted of a doubling of the PSA values for finasteride-treated men, but on the basis of the goal of an equal percentage of biopsies in each group, the factor was changed to 2.3 at the beginning of the man's fourth year in the study. PSA levels were initially reported as elevated or not elevated, but in October 1995, as clinical practice changed, adjusted values began to be reported for men with elevated PSA levels. The PSA values reported to the men were thus the adjusted values for men in the finasteride group and the unadjusted values for men in the placebo group. If the digital rectal examination was abnormal or if the reported PSA level was higher than 4.0 ng per milliliter at the annual examination, prostate biopsy was recommended.
Biopsy was performed with the use of transrectal ultrasonographic guidance, and a minimum of six specimens was obtained. If the biopsy was positive, the subject was removed from the study; if it was negative, he remained in the study. If prostatic intraepithelial neoplasia was found, a second biopsy was recommended.
All prostate biopsies were reviewed by a central pathology laboratory and by pathologists at the study site, all of whom were unaware of the treatment-group assignment. Prostate tissue from any other procedures performed (e.g., transurethral resection of the prostate) was sent to the central pathology laboratory for evaluation. Discordant interpretations were arbitrated by a referee pathologist, and concordance was achieved in all cases.
Statistical Analysis
The primary objective of the study was to determine whether the administration of finasteride for seven years could reduce the prevalence of prostate cancer during that period. We assumed that the prevalence of prostate cancer during the seven years of the study would be 6 percent in the placebo group and that a 25 percent reduction in the prevalence in the finasteride group at seven years would be of clinical significance. We calculated that with a two-sided alpha of 0.05, a power of 0.92, and a three-year accrual period, we needed a sample size of 18,000. We also assumed that 60 percent of the men either would have an interim diagnosis of prostate cancer or would undergo an end-of-study biopsy. It was estimated that 20 percent of the participants would die during the study, that 5 percent would decline to undergo a prostate biopsy, and that 15 percent would be lost to follow-up.
Another assumption was that the rate of nonadherence to the study treatment would be 14 percent and that 5 percent of the men in the placebo group would end up taking finasteride (the drop-in rate). Serum dihydrotestosterone was measured in a randomly selected 5 percent sample of men as a marker of adherence to study medication in the finasteride group and as a measure of the drop-in rate in the placebo group.6,7
The primary intention-to-treat analysis included men who received a diagnosis of prostate cancer during the study or who underwent an end-of-study biopsy. Medical events, side effects, and the rates of temporary discontinuation of treatment are reported for all eligible men. All reported P values are two-sided.
An independent data and safety monitoring committee met every six months and reviewed data on safety, adherence, and diagnoses of prostate cancer, as well as other data related to the monitoring of the study assumptions. This committee reported to the chair of the steering committee and made recommendations regarding revisions to the protocol or adjustments for possible differences in prostate-cancer–detection rates due to the effect of finasteride on the PSA level and prostate size. Because of the known PSA-related bias and other potential detection biases that were anticipated, no formal interim stopping rules were specified.
Results
Study Participants and Termination of the Study
Over a period of three years, 24,482 men were enrolled in the study, and of these men, 18,882 underwent randomization between January 1994 and May 1997 — 12,016 of them during the first year of the trial. Most of the men who did not undergo randomization (3997) had a PSA level of more than 3.0 ng per milliliter. On February 21, 2003, 15 months before the anticipated completion of the study, the data and safety monitoring committee met and, on the basis of sensitivity analyses, recommended early termination of the study, since the study objective had been met and the conclusions were extremely unlikely to change with additional diagnoses of prostate cancer and end-of-study biopsy results. Because of the rapid initial accrual of participants, at the time of the analysis of the data and safety monitoring committee, 81.3 percent of the men had completed the seven years of the study. The current analysis is based on the 86.3 percent of the men who have now completed the seven years of the study.
Rates of Prostate Cancer and End-of-Study Biopsy
The rate of diagnosis of prostate cancer or end-of-study biopsy was 59.6 percent in the finasteride group and 63.0 percent in the placebo group (P<0.001). Men with such a diagnosis made more than 7 years plus 90 days after randomization or with an end-of-study biopsy performed after that time were excluded from the primary analysis (Table 1Table 1
Status of Men at the Time of the Analysis.). Men were considered to have refused a biopsy if the biopsy was not performed because of a coexisting condition or because the personal physician recommended against the procedure, as well as if the men themselves refused the biopsy. The rate of refusal of biopsy was higher than had originally been estimated, but because the death rate and the rate of loss to follow-up were lower than had been anticipated, the overall ascertainment goal was achieved.Of the 9060 men who were included in the final analysis, prostate cancer was detected in 803 of the 4368 in the finasteride group (18.4 percent) and 1147 of the 4692 in the placebo group (24.4 percent), a relative risk reduction of 24.8 percent (95 percent confidence interval, 18.6 to 30.6 percent; P<0.001). The number of cases of prostate cancer detected either during the course of the study in a biopsy performed for cause (an elevated PSA level or an abnormal digital rectal examination) or in a biopsy performed at the end of the study was higher in the placebo group than in the finasteride group. Of the cases of prostate cancer that were diagnosed in a biopsy performed for cause, 96.0 percent were found on biopsy and 4.0 percent were found after other procedures such as transurethral resection of the prostate. Figure 1Figure 1
Cumulative Incidence of Prostate Cancer Diagnosed in a Biopsy Performed for Cause or after an Interim Procedure. shows the incidence of prostate cancer in the two treatment groups among all surviving men who underwent randomization, excluding cases diagnosed on end-of-study biopsy. Finasteride was associated with a reduced prevalence of prostate cancer in all subgroups we examined (Table 2Table 2
Prevalence of Prostate Cancer during the Seven Years of the Study, Overall and in Subgroups.).Rates of Recommended Biopsy
Biopsies were recommended during the trial if there was an elevated PSA level, an abnormal digital rectal examination, or both. Such recommendations for biopsy during the trial were given to 2122 of the 9423 men who were randomly assigned to the finasteride group (22.5 percent) and 2348 of the 9457 eligible men who were randomly assigned to the placebo group (24.8 percent, P<0.001) (Table 3Table 3
Reasons for Recommendations for Biopsy and Characteristics of Men Who Underwent the Recommended Biopsy and Men Who Did Not.).Although the rates of the prompts of biopsy among men in whom a biopsy was recommended and among men in whom a biopsy was performed differed according to treatment group, there was no significant difference between the proportions of recommended biopsies that were performed in the two groups either according to the number of recommendations for biopsy (P=0.10) or according to the number of men who had such a recommendation during the course of the trial (P=0.29). In the placebo group but not in the finasteride group, the degree of elevation of the PSA level was related to whether or not a recommended prostate biopsy was performed. The annual rate at which biopsies were performed for cause is shown in Figure 1. Of the 246 cancers found on biopsies performed for cause at seven years, 57 were in men in whom biopsies had previously been recommended but had not been performed. If a PSA-adjustment factor of 2.0 had been used for the finasteride group throughout the study, 222 men in the finasteride group who received a recommendation to undergo a biopsy during the course of the study because of an elevated PSA level would not have had such a recommendation. A total of 69 of these men underwent biopsy at the time of the recommendation, and 17 cases of prostate cancer were detected.
Rates of Nonadherence
The rate of nonadherence, estimated as the percentage of days of treatment missed in men who had a diagnosis of prostate cancer or an end-of-study biopsy, was 14.7 percent in the finasteride group and 10.8 percent in the placebo group. The rate of nonadherence in the finasteride group, as indicated by a dihydrotestosterone level of more than 16 ng per milliliter, was 14.5 percent, and the drop-in rate in the placebo group, as indicated by a dihydrotestosterone level of 16 ng per milliliter or lower, was 6.5 percent.
A total of 36.8 percent of men in the finasteride group and 28.9 percent in the placebo group temporarily discontinued treatment at some time during the study for reasons other than death or an interim diagnosis of prostate cancer (P<0.001 for the comparison between groups). The yearly rate of temporary discontinuation of treatment was highest during the men's first year in the study (10.0 percent in the finasteride group and 6.3 percent in the placebo group) and decreased steadily, so that by year 5, the rate was 3.6 percent in the finasteride group and 3.4 percent in the placebo group. Side effects of finasteride represented the primary reason for the difference in the proportion of men who temporarily discontinued treatment (1722 of 9423 men in the finasteride group [18.3 percent] vs. 931 of 9457 men in the placebo group [9.8 percent]).
Medical Events and Side Effects
Medical events and side effects (Table 4Table 4
Medical Events and Side Effects.) were graded according to the toxicity criteria of the Southwest Oncology Group.8 These events and side effects were reported by the men during directed interviews over the course of their treatment. Reduced volume of ejaculate, erectile dysfunction, loss of libido, and gynecomastia were more common in the finasteride group than in the placebo group (P<0.001 for all comparisons), whereas urinary urgency, urinary frequency, or both; prostatitis; urinary tract infection; and urinary retention were more common among men in the placebo group (P<0.001 for all comparisons). There was no significant difference in the number of deaths between the two groups: five men in each group died from prostate cancer.Biopsy Results
Table 5Table 5
Gleason Scores for Prostate Cancers Detected. shows Gleason scores assigned by the central pathology laboratory for all biopsies. There was a higher proportion of tumors with Gleason scores of 7, 8, 9, or 10 in the finasteride group (280 of 757 graded tumors [37.0 percent], or 6.4 percent of the 4368 men included in the analysis) than in the placebo group (237 of 1068 graded tumors [22.2 percent], or 5.1 percent of the 4692 men included in the analysis; P<0.001 for the comparison between groups in terms of the percentage of graded tumors; relative risk of a high-grade tumor, 1.67 [95 percent confidence interval, 1.44 to 1.93]; P=0.005 for the comparison between groups in terms of the percentage of all men; relative risk, 1.27 [95 percent confidence interval, 1.07 to 1.50]). To understand the risk of high-grade disease from the perspectives of a man considering taking finasteride and of a man who is found to have prostate cancer, we report these data in two ways. The rate of high-grade disease among men in whom prostate cancer was diagnosed on a biopsy performed for cause was 188 of 393 men in the finasteride group (47.8 percent) and 148 of 504 men in the placebo group (29.4 percent; P<0.001; relative risk, 1.62 [95 percent confidence interval, 1.37 to 1.93]); the rate among all men who underwent biopsy for cause was 188 of 1639 men in the finasteride group (11.5 percent) and 148 of 1934 men in the placebo group (7.7 percent; P<0.001; relative risk, 1.50 [95 percent confidence interval, 1.22 to 1.84]).Prostate volume was determined at the time of biopsy. The median volume among men in the finasteride group was 25.5 cm3, as compared with 33.6 cm3 among men in the placebo group (a 24.1 percent relative difference). There was no significant difference between the two groups in the number of biopsy specimens obtained: sextant biopsy was performed in 81.5 percent of men in the finasteride group and 81.0 percent of men in the placebo group. Most prostate cancers detected during the trial were clinically localized. A total of 97.7 percent of cancers in men in the finasteride group were classified as T1 or T2, as were 98.4 percent of those in men in the placebo group. Of the tumors found on end-of-study biopsies that were not performed for cause, 21.1 percent were in men who had a concurrent PSA level between 2.6 and 3.9 ng per milliliter. Of the remaining tumors found on end-of-study biopsies that were not performed for cause in men with a concurrent PSA level of 2.5 ng per milliliter or less, 15.4 percent had a Gleason grade of 7, 8, 9, or 10.
Discussion
The lifetime risk of prostate cancer in the United States is 16.7 percent, and 28,900 men are expected to die of this disease in 2003.9 This high rate and the unpredictable biology of prostate cancer make prevention of the disease an appealing strategy. Finasteride is an attractive chemopreventive agent, because it inhibits the conversion of testosterone to the more potent androgen dihydrotestosterone within the prostate and has low toxicity. At the inception of our study, finasteride became available for the treatment of benign prostatic hyperplasia (as Proscar [Merck]), and since then, it has been approved for the treatment of male pattern baldness (Propecia [Merck]). Although it is used by millions of men for these indications, little is known about its long-term effects on the prostate.
We faced a challenge in designing our study, because of the effect of finasteride on the PSA level, measurement of which is the primary method of screening for prostate cancer. For this reason, we planned to perform a prostate biopsy at the end of the study.6 We recognized the possibility that there would be an increased number of positive biopsies among men who received finasteride, because a proportionately greater volume of gland would be sampled from smaller glands.10,11 This effect could introduce a bias against any evidence of benefit from finasteride.
Every attempt was made to ensure that an equal proportion of men in each group was evaluated for prostate cancer; this was the logic behind the initial doubling of PSA values for men in the finasteride group and the later increase by a factor of 2.3 at the beginning of each participant's fourth year in the study.5 An additional difference in the rate of evaluation for prostate cancer between the two groups was a different number of abnormal digital rectal examinations (1845 in the finasteride group vs. 2090 in the placebo group) (Table 3) and transurethral resections of the prostate. In addition, more men in the finasteride group than in the placebo group were categorized as having refused the end-of-study biopsy (25.4 percent vs. 22.8 percent, P<0.001), most likely because of the higher rate of temporary discontinuation of treatment in a group of men less committed to the study requirements. Although the difference between the groups in the overall rate of ascertainment of prostate-cancer status of 3.4 percentage points (59.6 in the finasteride group vs. 63.0 percent in the placebo group) was statistically significant, we believe that this difference by itself is unlikely to have contributed substantially to the difference in the rate of detection of prostate cancer.
Seven years of finasteride treatment resulted in a 24.8 percent reduction in the prevalence of prostate cancer during that period. There was a reduction in relative risk among men who underwent a prostate biopsy before seven years and among men who underwent biopsy at the end of the study. The risk reductions were similar in subgroups defined according to age, race or ethnic group, family history of prostate cancer, and stratum of PSA level at randomization.
Decreases in sexual potency, libido, and ejaculate volume were frequently reported over the course of the trial, as would be expected in men in this age group who were followed for seven years with repeated queries regarding these symptoms.12 These side effects were more common in the finasteride group. Urinary symptoms or events related to benign prostatic hyperplasia were less common among men receiving finasteride — a finding that is consistent with a previous report.13
High-grade disease was noted in 6.4 percent of the men in the finasteride group, as compared with 5.1 percent of those in the placebo group. A difference in the rate of high-grade disease was seen within the first year of the study. One possible explanation for this difference is a grading bias: histologic changes that mimic those of high-grade disease are caused by androgen-deprivation therapy.14-18 There are, however, differences of opinion as to whether this effect occurs with finasteride. It is possible that finasteride induces high-grade tumors by reducing the level of intracellular dihydrotestosterone within the prostate. There is evidence that the prostate tumors that develop in men with low testosterone levels have higher Gleason grades and worse outcomes than the prostate cancers that develop in men with normal testosterone levels.19-21 It is also possible that finasteride selects for high-grade tumors by selectively inhibiting low-grade tumors. Long-term follow-up in these men and further laboratory research will be required to determine the reason for the association between finasteride and high-grade prostate cancer.
The tumors that were detected on biopsies performed for cause were clinically similar to those that are detected in clinical practice by screening of the PSA level and digital rectal examination. The clinical significance of cancers found in the end-of-study biopsies (those not performed for cause) is unknown. Of the men with such diagnoses, 21.1 percent had PSA levels between 2.6 and 3.9 ng per milliliter. Clinically significant tumors are as common among men with PSA levels in this range as they are among men with PSA levels between 4.0 and 10.0 ng per milliliter.22 Of the remaining tumors found in men with PSA levels of 2.5 ng per milliliter or less, 15.4 percent had high-grade cancer.
The overall cancer detection rate of 24.4 percent in the placebo group is a matter of concern, because the eligibility criteria for enrollment in the study selected for low-risk men with an expected lifetime incidence of prostate cancer of 16.7 percent and a rate of death from prostate cancer of 3 to 4 percent. The rate of 24.4 percent suggests the possibility of overdiagnosis of disease.
The study raises two interrelated questions: did finasteride prevent or treat prostate cancer,23 and did finasteride prevent or delay24,25 the appearance of prostate cancer? These issues are important for the field of cancer prevention. The early difference in the incidence of prostate cancer between the two groups suggests that finasteride may have treated subclinical, microscopical cancer early in the study, and the fact that the difference continued to increase suggests that it prevented or delayed the onset of cancer. In either case, the effect is beneficial.23-25
Physicians can use these results to counsel men regarding the use of finasteride. It is important to stress that finasteride reduced the risk of prostate cancer in a clinical trial marked by frequent monitoring for disease and was associated with an increased risk of diagnosis of high-grade prostate cancer. For a man considering using this medication, the greater absolute reduction in the risk of prostate cancer must be weighed against the smaller absolute increase in the risk of high-grade disease.
There is also the matter of side effects: the incidence of adverse effects on sexual function was higher with finasteride, but the finasteride group had a lower incidence of urinary symptoms and complications than the placebo group. Using published information on the outcomes of prostate-cancer treatment, men can weigh these trade-offs in the context of their own priorities regarding the avoidance of prostate cancer as well as their urinary and sexual function to reach a personal decision regarding finasteride use.26-28 As more is learned from the molecular biology of prostate cancer about the risk of aggressive disease, data from this and other studies will help to refine the appropriate use of interventions such as finasteride.
Supported in part by Public Health Service grants (CA37429, CA35178, and CA45808) from the National Cancer Institute.
This article was published at www.nejm.org on June 24, 2003.
We are indebted to the 18,882 men who participated in this study; to the members of the data and safety monitoring committee; to the steering committee; to the study-site principal investigators and clinical research associates; to collaborators from the Southwest Oncology Group, the Eastern Cooperative Oncology Group, and the Cancer and Leukemia Group B; and to Merck for providing the finasteride and the placebo.
This article is dedicated to the memory of Gary Miller, M.D., Ph.D.
Source Information
From the University of Texas Health Science Center, San Antonio (I.M.T.); the Southwest Oncology Group Statistical Center, Seattle (P.J.G., C.M.T., S.M.C., J.J.C.); the University of Colorado, Denver (M.S.L., G.J.M.); the National Cancer Institute, Bethesda, Md. (L.G.F., A.R.); the Mayo Clinic, Rochester, Minn. (M.M.L.); the Wilford Hall U.S. Air Force Medical Center, San Antonio, Tex. (R.D.C.); the Southeastern Medical Oncology Center, Goldsboro, N.C. (J.N.A.); the M.D. Anderson Cancer Center, Houston (S.M.L.); the Grand Rapids Community Clinical Oncology Program, Grand Rapids, Mich. (C.M.S.); and the Southwest Oncology Group Operations Office, San Antonio, Tex. (C.A.C.).
Address reprint requests to the Southwest Oncology Group (SWOG-9217), Operations Office, 14980 Omicron Dr., San Antonio, TX 78245-3217.
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