U.S. Preventive Services Task Force Recommendation Statement on Prostate Cancer Screening
U.S. Preventive Services Task Force Recommendation for Prostate Cancer Screening Statement
Virginia A. Moyer, MD, MPH, 1. on behalf of the United States Preventive Services Task Force*, 2. Author Affiliations
Abstract \sDescription: Prostate cancer screening recommendations from the U.S. Preventive Services Task Force (USPSTF) as of 2008 have been updated
Methods: The USPSTF examined fresh research on the advantages and disadvantages of PSA-based prostate cancer screening as well as the advantages and disadvantages of localized prostate cancer treatment.
Recommendation: Prostate cancer PSA-based screening is not advised by the USPSTF (grade D recommendation).
No of their age, men in the overall U.S. population should follow this advice. The use of the PSA test for surveillance following prostate cancer diagnosis or treatment is not covered by this recommendation since it falls beyond the purview of the USPSTF.
For individuals without associated symptoms or indications, the U.S. Preventive Interventions Task Force (USPSTF) publishes recommendations regarding the efficacy of particular clinical preventive services.
It bases its recommendations on evidence of the service’s advantages and disadvantages as well as an evaluation of the balance. The cost of delivering a service is not taken into account by the USPSTF in this evaluation.
The USPSTF is aware that therapeutic decisions entail more factors than just the available data. Clinicians should be aware of the facts, yet tailor their decisions to the particular patient or circumstance. Similar to this, the USPSTF observes that decisions about policy and coverage incorporate factors in addition to the evidence of clinical benefits and harms.
Section Summary of Recommendation and Evidence: Previous SectionNext Section
Prostate-specific antigen (PSA)-based prostate cancer screening is not advised by the USPSTF (grade D recommendation).
A discussion of how to put this suggestion into practice can be found in the Clinical Considerations section.
For a summary of the recommendation and ideas for clinical practice, see Figure 1. The USPSTF ratings are shown in Table 1, and the levels of assurance about net benefit are shown in Table 2.
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Figure 1: Clinical Summary of U.S. Preventive Services Task Force Recommendation for Prostate Cancer Screening
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Table 1. Meaning of the USPSTF Grades and Practice Suggestions
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Table 2 shows the USPSTF’s level of confidence in the net benefit.
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With a lifetime risk for diagnosis now estimated at 15.9%, prostate cancer is the most frequent non-skin cancer among males in the United States. Although some aggressive cases of prostate cancer have a good prognosis even without therapy, the lifetime risk of dying from prostate cancer is 2.8% in the majority of cases. Few men die of prostate cancer before the age of 60, and the disease seldom affects males under the age of 50. 70% of prostate cancer-related fatalities happen after the age of 75. (1).
The measurement of serum PSA levels is included in all current guidelines for prostate cancer screening, along with other possible means of detection such digital rectal examination or ultrasonography. There is strong evidence that PSA-based screening programs find many cases of prostate cancer that are asymptomatic. Additionally, there is strong proof that a sizable portion of men with asymptomatic cancer found by PSA screening have tumors that will either not advance or advance so slowly as to have remained dormant for the whole of the man’s life. Both cases are referred to as overdiagnosis or pseudo-disease, respectively. As more men have biopsies, there are more cases of prostate cancer being overdiagnosed. A substantial percentage of cancer cases could be identified in a group that underwent screening; in one study, men who were eligible for PSA screening underwent a biopsy regardless of their PSA level and found that approximately 25% of men had cancer (2). The life expectancy at the time of diagnosis affects the rate of overdiagnosis. Men who have reduced life expectancies due to chronic illnesses or advanced age are substantially more prone to have their cancer overdiagnosed. Although it is impossible to pinpoint the exact size of overdiagnosis associated with any screening and treatment program, estimates from the two largest trials imply that overdiagnosis rates for prostate cancer screening range from 17% to 50%. (3).
Advantages of Early Detection and Treatment
Prostate cancer screening’s main objective is to decrease prostate cancer-related deaths and, as a result, lengthen lives. Reduced symptomatic metastatic disease development would be another significant result. In the available randomized, controlled trials of prostate cancer screening, the primary outcome used was a decrease in prostate cancer mortality. It is challenging to determine the impact of lead-time bias on the reported rates because, despite the fact that one screening trial reported on the presence of metastatic disease at the time of prostate cancer diagnosis, no study reported on the impact of screening on the emergence of subsequent metastatic disease.
Men with screen-detected cancer may fall into one of three categories: those who will survive their cancer despite early diagnosis and treatment, those who will do well without screening, or those for whom early diagnosis and treatment increase survival. The number of men in the latter group can only be accurately estimated by randomized screening procedures. There is strong evidence to suggest that, at most, relatively few men survive prostate cancer because of screening beyond 10 to 14 years. The USPSTF took into account the PLCO (Prostate, Lung, Colorectal, and Ovarian) Cancer Screening Trial and the ERSPC, two significant PSA screening trials (European Randomized Study of Screening for Prostate Cancer). The US trial did not show a decrease in prostate cancer mortality. In a subgroup of males aged 55 to 69 years, the European study discovered a reduction in prostate cancer fatalities of roughly 1 death per 1000 men who had screening. Five of the seven reporting countries did not detect a statistically significant drop, which strongly influenced this finding. In the European experiment, the all-cause mortality rates in the screened and nonscreened groups were very similar.
The value of PSA testing and early treatment ranges from 0 to 1 averted prostate cancer deaths per 1000 men tested, according to sufficient data.
The risks of early detection and treatment
Risks Associated with Diagnostic and Screening Procedures
There is strong evidence that the PSA test frequently yields false-positive findings (when cutoffs between 2.5 and 4.0 g/L are employed, nearly 80% of positive PSA test results are false-positive) (4). The link between false-positive PSA test results and detrimental psychological impacts, such as constant fear about prostate cancer, is sufficiently established. Men who receive a false-positive test result are more likely than men who receive a negative test result to have additional testing, including one or more biopsies, in the year that follows (5). Depending on the PSA threshold and testing frequency utilized, 15% to 20% of men will experience a PSA test result that necessitates a biopsy over a 10-year period (4). According to recent research from a randomized trial of the treatment of screen-detected cancer, about one-third of men who undergo prostate biopsy experience pain, fever, bleeding, infections, temporary urinary problems, or other problems that need medical attention and that the men consider to be “moderate or major problems,” and about 1% of them need to be hospitalized (6).
The USPSTF believed that these risks connected to screening and diagnostic procedures were at least minimal in scope.
Risks Associated with Cancer Screen-Detected Treatment
Adequate evidence demonstrates that over 90% of American men with PSA-detected prostate cancer receive early androgen deprivation medication, surgery, or radiation treatment (7, 8). According to sufficient evidence, between 10 and 70 men will experience major complications but survive prostate cancer surgery, and up to 5 men per 1000 will pass away within a month. Of the 1000 males who receive radiotherapy or surgery, at least 200 to 300 develop erectile dysfunction or long-term side effects, such as urine incontinence. Bowel problems are also linked to radiotherapy (9, 10).
Although this is not a U.S. Food and Drug Administration (FDA)-approved indication and it has not been demonstrated to increase survival in localized prostate cancer, some doctors have utilized androgen deprivation therapy as the main treatment for early-stage prostate cancer, particularly in older men. Approximately 400 out of every 1000 men receiving androgen restriction therapy for localized prostate cancer experience erectile dysfunction, along with gynecomastia and hot flashes, according to adequate data (9, 10).
There is strong evidence that prostate tumors are significantly overdiagnosed as a result of PSA-based screening. A man with cancer who would remain asymptomatic for the rest of his life cannot benefit from screening or treatment, hence the rate of overdiagnosis of prostate cancer is a significant problem. Given our current inability to discriminate tumors that will remain indolent from those destined to be lethal, there is a significant predisposition for doctors and patients to choose to treat most cases of screen-detected cancer (7, 11). As a result, many men are suffering the negative effects of treating prostate cancer that never manifests as symptoms. Most men have the same outcome and are consequently subjected to the side effects of therapy for a substantially longer amount of time, even in cases where their screen-detected cancer would have been discovered later without screening (12, 13). There is strong evidence that prostate cancer screening based on PSA causes significant overtreatment and the related negative effects.
The USPSTF rated the severity of these side effects from therapy as at least moderate.
Existing studies sufficiently show that the reduction in prostate cancer mortality after 10 to 14 years is, at most, very small, even for men in what appears to be the optimal age range of 55 to 69 years, even though the precise, long-term effect of PSA screening on prostate cancer-specific mortality is still unknown. The overall mortality rate does not appear to have decreased. Conversely, the risks of early death that are connected to the diagnosis and treatment of cancer that is discovered through screening are minor but genuine, frequently occur early, and frequently persist. The negative effects of screening and treating diseases found through screening will be felt by much more men than the positive effects. Many men will suffer the negative impacts of diagnosis and treatment of a disease that would have remained asymptomatic throughout their lives due to screening’s inevitable overdiagnosis and overtreatment of prostate cancer. In order to evaluate the balance of benefits and harms, it is necessary to compare the very low likelihood of averting a long-term death from prostate cancer with the moderate to high risk of early and permanent harm from therapy.
The USPSTF comes to the conclusion that there is a reasonable degree of certainty that the risks of PSA-based prostate cancer screening outweigh the benefits.
Implementation Clinical Considerations Previous SectionNext Section
The USPSTF recognizes the widespread use of PSA screening in clinical practice and is cognizant that some men will continue to request screening and that some doctors will continue to provide it, even though it discourages the use of screening tests for which the benefits do not outweigh the risks in the target population. The choice to begin or continue PSA screening should be made with a clear understanding of the potential advantages and risks, while also respecting the choices of the patient. If a doctor is not willing to participate in shared decision making that allows patients to make an informed decision, they should not recommend or order PSA test. Similar to this, patients who seek PSA screening should be given the chance to make choices about their screening that match their preferences on particular advantages and hazards. Employer and community-based screening ought to end. Given the existing methods used in the United States for prostate cancer screening and treatment, Table 3 provides fair predictions of the anticipated results of screening.
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Table 3. PSA-Based Prostate Cancer Screening*
Although the prognosis for clinically localized cancer is typically good regardless of the method of detection, even in the absence of treatment, the treatment of some cases of clinically localized prostate cancer can change the natural history of the disease and may reduce morbidity and mortality in a small percentage of men. Finding males for whom treatment will lower morbidity and death is the main objective of PSA-based screening. Studies show that PSA-based screening, as it is now used in the United States, causes more harms than benefits in the population being screened, with the number of men who experience this benefit being, at most, extremely tiny. It is unknown if a different strategy for illness screening and management could produce equal or higher benefits while minimizing risks. The balance of benefits and harms may be improved by concentrating screening on men who have a higher risk of dying from prostate cancer, but current research does not allow for conclusions regarding whether screening is more beneficial in these populations in terms of absolute or relative terms. The only screening research that showed a benefit in prostate cancer-specific mortality utilized a 2- to 4-year screening interval; hence, extending the time between screening tests may reduce risks without affecting cancer mortality (15). Increasing the PSA threshold that determines whether a biopsy is necessary or not (12, 16) or decreasing the proportion of men receiving active treatment at the time of diagnosis through watchful waiting or active surveillance are additional potential strategies to lessen the negative effects of diagnostic and therapeutic procedures (11). A different tactic that merits more research is periodic digital rectal examinations. A large proportion of men had palpable cancer in the only randomized trial showing a mortality decrease from radical prostatectomy for clinically localized disease (17). All of these strategies need greater investigation to better understand their advantages and disadvantages and to more precisely establish a strategy for the detection and treatment of prostate cancer that maximizes the positive effects while reducing the negative ones.
Patient Population to Be Taken Into Account
The general male population of the United States should heed this advice. The biggest risk factor for prostate cancer development is getting older. Trials of either screening or treatment, though, failed to find any advantages for males beyond the age of 70. Males of all ages who are black and men with a family history of prostate cancer are more likely to get the disease and pass away from it. In the United States, black men have a prostate cancer mortality rate that is around twice that of other males(1); the cause of this discrepancy is uncertain. In the randomized clinical trials of screening, non-Hispanic black men made up a very small minority (4% of the men enrolled in the PLCO trial were non-Hispanic black; although the ERSPC and other trials did not report the specific racial demographic characteristics of participants, they likely comprised the majority of participants). As a result, it is impossible to draw any definitive conclusions about the relative merits and drawbacks of PSA-based screening in this population. However, in the absence of evidence that supports a more favorable balance of risks and benefits, it is hard to specifically advise PSA-based screening for black men. More cancer cases will lead to more diagnosis and treatments, but there may not be a larger absolute decline in mortality to go along with the increase. Since the release of the USPSTF-commissioned evidence evaluations, preliminary findings from the PIVOT (Prostate Cancer Intervention Versus Observation Trial), in which 30% of participants were black, have been available. Researchers discovered no distinction in prostate cancer treatment outcomes between black men and white men (12).
The defoliant Agent Orange, which was employed in the Vietnam War, is thought to be a risk factor for prostate cancer, while there is little information on the results or impact of PSA testing and therapy in those who have been exposed to it. The Veterans Health Administration classifies prostate cancer among Vietnam veterans who were exposed to Agent Orange as a condition related to their military service.
The utility of the PSA test as a component of a diagnostic plan for men with symptoms that could be indicative of prostate cancer was not evaluated by the USPSTF. However, in screening or treatment trials, the existence of urinary symptoms was not an inclusion or exclusion criterion, and about 25% of men in screening trials experienced bothersome lower urinary tract symptoms (nocturia, urgency, frequency, and poor stream). Benign prostatic hyperplasia is not a known risk factor for prostate cancer, and men with urinary symptoms had a lower risk of developing prostate cancer than men without symptoms when their PSA levels are excessive (18).
Additionally, this advice does not take into account PSA-based testing in males with known BRCA gene mutations who may be at elevated risk for prostate cancer and does not address the utility of the PSA test for surveillance following prostate cancer diagnosis or treatment.
Five distinct randomized, controlled trials using single or interval PSA testing with different PSA cutoffs and screening intervals, as well as additional screening techniques, like digital rectal examination or transrectal ultrasound, have investigated PSA-based screening in men aged 50 to 74 years (4, 19–22). Digital rectal examination alone, as well as other screening methods or programs that exclude PSA testing, have not been sufficiently assessed in controlled research.
In the annual screening group at 11.5 and 13 years, the PLCO study discovered a nonstatistically significant rise in prostate cancer mortality, with outcomes consistently favoring the usual care group (19, 23).
After a median follow-up of 9 years, a prespecified subgroup analysis of males aged 55 to 69 years in the ERSPC study found that the death rate ratio (RR) for prostate cancer was 0.80 (95% CI, 0.65 to 0.98) in screened men, with similar results at 11 years (RR, 0.79 [CI, 0.68 to 0.91]). (4, 15). Only two nations—Sweden and the Netherlands—reported statistically significant declines in prostate cancer mortality after 11 years (the other five did not), and these findings appear to be the main contributors to the trial’s overall benefit (Figure 2). (15). No study identified any elements that could definitively explain why mortality reductions were greater in Sweden or the Netherlands than in other European nations or the United States, including patient age, adherence to the study site or protocol, duration of follow-up, PSA thresholds, or intervals between tests (PLCO trial). The clinical and methodological variations between trials may make it improper to combine the data using meta-analysis.
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Figure 2 shows the relative risk of dying from prostate cancer for males who underwent PSA screening in comparison to control group participants.
PLCO stands for the U.S. Prostate, Lung, Colorectal, and Ovarian Cancer Screening Trial. ERSPC is for the European Randomized Study of Screening for Prostate Cancer.
There was no change in overall or all-cause mortality according to any study. This reflects both the low ability of prostate cancer screening studies to identify differences in all-cause mortality, should they exist, and the high rates of competing mortality in this age range, as these men are more likely to die of prostate cancer. Only 462 of the 17 256 fatalities in the ERSPC trial’s “core” age range of 55 to 69 years were attributable to prostate cancer. In all men who were randomly assigned to screening versus no screening, the all-cause mortality RR was 1.00 (CI, 0.98 to 1.02). Results in men aged 55 to 69 years old were comparable (15). The difficulty of determining the cause of death in this age group makes the lack of any trend toward a decrease in all-cause mortality all the more significant.
Watchful waiting, active surveillance, repeated prostate biopsies, physical examinations, periodic PSA testing, and conversion to potentially curative treatment at the first sign of disease progression or deteriorating prognosis are the main management strategies for PSA-detected prostate cancer. Surgery or radiation therapy are also important management options (24). Regarding the best way to manage localized illness, there is no universal agreement. Comparative to the period prior to the introduction of the test, PSA-based screening is expected to have led to an additional 1 million American men receiving surgery, radiation therapy, or both between 1986 and 2005. (7).
Only 1 recent randomized, controlled study comparing surgical treatment to observation for clinically localized prostate cancer was available at the time of the USPSTF’s commissioned evidence evaluation (13). In the Scandinavian Prostate Cancer Group Study 4 trial, surgical management of localized, mostly clinically detected prostate cancer was linked to a 6% absolute reduction in prostate cancer and all-cause mortality at 12 to 15 years of follow-up; the benefit appeared to be restricted to men under 65 years old (13). Preliminary findings from a different randomized trial comparing external beam radiation (EBRT) with watchful waiting in 214 men with localized prostate cancer found before the start of PSA screening were then released. Men who were randomly assigned to watchful waiting or EBRT did not fare any better in terms of survival after 20 years (31% vs. 35%; P = 0.26). Although high in both groups, prostate cancer mortality at 15 years did not differ between them (23% vs. 19%; P = 0.51). External beam radiation did shorten recurrence-free survival and diminish distant progression (25). An intention to treat with radical prostatectomy did not improve disease-specific or all-cause mortality compared to observation in men with localized prostate cancer identified in the early PSA screening era; absolute differences were less than 3% and not statistically different (12). Nearly 2000 men with PSA-positive prostate cancer have registered in the ProtectT [Prostate Testing for Cancer and Treatment] experiment, which compares radical prostatectomy with EBRT or active monitoring. Results should be seen in 2015. (26).
Within 30 days of having a radical prostatectomy, up to 0.5% of men will pass away, and between 3% and 7% will experience major surgical complications. After 1 to 10 years, an additional 20% to 30% or more of men who underwent radical prostatectomy compared to men who chose watchful waiting will have erectile dysfunction, urine incontinence, or both. Additionally, radiation therapy is linked to an increase in bowel, bladder, and erectile dysfunction (9, 10).
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Research Deficits and Needs
Research is required to determine ways to prevent these occurrences because overdiagnosis and overtreatment greatly influence the balance of benefits and harms of prostate cancer screening. One such method would be to examine the impact of changing the PSA thresholds for an abnormal test or biopsy result on false-positive rates and the detection of indolent disease.
Similar to this, research is urgently needed to develop new screening techniques that can tell nonprogressive or slowly progressive disease from disease that is likely to shorten or shorten life, as doing so would cut down on the number of men who need a biopsy and subsequent treatment for a disease that has a good prognosis without intervention. The advantages and disadvantages of modifying the usage of the current prostate cancer screening techniques require additional study. Research is required to determine the impact of prolonging testing intervals, utilizing higher PSA criteria to initiate a diagnostic prostate biopsy, and the value of routine digital rectal examinations performed by qualified doctors. The data suggests that these measures may be linked to lowered mortality, despite the fact that they have not been thoroughly examined. They may reduce overdiagnosis and overtreatment. Additionally, studies are required to assess the long-term advantages and disadvantages of prompt treatment vs observation with delayed intervention or active monitoring in men with prostate cancer identified by screening. PIVOT (27) and the ProtecT trial (28), two randomized, controlled trials, are examining this problem. When men are later diagnosed with prostate cancer, preliminary PIVOT results may justify raising the PSA cutoff point for proposing a biopsy or curative therapy.
If the balance of advantages and disadvantages of prostate cancer screening alters in men at higher risk of acquiring or passing away from the disease, such as black men and those with a family history of the condition, more research is required to answer this question.
As a result, basing therapeutic recommendations on disease-specific mortality in the absence of an effect on all-cause mortality may not fully capture the health effect and aims of a screening and treatment program. Determining the cause of death accurately in older people can be challenging. The validity of prostate cancer mortality as an outcome measure in clinical trials, as well as the most effective use of the concurrent use of all-cause mortality, both require further study.
Finasteride and dutasteride, two sizable randomized, controlled trials of 5-reductase inhibitors, have demonstrated that these medications lower the risk for prostate cancer in men having routine PSA tests. The observed decrease, however, was due solely to a decline in the incidence of low-grade prostate cancer (Gleason score 6). Finasteride and dutasteride have not been approved by the FDA for the treatment or prevention of prostate cancer due to an unfavorable risk-benefit analysis. Most significantly, the FDA noted that there was an absolute increase in the incidence of high-grade prostate cancer in men randomly assigned to finasteride or dutasteride compared with control participants in both trials. The FDA listed associated side effects, including libido loss and erectile dysfunction (29). To determine the impact of 5-reductase inhibitors (or other potential preventive agents) on prostate cancer mortality and to pinpoint the group of men who might benefit most from prostate cancer prevention, additional research is necessary to better understand whether these medications are linked to the emergence of high-grade prostatic lesions (with these or other chemoprevention strategies).
Research is required to develop and implement effective informed decision-making tools that accurately communicate the best available evidence and can be implemented in primary care settings for a variety of patient groups, as well as to better understand patient and provider knowledge and values about the known risks and benefits of prostate cancer screening and treatment (for example, by race, age, or family history).
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Reaction to public remarks
From October 11 to December 13, 2011, a draft of this recommendation statement was available for public comment on the USPSTF website. Commenters expressed worry that a grade D recommendation from the USPSTF would prevent men from having a conversation with their personal healthcare providers, disrupt the doctor-patient relationship, and prevent men from being able to decide for themselves whether or not to get a prostate cancer screening. For men to continue making informed screening decisions, some commenters requested that the USPSTF change its recommendation to a grade C. The risk-benefit ratio of the intervention is taken into consideration when selecting USPSTF recommendations: A grade D recommendation indicates that the USPSTF believes there is at least moderate certainty that the intervention’s negative effects on the target population are equal to or greater than its positive effects, while a grade C recommendation indicates that the USPSTF believes there is at least moderate certainty that the service’s overall net benefit is minimal. Since the USPSTF did not come to the conclusion that the advantages exceed the drawbacks, it was unable to give a grade C recommendation for PSA screening. A D recommendation does not preclude discussions between clinicians and patients to encourage informed decision-making that supports individual values and preferences, the USPSTF has stated in the Implementation section.
Some commentators asked the USPSTF to offer more details regarding the effects of forgoing PSA screening. Table 3 offers a review of the advantages and drawbacks of screening. In conclusion, the USPSTF found that deciding against PSA testing would allow a patient to avoid the risks connected with the test and any following diagnostic procedures and therapies while still enjoying a similar lifespan with little to no change in mortality related to prostate cancer.
Commenters expressed concern that the USPSTF had not given a separate recommendation for black men enough thought. The Patient Population Under Consideration section contains more details about this population.
Many respondents were under the impression that the USPSTF’s findings about the effectiveness of PSA-based screening were based primarily on the PLCO trial, published meta-analyses, or their own meta-analysis. Because they satisfied the minimal inclusion criteria for the report, the commissioned systematic evidence review summarized the results of two previously published meta-analyses, but neither its authors nor the USPSTF conducted a new meta-analysis. The USPSTF is aware of the limitations of meta-analysis in this context as well as the heterogeneity in the existing randomized trials of prostate cancer screening. The USPSTF gave equal weight to the ERSPC and PLCO trials because they had the largest populations and the greatest quality, despite the fact that both had significant—yet distinct—methodological constraints. The PLCO trial’s screening intervals, PSA thresholds, utilization of digital rectal exams, enrollee characteristics, and follow-up diagnostic and treatment procedures are most comparable to contemporary contexts and practice patterns in the United States.
Commenters urged the USPSTF to take into account data from the Surveillance, Epidemiology, and End Results (SEER) database of the National Cancer Institute, which revealed a 40% decline in prostate cancer mortality in the United States between 1992 and 2007. (30). Since PSA-based screening was launched in the United States in the early 1990s and spread by the mid- to late-1990s, many people hypothesized that the decline must be related to the impact of screening. The problem with ecologic data is that it is impossible to accurately distinguish between the relative effects of any changes in screening, diagnosis, or treatment procedures (or fundamental changes in the population’s overall risk of contracting the disease or dying from it due to a variety of other causes) that may have been happening at the same time over a specific time period. The drop in mortality may have been influenced by all of these factors, including screening, but only a randomized study can accurately assess the degree of an intervention’s impact. According to the SEER database, prostate cancer death rates began at 29.9 instances per 100 000 men in the 1970s and 1980s, before the widespread adoption of PSA screening, and they gradually increased over time. This increase’s cause is not known. Between 1991 and 1993, around the time PSA testing were widely used in clinical settings, the mortality rate from prostate cancer reached a peak of 39.3 cases per 100 000 men. Thereafter, it started to fall by 1 to 2 cases per 100 000 men per year (2007 rate, 24.0 cases per 100 000 men). Any potential reduction in mortality from screening, according to data from randomized studies, probably won’t happen for 7 to 10 years. Therefore, it would be extremely unlikely that any decrease in death rates between 1990 and 2000 was caused by screening.
Some readers thought that instead of merely considering mortality, the USPSTF should have taken into account a decrease in morbidity from prostate cancer. When comparing the intervention and control groups in the ERSPC and PLCO trials after 11 and 13 years of follow-up, a significant difference in the rate of metastatic disease should have been present. If so, a greater impact on the decrease in mortality would have been anticipated. The USPSTF concurs that a shown impact of PSA-based screening on long-term quality of life or functional status would be a significant outcome to take into account, but there is not enough information from screening trials to make this kind of inference. The ERSPC experiment does not provide longitudinal follow-up for the development of such disease in screened versus unscreened individuals, just data on the incidence of metastatic disease at the time of diagnosis. Data on quality of life from early-stage prostate cancer randomized treatment studies indicate that treatment with observation or watchful waiting offers a similar long-term quality of life as early intervention, with a notable decrease in treatment-related side effects (31, 32).
Many respondents encouraged the USPSTF to evaluate a paper stating that the PLCO trial’s comorbidity status had an impact on the efficacy of PSA-based screening (33); they considered this provided proof that PSA-based screening may be advised for relatively healthy men. The hazard ratio for death in men without comorbid illnesses in the annual screening group compared to the usual care group was 0.56, according to the study by Crawford and colleagues (33) (CI, 0.33 to 0.95). However, the PLCO investigators later stated that this finding was dependent on the criteria of comorbidity employed as part of their prolonged follow-up of the trial (23). Crawford and colleagues decided on a broader definition of comorbidity that encompassed both “typical” Charlson comorbidity index disorders as well as obesity, diverticulosis, gallbladder disease, and hypertension (even if it was well-controlled). An interaction was no longer observed when the study was redone using just validated comorbidity measures (namely, Charlson comorbidity index conditions only). The biological plausibility of this discovery by Crawford and colleagues has been questioned by a number of researchers (PLCO investigators included), who point out, among other things, that the positive interaction appears to be largely driven by the inclusion of hypertension and obesity, conditions that seem to convey minimal excess treatment risks or differences in treatment options. These researchers also point out that, contrary to Crawford and colleagues’ initial claims, participants in the usual care group with higher levels of comorbidity actually had a statistically significant lower risk of dying from prostate cancer than healthier men. This is because comorbid conditions reduce the effectiveness of treatment, which makes screening ineffective in less healthy men (23, 34). The effect of radical prostatectomy compared to observation did not differ by comorbidity or health status, according to preliminary PIVOT data (12).
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Cost of Illness
Prostate cancer affected an estimated 240 890 American males in 2011, and the disease claimed an estimated 33 720 lives (35). Between 2003 and 2007, the median age of prostate cancer fatalities was 80 years, with 71% of deaths occurring in males older than 75 years. The average age of diagnosis was 67 years (1). Both the incidence and mortality rates of prostate cancer are significantly greater in black men than white men (232 vs. 146 cases per 100 000 men and 56 vs. 24 deaths per 100 000 men, respectively) (35).
Clinically, prostate cancer is a diverse illness. According to autopsy studies, almost one-third of men between the ages of 40 and 60 have histologically visible prostate cancer (36); the percentage rises to as high as three-fourths in men over the age of 85. (37). The majority of instances have microscopic, well-differentiated lesions that are not expected to have any bearing on clinical care. The discovery of lesions that are unlikely to be of clinical relevance is increased by increased PSA testing frequency, a lower threshold for biopsy, and an increase in the number of core biopsies taken.
Aims of the Review
For males under the age of 75, screening for prostate cancer did not appear to enhance health outcomes, including mortality from prostate cancer and all other causes, according to the previous evidence update conducted for the USPSTF in 2008. The USPSTF found sufficient evidence that the incremental benefits of treating prostate cancer identified through screening are minimal to none and that the hazards of both screening and therapy outweigh any possible benefits in men aged 75 or older (38). The USPSTF decided that a targeted update of the direct evidence on the advantages of PSA-based prostate cancer screening should be carried out after the publication of initial mortality results from 2 significant randomized, controlled trials of prostate cancer screening (39). The USPSTF also asked for a separate systematic study of the advantages and disadvantages of treating locally advanced prostate cancer (10). Updated results from the ERSPC and PLCO trials as well as information on the risks associated with prostate biopsy from the ProtecT trial have become available since the USPSTF’s draft recommendation statement on prostate cancer screening and its supporting systematic evidence reviews were published. These publications served as the basis for this final recommendation statement.
Precision of Screening
Many cases of prostate cancer are caught by the standard PSA cutoff of 4.0 ng/L, but some cases will go undetected. A lower cutoff discovers more cancer cases, but at the expense of classifying more men as having cancer at risk. For instance, lowering the cutoff for PSA to 2.5 g/L would more than treble the proportion of American men between the ages of 40 and 69 who would have abnormal readings (16), the majority of which would be false-positive results. Additionally, it enhances the possibility of finding benign, non-clinically significant cancers. On the other hand, raising the PSA cutoff to greater than 10.0 g/L would result in a reduction of over 1.2 million males aged 50 to 69 years having abnormal results to about 352 000. (16). There is no PSA threshold at which a guy can be certain that he is cancer-free (40).
When used as a reference standard to evaluate the accuracy of prostate cancer screening procedures, needle biopsy data have inherent issues. The number of biopsies performed during a single surgery affects the rate of cancer detection; the more biopsies performed, the more cancer cases discovered. The apparent specificity of an increased PSA level seems to rise with the number of cancer cases discovered using a “saturation” biopsy approach (20 core biopsies), although many of the additional cancer cases discovered in this way are unlikely to be clinically significant. Therefore, it is impossible to pinpoint the PSA test’s accuracy for identifying cases of prostate cancer that are clinically significant.
It has been suggested that different PSA screening methods, such as the use of age-adjusted PSA cutoffs, free PSA, and PSA density, velocity, slope, and doubling time, can help detect cases of clinically significant prostate cancer. However, there is no proof that any of these testing procedures improve health outcomes; in fact, several of them might possibly be harmful. According to one study, utilizing PSA velocity in the absence of other symptoms could result in 1 in 7 men receiving a biopsy without any improvement in the accuracy of the prediction (41).
Early detection and treatment’s efficiency
Two randomized controlled studies of low quality (high risk of bias) that were started in Sweden in the 1980s each showed a nonstatistically significant trend toward higher prostate cancer mortality in groups who had been invited to screening (21, 22). Similar outcomes were observed in a third low-quality (high risk of bias) Canadian trial when an intention-to-screen analysis was conducted (20). These trials employed various screening methods; all of them included one or more PSA tests with cutoffs ranging from 3.0 to 10.0 g/L. They also included various amounts of digital rectal examination and transrectal ultrasonography.
The USPSTF’s primary trials under consideration were the more recent PLCO and ERSPC trials. In the fair-quality prostate portion of the PLCO trial, 76 685 men between the ages of 55 and 74 were randomized to receive either usual care or a yearly PSA screening for 6 years (along with a concurrent digital rectal examination for 4 years). The PSA limit utilized was 4.0 g/L. The participant and his personal physician decided on the participant’s course of treatment and diagnostic follow-up for positive screening test findings; 90% of men with prostate cancer diagnoses underwent active treatment (surgery, radiation, hormonal therapy, or some combination). When compared to men in the control group, the screened group showed a nonstatistically significant tendency toward higher prostate cancer mortality after 7 years (full follow-up) (RR, 1.14 [CI, 0.75 to 1.70]). (19). After 13 years, similar results were observed (RR, 1.09 [CI, 0.87 to 1.36]). (23). The study’s high contamination rate is its main criticism; although the researchers increased both the number of screening intervals and the length of follow-up in an effort to counteract the contamination effects, about 50% of the men in the control group underwent at least one PSA test during the study. Additionally, about 40% of participants had a PSA test during the previous three years of enrolment, despite the fact that subgroup analyses stratified by history of PSA testing prior to study participation did not demonstrate distinct impacts on prostate cancer mortality rates (19). Contamination might lessen disparities between the 2 groups, but it couldn’t account for men assigned to screening having a higher incidence of prostate cancer or a higher fatality rate.
182 160 men from 7 European nations, ages 50 to 74, were randomly allocated to receive standard treatment or undergo PSA testing every two to seven years in the fair-quality ERSPC experiment. Depending on the study center, the prostate-specific antigen cutoffs ranged from 2.5 to 4.0 g/L (although one institution utilized a cutoff of 10.0 g/L for a while). Treatment and subsequent diagnostic techniques differed per center as well. When given a prostate cancer diagnosis, 66% of men opted for urgent treatment (surgery, radiation therapy, hormonal therapy, or some combination). After a median follow-up of 9 years, there was a marginal drop in prostate cancer mortality among all the males who were randomly allocated to the screening group (RR, 0.85 [CI, 0.73 to 1.00]). (4). After 11 years of follow-up, similar findings that were statistically significant were found (RR, 0.83 [CI, 0.72 to 0.94]). (15). A statistically significant decrease in prostate cancer deaths was observed in the screened group after a median follow-up of 9 years restricted to men aged 55 to 69 years (RR, 0.80 [CI, 0.65 to 0.98]). (4). The authors predicted that 1055 men needed to be invited to screening and 37 instances of prostate cancer needed to be discovered in order to prevent one prostate cancer mortality (RR, 0.79 [CI, 0.45 to 0.85] after 11 years of follow-up) (15). Two centers—Sweden and the Netherlands—showed statistically significant decreases in prostate cancer deaths with PSA screening among the seven distinct centers included in the mortality analysis. In comparison to other countries, the size of the effect was significantly bigger in these 2 centers (Figure 2). The study has mostly been criticized for its inconsistent age restrictions, screening intervals, PSA thresholds, and enrollment procedures, as well as for excluding out data from two study locations from the analysis. The fact that the study and control groups received different treatments raises additional concerns about possible outcomes. A participant in the control group with high-risk prostate cancer was more likely than a participant in the screening group to receive radiotherapy, expectant management, or hormonal therapy in place of radical prostatectomy, and men in the screening group were more likely than men in the control group to have received treatment in a university setting (42). In addition, men whose prostate cancer was found at autopsy were included in the analysis of causes of death in men with a prostate cancer diagnosis. Although it is unknown how this cause-of-death adjudication process may alter estimates, prior research has shown that it is difficult to determine the cause of death with accuracy and that even tiny inaccuracies may have a significant impact on outcomes (43, 44).
One site from that experiment, Göteburg, Sweden, provided data independently after the first ERSPC mortality statistics were published. The outcomes for 60% of this center’s participants were reported as part of the main ERSPC publication, and the ERSPC trial’s ensuing country-specific results (which included some males not included in the trial’s overall results) are consistent with the independently reported results from Sweden (45).
There aren’t many randomized, controlled trials that compare watchful waiting with therapies for localized prostate cancer. After 15 years of follow-up, a randomized, controlled trial of 695 men with localized prostate cancer (Scandinavian Prostate Cancer Group Study 4) found that patients assigned to radical prostatectomy versus watchful waiting had an absolute lower risk of distant metastases (11.7% [CI, 4.8% to 18.6%]). Over this time, there was also an absolute decline in prostate cancer mortality (6.1% [CI, 0.2% to 12.0%]) and a trend toward a decline in all-cause mortality (6.6% [CI, 1.3% to 14.5%]). According to subgroup analysis, males 65 years of age or younger were the only ones who benefited from prostatectomy. Because just 5% of patients had prostate cancer discovered through screening, 88% had palpable tumors, and more than 40% experienced symptoms, it is unlikely that these findings will be applicable to cancer found by PSA-based screening (13, 17). After 23 years of follow-up, a previous, subpar study found no mortality difference between radical prostatectomy and watchful waiting (46). Following the conclusion of the evidence review, preliminary mortality results from a second randomized trial comparing EBRT with watchful waiting among 214 men with localized prostate cancer identified before the start of PSA screening were made available. Men who were randomly assigned to watchful waiting or EBRT did not have significantly different observed survival rates at 20 years (31% vs. 35%; P = 0.26). Although high in both groups, prostate cancer mortality at 15 years did not differ between them (23% vs. 19%; P = 0.51). External beam radiation did shorten recurrence-free survival and diminish distant progression (25).
Since the conclusion of the evidence review, preliminary PIVOT results have now been accessible. The American study PIVOT included a substantially greater proportion of men with prostate cancer found through screening since it included men with prostate cancer found after the introduction of universal PSA testing. The experiment randomly allocated 731 men with clinically localized prostate cancer who were 75 years of age or younger (mean age, 67 years) and had a PSA level less than 50 g/L (mean, 10 g/L) to watchful waiting versus radical prostatectomy. Participants made up one-third black people. Approximately 43% of patients had low-risk cancers, 36% had intermediate-risk tumors, and 21% had high-risk tumors based on their PSA level, Gleason score, and tumor stage. Men treated with surgery vs observation did not statistically significantly differ in terms of prostate cancer-specific or all-cause mortality after a median follow-up of 10 years (absolute risk reduction, 2.7% [CI, 1.3% to 6.2%] and 2.9% [CI, 4.1% to 10.3%], respectively). According to subgroup analysis, patient characteristics such as age, race, health status, Charlson comorbidity index score, or Gleason score had no bearing on the effectiveness of radical prostatectomy compared to observation for overall and prostate cancer-specific mortality. However, there was a relationship between PSA level and possibly tumor risk category. There was an absolute risk reduction of 7.2% (CI, 0.0% to 14.8%) and 13.2% (CI, 0.9% to 24.9%) for prostate cancer-specific and all-cause mortality, respectively, in men in the radical prostatectomy group with a PSA level greater than 10 g/L at diagnosis, in comparison to men in the watchful waiting group. However, men in the radical prostatectomy group with PSA levels of 10 g/L or less or those with low-risk tumors did not experience a decrease in prostate cancer-specific or all-cause mortality, and a possible (nonstatistically significant) increase in mortality was suggested when compared to the watchful waiting group (12).
Screening and treatment risks
According to the PSA cutoff and the frequency of screening, false-positive PSA test results can occur frequently. Men in the PLCO trial’s screening group had a cumulative risk after 4 PSA tests of 12.9% for at least 1 false-positive finding (defined as a PSA level more than 4.0 g/L and no prostate cancer diagnosis after 3 years) and 5.5% for at least 1 biopsy because of a false-positive finding (47). Men with false-positive PSA test results are more likely than control subjects to worry specifically about prostate cancer, believe their chance of developing the disease to be higher, and experience issues with their sexual function for up to a year following testing (48). Men with false-positive PSA test results were more likely to have subsequent biopsies and repeat PSA testing within a year of the first negative biopsy, with 26% of those men reporting that they had felt moderate to severe pain during the biopsy (49). There are also false-negative outcomes, and there is no PSA level that conclusively excludes prostate cancer. Because of this, it is now recommended to perform prostate biopsies at PSA thresholds lower than those previously used in randomized screening trials (for instance, 2.5 g/L).
Persistent hematospermia (50.4%), hematuria (22.6%), fever (3.5%), urinary retention (0.4%), and hospitalization for signs of prostatitis or urosepsis (0.5%) are all side effects of prostate biopsy that were documented by the Rotterdamcenter of the ERSPC experiment (50). 32% of men experienced pain, fever, blood in the urine, semen, or stool, infection, temporary urinary difficulties, or other issues requiring clinician follow-up after prostate biopsy, according to the ProtecT study, an ongoing randomized, controlled trial evaluating the efficacy and acceptability of treatments for men with PSA-detected, localized prostate cancer. 20% of men said they would think a subsequent biopsy would be a “moderate or major problem” at 7 days after the biopsy, and 1.4% of men were hospitalized for complications. In a U.S. study of older, mostly white male Medicare enrollees, similar results were observed 30 days following biopsy (51).
Due to the PSA test’s high likelihood of producing false-positive results and inability to distinguish between slow-growing and fast-growing tumors, many men undergo unnecessary biopsies and receive excessive diagnoses and treatments for prostate cancer. The proportion of men who undergo biopsies is closely correlated with the proportion of men who undergo PSA testing, the PSA level that necessitates a biopsy, and the time between PSA tests. Estimates from the ERSPC and PLCO trials suggest that 17% to 50% of prostate cancer cases identified by the PSA test may have been overdiagnosed. Overdiagnosis is a problem because, despite the fact that these men cannot benefit from any associated treatments, they are still subject to the negative effects of a particular therapy. According to evidence, over 90% of American men who have clinically localized prostate cancer are treated early (most commonly with radical prostatectomy and radiation therapy) (7, 8).
Following one to ten years, watchful waiting is associated with a 20% absolute risk increase for urinary incontinence and a 30% absolute risk increase for erectile dysfunction compared to radical prostatectomy (i.e., increased 20% above a median rate of 6% and 30% above a median rate of 45%, respectively). About 0.5% of patients experience perioperative deaths, and 0.6% to 3% of patients experience cardiovascular events. A population-based observational cohort study using the SEER database and Medicare-linked data found that robotic or minimally invasive radical prostatectomy for prostate cancer was associated with higher risks for genitourinary complications, incontinence, and erectile dysfunction than open radical prostatectomy. Comparative data on outcomes using various surgical techniques are scarce (54).
After 1 to 10 years, radiation therapy is associated with an increased risk of bowel dysfunction (such as fecal urgency or incontinence) and an increased risk of erectile dysfunction (17% absolute increase over a median rate of 50%). The effect on bowel function is most noticeable in the early months following treatment.
Androgen deprivation therapy is not FDA-approved for the treatment of localized prostate cancer, and older men who receive it have worse clinical results than those who receive conservative management (55). In addition to systemic side effects like hot flashes and gynecomastia, androgen deprivation therapy is linked to an increased risk for impotence compared to watchful waiting (absolute risk difference, 43%). Androgen deprivation therapy may cause other serious side effects in men with advanced prostate cancer, such as diabetes, myocardial infarction, or coronary heart disease; these effects, however, have not been thoroughly researched in men receiving treatment for localized prostate cancer. Androgen deprivation therapy was not linked to an increased risk of cardiac mortality, according to a recent meta-analysis of 8 randomized, controlled trials in men with high-risk, nonmetastatic prostate cancer.
Estimate of Net Benefit in Dollars
With the exception of one, all randomized trials have been unable to show that the PSA test reduces prostate cancer deaths, and several—including the PLCO trial—have suggested an increased risk in screened men, possibly because of harms related to overdiagnosis and overtreatment. After a median follow-up of 11 years, a small (0.09%) absolute reduction in prostate cancer deaths was observed in a predetermined subgroup of men in the ERSPC trial who were aged 55 to 69. Since most men with prostate cancer die from non-prostate-cancer causes, it will be a while (at least 9 to 10 years) before any potential cancer-specific mortality benefit from PSA-based screening is realized. Through 14 years of follow-up, no prostate cancer screening study or randomized trial of treatment for cancer discovered through screening has shown a decrease in all-cause mortality.
The risks associated with PSA-based prostate cancer screening include a high rate of false-positive results and their accompanying detrimental psychological effects, a high rate of complications from diagnostic biopsies, and—most importantly—a chance of overdiagnosis and overtreatment. Treatment for prostate cancer carries the risk of death, cardiovascular events, urinary incontinence, erectile dysfunction, and bowel dysfunction depending on the method used. Many of these negative effects are frequent and enduring. Limiting estimates of the harms of PSA testing to the harms of the blood test alone, without taking other diagnostic and treatment harms into account, does not reflect current clinical practice in the United States, given the high propensity for doctors and patients to choose to treat screen-detected cancer.
Through 11 years, the mortality benefits of PSA-based prostate cancer screening are, at best, minimal and may even be nonexistent, while the harms are moderate to significant. Therefore, the USPSTF comes to the conclusion that the risks are not outweighed by the benefits of PSA-based prostate cancer screening as it is currently practiced and researched in randomized, controlled trials.
How Does the Evidence Complement Biological Knowledge?
As currently applied in the United States, prostate-specific antigen-based screening and subsequent treatment assume that the majority of asymptomatic prostate cancer cases will eventually become clinically significant and result in poor health outcomes and that early treatment effectively lowers both prostate cancer-specific and overall mortality. This hypothesis is not supported by long-term, population-based cohort studies or randomized treatment trials of men with locally advanced prostate cancer who are under conservative management. Men with a median age at diagnosis of 69 years and tumors that were mostly unintentionally discovered during transurethral resection or open surgery for benign prostatic hyperplasia were studied from the Connecticut Tumor Registry, which was established prior to the PSA screening era. Men either received early or delayed androgen deprivation therapy or observation alone. The mortality rate for prostate cancer was 18 deaths per 1000 person-years after 15 years of follow-up. It was 6 deaths per 1000 person-years for men with well-differentiated prostate cancer; significantly more of these men (75% vs. 7%) had passed away from causes other than prostate cancer. Men with localized prostate cancer who had not previously tried curative therapy were subjected to a risk analysis of death following the widespread adoption of PSA-based screening. Depending on tumor stage, the 10-year prostate cancer mortality rate for men aged 66 to 69 at diagnosis with well- or moderately differentiated tumors ranged from 0% to 7%, compared to 0% to 22% for other causes. Age at prostate cancer diagnosis significantly increased the relative proportion of deaths attributed to other causes compared to prostate cancer. Prostate cancer mortality at 12 years or more in the only randomized, controlled trial contrasting early intervention with watchful waiting that included men primarily detected by PSA testing was uncommon (7%), and men randomly assigned to surgery versus observation showed no differences.
Update of the Prior USPSTF Recommendation: Previous SectionNext Section
The 2008 recommendation is replaced by this one (38). The USPSTF now advises against PSA-based screening for prostate cancer in all age categories, as opposed to its earlier advice against it for men 75 years of age or older and its conclusion that there was not enough data to make a recommendation for younger men.
Recommendations from Others: Previous SectionNext Section
If predicted life expectancy is longer than 10 years, the American Urological Association advises offering PSA screening along with a digital rectal examination to asymptomatic males aged 40 or older who wish to be screened (60). This recommendation is currently being updated (61). According to the American Cancer Society, men at ordinary risk should start receiving information about prostate cancer screening at age 50, while black men and men with a family history of the disease should start receiving information at age 45. (62). The American College of Preventive Medicine advises doctors to individualize screening choices for individuals by discussing the potential advantages and disadvantages of PSA screening with males 50 years of age or older (63). The AmericanCollege of Physicians is currently creating a guidance statement on this subject, while the AmericanAcademy of Family Physicians is amending its guideline.
U.S. Preventive Services Task Force Appendix 1: Previous SectionNext Section
At the time that this recommendation was finalized, the U.S. Preventive Services Task Force was composed of Virginia A. Moyer, MD, MPH, Chair (Baylor College of Medicine, Houston, Texas); Michael L. LeFevre, MD, MSPH, Co-Vice Chair (University of Missouri School of Medicine, Columbia, Missouri); Albert L. Siu, MD, MSPH, Co-Vice Chair (Mount Sinai School of Medicine, New York, New York, and (University of Minnesota and Minneapolis Veterans Affairs Medical Center, Minneapolis, Minnesota). Ned Calonge, MD, MPH, and Rosanne Leipzig, MD, PhD, were former members of the USPSTF who helped create this proposal.
Appendix 2: Assumptions and References Previous SectionNext Section Table 3
Estimates of prostate cancer mortality in screened and unscreened males are based on data from the PLCO (23) and ERSPC (15) trials’ 11- and 13-year follow-up studies. The PLCO study and the Finnish center of the ERSPC experiment provide data on the false-positive rates for PSA tests (47, 64). Rosario and colleagues’ research provides details about the risks of biopsy (6). Based on the incidence observed in the screened group of the PLCO trial, the incidence of prostate cancer in a population that underwent screening is calculated (23). The SEER program and the Cancer of the Prostate Strategic Urologic Research Endeavor registry provide data on the treatment rates for localized prostate cancer in the US population (9, 10). The evidence evaluation conducted for the USPSTF yielded pooled estimates that were used to determine the expected complication rates from prostatectomy and radiation therapy (10).
Article and Author Information Previous SectionNext Section
Disclaimer: The USPSTF’s recommendations are not backed by the American government. They should not be taken to represent the official stance of the U.S. Department of Health and Human Services or the Agency for Healthcare Research and Quality.
The USPSTF receives financial support as a voluntary, independent organization. The Agency for Healthcare Research and Quality is required to support the USPSTF’s operations by the US Congress.
Potentially conflicting interests: Dr. Moyer received funding from the Agency for Healthcare Research and Quality to attend meetings for the study or other purposes, and the American Academy of Pediatrics provided consulting services. On the website www.acponline.org/authors/icmje/ConflictOfInterestForms.do?msNum=M12-1086, disclosure forms from USPSTF members can be viewed.
Single Reprint Requests: You can get reprints from the USPSTF website (https://www.uspreventiveservicestaskforce.org/).
↵* See Appendix 1 for a list of the USPSTF’s members.
On May 22, 2012, this article appeared on https://www.acpjournals.org/.
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Krysten Sowle on July 23, 2012 at 5:18 am said:
Rattling good information can be found on website.