Volume 117, Issue 10 , Pages 719-725, 15 November 2004
Psychological effects of a suspicious prostate cancer screening test followed by a benign biopsy result
Article Outline
Abstract
Purpose
To evaluate the psychological implications of an apparently false-positive screening result for prostate cancer.
Methods
The sample comprised 167 men with a benign biopsy result in response to a suspicious screening test result (biopsy group) and 233 men with a normal prostate-specific antigen (PSA) test result (control group). The men responded to a questionnaire within about 6 weeks of their biopsy or PSA results. They were asked about demographic characteristics, medical history, psychological effects, biopsy experience, and prostate cancer knowledge.
Results
The survey response rate was 85% (400/471). The mean (± SD) age of respondents was 60 ± 9 years (range, 40 to 88 years); 88% (n = 350) were white. Forty-nine percent (81/167) of men in the biopsy group reported having thought about prostate cancer either “a lot” or “some of the time”, compared with 18% (42/230) in the control group (P < 0.001). In addition, 40% (67/167) in the biopsy group reported having worried “a lot” or “some of the time” that they may develop prostate cancer, compared with 8% (18/231) in the control group (P < 0.001).
Conclusion
Men who underwent prostate biopsy more often reported having thought and worried about prostate cancer, despite having received a benign result. This underrecognized human cost of screening should be considered in the debate about the benefits and harms of prostate cancer screening. Am J Med. 2004;117:719 -725.
Screening reduces mortality from breast and colon cancer, but the benefits of prostate cancer screening are uncertain, owing to the absence of controlled clinical trials (1). A randomized trial conducted in Sweden reported ambiguous results regarding radical prostatectomy compared with watchful waiting for men whose prostate cancer was discovered by means other than screening (2). Prostate cancer deaths and distant metastases were reduced in men who underwent surgery, but overall mortality was not. Since most of the men were not detected with prostate-specific antigen (PSA) tests, the implications for PSA screening remain unclear. Despite this controversy, prostate cancer screening is widespread in the United States (3).
The effect of cancer screening programs on the psychological health of participants has received little attention, although the value of mass screening has been questioned (4). Studies in breast cancer have shown that a false-positive mammogram is associated with increased morbidity in terms of increased anxiety (5, 6, 7), perception of breast cancer risk (8), and resource utilization (9, 10, 11). Given the large numbers of men serially screened for prostate cancer and the high false-positive rate, the consequences for men with a suspicious test result followed by a benign biopsy result (cautiously called “false positive” because some of these men may have a false-negative biopsy result) need to be considered. The aim of our study was to evaluate the short-term psychological implications of an apparently false-positive test result for prostate cancer.
Methods
Study sample and design
A prospective cohort of 400 consecutive men was assembled between August 2001 and September 2002 from the primary care practices of Massachusetts General Hospital, Brigham and Women’s Hospital, and Boston Medical Center. Men were identified for the biopsy and control groups through weekly review of pathology reports and PSA test results. The inclusion criteria were age ≥40 years, residence in the United States, a primary care physician at one of the participating institutions, and either a benign result from a biopsy that had been performed because of a suspicious screening test result (biopsy group) or a normal PSA test result (defined conservatively as <2.5 ng/mL) (control). The exclusion criteria were prostate cancer, inability to understand English, and no permission granted from the physician; a previous biopsy was an additional exclusion criterion in the control group.
Participants were mailed a brief (<10 minutes), self-administered, pretested questionnaire about 6 weeks after their benign biopsy result (biopsy group) or normal screening PSA test result (control). The mailing included a cover letter signed by the patient’s primary care physician, a fact sheet describing the study, and a postage-paid return envelope. A telephone reminder and mailing to nonrespondents followed. Identical questionnaires were used, except that the biopsy group survey included questions about the biopsy experience.
The institutional review board of each institution approved the study. Based on recommendations from the human subjects committees, the protocol varied slightly among the institutions. The first step at all sites was contacting the primary care physicians by mail for permission to contact eligible patients. Once a signed letter of introduction was obtained from these physicians, the second step differed among sites; at Boston Medical Center, where telephone informed consent was not permitted, the men were mailed a survey along with a token incentive, and the return of the completed survey constituted informed consent. At Massachusetts General Hospital and Brigham and Women’s Hospital, informed consent was obtained by telephone before mailing the survey, without an incentive.
Response
Eighty-five percent (175/205) of men in the biopsy group and 70% (246/349) in the control group from Massachusetts General Hospital and Brigham and Women’s Hospital agreed to participate; 11% (n = 22) in the biopsy group and 24% (n = 84) in the control group declined to participate. The remaining could not be reached by telephone. Of those who agreed to participate, 91% (n = 159) from the biopsy group and 86% (n = 212) from the control group returned the survey. Nineteen men were ineligible at the time of telephone consent. At Boston Medical Center, 44% (8/18) of men in the biopsy group and 51% (21/41) of men in the control group returned the survey.
Overall, 471 eligible men were sent a survey and 400 men (85%) responded. In the biopsy group, 191 were sent a survey and 167 (87%) responded, and among the control group, 280 were sent a survey and 233 (83%) responded. The slightly higher response rate in the biopsy group may reflect that men in that group were more interested and concerned about the topic, having just had a suspicious result, in comparison with controls who had a normal screening result.
Questionnaire development
We performed a literature review of assessments of the psychological effects of suspicious prostate cancer screening results. Few relevant studies were identified (12, 13, 14, 15); therefore, assessments quantifying the effects of suspicious mammograms were also reviewed (5, 6, 10, 16).
We conducted three focus groups of men who had a benign biopsy result in response to a suspicious screening test result, and one focus group of men who had a normal screening PSA test result. A preliminary questionnaire was developed, which was subsequently refined using in-person pretesting (n = 5) (17, 18).
Questionnaire data
Information on age, race, marital status, and education was collected, as was information on family history of prostate cancer, medical history (19), and health status information (20). Questions about the prostate biopsy experience included the following: how many times the patient had a biopsy; reason for the biopsy (abnormal PSA test result, digital rectal examination, or both); whether results showed “atypical cells but no cancer”; and how painful was the biopsy (rated on a scale of 0 to 10, with 0 being “no pain at all” and 10 being “pain as bad as you can imagine”). Three validated questions about prostate cancer knowledge (21) were included, as well as three additional questions about prostate biopsy (19).
Men were asked how often during the past month they had thought about prostate cancer, worried about developing prostate cancer, and worried about dying soon. They were also asked about reassurance as a result of their most recent biopsy or PSA test result; whether their life had changed for the better, worse, or not at all by that most recent result; and what they thought was their chance of getting prostate cancer some day (5, 6).
Statistical analysis
Differences in proportions between the two groups were compared with the chi-squared or Fisher exact test. P values <0.05 were considered significant. Analyses were performed using SPSS software (Chicago, Illinois).
Results
Overall, the mean (± SD) age of the men surveyed was 60 ± 9 years (range, 40 to 88 years). There were no significant differences between the groups in demographic characteristics or family history of prostate cancer (Table 1). However, compared with the control group, men in the biopsy group were more likely to have a history of benign prostatic hyperplasia (34% [57/167] vs. 13% [30/233], P < 0.001) or prostatitis (23% [38/167] vs. 9% [21/233], P < 0.001), or a greater number of previous PSA tests (62% [99/161] vs. 45% [92/209] had five or more tests, P = 0.002).
Table 1. Characteristics of the Participants*
| Characteristic | Biopsy Group (n = 167) | Control Group (n = 233) | P Value |
|---|---|---|---|
| Number (%) | |||
| Age (years) | 0.40 | ||
 <50 | 16 (10) | 29 (13) | |
| 50–59 | 58 (35) | 89 (38) | |
| 60–69 | 63 (38) | 77 (33) | |
| 70–79 | 29 (17) | 32 (14) | |
| ≥80 | 1 (1) | 5 (2) | |
| White (not Hispanic) | 149 (90) | 201 (87) | 0.13 |
| Married | 131 (79) | 171 (74) | 0.26 |
| Education | 0.23 | ||
| High school or less | 31 (19) | 29 (12) | |
| Some college or college degree | 69 (42) | 104 (45) | |
| Advanced degree | 66 (40) | 100 (43) | |
| Family history of prostate cancer | 23 (14) | 31 (13) | 0.87 |
| Benign prostatic hyperplasia | 57 (34) | 30 (13) | <0.001 |
| Prostatitis | 38 (23) | 21 (9) | <0.001 |
| Number of previous PSA tests | 0.002 | ||
| 1 | 16 (10) | 35 (17) | |
| 2–4 | 46 (29) | 82 (39) | |
| 5–10 | 61 (38) | 68 (33) | |
| ≥11 | 38 (24) | 24 (12) | |
* Numbers for individual items vary slightly because of nonresponse. |
Psychological effects
Forty-nine percent (81/167) of men in the biopsy group reported having thought about prostate cancer either “a lot” or “some of the time,” compared with 18% (42/230) of controls (P <0.001) (Table 2). Men in the biopsy group were also far more likely to report having worried “a lot” or “some of the time” about the possibility of developing prostate cancer (40% [67/167] vs. 8% [18/231], P < 0.001). More men in the biopsy group reported their lives having changed for the better because of their most recent test results, compared with controls (31% [51/164] vs. 13% [30/225], P < 0.001). However, despite the positive effect reported associated with the benign biopsy result, 36% (59/165) of men in the biopsy group thought their chance of getting prostate cancer was “much more” or “a little more than average,” compared with 18% (40/230) of men in the control group (P = 0.001). There was no difference between the two groups regarding worry about dying soon or reassurance from the recent result.
Table 2. Short-term Psychological Effects of a Suspicious Prostate Cancer Screening Test Result Followed by a Benign Biopsy Result*
| Item | Biopsy Group (n = 167) | Control Group (n = 233) | P Value |
|---|---|---|---|
| Number (%) | |||
| In the past month, how much have you thought about prostate cancer? | <0.001 | ||
| A lot | 25 (15) | 5 (2) | |
| Some | 56 (34) | 37 (16) | |
| Only a little | 52 (31) | 64 (28) | |
| Not at all | 34 (20) | 124 (54) | |
| In the past month, how often has the possibility that you might develop prostate cancer worried you? | <0.001 | ||
| A lot | 12 (7) | 3 (1) | |
| Some | 55 (33) | 15 (7) | |
| Only a little | 51 (31) | 59 (26) | |
| Not at all | 49 (29) | 154 (67) | |
| In the past month, how much of the time have you worried about dying soon? | 0.17 | ||
| A lot | 7 (4) | 2 (1) | |
| Some | 17 (10) | 27 (12) | |
| Only a little | 50 (30) | 71 (31) | |
| Not at all | 93 (56) | 132 (57) | |
| How reassured about prostate cancer do you feel as a result of your most recent prostate biopsy (biopsy group) or PSA test (control group) result? | 0.08 | ||
| A lot | 103 (62) | 126 (56) | |
| Some | 41 (25) | 62 (27) | |
| Only a little | 19 (11) | 20 (9) | |
| Not at all | 4 (2) | 18 (8) | |
| Has your life changed for the better, the worse, or not at all, because of your most recent prostate biopsy (biopsy group) or PSA test (control group) result? | <0.001 | ||
| For the better | 51 (31) | 30 (13) | |
| For the worse | 7 (4) | 0 | |
| Not at all | 106 (65) | 195 (87) | |
| What do you think is your chance of getting prostate cancer some day? | <0.001 | ||
| Much more than average | 17 (10) | 11 (5) | |
| A little more than average | 42 (26) | 29 (13) | |
| Same as average | 73 (44) | 118 (51) | |
| A little less than average | 23 (14) | 43 (19) | |
| Much less than average | 10 (6) | 29 (13) | |
* The survey was administered to participants about 6 weeks after a benign prostate biopsy (biopsy group) or a normal screening prostate specific antigen test (control group) result. Numbers for individual items vary slightly because of nonresponse. |
Prostate cancer knowledge
More men in the biopsy group than in the control group answered questions about prostate cancer and biopsy correctly (Table 3). However, the overall frequency of correct responses in the biopsy group was still relatively low: 2% (4/165) answered all three prostate cancer knowledge questions correctly and 31% (51/165) answered all questions incorrectly, and 20% (33/167) answered all three biopsy questions correctly and 27% (45/167) answered all three questions incorrectly.
Table 3. Prostate Cancer Knowledge after a Benign Prostate Biopsy or a Normal Screening Prostate Specific Antigen Test Result*
| Item | Biopsy Group (n = 167) | Control Group (n = 233) | P Value |
|---|---|---|---|
| Number (%) | |||
| How many men with early-stage prostate cancer do you think will die of the disease? | 0.60 | ||
| Most or all will | 2 (1) | 2 (1) | |
| About half | 14 (8) | 12 (5) | |
| Most will not† | 93 (56) | 135 (58) | |
| Don’t know | 57 (34) | 84 (36) | |
| Does active treatment for early-stage prostate cancer extend life? | 0.97 | ||
| Very or pretty sure it can | 134 (80) | 189 (81) | |
| Not sure† | 31 (19) | 41 (18) | |
| Very or pretty sure it can not | 2 (1) | 3 (1) | |
| How many men with elevated PSA levels do you think have prostate cancer? | 0.02 | ||
| Most or all do | 5 (3) | 18 (8) | |
| About half do | 31 (19) | 38 (16) | |
| Most do not† | 36 (22) | 29 (13) | |
| Don’t know | 94 (57) | 147 (63) | |
| Do you think an infection or inflammation of the prostate can elevate PSA levels? | 0.01 | ||
| Yes† | 71 (43) | 68 (30) | |
| No | 10 (6) | 10 (4) | |
| Don’t know | 86 (52) | 152 (66) | |
| Do you think a large prostate can elevate PSA levels? | <0.001 | ||
| Yes† | 77 (46) | 57 (25) | |
| No | 16 (10) | 22 (10) | |
| Don’t know | 74 (44) | 152 (66) | |
| Do you think a prostate biopsy can miss some cancer? | 0.35 | ||
| Yes† | 83 (50) | 111 (48) | |
| No | 19 (11) | 18 (8) | |
| Don’t know | 65 (39) | 103 (44) | |
* Numbers for individual items vary slightly because of nonresponse. |
† Denotes correct answer. |
Prostate biopsy experience
About half of the biopsy group (84/164) reported having had only one prostate biopsy, 20% (32/164) reported two, and 25% (41/164) reported having had three or more. Twenty-nine percent (46/159) reported a biopsy result showing “atypical cells but no cancer” (i.e., prostatic intraepithelial neoplasia). Twenty-six percent (42/163) of men reported moderate-to-severe pain (grade of 7 or greater) at their most recent biopsy; only 24% (39/163) reported minimal or no pain (grade 2 or lower). Ninety-five percent (151/159) reported that they would have another biopsy if it was recommended by their doctor.
Discussion
We found that a considerable proportion of men with a benign prostate biopsy result after a suspicious screening test result reported negative psychological effects about 6 weeks later. Thus, at least in the short-term, there had been substantial thinking and worrying about prostate cancer, even after obtaining a benign result. Given that men in the biopsy group had received a suspicious test result that was later determined not to be cancer on biopsy, it is not surprising that one third of these men reported having thought their life had changed for the better because of their most recent benign result. Men in the biopsy group, however, still reported having thought they were at increased risk of prostate cancer.
Our results differ from those of Essink-Bot et al (12) who found no evidence of an anxiety-raising effect associated with screening for prostate cancer. However, their method of assessing anxiety may have been too general, and they advised using a measure directed specifically at worries related to prostate cancer, which our study included. Our results were similar to those found in studies of breast cancer screening (5, 6, 7), and the findings were comparable since we adapted several questions from these same studies.
Schwartz and colleagues (22) found that women tended to be tolerant of false-positive mammography results, seemingly because the false-positive result was worth the reassurance of being told that they did not have cancer. In our study, more than 60% of men reported being reassured “a lot” by the biopsy result. However, since at least 10% of men with a benign biopsy result will have prostate cancer on a subsequent biopsy (approximately 6 weeks later) (23) owing to the poor negative predictive value of the random biopsy, perhaps this reassurance level is inappropriately high and many men were falsely reassured.
In addition to psychological distress, we also found evidence of physical distress. Many men reported moderate-to-severe pain from the biopsy, even though prostate biopsy has become one of the most common urologic procedures and is considered “well-tolerated” (24). Our findings suggest that the discomfort associated with biopsy deserves more attention, and that this procedural part of the evaluation of suspicious screening test results could be improved to make the biopsy itself easier on men.
The degree of psychological (and physical) distress noted in our study raises the question of whether men in the biopsy group will adhere to subsequent screening tests. Our study suggests that adherence may not be a problem, as almost all of the men reported being committed to having subsequent screening tests, and the vast majority of men in the biopsy group would have another biopsy if it was recommended by their doctor.
Our study had several limitations. The absence of prescreening data precluded the determination of whether men in the two groups had equivalent baseline psychological profiles. In addition, the two groups were not comparable at baseline with regard to history of benign prostate conditions. Lastly, the sample primarily included well-educated white men, and the results may not be generalizable to other racial/ethnic groups and those with less education. Different recruitment methods at one of the study institutions, which was selected for its diverse patient population, but where telephone informed consent was not permitted, resulted in a lower response rate at that site. We recommend verification of the results of this study in other samples, particularly African Americans, who are at a higher risk of prostate cancer.
In conclusion, we documented that men who underwent prostate biopsy reported having thought and worried about prostate cancer despite a benign result, and this underrecognized human cost of screening should be considered in the debate about the benefits and harms of prostate cancer screening, particularly in men with benign prostatic hyperplasia or prostatitis, who are at higher risk of false-positive screening results. Moreover, the recent call for biopsies for lower PSA levels will only make this problem of false-positive results worse (25). Therefore, for men who make an educated decision to undergo prostate cancer screening, we recommend the following interventions to reduce the human costs associated with screening: using periprostatic local anesthesia to reduce the discomfort of biopsy (26, 27); providing counseling about the risks of false-positive results before screening, especially to patients with benign prostatic hyperplasia and prostatitis (because of the increased chance of having a false-positive result) (28); and decreasing annual prostate cancer screening to no more than every 2 years, depending on the initial screening PSA level (29), to reduce the risk of a false-positive result.
Acknowledgment
The authors greatly appreciate the scientific input and study design contributions of the late Mark Moskowitz, MD, former Chief of General Medicine at Boston Medical Center. They are also extremely grateful to the primary care physicians from Massachusetts General Hospital, Brigham and Women’s Hospital, and Boston Medical Center who gave permission to contact their patients.
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A Doris Duke Charitable Foundation Clinical Scientist Career Development Award to Dr. McNaughton-Collins supported this work.
PII: S0002-9343(04)00542-X
doi:10.1016/j.amjmed.2004.06.036
© 2004 Elsevier Inc. All rights reserved.
Volume 117, Issue 10 , Pages 719-725, 15 November 2004
