VOLUME 31 䡠 NUMBER 33 䡠 NOVEMBER 20 2013

JOURNAL OF CLINICAL ONCOLOGY

O R I G I N A L

R E P O R T

Psychological Impact of Prostate Biopsy: Physical Symptoms, Anxiety, and Depression Julia Wade, Derek J. Rosario, Rhiannon C. Macefield, Kerry N.L. Avery, C. Elizabeth Salter, M. Louise Goodwin, Jane M. Blazeby, J. Athene Lane, Chris Metcalfe, David E. Neal, Freddie C. Hamdy, and Jenny L. Donovan Julia Wade, Rhiannon C. Macefield, Kerry N.L. Avery, C. Elizabeth Salter, Jane M. Blazeby, J. Athene Lane, Chris Metcalfe, and Jenny L. Donovan, University of Bristol, Clifton, Bristol; Derek J. Rosario and M. Louise Goodwin, Royal Hallamshire Hospital, University of Sheffield, Sheffield; David E. Neal, University of Cambridge, Addenbrooke’s Hospital, Cambridge; and Freddie C. Hamdy, University of Oxford, John Radcliffe Hospital, Oxford, United Kingdom. Published online ahead of print at www.jco.org on October 21, 2013. The ProBE study was funded by the UK Prostate Cancer Risk, Management Group. The ProtecT study is funded by the UK National Institute for Health Research Health Technology Assessment Programme (Projects No. 96/20/ 06, 96/20/99). The study and authors are independent of the funding bodies. Terms in blue are defined in the glossary, found at the end of this article and online at www.jco.org. Authors’ disclosures of potential conflicts of interest and author contributions are found at the end of this article. Corresponding author: Jenny Donovan, PhD, School of Social and Community Medicine, University of Bristol, 39 Whatley Rd, Clifton, Bristol, BS8 2PS, UK; e-mail: jenny.donovan@ bristol.ac.uk. © 2013 by American Society of Clinical Oncology 0732-183X/13/3133w-4235w/$20.00 DOI: 10.1200/JCO.2012.45.4801

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Purpose To investigate the psychological impact of prostate biopsy, including relationships between physical biopsy-related symptoms and anxiety and depression. Patients and Methods A prospective cohort of 1,147 men, nested within the Prostate Testing for Cancer and Treatment trial and recommended to receive prostate biopsy, completed questionnaires assessing physical and psychological harms after biopsy in the Prostate Biopsy Effects study. Psychological impact was measured using the Hospital Anxiety and Depression Scale, and scores were compared according to experiences of biopsy-related symptoms at biopsy, and at 7 and 35 days afterward, and in relation to biopsy results. Results A total of 1,144 men (99.7%) returned questionnaires at biopsy, with 1,090 (95.0%) and 1,016 (88.6%) responding at 7 and 35 days postbiopsy. Most men experienced biopsy-related symptoms as no problem or a minor problem, and overall levels of anxiety and depression were low and similar to normative levels. Of men receiving a negative biopsy result (n ⫽ 471), anxiety was greater in those experiencing problematic biopsy-related symptoms compared with those experiencing nonproblematic symptoms at 7 days for the following symptoms: pain (P ⬍ .001), shivers, (P ⫽ .020), hematuria (P ⬍ .001), hematochezia (P ⬍ .001), and hemoejaculate (P ⬍ .001). Anxiety was reduced, although symptoms were not, after 35 days. Overall levels of anxiety were low across all time points except at the 35-day assessment among men who had received a cancer diagnosis. Conclusion Problematic postbiopsy symptoms can lead to increased anxiety, distinct from distress related to diagnosis of prostate cancer. Men and doctors need to consider these additional potential harms of biopsy when deciding whether to initiate prostate-specific antigen testing. J Clin Oncol 31:4235-4241. © 2013 by American Society of Clinical Oncology

INTRODUCTION

Prostate cancer (PCa) is the most commonly diagnosed cancer in the United States.1 Incidence of PCa has risen rapidly after introduction of PSA (prostate-specific antigen) blood tests.2 In men who have PSA testing, histologic diagnosis of PCa requires a prostate needle biopsy, and numbers of men undergoing biopsy have increased correspondingly, with up to a million prostate biopsies performed annually among Medicare beneficiaries.3 The age-adjusted rate of prostate biopsy per 100,000 Medicare beneficiaries in white and black men is 1,580 and 1,851 respectively.3 Among an asymptomatic PSA-tested cohort, approximately one third will receive a diagnosis of PCa after

biopsy.4 Risk of subsequent biopsy in men without a cancer diagnosis on initial biopsy is 12% at 1 year and 38% at 5 years.5 Opinion remains divided over potential benefits and harms of screening for PCa. In two recent trials, one showed a benefit for PSA-based population screening6; the other did not.7 The US Preventive Services Task Force recently reviewed the literature on PCa screening and recommended against PSA screening, concluding that screening resulted in a small or no reduction in PCa-specific mortality, but was associated with harms related to subsequent investigation or treatment.8,9 Between 1.0% and 6.9% of men undergoing biopsy require hospital admission within 30 days, most for febrile infections.10-12 Biopsy may also cause bleeding, pain, © 2013 by American Society of Clinical Oncology

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Table 1. Inclusion and Exclusion Criteria for the ProtecT and ProBE Studies Study ProtecT: pragmatic RCT

ProBE: prospective cohort study nested within the ProtecT RCT

Inclusion

Exclusion

Age 50-69 years on the date of preparation of the invitation list by the family physician Male sex Able to give informed written consent

Concomitant or past malignancies (other than a small treated skin cancer) Prior treatment for prostate malignancy Serious cardiac or respiratory problems in the previous 12 months (ie, stroke, MI, heart failure, COPD) Kidney dialyses or transplantation

Fit for any of the three treatmentsⴱ and with an estimated life expectancy of at least 10 years Registration with the participating family physician Men with an elevated PSA result of 3.0 ng/mL and ⬍ 20 ng/mL from the recruitment PSA test Men with an elevated PSA result of ⬎ 19.99 ng/mL only eligible for a ProtecT biopsy if a reason for the elevated PSA at initial PSA test is identified (eg, prostatitis) All above

Bilateral hip replacement Previous entry to the ProtecT study at a prior clinic

All above, plus previous prostate biopsy either within or outside the ProtecT study

Abbreviations: COPD, chronic obstructive pulmonary disease; MI, myocardial infarction; ProBE, Prostate Biopsy Effects; ProtecT, Prostate Testing for Cancer and Treatment; PSA, prostate-specific antigen; RCT, randomized controlled trial. ⴱ Trial treatments: radical surgery, radical conformal radiotherapy, active monitoring.

and urinary and sexual symptoms.7 Evidence of the psychological impact of biopsy is lacking.9 A recent prospectively defined cohort study (Prostate Biopsy Effects [ProBE] study),13 nested within the Prostate Testing for Cancer and Treatment (ProtecT) trial,4 investigated patient-reported adverse effects and health care use during the 35 days after biopsy. The ProBE study found hospital admission was required by 1.3%; consultation with a health professional was reported by 10.4%.13 Biopsy was associated with experiences of pain (43.6%), fever (17.5%), hematuria (65.8%), hematochezia (36.8%), and hemoejaculate (92.6%). These symptoms were indicated to be a major or moderate problem for the following: pain, 7.3%; fever, 5.5%; hematuria, 6.2%; hematochezia, 2.5%; and hemoejaculate, 26.6%.13 This article investigates the psychological impact of prostate biopsy as reported by men participating in the ProBE study.13 Specifically, it explores the relationships between men’s experience of physical biopsyrelated symptoms and levels of anxiety and depression. PATIENTS AND METHODS Study Design The ProBE study investigated the impact of prostate biopsy in asymptomatic men aged 50 to 59 years invited for PSA testing and is reported in detail elsewhere.13 It was nested in the ongoing ProtecT pragmatic randomized controlled trial comparing radical prostatectomy (RP), radical conformal radiotherapy (RT), and active monitoring (AM) for localized PCa.4,14 Inclusion and exclusion criteria for the ProBE and ProtecT studies are shown in Table 1. In ProtecT, more than 100,000 asymptomatic men aged 50 to 69 years in primary care practices around nine United Kingdom cities responded to invitations for PSA testing from 1999 to 2009. More than 11,000 with an elevated PSA result (3.0 to 19.9 ng/mL) were invited for digital rectal examination (DRE), repeat PSA test, and standardized 10-core transrectal ultrasound-guided (TRUS) biopsy using periprostatic infiltration of local anesthesia and antibiotic cover.13 From February 2006 to May 2008, 1,147 (65%) of 1,753 invited ProtecT study participants, with no previous prostate biopsy, consented to participate in the ProBE study13 (Table 2). Ethical approval was obtained from Trent Multicenter Research Ethics Committee, United Kingdom. All participants gave written informed consent. 4236

© 2013 by American Society of Clinical Oncology

Data Collection ProBE study participants completed self-report questionnaires assessing anxiety and depression at four time points: (1) in clinic, at time of initial PSA testing; (2) in clinic, immediately before biopsy; (3) by post, approximately 7 days after biopsy; and (4) by post, approximately 35 days after biopsy, after receipt of biopsy result. It was intended that the 7-day questionnaire would be completed before the biopsy result was known; nonresponders were prompted at 10 days by telephone. Biopsy outcome was communicated a minimum of 14 days after biopsy. A finding of no cancer was conveyed via standard letter, which explained the residual risk of PCa; a positive cancer diagnosis was

Table 2. Characteristics of ProBE Study Participants (N ⫽ 1,147, stratified by biopsy result) Negative Biopsy (n ⫽ 471) Characteristic Age at time of biopsy, years Mean SD Employment status Full time Not working Part time Not specified/missing Ethnicity White Other Missing Initial PSA result, ng/mL Median Interquartile range

No.

%

Cancer (n ⫽ 405) No.

62.0 4.9

%

Uncertainⴱ (n ⫽ 270) No.

62.3 5.2

% 62.0 5.1

171 193 41 66

36.3 41.0 8.7 14.0

149 156 43 57

36.8 38.5 10.6 14.1

97 120 15 38

35.9 44.4 5.6 14.1

466 0 5

98.9

393 5 7

97.0 1.2 1.7

264 1 5

97.8 0.4 1.8

0.1

4.1 3.4-5.1

4.8 3.7-7.0

4.0 3.4-5.5

Abbreviations: ProBE, Prostate Biopsy Effects; PSA, prostate-specific antigen; SD, standard deviation. ⴱ High-grade prostatic intraepithelial neoplasia or atypical small acinar proliferation or epithelial atypia. One biopsy specimen from the 1,147 sampled was inadequate; therefore, the participant’s demographic data are not included in this table.

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Prostate Biopsy: Psychological Impact of Physical Biopsy Symptoms

Table 3. Summary HADS Anxiety and Depression Scores at the Time of the Initial PSA Test, Biopsy, and at 7 and 35 Days After Biopsy (stratified by biopsy result) Initial PSA Test HADS Subscale Anxiety No. of respondents Score Median IQR % cases† No. of cases Depression No. of respondents Median IQR % cases† No. of cases

Negative Biopsy 410

Cancer 364

Biopsy

Uncertainⴱ 228

Negative Biopsy 422

Cancer 367

Day 7 Postbiopsy Uncertainⴱ 229

Negative Biopsy 443

Cancer 384

Day 35 Postbiopsy

Uncertainⴱ 255

Negative Biopsy 412

Cancer 358

Uncertainⴱ 240

5 2-7 5.4 22

5 3-7 6.0 22

4 2-7 3.1 7

5 3-7 7.4 31

5 3-7 6.5 24

5 2-7 4.8 11

3 1-6 6.1 27

4 1-7 6.5 25

3 1-5 5.5 14

3 1-6 5.6 23

5 2-8 12.9 46

2 0.5-5 4.6 11

406 2 1-4 1.2 5

365 2 1-5 1.4 5

229 2 1-4 1.3 3

421 2 1-4 1.4 6

365 2 1-4 1.9 7

228 2 1-3 0.9 2

411 1 0-3 1.8 8

386 1.5 0-4 2.6 10

255 1 0-3 1.6 4

414 1 0-4 2.2 9

357 2 0-5 3.4 12

239 1 0-3 1.3 3

Abbreviations: HADS, Hospital Anxiety and Depression Score; IQR, interquartile range; PSA, prostate-specific antigen. ⴱ High-grade prostatic intraepithelial neoplasia or atypical small acinar proliferation or epithelial atypia. †A score ⬎ 11 on the relevant subscale is considered to indicate a clinically significant level or case of anxiety or depression.

delivered in consultations. Men with other biopsy results (suspicious or inadequate finding or a free/total PSA ratio of ⱕ 0.12%) were offered repeat biopsy. Anxiety and depression were measured using the Hospital Anxiety and Depression Scale (HADS),15-17 a 14-item questionnaire asking respondents to rate the degree or frequency of feelings experienced during the past week on a four-point scale (scored 0 to 3). Seven items form an anxiety subscale and seven a depression subscale, each with a possible score ranging from 0 to 21. A score of more than 11 on the relevant subscale is considered to indicate a clinically significant level or case of anxiety or depression.15 Experiences of physical biopsy-related symptoms (pain, fever, shivers, hematuria, hematochezia, and hemoejaculate) were collected in the 7- and 35-day follow-up postal questionnaires.13 Symptoms were assessed using purpose-designed questions as present or absent, and if present, how problematic each was: not a problem, minor, moderate, or major problem. The 7-day postbiopsy assessment asked responders to report on experiences over the previous week. The 35-day postbiopsy assessment required responders to recall the previous 4 weeks. Data Analysis Summary HADS scores for anxiety and depression were calculated for each time point overall and by final biopsy result. Binary variables were generated for problematic symptoms (symptom reported as a moderate/ major problem) or nonproblematic symptoms (symptom reported as not a problem/a minor problem). Linear regression models compared HADS anxiety and depression scores according to presence/absence and problematic/ nonproblematic symptoms, adjusted for recruiting center, age, and PSA level. Data were stratified by final biopsy result (prostate cancer positive, negative, or other) to avoid the potential for confounding by diagnosis. Data are primarily presented for men with an eventual benign biopsy result, with analyses of all men and other biopsy results for comparison online. Because of positive skew of HADS scores, sensitivity analyses used rank sum tests for comparison of medians. No imputations were made for missing questionnaire data. Few men reported high levels of depressive symptoms, so analyses focused on anxiety. Analysis was conducted using STATA statistical software version 12 (STATA, College Station, TX).

RESULTS

Of 1,147 men participating in ProBE, 1,144 (99.7%) completed questionnaires at biopsy. Seven-day and 35-day follow-up questionnaires www.jco.org

were received by post from 1,090 (95.0%) and 1,016 (88.6%), respectively. Sociodemographic and baseline clinical characteristics according to eventual diagnosis are included in Table 2. Depression scores were low at all time points and with all eventual diagnoses (Table 3), so the remaining analyses focused on anxiety. Overall anxiety levels were relatively low and stable across all time points (approximately 3% to 7% of men had HADS scores indicating a case), except for men who had received a cancer diagnosis, who showed elevated anxiety (12.9% cases) at the 35-day assessment when diagnosis was known (Table 3). Within 7 days of the biopsy, many men reported experiencing symptomatic adverse effects of the procedure: 38.3% pain, 10.9% fever, 11.5% shivers, 65.2% hematuria, 29.7% hematochezia, and 84.5% hemoejaculate (Table 4; figures are for those with a negative biopsy result). For the majority of men, these biopsy-related symptoms were not a problem or a minor problem. However, 11.4% of those experiencing pain, 21.7% experiencing fever, 18.4% experiencing shivers, 8.5% experiencing hematuria, 5.6% experiencing hematochezia, and 26.3% experiencing hemoejaculate indicated that they found these symptoms to be a moderate or major problem (Table 4). With the exception of fever, men who reported biopsy symptoms as a moderate/major problem at 7 days had markedly higher levels of anxiety (with a higher proportion classified as cases) compared with those reporting biopsy symptoms as not a problem/a minor problem (Table 4). At 35 days after biopsy, the proportion of men reporting biopsy-related symptoms and that these symptoms were a moderate/ major problem were similar, but for the latter, levels of anxiety were considerably reduced (Table 4). Similar relationships between the experience of problematic symptoms and increased anxiety were found for those with a cancer diagnosis and all men combined (Appendix Tables A1 and A2, online only), although the relatively small number of men with an uncertain diagnosis seemed to continue to report anxiety at 35 days, if they experienced problematic symptoms (Appendix Table A3, online only). Sensitivity analyses to account for skew in HADS scores (but © 2013 by American Society of Clinical Oncology

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Table 4. Anxiety Scores Compared by Men’s Experiences of Physical Biopsy-Related Symptoms 7 and 35 Days After Biopsy, Shown Only for Men With a Negative Biopsy Result (n ⫽ 471) Symptom Present Yes

No

Symptom Reported

No.

Total No.

%

Pain in area of biopsy Anxiety cases Anxiety score Mean SD P for differenceⴱ Fever Anxiety cases Anxiety score Mean SD P for differenceⴱ Shivers Anxiety cases Anxiety score Mean SD P for differenceⴱ Hematuria Anxiety cases Anxiety score Mean SD P for differenceⴱ Hematochezia Anxiety cases Anxiety score Mean SD P for differenceⴱ Hemoejaculate† Anxiety cases Anxiety score Mean SD P for differenceⴱ

169 13

441

38.3 7.8

Pain in area of biopsy Anxiety cases Anxiety score Mean SD P for differenceⴱ Fever Anxiety cases Anxiety score Mean SD P for differenceⴱ Shivers Anxiety cases Anxiety score Mean SD P for differenceⴱ

No.

442

442

10.9 16.7

.004 394 19

440

⬍ .001 11.5 391 11.8 21

438

.006 65.2 153 7.3 6

310

%

No.

Total No.

%

19 7

167

11.4 36.9

148 6

167

88.6 4.1

9.0 5.4 89.1 4.8

10 3

46

442

440

29.7 7.7

.062 308 17

438

88.5 5.4

9 3

49

.384 48 5

4.0 3.6

310

34.8 3.9

24 7

283

70.3 5.5

7 3

124

399

68 7

4.6 4.3

42.1 7.7

259

64 9

400

5.2 4.1 76 9

400

4.9 3.8

49

81.6 7.5

283

92.5 5.0

4.0 3.6 ⬍ .001 5.6 117 42.9 7

124

94.4 5.9

4.2 3.7 ⬍ .001 26.3 191 10.3 5

259

73.7 2.7

3.4 3.2 ⬍ .001

21 2

400

400

166

12.7 9.5

145 10

5.0 5.2 84.0 3.9

12 3

3.3 3.3 ⬍ .001 19.0 324 11.9 13

.020 8.5 259 29.2 13

5.8

3.3 3.2 .036 16.0 336 14.1 13

78.3 13.9

4.8 4.0

4.0

Within 35 days postbiopsy‡ 231 399 57.9 9 3.9

4.1 3.9

.065 18.4 40 33.3 3

10.7 6.4 15.5 10.4

46

5.6 4.1

7.9 5.4

.171 168 13

⬍ .001 21.7 36 30 5

9.3 5.8

4.0 3.6 84.5 4.6

4.3 3.4

8.7 5.9

3.7 3.3

4.4 4.1 262 12

Total No.

3.9 3.6

4.4 4.0 130 10

442

Not a Problem/Minor

No.

3.9 3.5

5.5 4.6 287 21

Moderate/Major %

3.7 3.6

6.0 4.7 51 6

Total No.

Within 7 days postbiopsy 272 441 61.7 14 5.2

4.8 3.9 48 8

Problematic Symptom

61

3.3 3.4 ⬍ .001

14 2

72

87.3 6.9

3.9 3.7 .335 19.7 49 25.0 6

5.8 4.1 81.0 4.0

166

61

80.3 12.2

5.1 4.3 .767 19.4 58 14.3 6

5.6 3.4

72

80.6 10.3

4.6 4.0 .336

(continued on following page)

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Prostate Biopsy: Psychological Impact of Physical Biopsy Symptoms

Table 4. Anxiety Scores Compared by Men’s Experiences of Physical Biopsy-Related Symptoms 7 and 35 Days After Biopsy, Shown Only for Men With a Negative Biopsy Result (n ⫽ 471) (continued) Symptom Present Yes Symptom Reported Hematuria Anxiety cases Anxiety score Mean SD P for differenceⴱ Hematochezia Anxiety cases Anxiety score Mean SD P for differenceⴱ Hemoejaculate§ Anxiety cases Anxiety score Mean SD P for differenceⴱ

Problematic Symptom No

Moderate/Major

Not a Problem/Minor

No.

Total No.

%

No.

Total No.

%

No.

Total No.

%

No.

Total No.

%

261 18

394

66.2 6.9

133 22

394

33.8 3.0

25 3

253

9.9 12.0

228 13

253

90.1 5.7

3.8 3.6 127 8

390

3.3 3.4 32.6 6.3

.039 263 14

3.9 3.4 250 10

272

390

5.2 4.9 67.4 5.3

10 2

3.6 3.6 .477 91.9 4.0

3.5 3.3

22 2

272

4.2 4.0

121

3.7 3.3 8.3 20.0

.034 111 6

5.7 4.4 8.1 9.1

77 5

244

121

91.7 5.4

3.9 3.3 .189 31.6 167 6.5 5

4.4 3.7

.186

244

68.4 3.0

3.2 3.1 .017

Abbreviations: PSA, prostate-specific antigen; SD, standard deviation. ⴱ Comparison of mean anxiety scores, controlling for any differences between the eight recruiting centers, age, and PSA level. †Excludes men who reported no ejaculation at the 7-day assessment. ‡Includes only men with evaluable data for both 7-day and 35-day assessments. §Excludes men who reported no ejaculation at the 7-day or 35-day assessment.

unable to adjust for differences in recruiting center, age, and PSA level) gave similar results (data not presented). DISCUSSION

This study investigated the psychological impact of prostate biopsy in a population invited for PSA testing. Postbiopsy symptoms such as pain/discomfort and bleeding were experienced relatively commonly, although for the majority of men, the symptoms were tolerated as a minor problem or as no problem. Overall levels of anxiety and depression were comparable to those of the general male population.18 However, with the exception of fever, men who rated the physical symptoms they experienced as a moderate or major problem 7 days after the procedure had considerably higher levels of anxiety than those who did not (Table 4). These findings suggest that men experiencing problematic postbiopsy adverse effects are more likely to experience higher levels of anxiety. The proportion of men reporting symptoms as problematic was maintained at 35 days, but levels of anxiety in these men reduced, suggesting that they were reassured by this time, even when symptoms had been or were still problematic. In the ProBE study, 10% of participants sought help or advice regarding postbiopsy symptoms from a health care practitioner,13 and 1.3% were admitted to hospital. Reduced anxiety at 35 days may have resulted from successful treatment of problematic symptoms or from reassurance that symptoms were not significant provided either by consultation with health professionals or by a negative biopsy result. After recovery from the short-term impact of biopsy symptoms, anxiety remained higher in those with a cancer diagnosis (Table 3). Pawww.jco.org

tients and doctors need to be aware of these two types of anxiety after biopsy. A major strength of this study was its integration within the large ProBE study,13 itself embedded in a population-based cohort of more than 100,000 men invited for PSA testing across the United Kingdom and receiving a standardized 10-core TRUS-biopsy protocol as part of the ProtecT trial.14 Bias was minimized by collecting 7-day questionnaire data when men were expected to be unaware of biopsy results. The relationship between problematic biopsy symptoms and anxiety at 7 days was shown among those with a benign biopsy result (Table 4) and in other diagnostic groups (Appendix Tables A1 through A3), suggesting that symptom-related anxiety occurred regardless of eventual diagnosis. Limitations arise from the possibility that the biopsy and aftercare procedures followed for men in the United Kingdom may differ from practices elsewhere and from the lack of ethnic diversity in the cohort. Prostate biopsy is essential for histologic diagnosis of PCa, and increasing rates of PSA testing are leading to more biopsies.2 Yet the US Preventive Services Task Force concluded recently that there is moderate or high certainty that harms of screening and diagnosis are equal to, or outweigh benefits, and identified the lack of evidence about the impact of biopsy on quality of life as a particular concern.8,9 Experiences of problematic symptoms and anxiety could have consequences for PCa diagnosis and treatment. In the ProBE study,13 10% of men reported immediately after biopsy that they would have a moderate/major problem having a further biopsy. This increased to nearly 20% after 7 days, and experiences of pain, infection, and bleeding during the week after biopsy were strongly associated with this © 2013 by American Society of Clinical Oncology

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response. Men with increased PSA levels refusing biopsy in the ProtecT study have previously explained that fears of adverse effects or embarrassment were the reasons.19 Up to 25% of clinically significant tumors may be missed at first biopsy.20 Men with initially negative biopsy but persistently elevated PSA levels face further biopsies to confirm the diagnosis or continued uncertainty.21 Anxiety related to symptoms of pain, infection, and bleeding may influence willingness to undergo repeat biopsy. Studies of the psychological impact of biopsy have previously shown variable findings ranging from no discernible impact22 to a majority experiencing anxiety.23 Evidence suggests that concerns about diagnosis may contribute to anxiety,23 that anxiety may persist for 12 months,24 and that anxiety may occur in men receiving a negative biopsy outcome.25 Rosario et al13 also found no difference in biopsy-related symptoms reported between men diagnosed with cancer and men without cancer, supporting the finding that heightened anxiety observed at 7 days in this study was symptom-related rather than diagnosis-related. Further research is required to investigate whether it is possible to reduce either the incidence of symptomatic adverse effects or the anxiety related to them. As anxiety (but not symptoms) was reduced at 35 days, it seems possible that better information provision in preparation for and after biopsy may reduce unnecessary anxiety and excess health care contact associated with postbiopsy symptoms. REFERENCES 1. American Cancer Society: Cancer Facts and Figures 2011. Atlanta, GA, American Cancer Society. http:// www.cancer.org/acs/groups/content/@epidemiology surveilance/documents/document/acspc-029771.pdf 2. Collin SM, Martin RM, Metcalfe C, et al: Prostate-cancer mortality in the USA and UK in 1975-2004: an ecological study. Lancet Oncol 9:445452, 2008 3. Welch HG, Fisher ES, Gottlieb DJ, et al: Detection of prostate cancer via biopsy in the Medicare–SEER population during the PSA era. J Natl Cancer Inst 99:1395-1400, 2007 4. Donovan J, Hamdy F, Neal D, et al: Prostate Testing for Cancer and Treatment (ProtecT) feasibility study. Health Technol Assess 7:1-88, 2003 5. Litwin MS, Saigal CS: Prostate cancer, in Urologic Disease in America. National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Public Health Service, United States Department of Health and Human Services. National Institutes of Health Publication No. 07-5512. Washington, DC, United States Government Publishing Office, 2007, p 76 6. Schro¨der FH, Hugosson J, Roobol MJ, et al: Screening and prostate-cancer mortality in a randomized European study. N Engl J Med 360:13201328, 2009 7. Andriole GL, Crawford ED, Grubb RL 3rd, et al: Mortality results from a randomized prostatecancer screening trial. N Engl J Med 360:13101319, 2009

This study has shown that problematic postbiopsy symptoms are linked with raised anxiety, which is distinct from anxiety related to a later diagnosis of cancer. In the context of inconclusive evidence about the benefits of prostate cancer screening, it is imperative that men and doctors fully consider these and other potential risks associated with prostate biopsy before commencing the diagnostic process with PSA testing. AUTHORS’ DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST The author(s) indicated no potential conflicts of interest.

AUTHOR CONTRIBUTIONS Conception and design: Julia Wade, Derek J. Rosario, Kerry N.L. Avery, Jane M. Blazeby, J. Athene Lane, Chris Metcalfe, David E. Neal, Freddie C. Hamdy, Jenny L. Donovan Collection and assembly of data: Julia Wade, Kerry N.L. Avery, C. Elizabeth Salter, M. Louise Goodwin Data analysis and interpretation: Julia Wade, Rhiannon C. Macefield, Chris Metcalfe, Jenny L. Donovan Manuscript writing: All authors Final approval of manuscript: All authors

8. Screening for prostate cancer: US Preventive Services Task Force statement. Ann Intern Med 157:1-44, 2012 9. Chou R, Croswell JM, Dana T, et al: Screening for prostate cancer: A review of the evidence for the U.S. Preventive Services Task Force. Ann Intern Med 155:762-771, 2011 10. Loeb S, Carter HB, Berndt SI, et al: Complications after prostate biopsy: Data from SEERMedicare. J Urol 186:1830-1834, 2011 11. Nam RK, Saskin R, Lee Y, et al: Increasing hospital admission rates for urological complications after transrectal ultrasound guided prostate biopsy. J Urol 183:963-969, 2010 12. Loeb S, van den Heuvel S, Zhu X, et al: Infectious complication and hospital admissions after prostate biopsy in a European randomized trial. Eur Urol 61:1110-1114, 2012 13. Rosario DJ, Lane JA, Metcalfe C, et al: Shortterm outcomes of prostate biopsy in men tested for cancer by PSA: A prospective evaluation within the ProtecT study. BMJ 344:d7894, 2012 14. Lane JA, Hamdy FC, Martin RM, et al: Latest results from the UK trials evaluating prostate cancer screening and treatment: The CAP and ProtecT studies. Eur J Cancer 46:3095-3101, 2010 15. Zigmond AS, Snaith RP: The Hospital Anxiety and Depression Scale. Acta Psychiat Scand 67:361370, 1983 16. Vordermaier A, Linden W, Siu C: Screening for emotional distress in cancer patients: A systematic review of assessment instruments. J Natl Cancer Inst 101:1464-1488, 2009 17. Lampic C, Thurfjell E, Bergh J, et al: Short- and long-term anxiety and depression in women recalled

after breast cancer screening. Eur J Cancer 37:463469, 2001 18. Crawford JR, Henry JD, Crombie C, et al: Normative data for the HADS from a large nonclinical sample. Br J Clin Psychol 40:429-434, 2001 19. Avery KN, Blazeby JM, Lane JA, et al: Decision-making about PSA testing and prostate biopsies: A qualitative study embedded in a primary care randomized trial. Eur Urol 53:11861193, 2008 20. Rocco B, de Cobelli O, Leon ME, et al: Sensitivity and detection rate of a 12-core trans-perineal prostate biopsy: Preliminary report. Eur Urol 49:827833, 2006 21. Pinsky PF, Crawford ED, Kramer BS, et al: Repeat prostate biopsy in the prostate, lung, colorectal and ovarian cancer screening trial. BJU International 99:775-779, 2007 22. Essink-Bot ML, de Koning HJ, Nijs HG, et al: Short-term effects of population-based screening for prostate cancer on health-related quality of life. J Natl Cancer Inst 90:925-931, 1998 23. Zisman A, Leibovici D, Kleinmann J, et al: The impact of prostate biopsy on patient well-being: A prospective study of pain, anxiety and erectile dysfunction. J Urol 165:445-454, 2001 24. Fowler FJ Jr, Barry MJ, Walker-Corkery B, et al: The impact of a suspicious prostate biopsy on patients’ psychological, socio-behavioral, and medical care outcomes. J Gen Intern Med 21:715-721, 2006 25. Macefield RC, Metcalfe C, Lane JA, et al: Impact of prostate cancer testing: An evaluation of the emotional consequences of a negative biopsy result. Br J Cancer 102:1335-1340, 2010

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Prostate Biopsy: Psychological Impact of Physical Biopsy Symptoms

GLOSSARY TERMS

Population-based: Study in which the subjects are drawn from a defined population in a manner that is representative of the source population studied. Such a design can avoid bias arising from the selective factors that guide affected individuals to a particular medical facility, allowing for greater generalizability of the findings.

Prospectively defined: refers to study design (e.g. study

PSA (prostate-specific antigen): A protein produced by cells of the prostate gland, the blood level of PSA is used as a tumor marker for men who may be suspected of having prostate cancer. Most physicians consider 0 to 4.0 ng/mL as the normal range. Levels of 4 to 10 and 10 to 20 ng/mL are considered slightly and moderately elevated, respectively. PSA levels have to be complemented with other tests to make a firm diagnosis of prostate cancer.

objectives, outcome measures, analytical methods, analysis plan) specified and documented prior to study conduct. Prospective definition of the study design and analysis plan is critical to produce Level 1 evidence for clinical utility of a biomarker as defined by Simon et al (J Natl Cancer Inst 101:1446-1452, 2009).

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Acknowledgment We thank the following for their contributions to the Prostate Biopsy Effects Study Group: Prasad Bollina, Sue Bonnington, Lynn Bradshaw, Debbie Cooper, Liz Down, Alan Doherty, Garrett Durkan, Emma Elliott, David Gillatt, Pippa Herbert, Peter Holding, Joanne Howson, Mandy Jones, Roger Kockelbergh, Howard Kynaston, Teresa Lennon, Norma Lyons, Hing Leung, Malcolm Mason, Hilary Moody, James N⬘Dow, Philip Powell, Alan Paul, Stephen Prescott, Patricia O’Sullivan, Pauline Thompson, and Sarah Tidball. We also thank the ProtecT study group of James Catto, Michael Davis, and Andrew Doble. Appendix

Table A1. Anxiety Scores Compared by Men’s Experiences of Physical Biopsy-Related Symptoms 7 and 35 Days After Biopsy, Shown Only for Men Receiving a Cancer Diagnosis at Biopsy (n ⫽ 405) Symptom Present Yes Symptom Reported Pain in area of biopsy Anxiety cases Anxiety score Mean SD P for differenceⴱ Fever Anxiety cases Anxiety score Mean SD P for differenceⴱ Shivers Anxiety cases Anxiety score Mean SD P for differenceⴱ Hematuria Anxiety cases Anxiety score Mean SD P for differenceⴱ Hematochezia Anxiety cases Anxiety score Mean SD P for differenceⴱ Hemoejaculate† Anxiety cases Anxiety score Mean SD P for differenceⴱ

No. 157 14

Total No. 384

% 40.9 8.9

No.

384

382

12.5 18.8

.003 336 16

⬍ .001 13.4 331 15.7 17

381

4.5 4.0 135 11

376

Total No.

%

No.

Total No.

%

30 6

156

19.2 20

126 8

156

80.8 6.4

6.9 5.9 87.5 4.8

21 6

.193 241 11

4.6 4.2

48

43.8 28.6

258

31 2

4.0 3.6

56.3 11.1

.264 382

86.6 5.1

14 6

381

376

50

28.0 42.9

258

36 2

10.1 6.1 39.4 5.3

13 3

226

64.1 4.6

8 0

127

5.8 23.1

.002 213 13

4.5 3.5

47 6

224

72.0 5.6

226

94.2 6.1

4.3 3.7 6.3

.017 119 9

2.8 2.5 12.0 6.5

50

5.2 3.9

7.5 5.9

4.1 3.5 88.0 5.3

48

5.6 4.3

127

93.7 7.6

4.6 3.9

.193 227 12

27 3

8.0 6.1

4.1 3.7 35.9 8.2

4.6 3.6 .032

384

4.0 3.6 ⬍ .001 60.6 150 7.4 8

Not a Problem/Minor

No.

4.0 3.5

6.6 5.0 231 17

%

3.8 3.6

6.7 5.2 51 8

Total No.

Moderate/Major

Within 7 days postbiopsy 227 384 59.1 11 4.9

5.1 4.2 48 9

Problematic Symptom No

21.0 12.7

.263 177 6

6.1 4.4

224

79.0 3.4

3.5 3.2 ⬍ .001

.390 (continued on following page)

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Table A1. Anxiety Scores Compared by Men’s Experiences of Physical Biopsy-Related Symptoms 7 and 35 Days After Biopsy, Shown Only for Men Receiving a Cancer Diagnosis at Biopsy (n ⫽ 405) (continued) Symptom Present Yes

No

Symptom Reported

No.

Total No.

%

No.

Pain in area of biopsy Anxiety cases Anxiety score Mean SD P for differenceⴱ Fever Anxiety cases Anxiety score Mean SD P for differenceⴱ Shivers Anxiety cases Anxiety score Mean SD P for differenceⴱ Hematuria Anxiety cases Anxiety score Mean SD P for differenceⴱ Hematochezia Anxiety cases Anxiety score Mean SD P for differenceⴱ Hemoejaculate§ Anxiety cases Anxiety score Mean SD P for differenceⴱ

160 27

344

46.5 16.9

184 18

Total No.

344

17.2 18.6

.030 285 34

343

.044 274 32

6.1 4.7 215 30

342

337

62.9 14.0

.045 127 15

222

No.

Total No.

%

34 8

158

21.5 23.5

124 19

158

78.5 15.3

6.7 5.1

40.7 15.3

.225 200 22

82.8 11.9

25 7

.092 14 3

5.0 4.3

59

42.4 28.0

34 4

7.3 5.3

59

57.6 11.8

5.4 4.4 .135

343

79.9 11.7

18 6

342

337

222

67

26.9 33.3

49 6

8.1 5.6 37.1 11.8

16 3

211

59.3 11.0

10 1

129

7.6 18.8

.018 195 26

54 11

5.2 4.2 .366

205

73.1 12.2

211

92.4 13.3

5.3 4.3 7.8 10.0

.557 119 18

5.0 3.9 6.3 21.4

67

5.4 4.2

6.4 5.7

4.9 4.2 93.7 12.0

5.5 4.1 .181

344

5.0 4.0

5.7 4.4 208 25

%

5.0 4.2

5.4 4.5 137 21

Total No.

5.1 4.2 20.1 17.4

Not a Problem/Minor

No.

4.8 4.2

6.2 4.8 69 12

Moderate/Major %

Within 35 days postbiopsy‡ 344 53.5 9.8

5.8 4.4 59 11

Problematic Symptom

129

92.2 15.1

5.6 4.2 26.3 20.4

.837 151 14

6.5 4.6

205

73.7 9.3

4.6 4.1 .002

Abbreviation: SD, standard deviation. ⴱ Comparison of mean anxiety scores, controlling for any differences between the eight recruiting centers. †Excludes men who reported no ejaculation at the 7-day assessment. ‡Includes only men with evaluable data for both 7-day and 35-day assessments. §Excludes men who reported no ejaculation at the 7-day or 35-day assessment.

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Table A2. Anxiety Scores Compared by Men’s Experiences of Physical Biopsy-Related Symptoms 7 and 35 Days After Biopsy Shown for All Men Symptom Present Yes Symptom Reported Pain in area of biopsy Anxiety cases Anxiety score Mean SD P for differenceⴱ Fever Anxiety cases Anxiety score Mean SD P for differenceⴱ Shivers Anxiety cases Anxiety score Mean SD P for differenceⴱ Hematuria Anxiety cases Anxiety score Mean SD P for differenceⴱ Hematochezia Anxiety cases Anxiety score Mean SD P for differenceⴱ Hemoejaculate† Anxiety cases Anxiety score Mean SD P for differenceⴱ Pain in area of biopsy Anxiety cases Anxiety score Mean SD P for differenceⴱ Fever Anxiety cases Anxiety score Mean SD P for differenceⴱ Shivers Anxiety cases Anxiety score Mean SD P for differenceⴱ

No. 422 33

Total No. 1,080

No %

No.

39.1 7.8

1,081

1,080

⬍ .001 11.7 954 15.8 45

1,076

⬍ .001 12.3 947 12.8 49

1,067

⬍ .001 63.8 389 7.0 18

739

%

No.

Total No.

%

62 15

416

14.9 24.2

354 18

416

85.1 5.1

7.1 5.6 88.3 4.7

44 11

1,080

1,076

33 8.0

.047 715 35

1,067

87.7 5.2

35 10

.042 100 8

3.9 3.6

739

130

36.2 4.6

51 13

676

67 4.9

18 4

337

977

146 18

4.5 4.0

43.7 11.0

978

632

978

71 13

3.7 3.7 ⬍ .001 17.6 806 14.5 53

130

73.1 7.4

4.8 3.9 7.5 25.5

.001 625 32

676

92.5 5.1

3.9 3.6 ⬍ .001 5.3 319 22.2 22

337

94.7 6.9

4.3 3.7 23.1 12.3

.007 486 16

632

76.9 3.3

3.4 3.3

978

⬍ .001 18.9 793 14.6 50

978

421

16.9 18.3

350 33

6.2 5.1 82.4 6.6

54 14

3.9 3.7

5.3 4.3

64.8 11.1

⬍ .001

5.3 4.4 185 27

.015 95 7

5.8 4.1

Within 35 days postbiopsy‡ 550 977 56.3 31 5.6

4.7 4.1 172 25

26.9 28.6

7.0 6.0 13.5 8.0

125

5.3 4.0

7.3 5.3

.057 427 47

⬍ .001 35.2 81 25.0 9

7.9 5.8

3.9 3.5 86.5 5.3

125

4.4 3.5

7.3 5.8

3.8 3.5

4.4 4.0 639 34

Total No.

3.9 3.6

4.2 3.9 352 28

1,081

Not a Problem/Minor

No.

3.8 3.5

5.6 4.6 687 48

Moderate/Major %

3.6 3.5

6.0 4.8 133 17

Total No.

Within 7 days postbiopsy 658 1,080 60.9 33 5.0

4.7 4.0 127 20

Problematic Symptom

168

3.9 3.7 ⬍ .001

49 13

179

83.1 9.4

4.4 3.8 ⬍ .001 32.1 114 25.9 11

6.7 4.9 81.1 6.3

421

168

67.9 9.7

4.8 4.0 27.4 26.5

.006 130 13

6.8 4.9

149

87.2 10.0

4.8 4.0 .001

(continued on following page)

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Prostate Biopsy: Psychological Impact of Physical Biopsy Symptoms

Table A2. Anxiety Scores Compared by Men’s Experiences of Physical Biopsy-Related Symptoms 7 and 35 Days After Biopsy Shown for All Men (continued) Symptom Present Yes Symptom Reported Hematuria Anxiety cases Anxiety score Mean SD P for differenceⴱ Hematochezia Anxiety cases Anxiety score Mean SD P for differenceⴱ Hemoejaculate§ Anxiety cases Anxiety score Mean SD P for differenceⴱ

Problematic Symptom No

Moderate/Major

Not a Problem/Minor

No.

Total No.

%

No.

Total No.

%

No.

Total No.

%

No.

Total No.

%

636 57

968

65.7 9.0

332 21

968

34.3 6.3

58 8

618

9.4 13.8

560 45

618

90.6 8.0

4.3 4.0 350 36

958

3.9 3.7 36.5 10.3

.054 608 40

4.7 4.0

958

5.8 4.9 63.5 6.6

23 4

3.8 3.8

334

4.1 3.8 6.9 17.4

6.0 4.4

648

92.7 7.0

47 5

4.0 3.9

648

7.3 10.6

171 20

4.4 3.8 .264

588

334

93.1 9.7

4.6 3.8

.001 601 42

.004 311 30

29.1 11.7

.067 417 22

5.3 4.1

588

70.9 5.3

3.6 3.6 ⬍ .001

Abbreviation: SD, standard deviation. ⴱ Comparison of mean anxiety scores, controlling for any differences between the eight recruiting centers. †Excludes men who reported no ejaculation at the 7-day assessment. ‡Includes only men with evaluable data for both 7-day and 35-day assessments. §Excludes men who reported no ejaculation at the 7-day or 35-day assessment.

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Wade et al

Table A3. Anxiety Scores Compared by Men’s Experiences of Physical Biopsy-Related Symptoms 7 and 35 Days After Biopsy, Shown Only for Men Receiving an Uncertain Diagnosis at Biopsy (n ⫽ 270) Symptom Present Yes

No

Symptom Reported

No.

Total No.

%

No.

Pain in area of biopsy Anxiety cases Anxiety score Mean SD P for differenceⴱ Fever Anxiety cases Anxiety score Mean SD P for differenceⴱ Shivers Anxiety cases Anxiety score Mean SD P for differenceⴱ Hematuria Anxiety cases Anxiety score Mean SD P for differenceⴱ Hematochezia Anxiety cases Anxiety score Mean SD P for differenceⴱ Hemoejaculate† Anxiety cases Anxiety score Mean SD P for differenceⴱ

96 6

254

37.8 6.3

158 8

Pain in area of biopsy Anxiety cases Anxiety score Mean SD P for differenceⴱ Fever Anxiety cases Anxiety score Mean SD P for differenceⴱ Shivers Anxiety cases Anxiety score Mean SD P for differenceⴱ

4.1 3.6 31 3

254

255

12.2 9.7

.184 223 10

255

12.2 9.7

.110 224 11

253

Within 7 days postbiopsy 254 62.2 5.1

66.3 5.9

.520 86 4

Total No.

%

No.

Total No.

%

13 2

93

14 15.4

80 4

93

86 5.0

5.1 4.6

.774 166 7

4.1 3.7

4.0 3.5 .529

254

87.8 4.5

13 2

255

255

31

41.9 15.4

171

87.8 4.9

12 1

31

38.7 8.3

21 1

3.6 3.7

33.7 4.7

14 3

167

233

233

65.6 4.2

3 1

8.4 21.4

234

171

12.3 4.8

31 5

.042 184 6

.018 194 5

4.8 4.3

91.6 3.9

3.2 3.2

86

3.5 33.3

83 6

149

86

96.5 7.2

3.9 3.5 20.8 16.1

.014 118 5

5.3 4.1

16 3

149

79.2 4.2

3.1 3.5

97

16.5 18.8

81 4

6.6 4.9

97

83.5 4.9

3.6 3.4 .004

233

79 3.3

17 4

3.1 3.3 17.1 15.0

167

.016

4.4 4.0 40 6

.449 153 6

9.7 5.5

2.9 3.2 21.0 10.2

61.3 10.5

.004 253

Within 35 days postbiopsy‡ 134 233 79 4 3.0

4.1 3.8 49 5

31

6.3 4.9

4.3 4.3

42.5 7.1

58.1 5.6

4.2 3.5

.237 99 7

.475 19 2

4.3 4.0

3.3 3.5 87.7 6.7

31

4.4 3.4

.210 150 10

18 1

5.3 4.6

3.6 3.4 34.4 8.1

Not a Problem/Minor

No.

3.5 3.5

3.6 3.6 87 7

Moderate/Major %

3.4 3.4

4.2 3.6 169 10

Total No.

3.3 3.5

4.8 4.0 31 3

Problematic Symptom

48

35.4 23.5

31 1

6.3 5.0

48

64.6 3.2

3.6 3.0 .047

234

82.9 2.6

3.1 3.2 .004

17 5

40

42.5 29.4

23 1

6.4 5.2

40

57.5 4.4

3.6 3.3 .041

(continued on following page)

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Table A3. Anxiety Scores Compared by Men’s Experiences of Physical Biopsy-Related Symptoms 7 and 35 Days After Biopsy, Shown Only for Men Receiving an Uncertain Diagnosis at Biopsy (n ⫽ 270) (continued) Symptom Present Yes Symptom Reported Hematuria Anxiety cases Anxiety score Mean SD P for differenceⴱ Hematochezia Anxiety cases Anxiety score Mean SD P for differenceⴱ Hemoejaculate§ Anxiety cases Anxiety score Mean SD P for differenceⴱ

Problematic Symptom No

Moderate/Major

Not a Problem/Minor

No.

Total No.

%

No.

Total No.

%

No.

Total No.

%

No.

Total No.

%

160 9

232

69 5.6

72 2

232

31 2.8

17 2

154

11 11.8

137 6

154

89 4.4

3.5 3.5 86 7

231

3.2 3.3 37.2 8.1

.715 145 4

4.3 3.9

6.2 3.9

3.1 3.3 .001

231

62.8 2.7

3 1

2.8 3.0

84

3.6 33.3

10.7 4.7

154

92.9 4.9

96.4 7.4

.004 11 0

3.5 3.7

84

4.0 3.7

.002 143 7

81 6

154

7.1

40 4

3.4 2.6 .999

139

28.8 10.0

99 3

5.4 3.9

139

71.2 3.0

2.7 3.4 .001

Abbreviation: SD, standard deviation. ⴱ Comparison of mean anxiety scores, controlling for any differences between the eight recruiting centers. †Excludes men who reported no ejaculation at the 7-day assessment. ‡Includes only men with evaluable data for both 7-day and 35-day assessments. §Excludes men who reported no ejaculation at the 7-day or 35-day assessment.

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Psychological impact of prostate biopsy: physical symptoms, anxiety, and depression.

To investigate the psychological impact of prostate biopsy, including relationships between physical biopsy-related symptoms and anxiety and depressio...
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