Findings from an International Survey of Urology Trainee Experience with Prostate Biopsy

Abstract

Objective:

To assess urology trainees’ exposure to transperineal prostate biopsy (TP-Bx) and intent to use transperineal prostate biopsy in practice.

Subjects and Methods:

A 34-question survey about prostate biopsy was distributed to urology trainees in the United States (US) and Europe. Primary outcomes were exposure to TP-Bx in training and intent to use TP-Bx post-training. Exposure to transrectal prostate biopsy (TR-Bx) and magnetic resonance imaging-targeted biopsy (MRI-Bx) was also assessed. Survey answers between groups were compared as categorical variables using Fisher’s exact test. Multivariable logistic regression was used to identify factors associated with intent of performing TP-Bx post-training.

Results:

Six hundred fifty-eight trainees from 19 countries completed the survey. Three hundred and thirteen (48%) trainees reported exposure to TP-Bx, 370 (56%) reported exposure to MRI-Bx, and 572 (87%) reported exposure to TR-Bx. There was significant heterogeneity in TP-Bx exposure among countries (p<0.001), with highest prevalence in Italy (72%) and lowest prevalence in Greece (4%). Intent to perform TP-Bx post-training was higher in those exposed to TP-Bx during training (89% vs. 58%, p<0.001) and did not differ between trainees in post-graduate year (PGY) 1–3 vs. PGY ≥4 (73% vs 72%, p=0.7). On multivariable regression, exposure to TP-Bx in training was independently associated with increased intent to perform TP-Bx post-training (odds ratio: 5.09, 95% confidence interval: 3.29 – 8.03, p<0.001).

Conclusions:

Less than half of 658 surveyed urology trainees reported exposure to TP-Bx, with significant heterogeneity between countries. Greater experience with TP-Bx in training was associated with greater intent to perform TP-Bx post-training. A minimum requirement of TP-Bx cases during urological training may increase resident familiarity and adoption of this guideline-endorsed prostate biopsy approach.

Introduction:

For many years, transrectal prostate biopsy (TR-Bx) with ultrasound guidance was the gold standard in prostate cancer diagnosis, with advantages owing to its short learning curve, low-cost, wide accessibility, and reasonable patient tolerability.¹ However, due to an increasing body of evidence that magnetic resonance imaging-targeted biopsy (MRI-Bx) improves detection of clinically significant prostate cancer^2–3 (Gleason Grade Group 2–5) and that a transperineal biopsy (TP-Bx) approach reduces the risk of post-procedural infections,^4–5 this standard has changed. Supported by evidence from the PROMIS and PRECISION trials, which found that MRI-Bx improved detection of clinically significant prostate cancer,^2–3 the American Urologic Association (AUA) released a statement in 2020 endorsing MRI-Bx for all men undergoing initial biopsy as well as for men with prior negative standard biopsy and rising prostate-specific antigen (PSA).⁶ Similarly, The European Association of Urology (EAU) has given a “strong” recommendation for the use of MRI in biopsy-naïve patients, in patients undergoing repeat biopsy with prior negative standard biopsy, and in patients on active surveillance undergoing confirmatory biopsy.⁷

While MRI-Bx has gained traction due to improved detection of high-grade prostate cancer, TP-Bx is increasingly supported given evidence of decreased infection risk. A meta-analysis of seven randomized controlled trials found that men who underwent TR-Bx were 1.8 times as likely to experience a post-procedural infection compared to TP-Bx,⁴ while a systematic review of 165 studies found a nine-fold greater risk of post-procedural sepsis in TR-Bx vs. TP-Bx.⁵ Furthermore, prospective randomized trials and systematic reviews have shown that infectious complications are virtually avoided with TP-Bx even in the absence of antibiotic prophylaxis.^8–9 Resultantly, the European EAU strongly recommends TP-Bx as the preferred biopsy approach,⁷ and the American Urological Association (AUA) lists this approach as an infection prevention strategy.¹⁰

Despite the recent scientific support towards TP-Bx as the preferred approach and MRI-Bx as the preferred imaging modality for prostate cancer detention, it is uncertain how residency and fellowship programs are incorporating TP-Bx and MRI-Bx in training the next generation of practicing urologists. In light of this, we used a cross-sectional survey of urologists-in-training in the United States (US) and Europe to gauge their experience and attitudes regarding prostate biopsy. We hypothesized that there is a lack of involvement of urology trainees in the currently recommended prostate biopsy technique.

Subjects and Methods:

Study Design

A cross-sectional, web-based survey was conducted from August to December 2021 in the US and from February to April 2022 in Europe to assess urology trainees’ experience and attitudes regarding prostate biopsy. Using REDCap, a secure web-based software platform designed to support data capture for research studies with an intuitive interface for validated data capture and audit trails for tracking data manipulation,^11–12 a 34-item questionnaire was designed and sent via email to urology residents and fellows in the US and Europe. Prior to administering the survey, this was tested for usability and technical functionality by independent urologists. In the US, the survey was distributed via program coordinators of the AUA and Society of Urologic Oncology-affiliated programs, and in Europe, the survey was distributed via National Communication Officers from the European Society of Residents in Urology. The Checklist for Reporting Results of Internet E-Surveys (CHERRIES) was used in developing the study design.¹³

Trainees were incentivized to complete the survey with entry into a raffle for a $100 gift card after completion of the study. Participants were implied to have consented to participate upon registration and responding to the survey. To avoid missing data, the online version requested that all questions in the survey be answered. The participant responses were accrued and accessed through REDcap. Internet Protocol addresses of respondents were not tracked. All survey responses were accessible only to the investigators.

Survey Overview

Respondents were asked to identify their year of training and AUA section (For US-based trainees). The remaining questions focused on trainee experience regarding biopsy approach (TP-Bx and TR-Bx) and imaging technologies used (MRI-Bx). Questions regarding MRI-Bx pertained to MRI/US fusion biopsy using either a TP or TR approach. A full description of the survey is included in Supplementary Figure 1. The primary outcomes were exposure to TP-Bx, defined as having performed or assisted at least one TP-Bx during residency or fellowship, and reported intent to perform TP-Bx post-training. Secondary outcomes were reported exposure to TR-Bx and MRI-Bx, reported comfort in performing TR-Bx and TP-Bx independently (without attending supervision), and reported intent to perform TR-Bx and MRI-Bx post-training.

Statistical Analysis

Respondents’ data were compared by level of training and by country. Trainees in their first three years of training (post-graduate year (PGY) 1 to 3) were classified as junior trainees, while those with more than three years of training (PGY ≥4) were classified as senior trainees. Survey answers between groups were compared as categorical variables using Fisher’s exact test. Only countries with a response rate ≥10% of the total number of residents within each country were included in comparisons between countries. The total number of trainees in European countries was calculated from listservs of active trainees provided by the National Communication Officers of each participating country. Total number of trainees in the United States was determined from information published on the websites of all AUA-affiliated urology programs. For other comparisons, sensitivity analysis was done both including and excluding respondents from countries with response rates <10%, with no notable differences in the findings. Therefore, respondents from countries with <10% response rate were included in the remainder of the analysis. A multivariable logistic regression model was used to identify factors associated with intent of performing TP-Bx after training including only trainees from countries with a response rate ≥10%. All analysis was conducted using R Statistical Software (version 4.1.1, RStudio, Boston, MA).

Results:

Response Rates

A total of 658 trainees from 19 countries completed the survey. Table 1 illustrates the breakdown of respondents by year and country of training. Response rates were ≥10% in eight countries (Belgium: 17 of 150 [11%], Georgia: 20 of 27 [74%], Greece: 53 of 119 [45%], Italy: 200 of 804 [25%], Portugal: 13 of 96 [14%], Switzerland: 20 of 80 [25%], Turkey: 25 of 249 [10%], and the US (231 of 1,908 [12%]), accounting for 579 total respondents. Countries with at least one response but <10% response rate included Austria, Croatia, Cyprus, France, Germany, the Netherlands, Poland, Romania, Slovakia, Spain, and the United Kingdom.

Table 1:

Description of Cohort by Training Level and Country of Training

Characteristic	Respondents, n (%)
Training Level
PGY-1	69 (11%)
PGY-2	128 (20%)
PGY-3	112 (17%)
PGY-4	118 (18%)
PGY-5/6	160 (24%)
Fellow	68 (10%)
Country of Training
Belgium	17 (3%)
Georgia	20 (3%)
Greece	53 (8%)
Italy	200 (31%)
Portugal	13 (2%)
Romania	11 (2%)
Spain	23 (4%)
Switzerland	20 (3%)
Turkey	25 (4%)
United States	231 (35%)
Other	42 (6%)
AUA Section
Mid-Atlantic	18 (8%)
New England	19 (8%)
New York	38 (16%)
North Central	34 (15%)
Northeastern	19 (8%)
South Central	33 (14%)
Southeastern	40 (17%)
Western	30 (13%)

AUA: American Urological Association. PGY: post-graduate year.

Availability and Exposure

Of the 658 trainees surveyed, 393 (60%) responded that TP-Bx was available at their institution, and 468 (71%) responded that MRI-Bx was available (Figure 1A). A total of 313 (48%) respondents reported exposure to TP-Bx, 370 (56%) reported exposure to MRI-Bx, and 572 (87%) reported exposure to TR-Bx (Figure 1D). Of the 313 trainees who reported exposure to TP-Bx, 124 (39%) reported exclusively using a template/grid-based approach, 119 (38%) reported exclusively using a free-hand approach, and 51 (16%) reported using both template/grid and free-hand approaches. The majority of trainees (187 of 313, 60%) reported using sedation for at least part of their experience with TP-Bx, while 126 (40%) trainees had experience only using local anesthesia.

Figure 1. Survey results by year of training and country of training.

Results of 658 surveyed urology trainees in Europe and the United States regarding biopsy availability at training program (panels A – C), exposure to biopsy in training (panels D – F), comfort using biopsy modality independently (panels G – I), and intent to use modality after training (panels J – L). Respondents were compared by post-graduate year (PGY) and country of training using Fisher’s exact test, with an asterisk indicating p-value <0.05. Only countries with a response rate ≥10% (n = 579) were included in comparisons by country

Compared to junior trainees, senior trainees reported greater exposure to TR-Bx (93% vs. 80%, p<0.001), MRI-Bx (61% vs. 51%, p=0.01), and TP-Bx (51% vs. 43%, p=0.04) (Figure 1E). When stratified by country of training, there was significant heterogeneity in exposure to TR-Bx (p<0.001), MRI-Bx (p<0.001), and TP-Bx (p<0.001) (Figure 1F). Exposure to TP-Bx was highest in Italian trainees (72%) and lowest in Greek trainees (4%). In the US, 90% of trainees were exposed to TR-Bx, and 43% of trainees were exposed to TP-Bx. Among US-based trainees, significant heterogeneity in exposure was not found for TR-Bx (p=0.8), MRI-Bx (p=0.3), or TP-Bx (p=0.5) when stratified by AUA sections.

Perform Biopsy Independently

Comfort performing TR-Bx independently was reported by 445 (68%) trainees, and comfort performing TP-Bx independently was reported by 190 (29%) trainees. Compared to junior residents, senior residents and fellows were more likely to report comfort performing independent TR-Bx (82% vs. 51%, p<0.001) and TP-Bx (38% vs. 19%, p<0.001) (Figure 1H). There was a significant association between the number of procedures performed and independence for both TR-Bx and TP-Bx (Figure 2). Comfort with independent TR-Bx was reported by 24% of trainees who performed 1 to 9 procedures, 74% of trainees who performed 10 to 24 procedures, 89% of trainees who performed 25 to 49 procedures, and 98% of trainees who performed ≥50 procedures (p<0.001). Comfort with independent TP-Bx was reported by 25% of trainees who performed 1 to 9 procedures, 63% of trainees who performed 10 to 24 procedures, 79% of trainees who performed 25 to 49 procedures, and 100% of trainees who performed ≥50 procedures (p<0.001).

Figure 2. Independence with Biopsy and Post-Training Goals Stratified by Number of Biopsies Performed.

Results of surveyed urology trainees in Europe and the United States regarding comfort performing transrectal transperineal biopsy independently (panel A) and intent to perform transrectal, MRI-targeted, and transperineal prostate biopsy after training (panel B) stratified by the number of biopsies performed. Fisher’s exact test was used to compare respondents by the number of biopsies performed (in panel B both excluding and including respondents with zero biopsies) with an asterisk indicating p-value <0.05.

Significant heterogeneity was found for comfort with independent use of TR-Bx (p<0.001) and TP-Bx (p<0.001) when stratified by country (Figure 1I). Among US-based trainees, significant heterogeneity was not found for comfort with TR-Bx (p=0.2) or TP-Bx (p=0.15) when stratifying by AUA sections.

Post-training Plans

The majority of trainees reported intent to use TR-Bx (523 of 658, 79%), MRI-Bx (545 of 658, 83%), and TP-Bx (477 of 658, 72%) post-training. No differences were found between junior and senior trainees regarding intent to use TR-Bx (82% vs. 78%, p=0.2) or TP-Bx (73% vs. 72%, p=0.6) after training (Figure 1K). However, junior trainees were more likely to report intent to use MRI-Bx compared to senior trainees (87% vs. 79%, p=0.004). Significant heterogeneity was found among countries for intent to perform TR-Bx (p<0.001), MRI-Bx (p<0.001), and TP-Bx (p<0.001) after training (Figure 1L). Reported intent to perform TP-Bx post-training was highest among trainees in Portugal (92%), Switzerland (90%), Italy (90%), and Belgium (88%) and lowest among trainees in Greece (60%), the US (60%), Georgia (55%), and Turkey (40%). Among US-based trainees, significant heterogeneity was not found among AUA sections regarding intent to perform TR-Bx (p=0.9), MRI-Bx (p=0.7), or TP-Bx (p=0.18) post-training.

Exposure to each biopsy modality was associated with greater intent to use that modality post-training (TR-Bx: 85% vs. 43%, p<0.001; MRI-Bx: 89% vs. 75%, p<0.001; TP-Bx: 89% vs. 58%, p<0.001). Among trainees who performed at least one TR-Bx biopsy, there was an association between intent to perform TR-Bx biopsy and number of biopsies performed (1 to 9: 76%, 10 to 24: 78%, 25 to 49: 90%, ≥50: 91%, p<0.001), but this association was not seen in respondents exposed to MRI-Bx (p=0.4) or TP-Bx (p=0.4) (Figure 2B). Of the 261 trainees who had experience with both TR-Bx and TP-Bx, 176 (67%) reported intent to use both approaches post-training, 55 (21%) reported intent to use TP-Bx exclusively, and 20 (8%) reported intent to use TR-Bx exclusively.

On multivariable logistic regression, exposure to at least one TP-Bx during training was associated with an increased likelihood of intent to use TP-Bx post-training (OR: 5.09, 95% CI: 3.29 – 8.03, p<0.001) (Table 2). Compared to training in the US, training in Belgium (OR: 5.20, 95% CI: 1.35 – 34.4, p=0.04), Italy (OR: 4.11, 95% CI: 2.41 – 7.26, p<0.001), Portugal (OR: 12.4, 95% CI: 2.31 – 231, p=0.02), and Switzerland (OR: 6.83, 95% CI: 1.81 – 44.7, p=0.01) were associated with increased likelihood of intent to perform TP-Bx post-training. Year of training (PGY1–3 vs. PGY≥4) (p=0.4) and exposure to TR-Bx (p=0.3) were not associated with increased intent to use TP-Bx post-training.

Table 2:

Multivariable logistic regression for intent to use transperineal prostate biopsy after training

Characteristic	Odds Ratio	95% Confidence Interval	p-value
Transperineal Biopsy Experience
Yes	5.09	3.29 – 8.03	<0.001
No	Ref	-
Transrectal Biopsy Experience
Yes	0.70	0.35 – 1.36	0.3
No	Ref	-
Trainee Level
Senior (PGY ≥4)	0.83	0.55 – 1.24	0.4
Junior (PGY <4)	Ref	-
Country
Belgium	5.2	1.35 – 34.4	0.04
Georgia	0.96	0.36 – 2.63	>0.9
Greece	1.83	0.97 – 3.50	0.064
Italy	4.11	2.41 – 7.26	<0.001
Portugal	12.4	2.31 – 231	0.02
Switzerland	6.83	1.81 – 44.7	0.01
Turkey	0.63	0.25 – 1.52	0.3
Other	2.75	1.48 – 5.30	0.002
United States	Ref	-

PGY: Post-graduate year

Discussion:

In this survey of 658 urology residents and fellows from Europe and the US, we found that less than half of all trainees reported experience with TP-Bx, and less than half of senior residents and fellows reported comfort using TP-Bx independently. There was significant heterogeneity in exposure to TP-Bx based on country of training, and exposure to TP-Bx was independently associated with an increased likelihood of expressing intent to use TP-Bx after training. These results provide an overview of the current state of prostate biopsy in urology training programs of the countries surveyed and suggest that increasing trainee exposure to TP-Bx is likely to increase trainee adoption of the approach when in practice.

A prior survey of practicing urologists found that concerns related to access to additional equipment and cost of supplies as well as peri-procedural pain management were the two largest barriers to TP-Bx adoption.¹⁴ Nonetheless, multiple studies have shown that with a well-distributed regional (pudendal, perineal, and periprostatic) block using local anesthesia the procedure is tolerable with rare need for sedation.^15–16 Furthermore, although the initial cost of TP-Bx equipment purchase may lead to added expenses, over time the costs per procedure between TP-Bx and TR-Bx are similar with potential long-term cost reduction from TP-Bx due to lower downstream costs from hospital readmission.^17–18

Another potential barrier to TP-Bx adoption is that although metanalyses have shown reduced infection with TP-Bx, there are no large randomized controlled trials that have demonstrated an increased benefit in post-procedural infection prevention with TP-Bx over TR-Bx in the setting of current prophylactic strategies.⁴ Currently three ongoing prospective randomized trials are comparing TP-Bx vs. TR-Bx: the TRANSLATE trial (based in the UK), PCORI trial (Weill Cornell Medicine), and PROBE-PC (Albany Medical College), the latter of which has an estimated completion date by December, 2022.¹⁹ If these trials confirm a reduced risk of infection from TP-Bx, as well as similar cancer detection rates and patient tolerability, wider adoption of the TP approach by urology training programs may occur.

The proportion of trainees reporting intent to use TP-Bx after training was among the lowest in the US, despite exposure to TP-Bx in the US being similar to or higher than the majority of other countries included. While the AUA lists TP-Bx as a method for reducing prostate biopsy-associated infection in their white paper published in 2017,¹⁰ the organization does not recommend TP-Bx over TR-Bx in current guidelines. The EAU guidelines, on the other hand, state that TP-Bx is preferred over TR-Bx due to strong evidence.⁷ It is unclear why US-based trainees were less likely to report an intention to use TP-Bx in practice, but it is possible that discrepancies in guideline recommendations play a role.

After adopting a new biopsy approach, it does not appear to take long for trainees to gain proficiency. In our study, the majority of trainees who performed at least 10 TP-Bxs reported comfort with performing the procedure independent of attending supervision. A prior survey of urology attendings also reported approximately 10 procedures needed for self-reported proficiency.¹⁴ In a study of resident learning curve with MRI-Bx, overall rates of cancer detection and complications were similar regardless of the trainee’s experience, but for diagnosing cancer in lesions <8 mm, trainees who performed at least 100 biopsies had a higher detection rate.²⁰ The US Accreditation Council of Graduate Medical Education (ACGME) currently requires residents to perform or assist at least 25 prostate biopsies prior to graduation, with no distinction of biopsy approach.²¹ It may be prudent for the ACGME to include distinct minimum case requirements for both TR-Bx and TP-Bx, thus ensuring graduating residents are proficient with both approaches.

We found that exposure to TP-Bx during training was associated with increased intent to use the approach biopsy after training. However, among trainees with exposure to TP-Bx, those with more experience did not report greater intent to perform TP-Bx post-training. This suggests that providing trainees with even a limited degree of exposure to TP-Bx will likely result in increased utilization of the approach post-training. Programs that do not have the resources for TP-Bx may consider allowing trainees to complete short visiting rotations at other institutions with the intention to gain exposure to TP-Bx and thus be more likely to use it in practice.

There are several limitations to this study that must be acknowledged. Survey studies may be prone to self-selection bias, as trainees who opted to complete the survey may have stronger opinions regarding prostate biopsy compared to an average trainee. Moreover, interpretation of the results must be done with caution, as the responses by country were not evenly distributed, with the majority of responses coming from Italy and the US and several EAU countries declining to participate in the study. To protect participant anonymity, we did not ask trainees to identify their training centers, and thus with the exception of the United States, we did not gather information on trainee distribution within their countries, which limits the conclusions that can be made about countrywide trainee experience. We also did not assess trainee experience with cognitive targeting of MRI lesions nor their confidence with TP and TR approaches using local anesthesia, which may influence their preference for a given approach as well as their preparedness for using that approach post-training. Finally, survey research is inherently subject to response bias, and trainees may have inaccurately reported their experience and competency with each biopsy approach. Nevertheless, the present study is to our knowledge the first to provide the current state of trainee-level experience and attitudes towards the prostate biopsy approach recommended by European guidelines.

Conclusion

In this survey of urology trainees in the US and Europe, less than half of trainees reported exposure to TP-Bx, and only 29% of trainees reported comfort with performing TP-Bx independently, with significant heterogeneity among countries. Exposure to TP-Bx was associated with intent to perform TP-Bx after training. The inclusion of a minimum number of TP-Bx cases as part of the case requirements during urological training may increase resident familiarity and adoption of this guideline-endorsed prostate biopsy approach.