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Optimizing prostate biopsy techniques

Omer, Altana,b; Lamb, Alastair D.a,c

doi: 10.1097/MOU.0000000000000678
CALCULATING PROSTATE CANCER RISK, AVOIDANCE OF OVERTREATMENT IN LOCALIZED PROSTATE CANCER: Edited by Matthew R. Cooperberg and Declan G. Murphy
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Purpose of review Prostate cancer (PCa) diagnostics have undergone a number of changes as a result of efforts to reduce the detection rate of indolent prostate cancer and to increase the hit rate for clinically significant prostate cancer (csPCa). Here, we look at those studies that have shifted our knowledge and the impact these have had on clinical practice.

Recent findings The introduction of multiparametric MRI (mpMRI) and approaches to active surveillance have changed the landscape in prostate cancer diagnostics, reducing the number of men that need biopsy, but increasing the need for accuracy in mapping the extent of prostate cancer. As mpMRI reporting has become more accurate at predicting PCa, biopsy techniques have also evolved towards lesion (PI-RADS score 3–5) targeted biopsies. Uncertainty remains regarding the preferred approach to targeted biopsy, the need for systematic biopsies, and the place of software ultrasound/MRI fusion or in-bore MRI biopsy techniques versus ‘cognitive’ fusion techniques.

Summary Prostate biopsies remain essential for the diagnosis of PCa. But how best to do this? Latest guidelines advocate performing both targeted and systematic biopsies. Traditionally, prostate biopsies have been performed transrectally (TRUS) with hospital readmission rates of around 3% mainly because of infection. Additionally, TRUS prostate biopsies can miss anterior prostatic lesions. The transperineal approach addresses both these issues, but has historically required general anaesthetic such that adoption for front-line diagnostics is very difficult. Recent techniques to undertake transperineal biopsy under local anaesthetic have fundamentally changed this paradigm offering the genuine possibility that in 5 years’ time, all front-line diagnostic biopsies will be performed as LATP.

aDepartment of Urology, Oxford University Hospitals NHS Foundation Trust, Oxford

bUniversity Hospital Coventry & Warwickshire, Coventry

cNuffield Department of Surgical Sciences, University of Oxford, Oxford, UK

Correspondence to Alastair D. Lamb, PhD, MBChB, Nuffield Department of Surgical Sciences, University of Oxford, Old Road Campus Research Building, Roosevelt Drive, Oxford Ox3 7DQ, UK. Tel: +44 7779 593099; e-mail: alastair.lamb@nds.ox.ac.uk

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INTRODUCTION

Prostate biopsy still represents the mainstay for prostate cancer diagnosis being the last confirmatory step in the diagnosis pathway that reveals the type of prostate cancer (e.g. acinar, ductal, neuroendocrine), stage, laterality and focality [1].

The annual incidence of prostate cancer in the UK sits at 47 700 (2018) and the vast majority of these patients require a prostate biopsy in order to confirm diagnosis. Add to this number those patients with negative biopsies and those on active surveillance, and the annual burden in the UK increases to approximately 100 000 prostate biopsies performed every year in a population of 60 million [2]. Any efforts, therefore, to improve prostate biopsy techniques are to be commended, particularly in accuracy in detecting clinically significant prostate cancers and also improving the safety profile. Over the last few years, globally, attention has started to shift from ‘traditional’ transrectal ultrasound-guided (TRUS) prostate biopsy to local anaesthetic transperineal (LATP) prostate biopsy [3,4▪▪,5]. Although the evidence regarding cancer detection rates still remains to be proven, there is categorical evidence that the postbiopsy infection rates are very low and with good procedure tolerability [3,4▪▪,5–10].

In this review, we assess the state-of-the-art in approaches to prostate cancer biopsy, discuss recent advances in transperineal and local anaesthetic techniques and consider future directions in prostate biopsy including robotics and noninvasive diagnostics.

Box 1

Box 1

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METHODS

In addition to providing an overview of the history, indications and approaches used to prostate biopsy in general, we offer a detailed focus on transperineal biopsies performed under local anaesthetic. To this end, we have performed a mini systematic review, interrogating MEDLINE/PubMed between the years January 2014 and July 2019 using the MESH terms: (prostate cancer OR prostatic adenocarcinoma) AND biopsy AND transperineal AND (local anaesthesia OR LATP). The search returned 33 titles, of which eight were relevant to our subject. The outcomes analysed were patient tolerability, cancer detection rates and procedure-related complications.

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APPROACH: TRANSRECTAL VERSUS TRANSPERINEAL PROSTATE BIOPSIES

Historically, the first prostate biopsies were performed blindly under finger guidance either transrectally or transperineally. For the last two decades, finger guidance prostate biopsy has been gradually abandoned, being replaced by TRUS prostate biopsy. Interestingly, Jehle and Barnes concluded that in those patients with suspicious DRE and PSA greater than 10 ng/ml, there is no statistically significant difference between cancer detection rates, with 45.6 and 48.6% for finger guidance and TRUS, respectively (P = 0.27) [11].

Finger guidance biopsies still represent an option to diagnose PCa in some low-resource departments where TRUS is not available and are indicated in case of a palpable nodule or locally advanced disease.

Transrectal ultrasound of the prostate has a history of more than 50 years since it was first used as a tool to aid prostate visualisation [12], but it was not until the 1980s that technological advances allowed TRUS to be used routinely for prostate biopsies in clinical practice [13–15]. This was considered a major step forward in prostate cancer diagnosis and, in the following decade, it became the standard of practice. The biopsy pattern has also evolved over time from the initial sextant biopsy to the extended protocol including 10–12 cores by adding extra biopsies from the lateral peripheral zone at the level of base and mid prostate, but also parasagittal biopsies for prostates larger than 50 g [16–18].

The TRUS-guided transrectal biopsy (TRB) still represents the standard test in most units to confirm the diagnosis of prostate cancer (PCa) despite having been shown to miss csPCa and overdiagnose insignificant prostate cancer isPCa [19] and being associated with a high complication rate, particularly sepsis, requiring careful antibioprophylaxis, which in turn may lead to an increase in antibiotic resistance [20]. TRB is widely available, can be performed in a clinic under local anaesthesia, has reduced costs compared with other prostate biopsy techniques (e.g. general anaesthetic transperineal mapping biopsies and in-bore MRI-guided prostate biopsies) [21] and has a relatively short learning curve. Although reports vary, competence in TRUS biopsy can be achieved at around 10 cases [22].

The guidelines currently recommend the extended TRUS prostate biopsy strategy, which entails taking 10–12 core biopsies covering both sides, including the apical (anterior horn) and far lateral regions [1,17,23]. ‘Saturation’ TRUS biopsy, defined by taking a higher number of cores (usually 18–24 cores) is not generally thought to lead to a higher number of detected cancers [24,25].

In contrast to TRB, transperineal prostate biopsy (TPB) holds certain advantages, specifically more comprehensive sampling of all prostatic regions and reduced infection rates [3,5,7–10,26,27]. TPB has been the recommended approach in a rebiopsy setting for patients with a previous negative or low-grade PCa biopsy but high clinical suspicion of csPCa suggested by DRE, high PSA values, PSA density or high PI-RADS score on mpMRI as well as ASAP or HGPIN [1,23].

Although TPB is an efficient method to diagnose prostate cancer, it has had certain drawbacks including the need to be performed in the operating theatre, under general anaesthesia (GATP) or regional anaesthesia, and requiring the use of a brachytherapy stepper device and template grid, which increase the cost, time and complexity of the procedure.

Consequently, over the last 5 years, a fresh strategy to overcome the disadvantages associated with TRUS prostate biopsies has been proposed by several centres, to permit local anaesthesia transperineal (LATP) prostate biopsies under TRUS guidance in order to harness the advantages of TPB while minimizing the disadvantages. In order to further improve the cancer detection rate by LATP, mpMRI currently plays a quintessential role.

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INDICATION FOR PROSTATE BIOPSY

Multiparametric prostate MRI

The use of prostatic multiparametric MRI (mpMRI) in a prebiopsy setting was proposed in order to improve the diagnostic accuracy of prostate biopsies but also to avoid them. Both the PROMIS and PRECISION studies showed that, compared with TRUS biopsy alone, mpMRI has better accuracy in detecting csPCa and detects less isPCa [28▪▪,29▪▪]. Since the results of these studies were published, guidelines have endorsed the use of prebiopsy prostate mpMRI; however, there is still a diagnostic gap, the negative predictive value (NPV) of mpMRI, sitting at around 91.7% for ‘negative’ lesion (PI-RADS 1 or 2) in excluding csPCa (Gleason Grade Group 2–5) [30▪]. There is also a wide heterogeneity in the reported NPV of mpMRI with the NPV value ranging from 0.88 (0.77–0.99) for a PCa prevalence of 30% to 0.52 (0.42 – 0.59) for a PCa prevalence of 75% [31]. All-in-all, prostate biopsies are still required to confirm the presence of csPCa, including, some might argue, in the presence of a nonsuspicious mpMRI. The alternative, more pragmatic approach is to monitor patients with a negative MRI with PSA observation and only undertake a biopsy if features change on the MRI or, indeed, PSA kinetics or prostate examination.

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Negative MRI and systematic prostate biopsies

Systematic prostate biopsies are still warranted in case of a negative MRI if there is a strong clinical suspicion of prostate cancer (e.g. high PSA density or abnormal DRE), in the presence of a strong family history or genetic predisposition, or if confirmatory biopsies are needed after diagnosis of low-grade cancer (Gleason Grade Group 1) where active surveillance is being considered [23].

One approach suggested in the methods of the PROMIS and PRECISION trials was for patients with a negative MRI to avoid having systematic TRUS biopsies but the authors do recommend PSA surveillance should such a strategy be considered [28▪▪,29▪▪]. TRUS biopsy, compared with MRI can underdiagnose csPCa and overdetect isPCa [19].

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Planning focal therapy

Targeted biopsies are at the centre of focal therapies for prostate cancer [32]. As transperineal biopsies lead to a more accurate assessment and geographical description of the prostatic lesion, they are an important element of selection for and planning subsequent focal treatment. A number of techniques have been developed around the mpMRI to better guide the needle biopsy towards ‘suspicious’ areas, often defined as PI-RADS (or Likert) score 3–5 (some studies use PI-RADS >3).

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MODE OF GUIDANCE AND METHODS OF FUSION

Positive MRI and targeted biopsies

Both the NICE and the EAU guidelines recommend both targeted and systematic biopsies in case of a visible MRI lesion, particularly for repeat biopsies [1,23]. Although, increasingly, the need for systematic biopsy is being called into question [28▪▪].

There are a variety of ways to target MRI lesions, and currently there is no consensus as to which modality is the most sensitive and specific. The three main modalities used in current practice for MRI suspicious prostates are: MRI-directed ‘cognitive’ fusion TRUS prostate biopsies; software-aided TRUS–MRI fusion prostate biopsies and ‘in-bore’ MRI-guided biopsies. For each of these the radiologist needs to either report or highlight the suspicious areas according to the PI-RADS v2 or Likert scoring system [33].

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MRI-targeted fusion biopsies

MRI cognitive fusion-guided targeted biopsies (CTB) are based on targeting the region of interest (ROI) seen on an MRI, but using a standard TRUS probe providing real-time vision during the procedure. Biopsies are taken from the area bookmarked by the radiologist on a predefined prostate sector map or by referring to other anatomical landmarks (e.g. urethra, base, midline, seminal vesicles, cysts, calcifications). Reports suggest that cognitive fusion biopsies improve the diagnostic accuracy of anterior PCa and csPCa, in relation to the PI-RADS score [34]. The number of cores taken per lesion varies between studies. In a recent retrospective analysis, Zhang et al. suggested that increasing the number of biopsy cores per lesion from one to three and from three to five lead to an increase in detected csPCa by 6.4 and 2.4%, respectively [35].

CTB remain the main modality through which targeted biopsies are delivered in clinical practice. By contrast to CTB, MRI–ultrasound fusion biopsy uses software to superimpose the ROI identified on the MRI image, over the real-life TRUS-acquired images. The optimal number of target cores per ROI may vary from one to four with a detection rate of up to 88.9% for Gleason Grade Group > 2 for the first two biopsied cores, with the third and fourth core adding the extra 11% [36].

MRI-targeted TPB is more sensitive at detecting csPCa compared with MRI-targeted TRB according to a recent literature review conducted by Tu et al., with a pooled sensitivity for csPCa of 86% (95% CI 77–96) and 73% (95% CI 62–88%) for TPB and TRUS biopsies, respectively. This also demonstrated that TRB missed a higher number of anterior csPCa compared with TPB (20 versus 3 missed biopsies) [37]. As yet, there is no evidence assessing the diagnostic power of targeted LATP biopsies versus GA template TPB. MRI-guided ‘in-bore’ biopsies of the prostate permit targeting of the ROI while an MRI scan is being performed in real-time. In a comparison between cognitive-guided and MRI-guided (in-bore) biopsy, there was a high detection rate for CTB and TRUS systematic biopsies, comparable with MRI in-bore biopsies. For lesions less than 1.5 ml, however, the MRI-guided biopsies were better at sampling those smaller lesions [38].

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LOCAL ANAESTHETIC TRANSPERINEAL (LATP) PROSTATE APPROACHES

A range of devices have been used for undertaking LATP biopsies (Fig. 1). In an effort to address the aforementioned shortcomings of TPB, Smith et al.[9] conducted a feasibility study on 50 patients using the brachytherapy stepper unit and brachytherapy grid to biopsy patients under local anaesthesia using a solution of 50 ml of 1% Lidocaine and 1 : 200 000 Adrenaline. The technique was based on the previously developed LA brachytherapy program described by Wallner [39].

FIGURE 1

FIGURE 1

An alternative is direct transcutaneous passage of the biopsy gun for every prostate biopsy [40]. More recently, devices have been developed which can be placed in the perineum such that repeated transcutaneous passage of the biopsy is not required. These include the standard ‘venflon’ 114" 14 Gauge needle, CAMbridge PROstate Biopsy DevicE (CamPROBE) and the PrecisionPoint Transperineal Access System [3–10,40]. All the recently developed systems (CamPROBE, PrecisionPoint, 14 Gauge needle) use a thick needle (14 G) for transperineal access through which the spinal needle for deep tissue local anaesthesia and later the biopsy gun are inserted [3,4▪▪,5,7,9,10]. Using the brachytherapy grid for LATP biopsies, although feasible, takes longer to perform and still is not as easy to perform in clinic compared with some of the newer devices that have been introduced (Table 1).

Table 1

Table 1

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Local anaesthesia

The technique for local anaesthesia has two stages; first the skin of the perineum is anaesthetized, including whenever possible, the anal verge to minimize discomfort with the TRUS probe; second the deep tissue of the subcutaneous connective tissue, perineal bulb and periprostatic neurovascular bundle. A recent randomized controlled trial assessed pain scores for different types of local anaesthetic used for TPB with a brachytherapy stepper grid. They assigned 245 patients to three groups: group 1 for prostate capsule local anaesthesia (PLA), group 2 had PLA and periprostatic nerve block (PNB) and group 3 had PLA and pelvic plexus nerve block. The pain was measured using the visual analogue scale (VAS) for pain, from 0 to 10 (0 no pain; 10 unbearable pain). They found that, in group 1, the procedure was well tolerated with VAS scores for probe insertion, local anaesthetic administration and biopsy procedure of 3.08 (SD 1.64), 3.29 (SD 1.13) and 2.88 (SD 1.28), respectively. Periprosthetic nerve block should be guided by using Doppler ultrasound technique to better detect the neurovascular bundle [6]. The anaesthetic of choice is Lidocaine 1%, plain or in combination with adrenaline, which delivers rapid onset of anaesthesia compared to, say, the longer acting but slower onset local anaesthetic bupivicaine. The amount of LA injected ranged between 20 and 60 ml, and was generally higher for TPB using the biopsy grid compared with the transperineal needle access systems [3,4▪▪,5,7,9,10] (Table 2).

Table 2

Table 2

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Biopsy template

The template biopsy pattern differs amongst different centres. Some clinicians favour the fan-pattern biopsy described by Emiliozzi et al.[41] in one of the earliest series of patients undergoing LATP in 2001. Others have used a sector map, which facilitates cognitive fusion biopsies as it is more helpful in superimposing the mpMRI ROI reported by the radiologist to the real-life TRUS images, such as the protocol suggested by the Ginsburg consensus [42]. It has been suggested by a recent study that csPCa can be missed should target only biopsies be considered, reiterating the EAU guidelines recommendation to perform both targeted and systematic biopsies [1,3].

According to the Ginsburg biopsy protocol, extra cores are required depending on the prostate size/length. For prostates volumes below 30 cm3, this protocol recommends 24 core biopsies (six sectors and four biopsies per sector), 32 biopsies for prostate volumes 30–50 cm3 (eight extra basal biopsies, four on each side) and 38 cores for prostates larger than 50 cm3 adding one extra core to the anterior, mid and posterior regions [42]. In practice most units that have adopted the Ginsburg protocol take between 24 and 30 biopsies [3,4▪▪].

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Cancer detection

In an initial retrospective study using the Precision Point system, Meyer et al. reported a cancer detection rate of 21/43 (48.8%) and csPCa in 16.3% of cases. In eight patients they found csPCa in the anterior prostate and exclusively anterior prostate cancer in two patients (9.5%) [7], which coincided with the results of two other studies that related rates of 9.55 and 9.67% PCa in the anterior prostatic zone [8,10] (Table 1).

Freehand transperineal biopsies have completely replaced TRUS prostate biopsies at one large UK hospital. Kum et al.[3] reported their initial experience with LATP Precision Point biopsies on 176 patients undergoing primary, active surveillance or repeat biopsy. This study also allowed the use of prostatic mpMRI and included targeted biopsies for PI-RADS 3–5 lesion along with Ginsburg sectoral biopsies [42]. In the primary biopsy group, represented by 156 of 176 patients reported, the PCa detection rate was 76% with csPCa in 56%. Interestingly, in the targeted biopsy group 6/35 patients (17% would have had their cancer missed if they only had targeted biopsies. All their complications were minor, Clavien–Dindo less than 2 with a rate of 2.8% (5/176) and no admissions for sepsis.

In other studies, the diagnostic yield for both overall PCa and csPCa has increased from 21.6% for sextant biopsies to 37.6 and 42.1% for 10 and 12 cores systematic TPB [40].

On a much larger cohort of 1000 patients, Ristau et al. looked at the overall cancer detection rates and csPCa rates. They used, for the initial 883 of their patients, a fan-like systematic sampling and then switched to using the 10-sector prostate biopsy template. The overall cancer detection rate was 60.7% with csPCa present in 40.3% and anterior PCa in 9.55%.

The overall PCa rate ranges between included studies from 42 to 100% and the variation is because of the difference in the population analysed (biopsy naïve versus active surveillance or rebiopsy) and is generally higher than TRUS TR biopsy detection rates [28▪▪].

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Complications

The reported overall complication rate varies between 0.4 and 17.7% [3,5,7–10,27] (Table 2). Some complications are underreported, such as haematuria, which for some studies was reported only if it caused clot retention. One series, using the CamPROBE reported haematuria in 20/30 (66.6%) patients and hematospermia 12/30 (40%).

Although the postbiopsy urinary tract infection rate was reported in two studies at 0.31 and 6.6% [10,40], the sepsis rate was zero among all studies. This is a promising perspective for the future, as one of the main goals of LATP freehand biopsy has been to cut the sepsis rate. Interestingly some studies that have omitted prebiopsy prophylactic antibiotics had no recorded UTIs.

One author noted that acute urinary retention (AUR) rate was lower for LATP Precision Point biopsies compared with the literature reports for transperineal template biopsies but no direct comparison exists in the literature [3]. On the largest series included in our review, the AUR rate is 1.94% [10].

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Procedure tolerability

All the studies included in our review reported a good patient tolerability for the LATP prostate biopsies (Table 3), measured on the visual analogue score (VAS).

Table 3

Table 3

The six studies that used VAS to measure the pain score compared the VAS for local anaesthetic injection, probe insertion, and biopsy procedure. The most painful step was the injection of local anaesthetic, followed by the probe insertion (Table 3). One study revealed that patients having the procedure in the Outpatients Department had significantly less pain compared with those having the procedure in theatre (P < 0.004) for all three measured VAS outcomes [3].

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CONCLUSION

The cancer detection rate of LATP is comparable with reports in the literature for transperineal template mapping biopsy [28▪▪]. Furthermore, LATP has a good detection rate for anterior cancers of around 9.5%.

Although in its early days, LATP freehand prostate biopsy seems to be well tolerated by patients. Sepsis was avoided in all patients although some post-biopsy urinary tract infections (UTIs) were reported. Dipstick screening for UTI pre-biopsy and antibiotic prophylaxis should therefore be considered.

Whereas the initial series were using the brachytherapy stepper device, which made the procedure both cost and time ineffective, recent systems based on the principle of taking the biopsies through a transperineal needle (CamPROBE, PrecisionPoint, 14 Gauge needle), have proven to be very effective in performing good quality biopsies with minimal added costs compared to GATP biopsies, and in an outpatient setting. This raises the genuine possibility that all prostate biopsies could be performed by LATP in the near future. A randomised controlled trial comparing LATP versus standard TRB in detection of csPCa, infection rates and patient tolerability will soon be recruiting in the UK.

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Acknowledgements

None.

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Financial support and sponsorship

None.

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Conflicts of interest

There are no conflicts of interest.

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REFERENCES AND RECOMMENDED READING

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • ▪ of special interest
  • ▪▪ of outstanding interest
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Keywords:

biopsy; diagnosis; local anaesthetic transperineal; MRI; prostate cancer; transrectal ultrasound-guided

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