Abstract
Background
The aim of this study was to assess the diagnostic accuracy and spatial localization capability of transperineal template-guided mapping biopsy (TTMB) in the detection of prostate cancer in patients with negative magnetic resonance imaging (MRI).
Materials and methods
A retrospective study was conducted to analyze the clinical data and follow-up outcomes of patients with negative MRI who underwent transperineal prostate biopsy at Northern Jiangsu People's Hospital, between January 2017 and August 2020. The patients were categorized into TTMB group and the systematic biopsy (SB) group according to the biopsy method. The biopsy positivity rate, detection rate of clinically significant prostate cancer (csPCa), pathological grade upgrading and downgrading following radical surgery, repeat biopsy rate, and positive rate of repeat biopsy were compared between the two patient groups. The diagnostic accuracy of TTMB in detecting and localizing prostate lesions was assessed using whole-mount radical prostatectomy specimens.
Results
A total of 398 patients were enrolled in the study, of whom 185 were in the TTMB group and 213 in the SB group. The TTMB group had significantly higher biopsy cores (53.5 vs. 18.1), biopsy-positive rate [28.1% (52/185) vs. 15.5% (33/213)], and csPCa rate [15.7% (29/185) vs. 8.9% (19/213)] than the SB group. In radical prostatectomy, compared with SB, the pathological downgrade of TTMB was higher (36.4% vs. 19.2%), and the pathological upgrade was lower (6.8% vs. 30.8%). The incidence of hematuria (37.8%), perineal hematoma (34%), and urinary retention (11.9%) in TTMB is significantly higher than in SB (P < 0.05). The repeat biopsy rate (13.2%) and the csPCa detection rate (2.5%) in the TTMB group were both significantly lower than in the SB group (28.1% and 9.9). Whole-mount histopathological revealed 118 lesions, and 91.5% (108/118) lesions were detected by TTMB.
Conclusions
TTMB enhances biopsy accuracy and facilitates more precise detection and evaluation of tumor lesions patients with negative MRI.
Keywords: Accuracy, Negative MRI, Prostate, Transperineal template-guided mapping biopsy, Whole-mount histopathological
1. Introduction
The incidence of prostate cancer (PCa) has been steadily increasing, and prostate biopsy remains a critical diagnostic tool for detecting the disease.1 However, due to its nature as a sampling examination, biopsy carries an inherent risk of missed diagnosis. Therefore, strategies to reduce missed diagnosis and enhance detection rates—particularly in patients with prior negative biopsy results but ongoing clinical suspicion—are of significant clinical importance.
The integration of multiparametric magnetic resonance imaging (mpMRI) and MRI-based targeted biopsy techniques has significantly enhanced the diagnostic yield of PCa, particularly in both initial and repeat biopsy scenarios.2 Nevertheless, approximately 10% to 15% of clinically significant prostate cancer (csPCa) cases remain undetectable by magnetic resonance imaging (MRI) in routine clinical practice 3, 4, 5; therefore, prostate biopsy remains indispensable for patients with negative imaging findings.6 These MRI-invisible lesions are typically characterized by smaller tumor volumes, lower Gleason score (GS), earlier clinical stages, and reduced tumor glandular density.7 Detecting such lesions remains challenging, and conventional systematic biopsy (SB)—commonly used in clinical settings—frequently results in missed diagnoses. As a matter of fact, improving biopsy accuracy and minimizing diagnostic errors is of critical importance, particularly for patients with prior negative biopsy results. Furthermore, precise evaluation of tumor characteristics, including GS, anatomical location, and lesion size, plays a pivotal role in guiding therapeutic decisions, especially for strategies such as active surveillance (AS) and focal therapy.
Transperineal prostate saturation biopsy has demonstrated improved diagnostic accuracy while reducing the risk of infectious complications. Consequently, this approach is increasingly adopted in clinical practice.8 Additionally, the use of template-guided mapping allows for precise localization of tumor lesions and more accurate assessment of tumor volume, thereby enhancing overall tumor characterization. Accordingly, transperineal template-guided mapping biopsy (TTMB) has been implemented to enhance csPCa detection rates5 while enabling accurate lesion localization and evaluation.9,10 Our institution has enrolled patients with negative MRI to assess the diagnostic accuracy of this biopsy approach.
2. Methods
2.1. Study design and patient cohort
Clinical data and follow-up outcomes of patients who underwent transperineal prostate biopsy at the Department of Urology, Northern Jiangsu People's Hospital, between January 2017 and August 2020 were retrospectively analyzed. The study was conducted in accordance with the ethical principles of the 2013 revised Declaration of Helsinki.
Inclusion criteria were as follows: patients with a clinical indication for prostate biopsy who underwent transperineal prostate biopsy, patients who had undergone mpMRI of the prostate prior to biopsy, with a Prostate Imaging Reporting and Data System (PI-RADS) v 2 score of 1 or 2.
Exclusion criteria were as follows: prior diagnosis of PCa, absence of prebiopsy mpMRI, history of prostate surgery for benign prostatic hyperplasia, presence of contraindications to prostate biopsy, and incomplete clinical or imaging records.
Patients meeting any of the aforementioned exclusion criteria were excluded from the study.
The patients were categorized into TTMB group and the SB group according to the biopsy protocol.
All collected clinical data were analyzed including biopsy pathology, radical prostatectomy (RP) pathology, and follow-up outcomes [prostate-specific antigen (PSA) and subsequent treatments]. The baseline dates, biopsy-positive rates, csPCa rates, and pathological upgrading or downgrading according to International Society of Urological Pathology (ISUP) grade after RP were compared between the two groups. Patients with initially negative biopsy results were followed up to assess the rate of repeat biopsies and the positive.
For patients in the TTMB group who underwent RP, the number and spatial localization of lesions identified in the biopsy specimens were compared to RP specimens to assess the accuracy of TTMB in lesion characterization and anatomical localization.
2.2. Prostate biopsy
2.2.1. Template-guided mapping biopsy
Preoperative preparation: Following administration of spinal or general anesthesia, the patient is positioned in the lithotomy position, and a rectal ultrasound probe is inserted. After standard disinfection and sterile draping, the biopsy template (Fig. 1A) is securely mounted on the probe’s support mechanism.
Figure 1.
Operational procedure of the TTMB. (A) The template is positioned on the ultrasound stent. (B) The prostate is divided into two layers, each measuring 2–2.5 cm in thickness. (C) Identification and documentation of biopsy core locations: the biopsy template (white grid) is projected onto the ultrasound image, and all white dots falling within the prostatic boundary—defined by the region enclosed by the red line—are designated as biopsy sampling points. (D) The biopsy needle is introduced through the guide hole in the template to obtain prostate tissue samples. (E) Tissue samples are placed into the corresponding positions of the specimen bottle. Following biopsy completion, formalin is added for fixation, and the sampling locations are labeled on the bottle cap for pathological analysis. (F) Sampling position points are marked on the template diagram during the biopsy procedure. TTMB, transperineal template-guided mapping biopsy.
Determination of biopsy cores: The ultrasound probe is scanned from the base to the apex of the prostate, with the distance increments on the probe support serving as a measurement scale to calculate the anterior-posterior diameter of the gland (from apex to base). Typically, the prostate is divided into two layers (as shown in Fig. 1B), each measuring 2–2.5 cm in thickness. If the anterior-posterior diameter exceeds 6 cm, a three-layer division is applied. The number of biopsy cores per layer is primarily determined by the prostate size, as illustrated in the representative example (e.g., Fig. 1C). The biopsy template (white grid) is projected onto the ultrasound image, and all white dots falling within the prostatic boundary—defined by the region enclosed by the red line—are designated as biopsy sampling points.
Biopsy and specimen processing: Tissue sampling proceeds sequentially from the apex to the base. On each apical layer, needle biopsies are performed at positions corresponding to the template-guided grid (Fig. 1D). Retrieved tissue specimens are extracted from the biopsy needle using sterile paper strips. An assistant marks the distal end of each tissue core and then places the specimen into a labeled specimen container corresponding to its sampling location. Formalin is added for fixation, and the container cap is labeled with the specific biopsy site (Fig. 1E). Each sampled point is simultaneously annotated on the schematic diagram (Fig. 1F). This process continues sequentially for all predetermined biopsy sites. All collected specimens are submitted individually for pathological examination and reporting.
2.2.2. Systematic biopsy
Prebiopsy preparation procedures were consistent with those used in the TTMB group. According to the Zone 11 zonal mapping method, biopsy cores were planned as illustrated in Fig. 2, with one to two cores obtained from each zone.11
Figure 2.
Prostate systematic biopsy zones.
2.3. Pathological evaluation and findings
All histopathological evaluations were conducted by experienced urological pathologists, with individual reporting of each biopsy tissue core. In TTMB, the locations of positive cores were marked on the sampling schematic to determine the position and number of lesions (contiguous positive cores were considered a single lesion). A GS >6 was defined as csPCa in biopsy specimens. For patients with multiple positive cores, the one with highest GS was used for statistical analysis.
Patients with positive biopsy results underwent RP. The RP specimens were processed into whole-mount sections, digitized through scanning, and independently reviewed by the same pathologist, who outlined and measured the tumor lesions (illustrated in Fig. 3). According to the PI-RADS v2.1 criteria12 and Epstein criteria,13,14 the definition of csPCa in RP specimens is as follows: a GS ≥7, tumor volume ≥0.5 cm3, or the presence of capsular invasion or seminal vesicle.
Figure 3.
Schematic representation of pathological analysis using whole-mount techniques. (A) A whole-mount section of the prostate containing two distinct lesions. The precise locations of these lesions are illustrated in panels B and C.
2.4. Complications
The main complications associated with transperineal prostate biopsy include infection, hematuria, perineal hematoma, and urinary retention.
Hematuria was defined as the presence of blood in the first void after the procedure.
Perineal hematoma was classified as mild when confined to the puncture site, moderate when extending beyond the puncture area without involving the scrotum, and severe when spreading to the scrotum.
Infection was diagnosed if fever exceeding 38°C occurred within three days post biopsy, with or without chills.
Urinary retention was defined as acute inability to void following the biopsy, requiring catheterization.
2.5. Statistical analysis
All data were prospectively collected and retrospectively analyzed, and SPSS 22.0 software (Chicago, IL, USA) was used for statistical analysis. If normally distributed, data were described using mean ± standard deviation values and compared by the independent-sample t-test. What is more, the Chi-square test was used to compare the rates and a two-tailed P value <0.05 was taken to indicate statistical significance.
3. Results
3.1. General characteristics
A total of 398 patients were enrolled in the study, including 185 in the TTMB group and 213 in the SB group. To be specific, no statistically significant differences were observed between the TTMB and SB groups with respect to mean age (66.7 ± 8.8 vs. 66.7 ± 9.0 years), mean PSA (10.74 ± 6.84 vs. 11.67 ± 7.51 ng/ml), or average prostate volume (68.1 ± 33.0 vs. 69.5 ± 32.3 ml) (all P > 0.05) (in Table 1).
Table 1.
Baseline characteristics and biopsy findings of the two patient groups
| N | TTMB |
SB |
P | |
|---|---|---|---|---|
| 185 | 213 | |||
| Age (y) | 66.7 ± 8.8 | 66.7 ± 9.0 | 0.993 | |
| PSA (ng/ml) | 10.74 ± 6.84 | 11.67 ± 7.51 | 0.204 | |
| Prostate volume (ml) | 68.1 ± 33.0 | 69.5 ± 32.3 | 0.675 | |
| Biopsy needles | 53.5 ± 11.5 | 18.1 ± 3.2 | <0.001 | |
| Biopsy pathology (n %) | Positive rates | 52 (28.1%) | 33 (15.5%) | 0.02 |
| csPCa rates | 29 (15.7%) | 19 (8.9%) | 0.039 | |
| csPCa proportion | 29 (55.8%) | 19 (57.6) | 0.87 | |
| Biopsy GS(n) | 3 + 3 = 6 | 23 | 14 | – |
| 3 + 4 = 7 | 7 | 10 | – | |
| 4 + 3 = 7 | 7 | 4 | – | |
| 8 | 10 | 3 | – | |
| 9-10 | 5 | 2 | – | |
csPCa, clinically significant prostate cancer; GS, Gleason score; PSA, prostate-specific antigen; SB, systematic biopsy; TTMB, transperineal template-guided mapping biopsy.
csPCa proportion: the proportion of csPCa in positive patients.
3.2. Pathological of biopsy and RP
The biopsy needles were 53.5 ± 11.5 in the TTMB and 18.1 ± 3.2 in the SB methods (in Table 1). The biopsy-positive rates were 28.1% (52/185) in the TTMB group and 15.5% (33/213) in the SB group; the csPCa rates were 15.7% (29/185) and 8.9% (19/213), respectively. As a matter of fact, all observed differences between the two groups were statistically significant (P < 0.05) (in Table 2).
Table 2.
Comparative analysis of pathological outcomes following RP.
GS, Gleason score; ncsPCa, non–clinically significant prostate cancer; RP, radical prostatectomy; SB; systematic biopsy; TTMB, transperineal template-guided mapping biopsy.
Red annotation: GS upgrade.
Blue annotation: GS downgrade.
Among the patients who tested positive on biopsy, 44 in the TTMB group and 26 in the SB group underwent RP. Compared with the biopsy GS, the TTMB group showed 36.4% (16/44) downgrading and 6.8% (3/44) upgrading, whereas the SB group demonstrated 19.2% (5/26) downgrading and 30.8% (8/26) upgrading. The difference between the two groups was statistically significant (P < 0.05), and no significant difference was observed in the positive surgical margins between the TTMB group and the SB group (13.6% vs. 15.4%, P > 0.05). Among patients with non–clinically significant prostate cancer (ncsPCa) who underwent RP, 10% (2/20) in the TTMB group experienced pathological upgrading, which was significantly lower than 50% (5/10) in the SB group (P < 0.05). According to the definition of csPCa in RP specimens, two patients with pathological upgrading in the TTMB group were classified as having ncsPCa, whereas three patients in the SB group met the criteria for csPCa.
3.3. Comparison of TTMB with whole-mount sections
Among the 185 patients who underwent TTMB, a total of 9,881 biopsy cores were obtained. The total number of positive biopsy cores was 202, accounting for 2.0% of all samples. Pathological examination revealed that 52 cases (28.1%) were diagnosed with prostatic acinar adenocarcinoma. The GSs were distributed as follows: 21 cases with GS 3 + 3 = 6, 5 cases with GS 3 + 4 = 7, 6 cases with GS 4 + 3 = 7, 9 cases with GS 8, and 3 cases with a GS 9–10. A total of 124 lesions were identified, with an average of 2.4 lesions per patient.
All 44 specimens from patients who underwent RP were analyzed using whole-mount section pathological examination. A total of 118 lesions were detected, with an average of 2.68 lesions per patient. In total, 108 lesions were detected by TTMB, yielding an approximate detection sensitivity of 91.5%. The 10 undetected lesions were all GS 3 + 3 = 6 lesions with a diameter less than 5 mm.
3.4. Complications
The incidence rates of these complications are presented in Table 3. The TTMB group exhibited significantly higher rates of hematuria (37.8%), perineal hematoma (34.0%), and urinary retention (11.9%) than the SB group (26.7%, 24.9%, and 5.6%, respectively) (P < 0.05). In addition, it was shown that no significant differences were observed between the two groups regarding the severity distribution of perineal hematoma or the incidence of infection (P > 0.05).
Table 3.
Comparison of complications results of the two groups after biopsy
| N | TTMB |
SB |
P |
|---|---|---|---|
| 185 | 213 | ||
| Hematuria [n (%)] | 70 (37.8%) | 57 (26.7%) | 0.018 |
| Perineal hematoma [n (%)] | 63 (34%) | 53 (24.9%) | 0.045 |
| Mild [n (%)] | 24 (13%) | 28 (13.1%) | 0.154 |
| Moderate [n (%)] | 21 (11.4%) | 17 (8%) | – |
| Severe [n (%)] | 18 (9.7%) | 8 (3.8%) | – |
| Infection [n (%)] | 7 (3.8%) | 6 (2.8%) | 0.588 |
| Urinary retention [n (%)] | 22 (11.9%) | 12 (5.6%) | 0.026 |
SB, systematic biopsy; TTMB, transperineal template-guided mapping biopsy.
3.5. Follow-up
All patients with negative biopsy results were included in the follow-up program (in Table 4). The TTMB group consisted of 133 patients, and the SB group included 180 patients. The mean follow-up durations were 77.4 ± 12.1 months and 76.8 ± 13.5 months for the TTMB and SB groups, respectively. During the follow-up period, 12 (9%) patients in the TTMB group and 19 (10.6%) patients in the SB group were lost to follow-up or deceased. No statistically significant difference was observed between the two groups in this regard (P > 0.05). Among the patients followed up, 16 (13.2%) in the TTMB group and 48 (28.1%) in the SB group underwent repeat biopsy; and PCa was diagnosed in 3 (2.5%) patients in the TTMB group and 16 (9.9%) patients in the SB group. It was found that there are statistically significant differences between the two groups in both repeat biopsy rate and PCa detection rate (P < 0.05).
Table 4.
Comparison of follow-up results of the two groups of patients with negative biopsy results
| N | TTMB |
SB |
P |
|---|---|---|---|
| 185 | 213 | ||
| Follow-up period (m) | 77.4 ± 12.1 | 76.8 ± 13.5 | 0.668 |
| Loss to follow-up or mortality (n %) | 12 (9%) | 19 (10.6%) | 0.705 |
| Repeat biopsy (n %) | 16 (13.2%) | 48 (28.1%) | 0.003 |
| Repeatability of biopsy-positive rate (n %) | 3 (2.5%) | 16 (9.9%) | 0.013 |
SB, systematic biopsy; TTMB, transperineal template-guided mapping biopsy.
4. Discussion
Prostate biopsy is currently the significant method for diagnosing patients with suspected PCa. For some patients with negative MRI results but higher PSA or PSA density, there is no target for targeted biopsy, and simple SB is recommended for these patients. However, SB has the risk of missed diagnosis and the strategies to increase the positive rate of biopsy are still explored in this field. Previous studies have indicated that increasing the number of biopsy needles to perform saturation prostate biopsy can improve diagnostic accuracy4; alternatively, incorporating novel liquid-based testing methods or advanced molecular imaging techniques may enhance detection outcomes.15 The sampling length of the prostate biopsy needle is 2 cm, but the anterior-posterior diameter of the prostate (from the base to the apex) is significantly longer than the sampling length of the biopsy needle. Therefore, to reduce the drawback of incomplete prostate biopsy tissue, especially for patients with prostatic hyperplasia, this study divides the prostate into two layers for TTMB to achieve thorough sampling, improve the positive rate of biopsy, and reduce the risk of missed diagnosis.16 In this study, the average number of biopsy needles of TTMB was 53.5, which is significantly higher than the 18.1 needles of SB. Under this condition, the positive rate of TTMB group (28.1% vs. 15.5%) and the detection rate of csPCa (15.7% vs. 8.9%) were significantly higher than that of the SB group (P < 0.05). However, in the biopsy-positive patients, the proportion of csPCa (55.8% vs. 57.6%) showed no significant difference (P > 0.05). Therefore, TTMB can increase the positive rate and detection rate of csPCa in patients but does not increase the risk of detecting ncsPCa through biopsy. TTMB increased the complications related to biopsy, mainly including bleeding and urinary retention. However, no cases of Clavien–Dindo grade >Ⅱ complications occurred, and the clinical risk was controllable.
At the same time, all biopsy-negative patients were followed up for a long time. During the follow-up period, the repeat biopsy rate (13.2%) and the positive rate of repeat biopsy (2.5%) of TTMB were significantly lower than in SB (28.1% and 9.9%, respectively); the result indicated that through TTMB, the PCa patients can be sampled to the greatest extent and comprehensively and that the biopsy results can be as close as possible to the real situation of the prostate. Therefore, TTMB can improve the positive rate and detection rate of csPCa, while reducing the proportion of repeated biopsy, which can guide the follow-up and treatment in the later stage.
Van Hemelrijck M et al.17 conducted a global multicenter study and reported follow-up outcomes of AS for PCa. The findings revealed that 43.6% of patients discontinued AS during the 5-year follow-up period, primarily due to tumor progression, suggesting that conventional biopsy methods may underestimate tumor burden. Merrick et al.18 re-evaluated tumors in 131 patients undergoing AS using transperineal TTMB. The results demonstrated that 52 patients (39.7%) experienced pathological upgrading after TTMB, indicating that conventional biopsy may pose a significant risk in accurately identifying candidates suitable for AS. In this study, by comparing the GS obtained post radical surgery with the highest biopsy scores, it was found that 36.4% of patients in the TTMB group exhibited GS downgrading, which is significantly higher than the 19.2% observed in the SB group. Conversely, the upgrade rate was significantly lower in the TTMB group than in the SB group (6.8% vs. 30.8%). This discrepancy may be attributed to the comprehensive sampling capability of TTMB, which captures the majority of lesion components and incorporates the highest tissue strip score into statistical analysis, thereby increasing the likelihood of GS overestimation. For patients with biopsy GS 3 + 3 = 6 who underwent RP, the postoperative upgrade rate in TTMB group was significantly lower than that in the SB group (10% vs. 50%). According to the definition of csPCa, the two upgraded cases in the saturation biopsy group were classified as ncsPCa, whereas three cases in the SB group were csPCa. Therefore, TTMB demonstrates a higher rate of GS overestimation and a lower rate of underestimation. Furthermore, using large-section pathological specimens from RP to assess biopsy accuracy, TTMB was found to detect 91.5% of lesions, with only 10 missed lesions, all of which were ncsPCa. The TTMB strategy not only enhances biopsy positivity rates but also enables more accurate assessment of lesion grade and extent, thereby reducing the risk of underestimation. Consequently, TTMB can be considered the preferred biopsy strategy for patient selection and follow-up in AS protocols,19 as well as for lesion localization in focal therapy planning.
In fact, the present study still has several limitations. First, it is a retrospective follow-up study with a relatively small sample size, which may introduce selection bias and affect the reliability of the conclusions. Second, during the follow-up period, no standardized follow-up protocol was implemented, primarily due to variations in patient compliance and levels of disease awareness. Additionally, some cases of ncsPCa were detected through biopsy, yet RP was performed. This decision was mainly driven by concerns regarding potential disease progression and the psychological impact on patients.20 The concept of AS remains less accepted among the Chinese population and requires further time and education for broader adoption. Finally, TTMB is associated with greater invasiveness and a more complex procedural workflow, making it unsuitable for all patients undergoing prostate biopsy. It should be reserved for specific clinical scenarios. Therefore, TTMB should be applied cautiously, based on clear clinical indications, patient-specific needs, and with full informed consent.
In conclusion, TTMB can significantly improve the biopsy-positive rate, reduce the risks of missed diagnosis and underestimation of tumor GS, and detect up to 91.5% of prostate lesions. As such, it may be considered a more reliable biopsy strategy for use in AS and focal therapy protocols.
Data availability
The datasets used and/or analyzed in this study are available from the corresponding author on reasonable request.
Ethics approval and consent to participate
All procedures were conducted in accordance with the principles of the 1964 Helsinki Declaration and its subsequent amendments or comparable ethical standards.
Funding
Funding was received from the key scientific research project of Health Commission of Jiangsu Province, China (no. ZD2022010).
Conflict of interest
The authors declare no potential conflicts of interest.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The datasets used and/or analyzed in this study are available from the corresponding author on reasonable request.