Abstract
Nerve-sparing radical prostatectomy (NSRP) for prostate cancer (PC) enables better postoperative recovery of continence and potency but may increase the risk of positive surgical margins. This study aimed to investigate preoperative predictive factors for extracapsular extension (ECE) of PC to select patients for NSRP. We retrospectively evaluated 288 patients with PC (576 lobes) diagnosed with 12-core transrectal ultrasound-guided biopsy and magnetic resonance imaging (MRI) who underwent laparoscopic or robot-assisted radical prostatectomy at our institution. Surgical specimens and preoperative parameters (prostate-specific antigen, prostate volume, biopsy and MRI findings, preoperative therapy) were analyzed. Of 576 prostate lobes, the incidence Ipsilateral ECE was identified in 97 (16.8%) lobes. The higher number of unilateral positive biopsy cores, the highest Gleason score 8 or more and positive unilateral findings on MRI are significant higher in prostate sides with ECE in univariate analysis. In multivariate analysis, positive unilateral MRI findings (odds ratio [OR], 2.86; p < 0.001) and unilateral biopsy positive core ≥ 3 (OR, 3.73; p < 0.001) were independent predictors of unilateral ECE. The detection rate of unilateral ECE in those cases with two factors (side-specific positive biopsy core 2 or less and side-specific MRI findings negative) was 7.1% (19/269). Patients with fewer unilateral positive biopsy cores and negative unilateral MRI findings might be good candidates for NSRP.
Keywords: Extracapsular extension, Laparoscopic radical prostatectomy, Localized prostate cancer
Introduction
Prostate cancer (PC) is a common malignant tumor in men. Prostate-specific antigen (PSA) screening is widely used, and the number of patients with PC diagnosed in relatively early stages of disease is increasing [1, 2]. Radical prostatectomy is recommended as the standard of care for clinically localized PC [3]. However, postoperative erectile dysfunction and urinary incontinence are significant adverse events that affect the quality of life of these patients. The preservation of neurovascular bundles leads to better functional outcomes related to potency and continence [4, 5]. Current American Urological Association guidelines strongly recommend that clinicians counsel patients with localized PC that nerve-sparing procedures are associated with better erectile function recovery than non-nerve-sparing procedures [6]. However, the close contact between the prostate and the surrounding neurovascular bundles concerns surgeons that a nerve-sparing technique could lead to a higher risk of positive surgical margins as a surrogate for cancer control [7]. Current European Association of Urology guidelines recommend not to perform a nerve-sparing operation in cases of ipsilateral extracapsular extension disease (ECE) [8]. When ECE is highly suspected on preoperative evaluation, periprostatic tissues, such as neurovascular bundles, should be resected widely to reduce the possibility of positive surgical margins. To select patients who can undergo nerve-preserving surgery, there is an urgent need for accurate preoperative models to predict ipsilateral ECE. The aim of this study was to investigate preoperative predictive factors for ipsilateral ECE of PC to determine the indication for nerve-sparing radical prostatectomy.
Materials and Methods
We retrospectively evaluated patients with clinically localized PC who underwent laparoscopic radical prostatectomy or robot-assisted radical prostatectomy in our institution between June 2012 and May 2021. Patients who had not been assessed with magnetic resonance imaging (MRI), had not undergone prostate biopsy in our institution, and had not undergone 12-core biopsies were excluded. All patients underwent 12-core transrectal ultrasonography-guided prostate biopsies. Biopsy sites included 3 cores from the standard peripheral base, middle and apex zone, 2 cores from the far lateral peripheral zone (laterally directed cores) and 1 core from the middle transition zone in each lobe. In patients with MRI-suspicious lesions pre-biopsy, cognitive target prostate biopsy near the individual standard biopsy area was considered. MRI images were acquired on a 1.5T MRI scanner (Sibna, GE Medical Systems, Milwaukee, MI, USA). All patients underwent MRI examinations included T2WI, DWI and apparent diffusion coefficient (ADC) with or without dynamic enhanced-contrast imaging before the treatments (neoadjuvant hormonal therapy (NHT) in case of NHT + surgery or surgery in case of no NHT). MRI findings were evaluated by three urologists. We presented NHT as a treatment option for mainly clinical T3 stage patients who are expected to wait surgery two months or more. The histopathological examination of prostate biopsy specimens and radical prostatectomy specimens was performed by a single pathologist. Statistical analyses were performed with EZR (Saitama Medical Center, Jichi Medical University, Saitama, Japan), which is a graphical user interface for R (The R Foundation for statistical Computing, Vienna, Austria). More precisely, it is a modified version of R commander designed to add statistical functions frequently used in biostatics [9].
Results
The final study population consisted of 288 patients (576 prostate sides). Median age was 69 years (range, 50–79 years), median PSA levels were 9.1 ng/ml (range, 2.2–110.0 ng/ml), median prostate volume was 30.0 ml (range, 10–130 ml), and clinical T stages were T1 (n = 65), T2 (n = 186), and T3 (n = 37). Laparoscopic radical prostatectomy and robot-assisted laparoscopic radical prostatectomy were carried out in 183 (63.6%) and 105 (36.4%) patients, respectively, and 112 (38.9%) patients underwent NHT (Table 1). Most of the patients who received NHT were treated for three months or less. Pathological T3 (pT3) was 78 (27.1%) and, of 37 clinical stage T3 (cT3) patients, 14 patients were pT3 (37.8%). 6 patients were pT0 (2, 2 and 2 cases in cT1c, cT2 and cT3a, respectively). Of 576 prostate lobes, ipsilateral ECE was identified in 97 (16.8%) lobes. In the comparison between prostate sides with and without ECE, the number of unilateral positive biopsy cores was significantly higher in prostate sides with ECE. The highest Gleason score of 8 or more and positive unilateral findings on MRI were also related to existing unilateral ECE. Serum PSA level, PSA density (PSAD) and neoadjuvant therapy were not significantly related to the incidence of unilateral ECE in the definitive diagnosis (Table 2). In multivariate analysis, positive unilateral findings on MRI [odds ratio (OR) = 2.86; p < 0.001] and unilateral biopsy positive core ≥ 3 (OR = 3.73; p < 0.001) were independent predictors of unilateral ECE (Table 3). The incidence of prostate lobes with ECE according to the number of lobe-specific positive biopsy cores was 8.2% (27/330) for ≤ 1 positive cores and 11.3% (48/426) for ≤ 2 positive cores. The detection rate of unilateral ECE in those cases with two factors (lobe-specific positive biopsy core ≤ 2 and lobe-specific MRI findings negative) was 7.1% (19/269) (Table 4). In the subset cohort who underwent NHT (n = 227), unilateral biopsy positive core ≥ 3, the highest Gleason score of 8 or more, and positive unilateral findings on MRI were related to unilateral ECE, as well as all patients. However, in multivariate analysis, only unilateral biopsy positive core ≥ 3 (OR = 2.43; p = 0.038) was an independent predictor of unilateral ECE in NHT subgroup (Table 5).
Table 1.
Patients characteristics
| Baseline patient characeristics | n = 288 |
|---|---|
| Age (median):years old | 69 (50–79) |
| PSA (median): ng/ml | 9.1 (1.2–110.0) |
| Prostate volume (median): cc | 30 (10–130) |
| Clinical T stage (%) | |
| T1 | 65 (22.6) |
| T2 | 186 (64.6) |
| T3 | 37 (12.8) |
| Biopsy Gleason score (%) | |
| 6 | 108 (37.5) |
| 7 | 82 (28.5) |
| 8–10 | 98 (34.0) |
| Neoadjvant therapy (%) | |
| Yes | 112 (38.9) |
| No | 176 (61.1) |
| Surgical procedure (%) | |
| Laparoscopic | 183 (63.6) |
| Robot-assisted | 105 (36.4) |
| Nerve sparing (%) | |
| bilateral | 10 (3.5) |
| unilateral | 46 (16.0) |
| none | 232 (80.5) |
| Prostate weight (median): g | 40 (15–120) |
| Pathological T stage (%) | |
| T0 | 6 (2.1) |
| T2 | 204 (70.8) |
| T3 | 78 (27.1) |
| Definitive Gleason score (%) | |
| 6 | 68 (23.6) |
| 7 | 151 (52.4) |
| 8–10 | 63 (21.9) |
PSA Prostate-sepcific antigen
Table 2.
Comparison of preoperative factors according to unilateral extracapsular extension
| Without ECE (n = 479) | With ECE (n = 97) | P-value | |
|---|---|---|---|
| PSA | 12.0 ± 12.8 | 13.8 ± 10.7 | 0.196 |
| Prostate volume: cc | 33.3 ± 17.7 | 31.3 ± 14.6 | 0.314 |
| PSAD | 0.42 ± 0.42 | 0.51 ± 0.40 | 0.074 |
| Highest Gleason score | |||
| ≤ 7 | 326 | 52 | 0.01 |
| ≥ 8 | 153 | 45 | |
| Number of Unilateral positive biopsy core | 1.4 ± 1.6 | 2.8 ± 1.8 | < 0.001 |
| Findings of Unilateral MRI | |||
| Negative | 271 | 30 | < 0.001 |
| Positive | 208 | 67 | |
| Neoadjvant therapy | |||
| No | 291 | 59 | 1 |
| Yes | 188 | 38 | |
| Surgical mergin status | |||
| Negative | 458 | 67 | < 0.001 |
| Positive | 21 | 30 | |
ECE Extracapsular extension; PSA Prostate-specific antigen; PSAD PSA density
Table 3.
Univariate and multivariate analysis in detection of unilateral extracapsular extension
| Factor | Univariate model | Multivariate model | ||
|---|---|---|---|---|
| Odds ratio (95% CI) | P-value | Odds ratio (95% CI) | P-value | |
| Biopsy highest Gleason score (6, 7 v.s. ≥ 8) | 1.81 (1.16–2.83) | 0.009 | 1.36 (0.85–2.18) | 0.2 |
| Side-specific positive Biopsy core (< 3 vs ≥ 3) | 3.73 (2.36–5.89) | < 0.001 | 2.73 (1.66–4.50) | < 0.001 |
| Side specific MRI findings (Negative vs positive) | 2.86 (1.79–4.56) | < 0.001 | 1.93 (1.16–3.22) | 0.012 |
CI Confidence interval; MRI Magnetic resonance imaging
Table 4.
Parameters to detect extracapsular extension
| n | Extracapsular extension | |
|---|---|---|
| Side-specific positive biopsy core ≤ 3 (≤ 50.0%) | 486 | 63 (13.0%) |
| Side-specific positive biopsy core ≤ 2 (≤ 33.3%) | 426 | 48 (11.3%) |
| Side-specific positive biopsy core ≤ 1 (≤ 16.7%) | 330 | 27 (8.2%) |
| Side-specific positive biopsy core = 0 (0%) | 190 | 6 (3.2%) |
| Side-specific MRI findings negative | 301 | 30 (10.0%) |
| Side-specific positive biopsy core ≤ 2 (≤33.3%) and side-specific MRI findings negative | 269 | 19 (7.1%) |
MRI Magnetic resonance imaging
Table 5.
Neoadjuvant hormonal therapy subgroup chort
| A. Clinical stage and ECE status | ||||
| ALL (n = 288) | NHT chort (n = 112) | |||
| Clinical T stage (%) | ||||
| T1 | 65 (22.6) | 13 (11.6) | ||
| T2 | 186 (64.6) | 68 (60.7) | ||
| T3 | 37 (12.8) | 31 (27.6) | ||
| ECE status (%) | ||||
| No | 210 (72.9) | 84 (74.9) | ||
| Yes | 78 (27.1) | 28 (25) | ||
| B. Univariate and multivariate analysis of ECE | ||||
| Factor | Univariate model | Multivariate model | ||
| Odds ratio (95% CI) | P-value | Odds ratio (95% CI) | P-value | |
| Biopsy highest Gleason score (6, 7 v.s.≥8) | 2.48 (1.16–5.29) | 0.015 | 2.06 (0.94–4.51) | 0.07 |
| Side-specific positive Biopsy core (< 3 vs ≥ 3) | 3.76 (1.80–7.83) | < 0.001 | 2.43 (1.05–5.60) | 0.038 |
| Side specific MRI findings (Negative vs positive) | 3.48 (1.52–7.99) | < 0.001 | 2.12 (0.83–5.43) | 0.118 |
NHT Neoadjvant hormonal therapy; ECE Extracapsular extension; CI Confidence interval; MRI Magnetic resonance imaging
Discussion
Surgeons who perform radical prostatectomy must maximize both oncological and functional outcomes. Nerve-sparing procedures are crucial for improving functional outcomes, including urinary continence and erectile function [4, 5]. However, a concern with nerve-sparing surgery is that the risk of positive resection margins is increased due to the proximity of the dissection plane. Previous studies reported an association between nerve-sparing surgery and the risk of positive surgical margins [10, 11]. Preston et al. presented an analysis of 6,120 patients who underwent radical prostatectomy and concluded that in organ-confined prostate cancer, bilateral nerve sparing was associated with a higher risk of positive resection margins [10].
As ECE of PC is closely associated with the risk of a positive resection margin, patients with pathologically organ-confined PC are considered optimal candidates for nerve-sparing radical prostatectomy [8, 12]. Some prediction models of ECE have been reported that include PSA, clinical stage, and Gleason score of biopsies [13, 14]. These models are not sufficient to decide surgical planning for nerve-sparing procedures, because they do not predict side-specific ECE. Therefore, we evaluated preoperative factors with ipsilateral ECE to detect candidates for nerve-sparing radical prostatectomy. Some Previous studies assessed the predictive value of preoperative factors including PSA, digital examination, PSAD, and biopsy Gleason score for ipsilateral ECE [15–17].
Usefulness of the percent of side-specific positive biopsy cores has been reported. Tsuzuki et al. reported that greater than 33.3% of side-specific cores with tumor is an independent predictor of neurovascular bundle invasion (OR, 2.2; 95% CI, 1.7–3.5) [16]. Sayyid et al. reported that the percent of side-specific positive biopsy cores is a predictive factor for ECE in multivariate analysis (OR, 1.02; p < 0.01), and they also reported that a biopsy Gleason score ≥ 8 is also a significant predictive factor for ECE (OR, 5.86; p < 0.01) [18]. However, these data were based on traditional open surgery and MRI findings were not accounted. Our result can predict ECE accurately using only MRI findings and standard 12-core transrectal prostate biopsy based on current minimal invasive surgery.
The present study revealed that the side-specific positive biopsy core is an important factor for predicting ECE in the side of the prostate that underwent standard 12 core biopsies in multivariate analysis. The rate of ipsilateral ECE increased from 3.2% for a 0% positive core to 8.2% for a ≤ 16.7% positive core, 11.3% for ≤ 33.3% positive cores and 13.0% for ≤ 50% positive cores. We also found that positive unilateral findings on MRI is a significant factor to predict ECE (OR, 2.86; p = 0.012). In terms of the detection of PC, ultrasonography-guided standard 12 core biopsy is widely used, as it is well balanced between the cancer detection rate and adverse events [19, 20]. The present study revealed that 12 core standard biopsy is also helpful to predict ipsilateral ECE and to select candidates for NSRP.
Recently, the accuracy of MRI findings in predicting pathological stage in patients undergoing radical prostatectomy has been reported [21–23]. Gupta et al. reported that the sensitivity and specificity of MRI findings in detecting ECE were 77.8% and 83.4%, respectively [22]. There are some scoring systems that include MRI findings to predict ipsilateral ECE [24, 25]. Park et al. reported a scoring system including PSA, biopsy Gleason score, percentage of side-specific cores with tumor, and MRI findings that predicted ECE [24]. In this study, side-specific MRI findings were significantly related to the incidence of unilateral ECE in multivariate analysis, and the negative predictive value was 90%. In the combination with side-specific MRI findings and the rate of ipsilateral positive biopsy cores, the detection rate of side-specific ECE became more accurate (7.1% for positive biopsy core ≤ 33.3% with MRI findings negative). Our study also provide that no positive core of ipsilateral biopsy was the least detection rate of side-specific ECE (3.2%). Our study showed that in patients undergoing NHT, unilateral biopsy positive core ≥ 3 was a significant predictor of side-specific ECE. However, the sample size of this cohort was limited and further studies are needed.
Our study has several limitations. It was a single-center, retrospective study with a relatively small number of patients. MRI-transrectal ultrasonography real-time fusion target biopsy was not used for regions with suspected PC on MRI. However, our study is important in that we used only transrectal 12-core biopsy with a cognitive technique because not all institutions are equipped with real-time fusion biopsy systems.
Conclusion
The rate of unilateral positive biopsy core is a significant preoperative factor to predict ipsilateral ECE. Furthermore, patients with fewer side-specific positive biopsy cores and negative unilateral findings on MRI might be good candidates for NSRP.
Declarations
Conflict of Interests
The authors declare no conflict of interest.
Footnotes
Publisher's Note
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