Hemigland Cryoablation of Clinically Significant Prostate Cancer: Intermediate-Term Followup via Magnetic Resonance Imaging Guided Biopsy
2020; Lippincott Williams & Wilkins; Volume: 204; Issue: 5 Linguagem: Inglês
10.1097/ju.0000000000001133
ISSN1527-3792
AutoresRyan Chuang, Adam Kinnaird, Lorna Kwan, Anthony Sisk, Danielle Barsa, Ely Felker, Merdie Delfin, Leonard S. Marks,
Tópico(s)Prostate Cancer Treatment and Research
ResumoYou have accessJournal of UrologyAdult Urology1 Nov 2020Hemigland Cryoablation of Clinically Significant Prostate Cancer: Intermediate-Term Followup via Magnetic Resonance Imaging Guided BiopsyThis article is commented on by the following:Editorial CommentEditorial Comment Ryan Chuang, Adam Kinnaird, Lorna Kwan, Anthony Sisk, Danielle Barsa, Ely Felker, Merdie Delfin, and Leonard Marks Ryan ChuangRyan Chuang Department of Urology, University of California, Los Angeles, California Equal study contribution. More articles by this author , Adam KinnairdAdam Kinnaird Department of Urology, University of California, Los Angeles, California Equal study contribution. More articles by this author , Lorna KwanLorna Kwan Department of Urology, University of California, Los Angeles, California More articles by this author , Anthony SiskAnthony Sisk Department of Pathology, University of California, Los Angeles, California More articles by this author , Danielle BarsaDanielle Barsa Department of Urology, University of California, Los Angeles, California More articles by this author , Ely FelkerEly Felker Department of Radiology, University of California, Los Angeles, California More articles by this author , Merdie DelfinMerdie Delfin Department of Urology, University of California, Los Angeles, California More articles by this author , and Leonard MarksLeonard Marks Department of Urology, University of California, Los Angeles, California More articles by this author View All Author Informationhttps://doi.org/10.1097/JU.0000000000001133AboutAbstractPDF ToolsAdd to favoritesDownload CitationsTrack CitationsPermissionsReprints ShareFacebookTwitterLinked InEmail Abstract Purpose: Contemporary biopsy methods were used to determine the success rate of hemigland cryoablation as a primary treatment for prostate cancer. Previous studies, often including men at low risk, have used magnetic resonance imaging guided biopsy to a variable extent. Here, we uniformly used the new diagnostic modality to study all men, each with clinically significant cancer, at baseline and at short and intermediate-term followup. Materials and Methods: In an open label trial (NCT03503643) 61 men with unilateral cancer (all clinically significant, ie Grade Group 2 or greater) underwent primary hemigland cryoablation. Subjects were 80% Caucasian, average age 69 years, prostate specific antigen 6.6 ng/ml and prostate volume 38 cc. Biopsy was performed using magnetic resonance imaging/ultrasound fusion prior to treatment and at the followup intervals of near-term (6 months, in 61) and intermediate-term (18 months, in 27). All utilities of fusion biopsy, ie targeting of magnetic resonance imaging visible lesions, template systematic sampling, and in followup, tracking of prior positive sites, were used throughout the study to detect clinically significant cancer, the primary end point. Results: Following treatment 82% of men (50 of 61) had no biopsy detectable clinically significant prostate cancer at 6-month near-term followup and 82% of men (22 of 27) reaching the 18-month intermediate-term remained biopsy negative. Combination of the 3 sampling methods provided maximal cancer detection. During followup a new focus of cancer was found in the contralateral prostate in only 1 of 27 men. No adverse events above Clavien-Dindo grade 2 were encountered. Conclusions: Hemigland cryoablation, when rigorously evaluated by all utilities of magnetic resonance imaging guided biopsy, appears to eliminate clinically significant cancer in 82% of men, a success rate that endures for at least 18 months. Abbreviations and Acronyms csPCa clinically significant prostate cancer EPIC-CP Expanded Prostate Cancer Index Composite for Clinical Practice GG Grade Group HGCryo hemigland cryoablation I-PSS International Prostate Symptom Score MRGB MRI guided biopsy MRI magnetic resonance imaging PCa prostate cancer PGA partial gland ablation PSA prostate specific antigen US ultrasound Cryotherapy, a centuries-old method of tissue ablation, is currently of resurgent interest for focal therapy of prostate cancer, ie partial gland ablation.1 In 2008 a Best Practice Panel of the American Urological Association (AUA) concluded that, while conceptually attractive, cryotherapy PGA suffered from a lack of clinical data. Only 1 study had been published, long-term results were not available and criteria for patient selection were yet to be determined.2,3 Since that time, PGA with cryotherapy has been reported in increasing numbers. An online registry has been established, which includes thousands of treatments and results.4 Some of the earlier concerns about cryotherapy PGA have been addressed via the registry and in recent reports.5–9 However, focal cryotherapy has been assigned only a “C recommendation” based on currently available evidence.10 Before the 2008 AUA report on cryotherapy, prostate imaging was by ultrasound and biopsy was usually blind to tumor location. Soon after, multiparametric magnetic resonance imaging of the prostate gained traction and is now recommended for guidance of any biopsy when available.11 MRI allows most lesions of csPCa to be visualized, providing a targeted path to precise biopsy and focal treatment.12 Thus, a study using the full utilities of contemporary MRI guided biopsy as an aid to diagnosis and followup after PGA cryotherapy would be of interest. We detail a trial in which all participants had csPCa, defined as histopathology GG2 or greater. All were evaluated by MRGB at baseline and at 6 and 18 months after hemigland cryoablation. In contrast to other studies, treatment was administered only to men with lesions of at least intermediate risk and in all cases the biopsy samples were obtained by MRGB, using the multiple advantages of a MRI-ultrasound fusion device.13,14 A preliminary analysis of early results was reported previously.15 Materials and Methods Study Design In an open label, observational trial (NCT03503643) 67 men with unilateral prostate cancer were enrolled between February 2017 and March 2019. The study was approved by the UCLA institutional review board (IRB No. 17-001084). Outcomes The primary outcome was detection of csPCa by MRGB at 18 months after treatment (in 27). Secondary outcomes were detection of csPCa by MRGB at 6 months (in 61) as well as failure-free survival at both intervals, with no metastases, no cancer specific deaths and no definitive treatment.7 Other outcomes included Clavien-Dindo adverse events. Functional outcomes included changes in erectile function and urinary continence assessed by EPIC-CP and I-PSS. Cryoablation Procedure HGCryo was performed with the patient under general anesthesia in a transperineal fashion with 14-gauge argon gas cryotherapy probes (Galil Medical, Inc., Arden Hills, Minnesota) as previously described.15 All patients were discharged home on the same day as the procedure with a Foley catheter. Discharge medications included a quinolone antibiotic and oral nonnarcotic analgesia. Patients returned to clinic at 2 to 7 days for a voiding trial. Followup and MRI Guided Biopsies PSA measurements and digital rectal examinations were obtained at baseline and 3, 6 and 18 months, with questionnaires (I-PSS and EPIC-CP) at baseline, and 6 and 18 months. Multiparametric MRI was performed in all patients at baseline, 6 and 18 months using a 3 Tesla unit (Siemens MAGNETOM, Trio, Siemens Medical Solutions, Malvern, Pennsylvania). Biopsies were performed transrectally within 60 days of MRI, each of the 3 biopsy sessions using guidance of contemporaneous and, for the 6 and 18-month sessions, previous MRI images (Artemis MRI/US fusion device, Eigen, Grass Valley, California). The technique of MRGB was originally described in 2011 and has remained essentially unchanged to date.16,17 At baseline, MRGB was used to obtain tissue from MRI visible lesions (PI-RADS® v2 grade 3-5) and systematically from both sides of the prostate using a 12-point template (fig. 1). Figure 1. Biopsy schema used during trial. At baseline (A), diagnosis was made by obtaining targeted cores (green) from MRI visible lesions (red) and systematic cores (blue) from 12-point template. At 6-month followup after cryoablation (B), targeted cores (green) were obtained from site of original lesion (faded red) and systematically from ipsilateral side (blue). At 18-month followup (C), targeted cores (green) were obtained from original lesion site (faded red) and, using template guidance, systematically from both sides (blue). At 6 and 18 months all patients underwent tracking biopsy of previous positive sites, targeted biopsy of any new MRI lesions and systematic biopsy of the treated side. At 18 months bilateral template systematic biopsy was also performed. Adverse events were recorded and classified according to the Clavien-Dindo classification system.18 Statistical Analysis Continuous variables are presented as medians with IQR and categorical variables as numbers with percentages. Completed quality of life questionnaires were compared between baseline and followup points. All tests were 2-sided with significance defined as p <0.05. Statistical tests were conducted using R 3.6.0 (R Core Team 2019). Results Baseline Patient Characteristics Men diagnosed with unilateral csPCa were offered HGCryo as an alternative to surgery or radiation therapy, provided prostate volume was less than 75 cc and no GG5 component was present. Of the 67 patients treated 6 were excluded from analysis, including 5 with only GG1 lesions and 1 who had undergone previous laser ablation. All 61 patients had 6-month and 27 of 61 (44%) had 18-month followup MRGB. Nineteen patients had contralateral foci of GG1 PCa but these foci were not considered clinically significant, in line with NCCN® guidelines.14 Tumor location was not an influential variable. Baseline tumor was primarily in the peripheral zone in 44 of 61 and transition zone in 17 of 61. Biopsy outcomes were similar in the 2 groups (table 1). Table 1. Baseline patient characteristics Median age (IQR) 69 (65–73) No. ethnicity: Caucasian 49 Asian 5 African American 4 Other 3 Median ng/ml PSA (IQR) 6.6 (4.8–10) Median %-free PSA (IQR) 14 (9.0–17) Median cc prostate vol by multiparametric MRI (IQR) 38 (29–53) Median PSA density (IQR) 0.17 (0.11–0.29) No. Gleason GG: 2 40 3 15 4 6 Median mm max Ca core length (IQR) 7 (4.75–10) Median mm index lesion diameter region of interest (IQR) 15 (12–18) Outcomes Biopsy findings at baseline and at followup sessions are shown in figure 2. At baseline, all 61 men had csPCa, including 21 with GG3 or 4. At 6-month biopsy (ipsilateral only) 50 (82%) of 61 patients had no evidence of csPCa. GG2 and GG3 disease was found in 7 and 4 patients, respectively. Of the 11 patients with csPCa 6 with small residual foci elected to enter active surveillance, 5 elected repeat cryoablation (results to be reported elsewhere) and 1 proceeded to salvage brachytherapy. Figure 2. Gleason grade groupings at baseline and at 6 and 18 months after hemigland cryoablation. MRI guided biopsy was used in all men to document pathology at baseline and at 2 followup points. All 61 men had baseline pathology GG2 or greater (csPCa). Absence of csPCa was found in 82% of men at each of 2 followup evaluations after treatment (50 of 61 at 6 months, 22 of 27 at 18 months). At 18-month biopsy (bilateral) 22 of 27 (82%) patients had no evidence of csPCa (fig. 2). Of the 5 patients with csPCa, GG2, GG3 and GG4 disease was found in 2, 1 and 2 patients, respectively. Among the 5 with csPCa at 18 months 1 man was found to have a contralateral lesion (1 mm GG2) that was not diagnosed initially or at 6-month followup. Four men elected to continue active surveillance of low volume residual lesions (1 to 2 mm of GG2-4), and 1 with GG4 will undergo repeat cryoablation. Of the 6 men with baseline GG4 5 were found to be cancer-free at 6 months, 4 have reached 18 months and remain cancer-free, and 1 had treatment failure at 18 months and will undergo prostatectomy. Conditional failure-free survival at 6 and 18 months was 98% and 100%, respectively. No patients died of prostate cancer or had metastatic disease. In figure 3 outcomes are shown for each man who reached 6 and 18-month followup biopsy (27), stratified by order of treatment and side of lesion. No learning curve effect and no laterality were noted. Of interest, only 1 patient was later found to have csPCa contralateral to the treated side of the prostate. Figure 3. Biopsy results of hemigland cryoablation for all 27 patients. Each column represents 1 patient in chronological order, with first patient at left and most recent patient at right. Side of csPCa (left [L], right [R]) indicated at right of figure. Only 1 patient (number 3 at 18 months) was subsequently found to have csPCa on contralateral hemigland. Of 19 men with a contralateral focus of GG1 disease at baseline 2 were found to have persistent GG1 disease on 6-month biopsy. Four of 27 men who reached 18-month followup were found to have new GG1 foci at 18-month biopsy. None had progression of GG1 to GG2 or greater. In figure 4 examples of various MRI findings before and 6 months after HGCryo are shown in relation to findings on posttreatment targeted biopsy, a “ground truth.” Of the 61 men 59 had MRI visible lesions at baseline. At 6-month followup 44 men had no lesion on MRI after treatment, ie were negative, of whom 39 were true negatives (89%). There were 17 men with posttreatment MRI showing a suspicious area as defined by Felker et al.19 Six were positive by biopsy, ie true positives (35%). Figure 4. Disparate examples of MRI visible lesions (T2-weighted image) before and 6 months after hemigland cryoablation. Solid arrows denote original or persistent lesion and open arrows denote resolved lesion after treatment. Shown at right are histological findings on corresponding posttreatment biopsy, taken from region of original lesion. A, right HGCryo. Lesion resolves after treatment, biopsy is negative (MRI true negative) (note fibrosis). B, left HGCryo. Lesion remains after treatment, biopsy is positive (MRI true positive). C, left HGCryo. Lesion resolves after treatment but biopsy remains positive (MRI false-negative). Guided biopsy after treatment appears to be most definitive indicator of treatment result. In 44 of 61 cases MRI visible lesion resolved after treatment but in 5 of 44 (11%) biopsy showed persistent cancer in region of baseline lesion. Detection of Prostate Cancer by Biopsy Methods Three different biopsy approaches were used to diagnose the cancer and evaluate results of treatment. At baseline all 61 men were found to have csPCa, diagnosed by targeted biopsy of MRI visible lesions, template systematic sampling or both (fig. 5). Spatial location of all positive biopsy sites was recorded automatically by software in the image fusion device and stored for later re-sampling of that site (tracked biopsy).6 Figure 5. Biopsy methods leading to detection of csPCa at baseline and followup intervals. Note that at 6 months re-sampling original positive biopsy site (tracking) was most common way residual cancer was detected (in 7 of 11). At 6 months new MRI visible lesions were found ipsilateral to treatment side in 1 patient. At 18 months new lesions were found in 2. All 3 MRI visible lesions were targeted and found to contain csPCa. At both followup intervals combined biopsies were required for maximal cancer detection. At 6 months 11 patients were found to have csPCa. The cancer was detected by tracked biopsy alone in 7, targeted biopsy of a new ipsilateral lesion in 3 and systematic biopsy in 1. At 18 months, of the 5 patients found to have csPCa, 2 were found only by tracked biopsy, 2 by targeted biopsy and 1 by template-systematic biopsy. While tracking biopsy was the most sensitive, all 3 methods were required for maximal cancer detection. Had only 1 of the 3 approaches been used, biopsy would have been falsely negative in up to 8 of the 11 men at 6 months and up to 4 of the 5 at 18 months (fig. 5). Secondary Outcomes PSA decreased from 6.6 ng/ml (IQR 4.8–10) at baseline to 2.0 ng/ml (IQR 0.99–3.5) and 2.3 ng/ml (IQR 1.3–3.6) at 6 and 18 months, respectively (p <0.01). Compared to baseline, prostate volume decreased by 20% (IQR 13–31) and 19% (IQR 12–30) at 6 and 18 months (p <0.01), percent-free PSA increased from 14% (IQR 9–17) to 18% (IQR 13–25) and 24% (IQR 14–27) at 6 and 18 months (p <0.01), respectively. Multivariable Analysis Predicting csPCa-Free Survival Multivariate logistic regression was performed to assess the role of pretreatment PSA, prostate volume, percent-free PSA and PSA density, as well as 6-month and 18-month PSA, percent-free PSA, and PSA density. We found that smaller baseline prostate volume and higher PSA density were mildly and insignificantly associated with presence of csPCa on biopsy at 6 and 18 months. Complications and Quality of Life Outcomes No intraoperative complications occurred. Postoperative complications related to treatment were generally mild and short-lived. Clavien-Dindo grade 2 postoperative complications occurred in 5 patients. Two patients experienced epididymitis within the first postoperative week which resolved after treatment with oral antibiotics. Two patients required replacement of a Foley catheter after the initial voiding trial and both were ultimately able to void freely after several weeks. One patient reported new onset erectile dysfunction, which responded to oral phosphodiesterase type 5 inhibitor therapy. No higher grade complications occurred. Two men had significant sexual dysfunction with baseline EPIC-CP sexual function domain scores greater than 10, and all others had scores less than 9. Domain scores increased from a median of 5 at baseline to 6 at 6 months (p <0.05) and this difference is not considered meaningful.20 At baseline, median I-PSS was 8 (IQR 4–12) and at 18 months it was 5.5 (IQR 4–7) (p <0.05). No patient required use of pads after treatment. No complications above Clavien-Dindo grade 2 resulted after any followup biopsy. Discussion In the present report men with unilateral prostate cancer (csPCa) underwent hemigland cryoablation in a prospective observational trial. In contrast to other studies, all patients had csPCa (GG2 or greater), and outcomes were uniformly determined by comprehensive MRGB at baseline and at short and intermediate-term followup. The procedure was found to be safe and effective, csPCa being absent in 82% of men at followup MRGB 6 months after treatment. The 82% effectiveness was maintained upon repeat MRGB 18 months after treatment. Moreover, only 1 of 27 men had contralateral csPCa at 18 months, attesting to the reliability of the negative contralateral findings at baseline. While numbers of subjects studied are relatively small (61), the trial adds a depth of detail in support of HGCryo not provided by previous large studies.5–9,21 While others have noted a decrease in serum PSA levels after successful treatment, PSA changes in the present group were not statistically significant.8 Other contemporary studies of HGCryo report undetectable csPCa on followup biopsy in up to 84% of cases (table 2). The success rate in the present report approximates that found in these large studies, all with sample size greater than 96. However, the other studies used subjects with low risk PCa in variable numbers, followup MRGB was performed for cause, if at all, and length of followup biopsy was no more than 12 months, when reported. In the present study no man with low risk PCa was included, and 21 of 61 had GG3 or GG4 cancers. MRGB was performed per protocol in all men at baseline and at followup (fig. 1). Followup was extended to 18 months, documenting intermediate-term efficacy with biopsy confirmation. Thus, the present study, in which contemporary biopsy methods were uniformly used to study men who could most benefit from treatment, lends support to conclusions of previous studies. Table 2. Contemporary studies of partial gland ablation with cryotherapy Present Series Tourinho-Barbosa et al8 Oishi et al6 Shah et al7 Kongnyuy et al5 Barqawi et al9 Site UCLA Paris +São Paulo, Brazil USC UCL, London NYU-Winthrop U. Colorado No. treated 61 119 160 122 163 96 Prospective Yes No No Yes No Yes MRI before Yes Yes No Yes No No MRGB before Yes Yes Some Yes No No MRI after Yes Yes No Yes Some No MRGB after Yes For cause For cause For cause Not applicable No Tracking biopsy Yes No No Yes Not applicable No Latest biopsy followup (mos) 18 12 12 (some) Not applicable Not applicable Not applicable Length of followup (mos) 18 64 67 28 28 24 % GG1 0 72 24 10 46 Not applicable % csPCa-free at latest biopsy 82 Not applicable 70 84* 33 Not applicable Of 122 patients 29 underwent followup biopsy. The proper role of PGA, which was first reported in 2008, remains under study, but clearly followup biopsy is the most important criterion of success.2,22 In the present study of HGCryo, MRGB was performed with a MRI/US fusion device, which provides 3 utilities lacking in conventional biopsy, namely 1) targeted sampling of MRI visible lesions, 2) systematic sampling via a template built into the software, and 3) recording of biopsy sites for later recall and repeat sampling of specific cancer foci (tracking) (fig. 1). All 3 utilities of MRI/US fusion biopsy were applied to all men in the present series at all 3 time points. Thus, the biopsy evidence presented here, showing an 82% success rate of HGCryo of 18 months duration, is rigorous, uniform and highly likely to represent actual pathology of the whole organ.23,24 Men with intermediate risk PCa are currently considered the best candidates for PGA studies.14 In recent years increased numbers of men are presenting with intermediate lesions (GG2, GG3), likely the result of MRGB (fig. 6). In the era of ultrasound guided biopsy GG1 was the most common cancer (50%) and intermediate risk cancers accounted for 40% of the total.25 In a compilation of recent results of MRGB at UCLA (2017-2019), intermediate risk cancers were the most common cancer (52%) with GG1 cancers only accounting for 24% of the total (data on file). Figure 6. Prostate biopsy findings (Gleason GG) before and after advent of MRI guidance. Distribution of groupings found in earlier series (closed bars, 2005-2014), men diagnosed with ultrasound guidance, compared with findings in contemporary series of men diagnosed with MRI guided biopsy (open bars, 2017-2019).17,25 Previously GG1 was most common finding (50%) and only 10% of cancers were aggressive type (GG4, 5). In current series from UCLA (2017-2019) 59% of cancers found via MRI guidance are of intermediate risk (GG2, 3), ie possible candidates for focal therapy, and aggressive cancers now account for 26% of total. As use of MRGB increases, with resulting improved accuracy of prostate tissue characterization, numbers of candidates for PGA are expected to rise. In the future, selected men with high grade cancers may be offered PGA, like the 6 in the present report treated with HGCryo. Another possible future application of HGCryo might be for advanced PCa, where cytoreduction of the primary tumor is combined with androgen deprivation and/or chemotherapeutic agents, or even for oligometastatic disease (abscopal effect).26 The study has several limitations. Like many other prospective PGA inquiries to date, the study lacked a control arm and is observational in nature. The study was sited at a single institution, where investigators enjoy a voluminous experience with MRGB. The cohort was relatively small and consisted mostly of Caucasian subjects. Followup only extended to 18 months. Despite the limitations, the comprehensive biopsy data, which were collected prospectively, and the inclusion of only men with csPCa, help to provide at least intermediate-term confirmation that HGCryo is a safe, effective method of cancer ablation. Controlled studies, extending for at least 5 years, will be required to prove that HGCryo alters the long natural history of the disease. Conclusion Hemigland cryoablation, when evaluated by serial MRI guided biopsy, is an effective method for treating men with unilateral clinically significant prostate cancer. Freedom from csPCa as documented by biopsy, was found in 82% of cases at 18 months of followup. References 1. : Cancer cryotherapy: evolution and biology. Rev Urol, suppl., 2004; 6: S9. Google Scholar 2. : “Male lumpectomy”: focal therapy for prostate cancer using cryoablation. Urology 2007; 70: 16. Google Scholar 3. : Best practice statement on cryosurgery for the treatment of localized prostate cancer. J Urol 2008; 180: 1993. Link, Google Scholar 4. : Focal cryotherapy for localized prostate cancer: a report from the national Cryo On-Line Database (COLD) Registry. BJU Int 2012; 109: 1648. Google Scholar 5. : Predictors of biochemical recurrence after primary focal cryosurgery (hemiablation) for localized prostate cancer: a multi-institutional analytic comparison of Phoenix and Stuttgart criteria. 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Google Scholar No direct or indirect commercial, personal, academic, political, religious or ethical incentive is associated with publishing this article. © 2020 by American Urological Association Education and Research, Inc.FiguresReferencesRelatedDetailsRelated articlesJournal of UrologySep 28, 2020, 12:00:00 AMEditorial CommentJournal of UrologySep 28, 2020, 12:00:00 AMEditorial Comment Volume 204Issue 5November 2020Page: 941-949 Advertisement Copyright & Permissions© 2020 by American Urological Association Education and Research, Inc.Keywordsbiopsycryosurgeryprostatic neoplasmMetricsAuthor Information Ryan Chuang Department of Urology, University of California, Los Angeles, California Equal study contribution. More articles by this author Adam Kinnaird Department of Urology, University of California, Los Angeles, California Equal study contribution. More articles by this author Lorna Kwan Department of Urology, University of California, Los Angeles, California More articles by this author Anthony Sisk Department of Pathology, University of California, Los Angeles, California More articles by this author Danielle Barsa Department of Urology, University of California, Los Angeles, California More articles by this author Ely Felker Department of Radiology, University of California, Los Angeles, California More articles by this author Merdie Delfin Department of Urology, University of California, Los Angeles, California More articles by this author Leonard Marks Department of Urology, University of California, Los Angeles, California More articles by this author Expand All No direct or indirect commercial, personal, academic, political, religious or ethical incentive is associated with publishing this article. Advertisement Advertisement PDF DownloadLoading ...
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