LAPAROSCOPIC UROLOGY Laparoscopic Radical Prostatectomy after Previous Transurethral Resection of the Prostate in Clinical T1a and T1b Prostate Cancer: A Matched-Pair Analysis Yi Yang,1* Yun Luo,1* Guo-Liang Hou,2 Qun-Xiong Huang,1 Min-Hua Lu,1 Jie Si-tu,1 Xin Gao1** Purpose: To analyze and compare surgical, oncological and functional outcomes of laparoscopic radi- cal prostatectomy (LRP) in patients with and without previous transurethral resection of the prostate (TURP). Materials and Methods: In total, 785 men underwent LRP at our institution from January 2002 to December 2012. TURP had been performed previously in 35 of these patients (TURP group). A matched-pair analysis iden- tified 35 additional men without previous TURP who exhibited equivalent clinicopathological characteristics to serve as a control group. Perioperative complications and surgical, functional, and oncological outcomes were compared between the two groups. Results: The groups were similar in age, body mass index, serum prostate-specific antigen level, and pre- and post-operative Gleason scores. Patients in the TURP group had greater blood loss (231 vs. 139 mL), longer opera- tive times (262 vs. 213 min), a greater probability of transfusion (8.6% vs. 0%), and a higher rate of complications (37.1% vs. 11.4%) compared with the control group. The positive surgical margin rate was higher in the TURP group, but this difference was not statistically significant (P = .179). The continence rates at one year after surgery were similar, but a lower continence rate was identified in the TURP group (42.9% vs. 68.6%) at 3 months. Bio- chemical recurrence developed in 17.1% and 11.4% of the patients in the TURP and control groups, respectively, after a mean follow-up of 57.6 months. Conclusion: LRP is feasible but challenging after TURP. LRP entails longer operating times, greater blood loss, higher complication rates and worse short-term continence outcomes. However, the radical nature of this cancer surgery is not compromised. Keywords: laparoscopy; prostatectomy; methods; prostatic neoplasms; surgery; blood loss; operative time; tran- surethral resection of prostate; postoperative complications; adverse effects; treatment outcome. INTRODUCTION It is fairly common for patients with clinically local-ized prostate cancer (PCa) to undergo transurethral resection of the prostate (TURP) for benign prostat- ic hyperplasia (BPH). The rate of PCa that is detect- ed on histopathological examination of TURP chips using normal range age-specific serum prostate-spe- cific antigen (PSA) levels and negative digital rec- tal examination findings is 6.4%.(1) It is considered that the presence of periprostatic fibrosis, scar tis- sue and inflammation after previous TURP may hin- der optimal outcomes for radical prostatectomy.(2) Historically, open retropubic radical prostatecto- my (RRP) after previous TURP was associated with poor surgical, pathological, and functional outcomes. (3) During the past years, laparoscopic radical prosta- tectomy (LRP) has become a more commonly per- formed procedure for the treatment of localized PCa. (4,5) LRP has the advantages of clearer fields of vision, better preservation of anatomical structures, a shorter period of convalescence and less blood loss compared with RRP, and it seems ideal for the navigation of difficult tissue planes in a previously treated surgical field.(6,7) Menard and colleagues(1) showed that LRP could be performed after prior TURP without com- promising the oncological results but with worse in- traoperative and postoperative outcomes. However, several studies have shown no difference in complica- tion rates or morbidity, and the opportunity for surgi- cal cure was comparable to patients without previous TURP, although LRP was technically more difficult.(8) There are a few published data of a limited number of pa- tients exploring the influence of previous TURP on LRP, but no consensus has been reached. Limited reports are available on the long-term oncological and functional results in patients with a history of TURP who undergo LRP. To our knowledge, there is a lack of published data on outcomes of LRP in patients with previous TURP in China. In this retrospective review, we assessed the perioperative, oncological and functional outcomes of patients with a history of TURP who underwent LRP. MATERIALS AND METHODS Study Design A total of 785 men underwent LRP at our institution from January 2002 to December 2012. All of their 1Department of Urology, The Third Affiliated Hospital, Sun Yat-sen University, Guangzhou, 510630, China. 2 Department of Urology, Foshan First Municipal People’s Hospital, Foshan, 528000, China. *Authors contributed equally. **Correspondence: Department of Urology, The Third Affiliated Hospital, Sun Yat-sen University, Tianhe Road 600, Guangzhou, 510630, China. Tel: +86 20 85252990. Fax: +86 20 85252678. E-mail: urogx@hotmail.com Received June 2015 & Accepted June 2015 Laparoscopic Urology 2154 clinical data were recorded in our database. A pri- or conventional TURP for bladder outlet obstruction had been performed in 35 patients. The TURP group consisted of patients with PCa that was incidental- ly diagnosed following TURP (Stage T1a, T1b). This group included patients who had undergone preop- erative transrectal ultrasound-guided systematic 12- core prostate biopsy because of elevated serum PSA levels, but the histopathology showed only BPH. A match-paired analysis was performed using our da- tabase to identify men without a history of TURP with equivalent clinicopathological characteristics to serve as the control group (non-TURP group). Matching criteria included, age, body mass index (BMI), Amer- ican Society of Anesthesiology (ASA) score, preop- erative serum total PSA level, preoperative Gleason score, and pelvic lymph node dissection. The patients in the control group had all undergone transrectal ul- trasound-guided biopsies demonstrating PCa. The 2002 American Joint Committee on Cancer (AJCC) TNM staging of PCa was used for both clinical and patho- logic staging. Gleason score was evaluated by dedi- cated pathologist according to the International Socie- ty of Urological Pathology (ISUP) 2005 guidelines.(9) Treatment Plan A single surgeon (X.G.) performed all of the LRPs us- ing a transperitoneal or extraperitoneal approach as de- scribed previously.(10) Pelvic lymph node dissection was performed in all patients with a serum PSA level > 10 ng/mL and/or a Gleason score > 6. Complications were evaluated according to the Clavien-Dindo Classifica- tion.(11) All of the patients underwent cystography 7-10 days after surgery. Anastomotic leakage was defined as the presence of extravasation on cystography. The catheter was removed if no extravasation was recorded. Follow-up A 3-monthly follow-up was conducted to assess long- term oncological and functional outcomes. The mean follow-up period was 57.6 months (range 30–107). Continence was evaluated using the International Con- tinence Society (ICS) questionnaire. A requirement for > 1 pad daily with normal physical activity was consid- ered incontinence. Biochemical recurrence was defined as 2 consecutive detectable serum PSA levels > 0.2 ng/ mL. No patients received adjuvant hormonal therapy or radiotherapy without a PSA level higher than 0.2 ng/mL. Match-Paired Analysis Preoperative clinicopathological characteristics (age, BMI, prostate size, clinical stage, serum PSA level, preoperative Gleason score, and continence), intraoper- ative characteristics (neurovascular bundle [NVB] pres- ervation, lymph node dissection, estimated blood loss, need for transfusion, operative time, and intraoperative complications), postoperative oncological characteris- tics (Gleason score, pathological stage, positive surgical margin [PSM] and positive lymph nodes), postoperative complications, biochemical recurrence, and continence were compared between the TURP and control groups. Statistical Analysis We compared the two groups using one-way analy- sis of variance or Student’s t test for numeric values and a chi-squared test for non-numeric values. The univariate and multivariate models were performed for urinary function in combination with time of con- tinence with a correction in imbalance factors. Pear- Parameters TURP Control P Value Group Group Patients (n) 35 35 Age (years) .56 Mean 69.9 68.9 Range 54-82 51-79 BMI (kg/m2) .883 Mean 23.2 23.2 Range 22-25.5 20.2-25.6 ASA score (n) .597 1 26 24 2 9 11 Prostate volume (mL) < .001 Mean 19.2 ± 5.6 34.4 ± 15.5 Range 10.3-37.1 11.6-76.7 Biopsy Gleason score .773 Mean 6.5 6.6 Range 4-9 4-9 PSA (ng/mL) .474 Mean 9.21 10.49 Range 0.624-20.73 1.73-26.67 Clinical T stage (n) T1a 5 T1b 30 T1c 19 T2a 14 T2b 2 Interval between TURP and LRP (weeks) Mean 7.5 Range 1-12 Access (n) .003 Transperitoneal 15 27 Extraperitoneal 20 8 Operative time (min) < .001 Mean 262 213 Range 165-370 120-305 Estimated blood loss (mL) .002 Mean 231 139 Range 100-800 50-300 Transfusions (n) 3 0 Lymphadenectomy (n) 1.0 Yes 30 30 No 5 5 Nerve sparing (n) .001 None 26 (74.3) 14 (40) Unilateral 3 (8.6) 4 (11.4) Bilateral 6 (17.1) 17 (48.6) Complications (n) 13 (37.1) 4 (11.4) .012 Minor (Clavien I-II) 9 2 Anastomosis leakage 9 2 Urinary infection 3 0 Major (Clavien III-IV) 4 2 Rectal injury 2 0 Anastomotic stricture 4 2 Abbreviations: BMI, body mass index; PSA, prostate specific antigen; ASA, American Society of Anesthesiology; TURP, transurethral resection of prostate; LRP, laparoscopic radical prostatectomy. Data in parentheses are percentages. The level of statistical significance was defined as P < .05. Table 1. Comparison of perioperative parameters between the 2 study groups. Matched-Pair Analysis of Laparoscopic Radical Prostatectomy after Previous TURP-Yang et al. Vol 12 No 03 May-June 2015 2155 son’s contingency coefficient test was performed for a correlation analysis between continence (n) and biochemical recurrence (n). The data were analyz- ed using Statistical Package for the Social Science (SPSS Inc, Chicago, Illinois, USA) version 19.0. A P value < .05 was considered statistically significant. RESULTS Patient Characteristics This study was conducted in accordance with the guide- lines of the Ethics Committee of the Third Affiliated Hospital of Sun Yat-sen University. Comparative data on the two groups are provided in Table 1. Both groups were similar in age, BMI, preoperative Gleason score, serum PSA level, and the requirement for lymphad- enectomy. A significant difference was observed be- tween prostate volume in the TURP group vs. the con- trol group (19.2 ± 5.6 vs. 34.4 ± 15.5 mL, P < .001). The mean time interval between TURP and LRP was 7.5 weeks and ranged from 1 to 12 weeks (Table 1). The mean operative time was 49 min longer for the TURP group than the control group (262 vs. 213 min, P < .001). Intraoperative blood loss data were obtained from the anesthesia records. The mean estimated blood loss was 231 mL in the TURP group compared with 139 mL in the control group (P < .001). The intraoperative blood transfusion rate was 8.6% in the TURP group, and no patient needed transfusion in the control group. A nerve-sparing procedure was performed in only 25.7% of patients in the TURP group (unilaterally in 3 and bilaterally in 6) compared with 60% of patients in the control group (unilaterally in 4 and bilaterally in 17) (P = .001). Fourteen patients (40%) in the control group chose to maximize oncological safety, and they did not undergo a nerve-sparing procedure. The days of drain- age (DD), catheterization (DC), and hospital stay (HS) was 3~5, 7~10 and 10~14 in both groups, respectively. No perioperative mortality was observed in either group. Complications A statistically significant difference in the complica- tion rate was observed between the TURP group and the control group (37.1% vs. 11.4%, P = .012). The most common complication was anastomosis leakage, which was significantly higher in the TURP group than the control group (34.3% vs. 5.7%, P = .003). Rectal injury occurred in 2 men in the TURP group. Three patients in the TURP group developed urinary infections. Anastomotic strictures developed in 4 pa- tients in the TURP group and in 2 patients in the con- trol group. However, the stricture rate between the groups was not significantly different. These patients underwent bladder neck incision as and when the stric- ture developed, and good outcomes were achieved. Oncological Results Pathological results and follow-up information are shown in Table 2. No significant difference in post-op- erative Gleason scores was observed between the two groups. The percentage of Gleason scores ≥ 8 in the TURP group was somewhat higher than the con- trol group, but this difference was not significantly different. PSM was defined as the presence of tumor cells at the inked surface of the resected specimen. The overall PSM rate was 34.3% for the TURP group compared with 20% for the control group (P = .179). Eight patients in the TURP group had positive nodes compared with 4 patients in control group. These pa- tients were immediately started on hormonal ablation. There were no biochemical recurrence cases in 3 months postoperatively. Biochemical recurrence occurred in 6 and 4 patients in the TURP group and control group, re- spectively, after a mean follow-up of 57.6 months (range 30–107). Only 1 patient in the TURP group died of PCa. Parameters TURP Group Control Group P Value Post-operative Gleason score .569 Mean 6.9 6.7 Range 4-9 4-9 Gleason score group .466 ≤ 6 14 (40) 14 (40) 7 8 (22.9) 12 (34.3) ≥ 8 13 (37.1) 9 (25.7) PSM (n) 12 (34.3) 7 (20) .179 pT2 2 3 pT3a 5 3 pT3b 3 1 pT4 2 0 Nodes positive (n) 8 (22.9) 4 (11.4) .205 Pathological T stage (n) .127 T2 25 (71.4) 30 (85.7) T3a 5 (14.3) 3 (8.6) T3b 3 (8.6) 1 (2.9) T4 2 (5.7) 1 (2.9) Biochemical recurrence (n) 6 (17.1) 4 (11.4) .495 Prostate cancer-specific mortality (n) 1 0 1.0 Continence at last follow-up (n) 30 (85.7) 33 (94.3) .428 Abbreviations: PSM, positive surgical margin; TURP, transurethral resection of prostate. Data in parentheses are percentages. The level of statistical significance was defined as P < .05. Table 2. Pathological results and follow-up information of the 2 study groups. Matched-Pair Analysis of Laparoscopic Radical Prostatectomy after Previous TURP-Yang et al. Laparoscopic Urology 2156 Functional Results All of the patients were continent preoperatively. The continence rates at 3 months were significantly higher in the control group than in the TURP group (68.6% vs. 42.9%, P = .03). However, no statistically significant difference was found between the 2 groups at 12 months after LRP. At last follow-up, continence was achieved in 85.7% of patients in the TURP group and in 94.3% of pa- tients in the control group. Univariate (hazard ratio [HR] = 1.355, 95% confidence interval [CI]: 0.823-2.232, P = .233) and multivariate (HR = 1.324, 95% CI: 0.654- 2.677, P = .435) analysis showed that there were no sig- nificant difference in urinary continence between the 2 groups. Besides, Pearson’s contingency coefficient test showed that the correlation was not significant between urinary continence and biochemical recurrence status. DISCUSSION The relative paucity of PCa patients who have un- dergone a previous TURP makes any comparative analysis somewhat difficult. However, several stud- ies on this subject have been reported. Most of these studies have focused only on histopathological or surgical results rather than long-term oncological re- sults and functional outcomes. Our literature review did identify few studies that addressed LRP after pre- vious TURP in Chinese patients. The present study used a matched-pair design to compare the periop- erative, oncological, and functional results of LRP in Chinese patients with and without previous TURP. TURP results in periprostatic edema, inflammation and fibrosis, and distortion of the proper surgical plane, which increases the difficulties of subsequent procedures. Therefore, the optimal time interval be- tween TURP and LRP is theoretically when the reac- tive inflammation and fibrosis is lightest. Elder and colleagues(12) recommended performing surgery either during the first month after TURP or to wait until 4 months after TURP. Zugor and colleagues(6) suggest- ed a time interval between TURP and RP of at least 3 months in an attempt to decrease the amount of possi- ble postoperative inflammation. The mean time inter- val between TURP and LRP was 7.5 weeks (range 1 to 12 weeks) in this study, which is a shorter interval than the time recommended previously. We found that the periprostatic edema in this interval was indeed se- vere in some cases. However, the optimal time inter- val was impossible to evaluate in this study because no LRP was performed later than 3 months after TURP. Several studies reported that surgical procedures after TURP are challenging.(2,8,13,14) To our expe- rience, there are several concerns during the pro- cedure with respect to the post TURP scenario. (i) It is difficult to identify the prostatovesicular junc- tion after the removal of prostatic tissue during TURP. (ii) Urethrovesical anastomosis becomes technically difficult after previous TURP because of rigidity of the bladder neck and the loss of elasticity in the ure- thra.(13) (iii) The need for bladder neck reconstruction is increased because preservation of the bladder neck after TURP is difficult. Katz and colleagues(13) did not attempt to preserve the bladder neck but instead made a wide incision and redesigned the bladder neck in the form of a racket handle to increase the distance between the ureteral orifices and the region of the urethrovesical anastomosis. (iv) Posterior dissection is difficult, which increases the risk of rectal injury because of peripros- tatic adhesions and fibrosis. (v) The tumor that is diag- nosed by TURP chips was usually located in the tran- sitional zone. Therefore, seminal vesicular involvement may be increased because a transitional zone tumor may spread easily via the ejaculatory ducts. (vi) The risk of anastomotic leakage and incontinence may be increased because the bladder neck becomes thickened, fibrotic, and rigid after previous TURP. (vii) The NVBs were less dissociable from the prostatic capsule after previous TURP because of periprostatic adhesions. The influence of previous prostate surgery on the out- come of radical prostatectomy remains controversial, except for the intraoperative difficulties.(8,15) One pro- posed hypothesis is that previous TURP increases intra- operative and postoperative morbidity and complicates oncological and functional outcomes in patients under- going LRP because of the difficult dissection resulting from the obscured planes caused by periprostatic inflam- mation and fibrosis. The existing literature suggests that relatively poorer outcomes are achieved in men with previous prostatic surgery.(16,17) One study of 117 pa- tients reported that patients with a history of TURP who underwent LRP had worse outcomes of operative time, overall complication rate, and functional outcomes.(2) However, several previous studies demonstrated that although surgery may be technically more difficult, overall morbidity and long-term functional or oncolog- ical outcomes are not compromised.(1,7,13,18) Our study encountered longer operative times, greater intraopera- tive blood loss, and higher blood transfusion rates in the TURP group. These results may be attributed to the ex- travasation of blood and fluid irrigation during TURP, which resulted in periprostatic fibrosis and obscured the proper planes between tissues. The preoperative biopsy also induces some inflammatory and fibrotic reactions in and around the prostate, but these reactions are much lighter than TURP-induced reactions.(19) Anastomotic leakage rates were much higher in the TURP group. Jaffe and colleagues(2) found that patients with previous TURP had a significantly higher rate of anastomotic leakage (15.1%) following LRP than patients without previous surgery (6.7%). One possible explanation is that the scarring and fibrosis of the previously resected bladder neck complicates healing at the anastomosis. Some studies demonstrated that NVB preservation was technically feasible in approximately 33% to 56.5% of LRP patients after TURP.(1,18) The isolation and preser- vation of NVB in our study was technically feasible in only 25.7% of patients in the TURP group compared to 60% in the control group. As reported by Colombo and colleagues,(19) this reduced preservation may result from the more difficult dissection of the NVBs because of periprostatic fibrosis. Nerve-sparing techniques maybe have a significant effect on urinary continence because the autonomic nerve fibers from the pelvic plexus in- nervate the sphincteric mechanism.(20,21) Do and col- leagues(22) investigated a series of 100 patients who had undergone LRP after previous TURP and showed that 93% of patients were continent at 12 months, but data of NVB preservation were not shown. Teber and colleagues demonstrated that previous TURP was as- sociated with a lower continence rate than the control group at 3 months (49.1% vs. 61.8%).(23) Similar out- comes were encountered in our study. Therefore, pa- tients with a history of TURP should be informed of the potential risk of delayed continence before surgery. Matched-Pair Analysis of Laparoscopic Radical Prostatectomy after Previous TURP-Yang et al. Vol 12 No 03 May-June 2015 2157 Several studies reported higher PSM rates (21.8%– 34.2%) in patients who underwent LRP after TURP. (2,8) Katz and colleagues(8) noted positive margins in 12 of 35 patients who underwent LRP after previous TURP, including 22.2% of patients with pT2 and 75% of patients with pT3. Jaffe and colleagues(2) reported a greater overall PSM rate after TURP, but they did not detail the pathological stage. In contrast, other studies did not detect these differences.(1) Our study found no significant difference between the two groups. One possible explanation for the somewhat higher PSM rate in the current series is the difficulty in the iden- tification of the proper surgical planes because of periprostatic inflammation and fibrosis after TURP. (24) PSMs were associated with biochemical progres- sion in 21% to 30.8% of patients, depending on the location of the positive margins.(25) Our study found a higher biochemical recurrence rate in the TURP group than the control group (17.1% vs. 11.4%, respective- ly, P = .495) after a mean follow-up of 57.6 months, but this difference was not statistically significant. This result may be explained by the higher PSM rate, higher lymph-positive rate, and the greater percentage of cases with Gleason scores ≥ 8 in the TURP group. These findings should be interpreted within the context of the limitations of our study. There was a statistical- ly significant difference in clinical stage between the two groups. However, 94.3% of patients in the control group had a T stage ≤ T2a. This difference could poten- tially limit the study. However, we believe that the re- sults were not affected, because T stage ≤ T2a would be grouped as low risk according to the D’Amico classifi- cation. The time interval between TURP and LRP was not standardized because this study was a retrospective review. This factor may limit the results of the study. The procedural approach is another potential limitation of the study. LRP was transperitoneally performed in 42.9% and 77.1% of patients in the TURP group and control group, respectively. However, a previous study reported that these two techniques exhibited equivalent perioperative, oncological and functional results.(26) Therefore, this fact does not likely limit the findings in this study. Still, we have to acknowledge that a matched- pair analysis has certain limitations in this study and a relatively low number of total patients in both groups also may reduce the persuasion of research results. Besides, quality of life questionnaire (such as conti- nence) for patients was also influenced by many factors. CONCLUSION Previous TURP may cause technical difficulties during LRP. LRP after TURP is associated with a longer op- erating time, greater blood loss, difficult NVB preser- vation, a higher rate of anastomosis leakage and worse short-term continence outcomes compared to TURP naïve cases. The follow-up data suggest that LRP after TURP can be safely performed without compromis- ing the radical nature of cancer surgery and long-term continence rate. However, patients should be informed of these potential risks before undergoing LRP. ACKNOWLEDGMENTS The authors acknowledge financial support received from the National Natural Science Foundation of China (81201694), the Reserve Personnel Plan of the Third Affiliated Hospital of Sun Yat-sen Univer- sity, the Science and Technology Planning Project of Guangdong Province (2014A020212160) and the Specialized Research Fund for the Doctoral Program of Higher Education of China (20120171120059). CONFLICTS OF INTEREST None declared. REFERENCES 1. Menard J, de la Taille A, Hoznek A, et al. 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