Patient-reported Sexual Function After Nerve-sparing Radical Retropubic Prostatectomy

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1 European Urology European Urology 42 (2002) 118±124 Patient-reported Sexual Function After Nerve-sparing Radical Retropubic Prostatectomy Joachim Noldus *, Uwe Michl, Markus Graefen, Alexander Haese, Peter Hammerer, Hartwig Huland Department of Urology, University of Hamburg, Martinistrasse 52, Hamburg, Germany Accepted 26 April 2002 Abstract Objective: Improved selection criteria have lead to an increasing number of nerve-sparing radical retropubic prostatectomies (RRP) in patients with clinically localised prostate cancer (PCA). Patient questionnaire based outcome analysis on post-operative erectile function after uni- or bilateral nerve-sparing RRP is described. Methods: Between January 1992 and March 1999, 366 patients (mean age 62.5 years) underwent uni- or bilateral nerve-sparing RRP at our institution. Indication for nerve-sparing procedure was based on the results of a multivariate classi cation and regression tree analysis (CART). For evaluation of post-operative patient-reported rates of sexual and erectile function non-validated and validated questionnaires (IIEF 5) were administered after a follow-up of 12 months. Data of ve operation periods were analysed. Results: The unilateral procedure resulted in rates of 13±29% of erections suf cient for unassisted intercourse. Some degree of tumescence was reported by 37±73% of the remaining patients. Bilateral nerve-sparing procedures were almost exclusively performed in periods 3±5, only four patients of period 2 received the bilateral procedure. Here, rates of erections suf cient for intercourse were 25% (period 2), 61% (period 3), 50% (period 4), and 52% (period 5), respectively. Patients with grades 4 and 5 erections had IIEF scores of 19.2 and 20.2 and patients without rigidity or tumescence had scores of 5.7 and 7.0 after uni- and bilateral nerve-sparing procedure, respectively. Patients <60 years of age had better erections than those 60 (unilateral: 19% versus 13%, bilateral 45% versus 38%). Conclusion: Compared to a unilateral nerve-sparing procedure, the bilateral nerve-sparing technique revealed much better results inasmuch as about 50% of the patients reported recovery of erections suf cient for sexual intercourse without use of sexual aids. # 2002 Elsevier Science B.V. All rights reserved. Keywords: Erectile function; Prostate cancer; Radical prostatectomy; Questionnaire 1. Introduction Radical prostatectomy is one therapeutic option to effectively treat patients with clinically localised (T1, T2) prostate cancer. Improved patient and tumour selection as well as standardisation of the surgical procedure have not only lead to a decrease in preand post-operative morbidity but also to an increasing * Corresponding author. Tel ; Fax: address: noldus@uke.uni-hamburg.de (J. Noldus). number of nerve-sparing procedures [1,2]. Despite these improvements, many patients experience erectile dysfunction post-operatively either due to the local tumour extent which does not allow nerve sparing or due to the surgical technique itself. Experienced high output centres report on high potency rates with clear correlation to age and number of excised neurovascular bundles [3,4]. From post-operative evaluation of female incontinence surgery, it is known that in studies using retrospective chart analysis higher success rates are reported than from those using patient questionnaire based outcome analysis [5]; hence, a false positive bias is reported which does not re ect the true outcome /02/$ ± see front matter # 2002 Elsevier Science B.V. All rights reserved. PII: S (02)

2 J. Noldus et al. / European Urology 42 (2002) 118± This retrospective study presents patient-reported data on unassisted erectile function of 366 men after uni- or bilateral nerve-sparing radical retropubic prostatectomy (RRP). To our knowledge it is the only European study and the largest single-centre study using exclusively a patient questionnaire based outcome analysis. 2. Materials and methods Between January 1992 and March 1999, 1213 patients with clinically localised prostate cancer underwent RRP at our institution; of these, 366 (30%) had a nerve-sparing procedure. Histological parameters of all patients are presented in Table 1. Mean age of the patients was 62.5 years (range 42±74 years.). The pre-operative evaluation included serum prostate speci c antigen (PSA) determination with its molecular subforms, digital rectal examination, and transrectal ultrasound with guided systematic sextant biopsies; 79% of these biopsies were performed at our department. Bone scan was performed only if PSA was above 10 ng/ml. Nerve-sparing procedure was applied only to pre-operatively potent and sexually active patients; therefore patients were interviewed by the physician and potency was de ned as having erections hard enough to penetrate and maintain through sexual intercourse. Sexual activity was de ned as having sexual intercourse on a regular basis. Until April 1997, nerve-sparing procedure was based exclusively on the results of the prostate biopsies [6]: unilateral sparing of the neurovascular bundle was only performed if one side of the prostate was free of cancer by three negative biopsies from the apex, mid, and base. This selection criterion proved to be very safe in terms of positive surgical margins but also very strict, with a retrospectively performed analysis of the specimens showing many pt2 cancers which were excluded from a nerve-sparing procedure. Later, selection criteria were improved and changed on the basis of a multivariate tree structured regression analysis (CART) including nine preoperative parameters which predicted an organ-con ned cancer with an accuracy of 86% [7]. From that time, the extent of preservation of the neurovascular bundles (uni- or bilateral nerve-sparing procedure) was planned by the surgeon on the basis of this analysis. The nerve-sparing RRP was performed in the technique described elsewhere [2]. All prostate specimens were processed as described earlier by McNeal et al. [8]. Cancer staging and grading was performed in accordance with the fth edition of the TNMclassi cation [9] and the Gleason grading system [10]. Table 1 Histological parameters of RRP specimens after unilateral (n1rrp) and bilateral (n2rrp) (n ˆ 366) between January 1992 and March 1999 divided by ve operation periods Periods n1rrp n2rrp pt2 pt3 Positive margin pt2 pt ± a ± a ± a a No n2rrp was performed. Positive margin Table 2 Operation periods and number of patients who underwent nerve-sparing RRP between January 1992 and March 1999 Periods Time n 1 January 1992 to March April 1996 to March April 1997 to March April 1998 to October November 1998 to March Sum 366 Patients with a minimum follow-up of 12 months were included in this study. All patients received a non-validated questionnaire; patients of periods 4 and 5 additionally received a validated questionnaire according to the International Index of Erectile Function (IIEF 5) by mail to assess erectile and sexual function (Appendices A and B). The degree of unassisted erections or tumescences was classi ed into six grades from 0 ˆ no tumescence to 5 ˆ full rigidity [11]. Grades 4 and 5 were considered as satisfactory for sexual intercourse. Five consecutive operation periods were separately evaluated (Table 2), since the nerve-sparing technique has been slightly modi ed between the periods. The modi cations concerned the handling of the dorsal vein complex which is now sutured with two sutures of 3-0 PDS UR-6. With this technique the underlying striated sphincter muscle is best preserved. Moreover, we strictly avoid coagulation close to the neuro-vascular bundles and use headlight and magni cation loops. The nervesparing procedure itself is performed as described by Walsh [2]. 3. Results 3.1. Period 1 One hundred and three patients underwent unilateral nerve-sparing RRP, no bilateral nerve-sparing was performed. Eighty- ve men (82%) returned their questionnaires of which 53% reported on either tumescence or rigidity (grades 1±5). 16% reported erections suf cient for sexual intercourse (Table 3a) Period 2 Out of 57, 47 men (83%) returned their questionnaires. Forty-three received unilateral nerve-sparing procedures. Contrary to our indication for bilateral procedure at that time, four men underwent bilateral nerve-sparing RRP because tumour amount was estimated as being minimal on pre-operative systematic biopsies. 76% reported on tumescence or rigidity, however, erections suf cient for sexual intercourse were reported by 14% of the unilateral and 25% (one man) of the bilateral nerve-spared patients (Table 3a and b) Period 3 Eighty-four patients received a nerve-sparing RRP, of whom 73 men (87%) returned their questionnaires. Sixty (82%) received a unilateral and 13 (18%) a

3 120 J. Noldus et al. / European Urology 42 (2002) 118±124 Table 3 Questionnaire based analysis of erectile function Periods Grade 0 Grades 1±3 Grades 4±5 n % n % n % (a) After unilateral RRP (n ˆ 229) between January 1992 and March 1999 divided by 5 operation periods Sum (b) After bilateral RRP (n ˆ 60) between January 1992 and March 1999 divided by 5 operation periods (no bilateral procedures were performed in period 1) 1 ± ± ± ± ± ± Sum bilateral nerve-sparing procedure. None of the patients with pt3 cancer had involvement of the seminal vesicles, one had bladder neck in ltration by the tumour. Positive lymph nodes on nal pathology were seen in two patients which were negative grossly and in intraoperative frozen section. Only 15% of the patients with unilateral nerve sparing reported erections suf cient for intercourse (grades 4 and 5), however, 88% reported on either tumescence or rigidity (grades 1±5) (Table 3a). Bilateral nerve sparing revealed grades 4 and 5 rigidity in 61% (8/13), the remaining ve patients had some degree of tumescences (Table 3b) Period 4 Within 6 months, 63 patients underwent nervesparing RRP. Evaluated were 24 men after unilateral nerve-sparing procedure and 18 after bilateral nervesparing RRP (questionnaire returning rate of 67%). Two patients had positive lymph nodes on the nal pathology. Only 13% (n ˆ 3) of the men after unilateral nerve sparing had grades 4 and 5 rigidity and were able to have unassisted sexual intercourse, however, 62% (n ˆ 15) had either tumescence or rigidity. 25% (n ˆ 6) had no tumescence (grade ˆ 0) (Table 3a). Out of the 18 patients, 9 (50%) after the bilateral procedure had grade 4 and 5 erections, two patients (11%) had no tumescence (grade 0) (Table 3b) Period 5 Forty two of 59 patients (71%) who were operated on in this most recent period were evaluated, with 32 (54%) having a bilateral procedure. 29% (n ˆ 5 of 17) of the men after unilateral procedure and 52% (n ˆ 13 of 25) after bilateral nerve-sparing RRP reported on erections suf cient for intercourse (Table 3a and b) Results of IIEF questionnaires Patients of periods 4 and 5 additionally received the validated IIEF 5 questionnaire scored out of 25 points. Men who had good erections (grades 4 and 5) had a higher score (mean 19.9; unilateral 19.2, bilateral 20.2) than those with or without tumescence (mean 5.7; unilateral 5.2, bilateral 7.0) Age-dependent results Patients were divided into younger than 60 years of age and 60 years. Irrespective of the operation periods and the extent of nerve sparing, younger patients more frequently had an erection suf cient for sexual intercourse than those who were 60 years and older (unilateral, 19% versus 13%; bilateral, 45% versus 38%) Capability of orgasm With the non-validated questionnaire, men were also asked of their capability to reach orgasm and whether they noticed a change in experience of climax. Independent of the operation periods and whether they were potent or not, 80% of the men had an unchanged, 9% improved, and 11% decreased experience of orgasmic function. 4. Discussion Data from the National Cancer Data Base and from Europe have recently shown an increase of pathologically localised stages of prostate cancer after radical

4 J. Noldus et al. / European Urology 42 (2002) 118± prostatectomy [12,13]. This phenomenon paved the way for more nerve-sparing procedures performed during radical prostatectomies. Additionally, preservation of erectile function is increasingly an important concern of patients and often affects their choice of treatment. At our institution, 366 of 1213 patients underwent either unilateral or bilateral nerve-sparing radical retropubic prostatectomy within 7.25 years. All received questionnaires to assess their post-operative erectile and sexual function. Overall, 76% returned their questionnaires and were evaluated, no data were collected by telephone or direct contact during follow-up visits. Data of the non-validated questionnaires revealed different results after uni- and bilateral nerve-sparing procedure. Overall, unilateral nerve sparing led to a rate of 69% tumescence/rigidity (grades 1±5), while bilateral nerve sparing revealed 93%. Unassisted erections satisfactory for intercourse were achieved by only 13±16% of the patients after unilateral nerve-sparing RRP in periods 1±4, while 50±60% of the men after bilateral nerve-sparing RRP had unassisted grade 4 and 5 erections; however, in period 5 we noted an increase in grade 4 and 5 erections after unilateral procedure (29%). The extent of nerve sparing alters the post-operative rate of erections. In an early report from the Johns Hopkins University, Quinlan et al. published a 58% potency rate when one neurovascular bundle was excised versus 82% when both were intact [14]. Catalona et al. reported on a 68% recovery of erections after bilateral and 47% after unilateral nerve-sparing surgery [15]. Gralnek et al. reported a 39% potency rate in 46 men after sparing of one neurovascular bundle based on questionnaire approved by the Human Subjects Committee of the University of Arizona [16]. In a very recent study by Rabbani et al. reporting on factors predicting the recovery of erectile function after RRP, 21% with unilateral neurovascular bundle preservation had erection suf cient for intercourse [17]. Geary et al. from Stanford University reported a 15% rate of erection after preserving one bundle [18], Fowler et al. reported on only 11% of patients with erections after unilateral nerve sparing [19]. In summary, the literature reveals a wide range of potency rates after unilateral nerve sparing. However, the more recent data showed potency rates of only about 20%. These data are supported by a multivariate Cox proportional hazards analysis showing a 25% chance of recovering erections after unilateral nerve-sparing RRP compared to preserving both nerves [17], an important fact when counselling patients before RRP. In parts, the great difference in outcome after uniand bilateral nerve sparing can be explained, however, when examining the results after bilateral nerve-sparing procedure results are more favourable, though a wide range of erectile function rates is reported here as well. We report of relatively consistent rates of about 50±60%. Similar results have been reported by many centres [4,15,17]. Geary et al. reported a somewhat lower rate of 31% [18]. Walsh et al. recently published data on patient-reported sexual function by a validated questionnaire which were administered to 64 patients [20]. In 89% of these patients a bilateral preservation of the neurovascular bundles were performed and after a follow-up of 12 months, 72% reported of having erections satisfactory for intercourse; however, 33% of these men additionally used Sildena l. It is apparent that recovery of erections is a function of time and may occur after more than 1 year following nerve-sparing RRP, a longer duration than generally recognised. Walsh et al. reported an improvement of potency of 72±86% between 12 and 18 months post-operatively [20]. In the series by Rabbani et al., 75% of the men who were potent regained potency after 11.8 months, i.e. 25% of the men had recovery of erection after that time [17]; however, after 30 months of follow-up the Kaplan± Meier curves level which is also important to note when counselling patients before and after nerve-sparing RRP. The results from our 12 months post-operative evaluation may therefore improve when re-evaluated at 18 months post-operatively or even later. Recovery of potency seemed to be age related which was initially recognised by Walsh and Donker in 1982 [21], and has since been consistently reported in other series [15±18]. Several years later, a large series from the Johns Hopkins University con rmed these early data [14], in young patients <50 years of age there seemed to be no difference in potency rates regarding the extent of nerve sparing, between 50 and 60 years not only the overall potency rate declined but also whether one or both neurovascular bundles were preserved had a strong impact on recovery of erectile function; patients 70 years or older had only tumescence when unilateral nerve sparing was performed and those with bilateral nerve sparing had full erections in only 22%. Catalona et al. and Rabbani et al. reported on similar results [15,17]. Our data did not reveal such differences in potency rates which might be due to the simple distribution of patients into <60 and 60 years of age. Further parameters seemed to in uence the postoperative erectile outcome: (1) The quality of pre-operative erections proved to be an independent predictor of erectile recovery rather than frequency of sexual intercourse on multivariate

5 122 J. Noldus et al. / European Urology 42 (2002) 118±124 analysis [17]. Geary et al. could show that patients whose potency recovered post-operatively were more often sexually active pre-operatively [18]. (2) Whether pathological stage has an in uence on post-operative potency remains unclear which might be also in uenced by the statistical method used. On univariate analysis pathological stage was recognised as signi cant predictor which was not the case in a multivariate analysis [15,17]. In the multivariate analysis performed by Rabbani et al., they divided patients into extracapsular extension, seminal vesical invasion, and lymph node metastasis versus organ con ned status and did not nd signi cance ( p ˆ 0:10, 0.67, and 0.55) [17]. On the contrary, Geary et al. found cancer volume to be an independent predictor ( p ˆ 0:047) of recovery of potency but not for positive margin and capsular penetration on multivariate analysis [18]; they found that potent patients had smaller cancers probably due to patient and tumour selection [18]. (3) The experience of the surgeon and the fact whether one or more surgeons performed the prostatectomy series might be another in uencing factor [15,17,18,20,22]; a multicenter study revealed a postoperative potency rate of 10.6% [22] and clearly shows the discrepancy to the aforementioned rates of potency by single-surgeon centres [15,17,18,20]. Catalona et al. could show that with increasing number of performed nerve-sparing procedures, post-operative potency rate increased (61% for less than 500 cases, 68% for 500± 1000 cases, and 70% for 1000±1500 cases) [15]. Atour institution, more than 50% of all nerve-sparing procedures were performed by one surgeon (H.H.), the remaining by another four full-time faculties. All results might be in uenced by the method of data collection (Table 4); to rule out in uencing factors by the interviewing surgeon or nurse, we applied questionnaires to our patients. It is a known fact that studies using a retrospective chart review or interview usually report higher success rates, and those using patient questionnaire based outcome analysis had dramatically lower success rates [5]. This problem was recognised by many authors who admitted this weakness in their way of data collection [5,15,17]; however, on the AUA conference in 1999 Walsh et al. presented data with total consistency between patient- and physicianreported outcomes explaining the phenomenon: ``if patients are asked about their outcome with the intention of helping to improve it, they honestly report their status'' [23]. In the year 2000, three studies on erectile function after nerve-sparing RRP based on questionnaires were published [16,20,22]; two single-centre studies included 64 [20] and 170 [16] men, respectively; the third and largest multicentre study reported on 1396 patients [22]. To our knowledge, our study reports on the largest single-centre series with exclusively questionnaire based erectile outcome after nerve-sparing RRP. We mailed an addressed, stamped return envelope and a non-validated questionnaire to all our 366 patients; patients from the two most recent periods (4 and 5) additionally received the validated IIEF 5 questionnaire, the short form (questions 1, 2, 4, 5, and 7) of the 15 questions enclosing IIEF questionnaire [24]. These questions cover not only the topic of erections but also the aspect of quality of life. Not surprisingly, patients who had erections suf cient for intercourse had in average higher scores (19.9) than those whose erections were not suf cient for sexual intercourse (5.7). Since April 1999, for comparison reason to other series all our patients receive the validated questionnaire only. To better objectify pre- Table 4 Studies investigating post-operative erectile function after nerve-sparing RRP Authors Year n a Single/multi centre Questionnaire based n1rrp/ n2rrp b Age analysis Follow-up over time c Classi cation of erections d Quinlan et al. [14] Single No Yes Yes Yes No Geary et al. [18] Single No Yes Yes No No Catalona et al. [15] Single Yes f Yes Yes No No Walsh et al. [20] Single Yes No Yes Yes No Kao et al. [22] 2000? e Multi Yes? No No No Gralnek et al. [16] Single Yes No No No No Rabbani et al. [17] Single No Yes Yes Yes No Present study Single Yes Yes Yes No Yes a Patients who received nerve-sparing procedure. b Differentiation between uni-and bilateral nerve sparing. c Sexual function was evaluated over several months. d According to [11]. e Study does not separate nerve-sparing and non-nerve-sparing techniques. f Patients were interviewed or received questionnaires or were contacted by telephone.

6 J. Noldus et al. / European Urology 42 (2002) 118± operative baseline erections, the IIEF 5 questionnaire is now mailed pre-operatively to our patients which was suggested also by Rabbani et al. [17]. In the nonvalidated questionnaire, we additionally asked men about their experience of climax, a parameter none of the aforementioned questionnaire based studies covered [16,20,22]. Interestingly, 9% reported an improved experience of orgasm while 80% did not recognise a change in comparison to the pre-operative status. Furthermore, many of the patients report about ejaculation of urine during orgasm. 5. Conclusions This study con rms that recovery of erections depends on the extent of preservation of the neurovascular bundles and showed a slight age dependency. A high rate of men reported on tumescences which were not suf cient for unassisted intercourse; however, those men with presumably partly intact neurovascular structures might bene t from assisting drugs like Sildena l. Appendix A. Non-validated questionnaire for assessing erectile and sexual function Q1 Q2 Q3 Did you get unassisted tumescences or erections post-operatively? 0 ˆ no tumescence and no erection 1 ˆ slight tumescence 2 ˆ medium tumescence 3 ˆ complete tumescence with no rigidity 4 ˆ complete tumescence with medium rigidity 5 ˆ complete rigidity/erection When you had erections pre-operatively were these: good decreased not suf cient for sexual intercourse? Did you experience orgasm/climax: unchanged improved decreased post-operatively? Appendix B. Validated IIEF 5 questionnaire for assessing erectile and sexual function Q1 Q2 Q3 Q4 Q5 How often were you able to get an erection during sexual activity? 0 ˆ no sexual activity When you had erections with sexual stimulation, how often were your erections hard enough for penetration? 0 ˆ no sexual activity During sexual intercourse, how often were you able to maintain your erections after you had penetrated (entered) your partner? 0 ˆ did not attempt intercourse During sexual intercourse, how dif cult was it to maintain your erection to completion of intercourse? 0 ˆ did not attempt intercourse 1 ˆ extremely dif cult 2 ˆ very dif cult 3 ˆ dif cult 4 ˆ slightly dif cult 5 ˆ not dif cult When you attempted sexual intercourse, how often was it satisfactory for you? 0 ˆ did not attempt intercourse References [1] Thompson IM, Middelton RG, Optenberg SA, Austenfeld MS, Smalley SR, Cooner WH, et al. Have complication rates decreased after treatment for localized prostate cancer? J Urol 1999;62: 107±12. [2] Walsh PC. Anatomic radical prostatectomy: Evolution of the surgical technique. J Urol 1998;160:2418±24. [3] Catalona WJ, Bigg SW. Nerve-sparing radical prostatectomy: Evaluation of results after 250 patients. J Urol 1990;143:538±44.

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