Naoki Wada, Seiji Matsumoto, Masafumi Kita, Kazumi Hashizume and Hidehiro Kakizaki

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1 bs_bs_banner International Journal of Urology (1) 1, 15 1 doi: /iju.157 Original Article: Clinical Investigation Decreased urinary nerve growth factor reflects prostatic volume reduction and relief of outlet obstruction in patients with benign prostatic enlargement treated with dutasteride Naoki Wada, Seiji Matsumoto, Masafumi Kita, Kazumi Hashizume and Hidehiro Kakizaki Department of Renal and Urologic Surgery, Asahikawa Medical University, Asahikawa, Japan Abbreviations & Acronyms BCI = bladder contractility index BOO = bladder outlet obstruction BOOI = bladder outlet obstruction index BPE = benign prostatic enlargement Cre = creatinine DO = detrusor overactivity IPSS = International Prostate Symptom Score LUTS = lower urinary tract symptoms MCC = maximum cystometric capacity NGF = nerve growth factor OAB = overactive bladder PdetQmax = detrusor pressure at maximum flow rate PV = prostatic volume Correspondence: Naoki Wada M.D., Ph.D., Department of Renal and Urologic Surgery, Asahikawa Medical University, Midorigaoka Higashi, Asahikawa 7-51, Japan. nwada@asahikawa -med.ac.jp Received April 1; accepted 17 June 1. Online publication 15 July 1 Objectives: To examine urinary nerve growth factor before and after dutasteride treatment, and to analyze correlations between clinical parameters and change of urinary nerve growth factor in patients with benign prostatic enlargement. Methods: We prospectively studied 3 patients with benign prostatic enlargement who had not been satisfied with α-adrenergic antagonist monotherapy for more than 3 months. Before and weeks after dutasteride add-on treatment, we assessed International Prostate Symptom Score, prostatic volume, filling cystometry and pressure-flow study. Urinary nerve growth factor was measured by enzyme-linked immunosorbent assay, and normalized to the urinary creatinine (nerve growth factor/creatinine) before and weeks after dutasteride add-on treatment. Results: In baseline characteristics before dutasteride, there was no significant correlation between urinary nerve growth factor/creatinine and any clinical parameters including age, International Prostate Symptom Score, prostatic volume, presence of detrusor overactivity, detrusor pressure at maximum flow rate, bladder outlet obstruction index or bladder contractility index. Dutasteride significantly reduced prostatic volume (from ± 31 ml to 9 ± ml) and improved International Prostate Symptom Score (from 17. ±.7 to 13.1 ±.), storage (from. ±.3 to. ±.9) and voiding symptom subscore of International Prostate Symptom Score (from 9.3 ± 5.7 to 7.1 ±.5). In urodynamic study, detrusor pressure at maximum flow rate (from 77 ± 3 cmh Oto59± cmh O) and bladder outlet obstruction index (from ± 3 to ± 7) were significantly decreased after dutasteride treatment. Urinary nerve growth factor/creatinine was significantly decreased after dutasteride from.1 ±.5 to 1. ± 1.. The change of urinary nerve growth factor/ creatinine significantly correlated only with the change of prostatic volume (r =.3) and bladder outlet obstruction index (r =.3). Conclusions: Urinary nerve growth factor decreases in association with reduction of prostatic volume and relief of bladder outlet obstruction. Urinary nerve growth factor might be useful as a biomarker to monitor the improvement of bladder outlet obstruction in patients with benign prostatic enlargement. Key words: benign prostatic hyperplasia, dutasteride, lower urinary tract symptoms, nerve growth factor. Introduction NGF was discovered and explored in the regulation of the developing nervous system by Stanley Cohen and Rita Levi-Montalcini, Nobel prize winners in In the bladder, NGF is produced by detrusor smooth muscle cells and urothelial cells. This substance is known to be necessary to promote the growth and survival of sympathetic and sensory nerves, which are vital for normal bladder function. Increased expression of NGF in the bladder was reported to be associated with storage symptoms in patients with LUTS. Recent clinical studies investigated the utility of urinary NGF level as a potential biomarker in patients with OAB and interstitial cystitis. 3 Some of those studies also showed that urinary NGF level was significantly lower in responders to medical therapy for OAB symptoms than in non-responders., However, in male patients, prostatic enlargement and corresponding obstruction complicate the pathophysiology of OAB. Clinical research on the diagnostic value of urinary NGF in male patients with LUTS could increase our understanding of the pathophysiology of male LUTS and contribute to better management The Japanese Urological Association

2 Dutasteride and urinary NGF It is well known that in male patients with BPE, OAB and/or DO is induced secondarily by BOO. Medical and surgical treatment of BOO often resolves OAB and/or DO. Dutasteride, a 5α-reductase inhibitor, reduces PV and improves both voiding and storage symptoms. 9,1 Our previous study with urodynamics showed that in patients with BPE, dutasteride could relieve BOO and improve bladder storage function. 11 In the present study, we measured the urinary NGF level before and after dutasteride treatment, and analyzed if clinical parameters including urodynamics correlated with the change of urinary NGF levels. Methods The present study was approved by the Asahikawa Medical University Ethical Committee, and was carried out in accordance with the principles of the Declaration of Helsinki. Each patient was informed of the nature and purpose of the study, and informed consent was obtained. A prospective study was carried out in patients with BPE who had not been satisfied with α-adrenergic antagonist monotherapy. Inclusion criteria were PV 3 ml and IPSS or quality of life index 3 under administration of any α-adrenergic antagonist (for more than 3 months) without anticholinergic agent. PV was measured by transabdominal ultrasonography. Before and weeks after dutasteride (.5 mg daily) add-on treatment with preceding α-adrenergic antagonist, we assessed IPSS, filling cystometry and PFS. The dose of alpha-adrenergic antagonist was not changed during the -week study period. Before and weeks after dutasteride, we collected urine samples from each patient at normal desire to void. The samples were frozen at C and kept until analysis. Just before analysis, frozen samples were thawed at room temperature and centrifuged at 5 g for 1 min. A small aliquot of urine from each participant was analyzed for creatinine concentration using a fluorescence autoanalyzer. The urine sample was diluted with four volumes of Dulbecco s phosphate-buffered saline (KCl,.%; NaCl,.%; KH PO,.%; Na HPO,.115%; CaCl H O,.133%; MgCl H O,.1%; ph 7.35). The samples were acidified by 1N HCl to ph. 3. for 15 min at room temperature ( C) and then neutralized by 1N NaOH to ph The samples were assayed in duplicate by antigen capture enzyme-linked immunosorbent assay (Promega, Madison, WI, USA) according to the manufacturer s instructions. Plates were read at 5 nm on a SK1 microplate reader (Seikagaku Corporation, Tokyo, Japan). All NGF values were then standardized by Cre concentrations. Urodynamic assessment included filling cystometry and PFS. Filling cystometry was carried out with normal saline solution at a filling rate of 5 ml/min. A -Fr double-lumen transurethral catheter was used for infusion and recording intravesical pressure, and a hand-made intrarectal balloon catheter was used for recording abdominal pressure. The severity of obstruction was assessed using the BOOI, formerly known as the Abrams Griffiths number, defined as PdetQmax Qmax. 1 DO was defined as involuntary detrusor contraction during filling phase irrespective of its amplitude. BCI was defined as PdetQmax + 5Qmax. Otherwise the methods, definition and Table 1 units for filling cystometry conformed to the standards proposed by the International Continence Society. 13 To identify differences between before and after dutasteride treatment in the study patients, a paired t-test was used. Student s t-test was used to compare different subgroups of the study patients. Spearman s correlation was used for correlation analysis. P <.5 was considered statistically significant. Results Patients characteristics Age (years) 73. ( ) PV (ml) (3 139) IPSS 17. ( 3) Storage symptom score ( 15) Voiding symptoms score 9.3 ( ) Urodynamics MCC (ml) 3 (7 55) Presence of DO 3 (77%) PdetQmax (cmh O) 77 (1 17) BOOI ( 13) BCI 111 (51 1) We collected 3 patients whose clinical parameters were completed before and after dutasteride add-on treatment. The baseline characteristics of the 3 study patients are shown in Table 1. The mean age and PV of the study patients were 73. years (range years) and ml (range ml), respectively. On filling cystometry, mean MCC was 3 ml (range 7 55 ml) and DO was shown in 3 patients (77%). On PFS, mean PdetQmax, BOOI and BCI were 77 cmh O (range 1 17 cmh O), (range 13 cmh O) and 111 (range 51 1 cmh O), respectively. At baseline before dutasteride add-on, mean urinary NGF/Cre was.1 (range.1.9) and mean bladder volume at urine sample collection was ml (range ml). There was no significant difference of urinary NGF/Cre between patients with (n = 3) and without DO (n = 7;. ±.77 vs 1.7 ± 1., P =.1; Fig. 1a). Urinary NGF/Cre before dutasteride did not significantly correlate with age (r =.), IPSS (r =.11), voiding symptoms score (r =.19), storage symptoms score (r =.3), PV (r =.7), MCC (r =.), PdetQmax (r =.19), BOOI (r =.) or BCI (r =.11). When the study patients were dichotomized using cut-off value of PV, urinary NGF/Cre was significantly higher in patients with PV 5 ml (n = 19) than in those with PV <5 ml (n = 11; 3.5 ±. vs 1.9 ± 1.3, P <.5; Fig. 1b). There was no significant cut-off value for other clinical parameters that resulted in a significant difference in urinary NGF/Cre. Dutasteride add-on treatment significantly improved IPSS (from 17. ±.7 to 13.1 ±., P <.1), voiding (from 9.3 ± 5.7 to 7.1 ±.5, P <.1) and storage symptoms score of IPSS (from. ±.3 to. ±.9, P <.1), and significantly reduced PV from ± 31 ml to 9 ± ml (P <.1). On urodynamic study, MCC (from 3 ± 97 ml to 35 ± 3 ml) and BCI (from 111 ± 33 to 1 ± 7) did not change significantly. BOOI (from ± 3 to ± 7, P <.1) and PdetQmax (from 77 ± 3 cmh Oto59± cmh O, P <.1) 1 The Japanese Urological Association 159

3 N WADA ET AL. (a) (b) Absent Present Detrusor overactivity < 5 ml 5 ml Prostatic volume Fig. 1 before dutasteride treatment. (a) There was no significant difference in urinary NGF/Cre between patients with and without DO. (b) When study patients were dichotomized using several cut-off values of PV, urinary NGF/Cre was significantly higher in patients with PV 5 ml (n = 19) than in those with PV <5 ml (n = 11). 1 Before dutasteride After dutasteride Fig. before and after dutasteride treatment. Overall urinary NGF/Cre significantly decreased after dutasteride treatment (from.1 ±.5 to 1. ± 1., P <.5). were significantly improved. Overall urinary NGF/Cre significantly decreased after dutasteride treatment (from.1 ±.5 to 1. ± 1., P <.5; Fig. ). Any parameters after dutasteride treatment did not correlate with urinary NGF/Cre level after dutasteride treatment. Of the 3 patients, 3 (77%) had DO before dutasteride treatment. After dutasteride treatment, DO disappeared in three patients (13%). Urinary NGF/ Cre after dutasteride treatment was not different between those with (n = 3) and without DO resolution (n = ) after dutasteride treatment (1. ±.73 vs 1. ± 1.71). We additionally examined the correlation between reduction of urinary NGF/Cre and amount of change of each parameter. Reduction of urinary NGF/Cre significantly correlated with PV reduction (r =.3, P <.5) and BOOI improvement (r =.3, P <.5; Fig. 3). We explored the cut-off value of NGF reduction or reduction rate, which could dichotomize the changes of subjective or objective parameters, but could not detect any cut-off value. Discussion In the present study, dutasteride add-on treatment significantly decreased urinary NGF/Cre coupled with reduction of PV and relief of outlet obstruction in patients with BPE. This is the first report on the significant correlation between the changes of urinary NGF/Cre level and objective clinical parameters after dutasteride treatment in patients with BPE. Liu and Kuo previously showed that male patients with BOO and OAB, or those with BOO and DO had a significantly greater urinary NGF/Cre compared with the controls and BOO patients without OAB. In that study, urinary NGF/Cre in the patients of the well-treated BOO group (treated with alphablockers and 5-alpha reductase inhibitor for 1 5 years) was significantly greater than that in the controls, but not significantly different from that in BOO patients without OAB. Their data suggest that urinary NGF/Cre in patients with BOO is dependent on the presence of OAB and DO, but not on BOO itself. Differences in the methods and results between the previous and present study should be mentioned. In the previous study, well-treated BOO patients were defined as an IPSS less than after treatment. However, it is not clear in that study whether either of storage or voiding symptoms, or both symptoms, were improved after successful treatment. Furthermore, treatment durations varied from 1 to 5 years in that study. They did not compare urinary NGF/Cre before and after the treatment. In the present study, treatment duration of dutasteride add-on was weeks in every patient, and objective urodynamic parameters were also examined. In the present study, there was no significant difference in urinary NGF/Cre before dutasteride add-on treatment between patients with and without DO. We compared urinary NGF/Cre before and after dutasteride add-on treatment in the 3 patients. Although overall urinary NGF/Cre significantly decreased along with a reduction of BOO after dutasteride add-on treatment, there was no significant correlation between the changes of storage symptoms and urinary NGF/Cre level. In the present study, we examined the relationship between urinary NGF/Cre and objective parameters before and weeks after dutasteride treatment. It was found that reduction of urinary NGF/Cre after dutasteride treatment significantly correlated with PV reduction and relief of BOO. Yokoyama et al. reported similar results in male patients. 1 They showed that urinary NGF/Cre in BOO patients was significantly higher regardless of DO than that in controls. However, other clinical and animal studies suggest that urinary NGF reflects storage symptoms or bladder storage dysfunction. Lee et al. reported that urinary NGF was significantly increased in rats with DO after BOO. 15 They also showed that after relieving BOO, urinary NGF significantly decreased with DO resolution, but did not change in rats with persistent DO. Kim et al. showed that NGF expression was increased in the rat bladder with 1 1 The Japanese Urological Association

4 Dutasteride and urinary NGF Fig. 3 Correlation of reduction of urinary NGF/Cre level with reduction of PV and BOOI. Reduction of urinary NGF/Cre significantly correlated with reduction of (a) PV (r =.3) and (b) BOOI (r =.3). (a) Reduction of urinary NGF/Cre level Reduction of urinary NGF/Cre level (b) PV reduction (ml) BOOI reduction detrusor instability after relieving BOO. 1 Further research is required to reasonably explain the different results among the studies. NGF is expressed in bladder urothelium and bladder smooth muscle, and has been found in the urine. These findings have led to the evaluation of urinary NGF level as a potential biomarker for bladder disorders. However, in male patients, the presence of the prostate gland often complicates lower urinary tract dysfunction. Studies on NGF in the prostate showed that biologically significant levels of NGF are consistently detected in normal prostate. 17,1 Some studies demonstrated that prostatic epithelial and stromal cells in culture secreted NGF, and that prostatic epithelial cells expressed tyrosine kinase A and p75 receptors through which NGF acts It has been shown that NGF stimulates epithelial cell proliferation and the physiological NGF/tyrosine kinase A/p75 axis, present in normal prostate cells, undergoes changes during carcinogenesis. 1 Dutasteride acts on the prostate and reduces PV mainly by involution of epithelial tissue. Interestingly, in the present study, urinary NGF/Cre before dutasteride treatment was significantly higher in patients with a large prostate (PV 5 ml), and reduction of urinary NGF/Cre after dutasteride treatment significantly correlated with PV reduction. Thus, it is tempting to speculate that NGF produced by the prostate gland could affect the urinary NGF/Cre level in patients with BPE. That is one possible reason that DO and storage symptoms did not correlate with urinary NGF in the present study. However, there has been no study investigating the effect of the enlarged prostate on urinary NGF level. Another factor to consider with regard to the utility of urinary NGF for evaluating lower urinary tract dysfunction is a wide standard deviation in urinary NGF level, as shown in Figure. A previous study also reported the wide standard deviation in urinary NGF level, and speculated that one possibility was the effect of urine collection at varying bladder volume. In the previous study, urine samples were obtained with a comfortably full bladder (voided volume at urine sample collection not shown), whereas in the present study urine samples were obtained at normal desire to void (voided volume at urine sample collection ranging 7 ml). Thus, different bladder volume at urine sample collection might have differently affected NGF production and secretion in the bladder, and resulted in the wide standard deviation in urinary NGF level. In real practice, it is difficult to collect a urine sample from each patient at the same bladder volume. This problem should be resolved before clinical application of urinary NGF as a reliable biomarker for lower urinary tract dysfunction. Limitations of the present study include a small sample size. The number of patients without DO before dutasteride was just seven, and that might be a cause of a lack of significant difference of NGF between patients with and without DO. We need a large-sized study of urinary NGF in male patients. Another limitation was the lack of data before treatment with α-adrenergic antagonist, because all the patients recruited in the present study had been treated with α-adrenergic antagonist for more than 3 months. Nevertheless, the present study suggests that urinary NGF can be used as a biomarker to monitor the improvement of BOO in patients with BPE. In conclusion, urinary NGF decreases in association with reduction of PV and relief of BOO by dutasteride treatment. Urinary NGF might be useful as a biomarker to monitor the improvement of BOO in patients with BPE. 1 The Japanese Urological Association 11

5 N WADA ET AL. Conflict of interest None declared. References 1 Levi-Montalcini R, Calissano P. The nerve-growth factor. Sci. Am. 1979; : 77. Ochodnicky P, Cruz CD, Yoshimura N, Michel MC. Nerve growth factor in bladder dysfunction: contributing factor, biomarker, and therapeutic target. Neurourol. Urodyn. 11; 3: Kim JC, Park EY, Hong SH, Seo SI, Park YH, Hwang TK. Changes of urinary nerve growth factor and prostaglandins in male patients with overactive bladder symptom. Int. J. Urol. 5; 1: 75. Liu HT, Kuo HC. Urinary nerve growth factor levels are increased in patients with bladder outlet obstruction with overactive bladder symptoms and reduced after successful medical treatment. Urology ; 7: 1. 5 Kuo HC, Liu HT, Chancellor MB. Urinary nerve growth factor is a better biomarker than detrusor wall thickness for the assessment of overactive bladder with incontinence. Neurourol. Urodyn. 1; 9: 7. Liu HT, Chancellor MB, Kuo HC. Decrease of urinary nerve growth factor levels after antimuscarinic therapy in patients with overactive bladder. BJU Int. 9; 13: Liu HT, Tyagi P, Chancellor MB, Kuo HC. Urinary nerve growth factor but not prostaglandin E increases in patients with interstitial cystitis/bladder pain syndrome and detrusor overactivity. BJU Int. 1; 1: Liu HT, Tyagi P, Chancellor MB, Kuo HC. Urinary nerve growth factor level is increased in patients with interstitial cystitis/bladder pain syndrome and decreased in responders to treatment. BJU Int. 9; 1: Becher E, Roehrborn CG, Siami P, Gagnier RP, Wilson TH, Montorsi F. The effects of dutasteride, tamsulosin, and the combination on storage and voiding in men with benign prostatic hyperplasia and prostatic enlargement: -Year results from Combination of Avodart and Tamsulosin Study. Prostate Cancer Prostatic Dis. 9; 1: Tsukamoto T, Shirai T, Sakamoto S et al. The effect of dutasteride on voiding and storage symptoms in men with benign prostatic hyperplasia. Acta Urol. Jpn. 1; 5: Wada N, Kita M, Hashizume K, Matsumoto S, Kakizaki H. Urodynamic effects of dutasteride add-on therapy to alpha-adrenergic antagonist for patients with benign prostatic enlargement: prospective pressure-flow study. Neurourol. Urodyn. 13; 3: Abrams P. Bladder outlet obstruction index, bladder contractility index and bladder voiding efficacy: three simple indices to define bladder voiding function. BJU Int. 1999; : Abrams P, Cardozo L, Fall M et al. The standardization of the terminology of lower urinary tract function: report from the standardisation sub-committee of the International Continence Society. Neurourol. Urodyn. ; 1: Yokoyama T, Kumon H, Nagai A. Correlation of urinary nerve growth factor level with pathogenesis of overactive bladder. Neurourol. Urodyn. ; 7: Lee SR, Hong CH, Choi YD, Kim JH. Increased urinary nerve growth factor as a predictor of persistent detrusor overactivity after bladder outlet obstruction relief in a rat model. J. Urol. 1; 13:. 1 Kim JC, Kim DB, Seo SI, Park YH, Hwang TK. Nerve growth factor and vanilloid receptor expression, and detrusor instability, after relieving bladder outlet obstruction in rats. BJU Int. ; 9: Weeraratna AT, Arnold JT, George DJ, DeMarzo A, Isaacs JT. Rational basis for Trk inhibition therapy for prostate cancer. Prostate ; 5: 1. 1 Arrighi N, Bodei S, Zani D et al. Nerve growth factor signaling in prostate health and disease. Growth Factors 1; : Geldof AA, Van Haarst EP, Newling DW. Neurotrophic factors in prostate and prostatic cancer. Prostate Cancer Prostatic Dis. 199; 1: 3 1. Iczkowski KA, Qiu J, Qian J et al. The dual 5-alpha-reductase inhibitor dutasteride induces atrophic changes and decreases relative cancer volume in human prostate. Urology 5; 5: The Japanese Urological Association

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