URODYNAMIC CHANGES AT 18 MONTHS POST-THERAPY IN PATIENTS TREATED WITH EXTERNAL BEAM RADIOTHERAPY FOR PROSTATE CARCINOMA

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1 PII S (02) Int. J. Radiation Oncology Biol. Phys., Vol. 53, No. 2, pp , 2002 Copyright 2002 Elsevier Science Inc. Printed in the USA. All rights reserved /02/$ see front matter CLINICAL INVESTIGATION Prostate URODYNAMIC CHANGES AT 18 MONTHS POST-THERAPY IN PATIENTS TREATED WITH EXTERNAL BEAM RADIOTHERAPY FOR PROSTATE CARCINOMA RICHARD CHOO, M.D., F.R.C.P.C., F.A.C.R.,* VIET DO, M.B.B.S., F.R.A.N.Z.C.R.,* SENDER HERSCHORN, M.D., F.R.C.S.C., GERRIT DEBOER, PH.D.,* CYRIL DANJOUX, M.D., F.R.C.P.C.,* GERARD MORTON, M.D., F.R.C.P.C.,* CHUN HUNG CHENG, M.R.T. (T),* INNA BARAK, C.C.R.A.,* AND JOHN PREINER, M.D., F.R.S.C.S. *Toronto-Sunnybrook Regional Cancer Centre, University of Toronto; Division of Urology, Sunnybrook and Women s College Health Sciences Centre, University of Toronto, Toronto, Ontario, Canada Purpose: To quantify the effect of radiotherapy (RT) on urodynamics at 18 months post-therapy, using urodynamic study, in prostate cancer patients undergoing definitive external beam RT. Methods and Materials: A total of 17 patients with clinically localized prostate cancer were accrued into a single-arm prospective study. Fifteen of 17 patients completed scheduled multichannel video-urodynamic study at baseline as well as 3 and 18 months after RT. Baseline quantitative urodynamic parameters were compared with those at 18 months post-rt to assess the nature and extent of urodynamic change brought about by RT. These quantitative changes were further correlated to the change in self-assessed qualitative urinary function measured by International Prostate Symptom Score (IPSS), Quality of Life assessment index (QoL), and urinary functional inquiry. Results: The statistically significant quantitative changes detected by the urodynamic study at 18 months post-rt were decrease in bladder capacity and bladder volume at first sensation in both the supine and upright position, and reduction in bladder volume at desire to void in the supine position. In our cohort, the mean reduction in bladder capacity was 100 ml in the supine position and 54 ml in the upright position. No statistically significant change was observed with regard to pressure, maximum flow rate, voided volume, or postvoid residual volume. Furthermore, there was no statistically significant change in bladder compliance, bladder instability, or bladder outlet obstruction. No statistically significant change in self-assessed qualitative urological function was observed between baseline and 18 months post-rt, measured by the 3 parameters (IPSS, QoL, and urinary frequency over 24 h). Conclusions: This is the first quantitative study that prospectively evaluated the effect of RT on urodynamics in prostate cancer patients receiving definitive RT. The statistically significant changes at 18 months post-rt were reduction in bladder capacity, reduction in bladder volume at first sensation, and decrease in bladder volume at desire to void. Despite the decrease in these parameters, there was no statistically significant adverse effect of RT on bladder compliance, bladder stability, or bladder outlet flow. This observation corresponded well with no significant change in IPSS, QoL, or urinary frequency over 24 h. Furthermore, these results confirm the notion that most prostate cancer patients generally tolerate RT very well Elsevier Science Inc. Urodynamic, Radiotherapy, Prostate cancer. INTRODUCTION Adenocarcinoma of the prostate has become the most common malignancy in men in the Western countries. Options for active management of organ-confined prostate cancer include radical prostatectomy and definitive radiotherapy (RT) with either external beam RT or interstitial brachytherapy. In the absence of prospective randomized data, both treatment options are usually offered to patients as Reprint requests to: Dr. Richard Choo, Department of Radiation Oncology, Toronto-Sunnybrook Regional Cancer Centre, 2075 Bayview Avenue, Toronto, ON M4N 3M5. Tel: (416) ; Fax: (416) ; richard.choo@tsrcc.on.ca Presented as an oral presentation at the 43rd Annual Meeting of having equivalent efficacy (1). Each of these options, nonetheless, is associated with risk for significant morbidity (2, 3). Although serious urinary morbidity associated with definitive RT for prostate cancer is rare, it remains a major concern for both radiation oncologists and urologists. In the Radiation Therapy Oncology Group (RTOG) 7506 and 7706 trials with over 1000 patients, up to 7.7% of patients developed late Grade 3 or 4 RTOG urinary sequelae, which ranged from urethral stricture, chronic cystitis with or with- the American Society of Therapeutic Radiology and Oncology, San Francisco, Nov. 4 8, Received Sep 25, 2001, and in revised form Jan 14, Accepted for publication Jan 16,

2 Urodynamic findings at 18 months post-rt R. CHOO et al. 291 Fig. 1. Schema of the study. out hematuria, to bladder contracture (4). The average interval to the development of Grade 3 and 4 urinary toxicity was 14.1 months (range: ). Pilepich et al. reported a similar rate of late urinary morbidity in their retrospective series (5). All studies evaluating RT-related urinary morbidity in patients treated with RT for prostate cancer have been qualitative in nature up to now. There has been no clinical study applying quantitative objective parameters to assess the effect of RT on urodynamic function. Using urodynamic study as an objective quantitative tool, we conducted a prospective study to examine the nature and extent of change in urodynamic function caused by RT in patients who underwent definitive external beam RT for prostate cancer. Correlation of these quantitative changes with the change in self-assessed qualitative urinary function measured by International Prostate Symptom Score (IPSS), Quality of Life assessment index (QoL), and urinary functional inquiry was also investigated to assess the significance of these urodynamic changes in relation to subjective urological symptoms. METHODS AND MATERIALS A prospective single-arm study was conducted at the Toronto-Sunnybrook Regional Cancer Center between January 1998 and February The schema of the study is outlined in Fig. 1. The eligibility criteria included a histologic diagnosis of adenocarcinoma of the prostate, clinical stage T1b-T3N0M0, and planned definitive external beam RT. Patients with previous radical prostatectomy, previous RT to the pelvis, or failure to give informed consent were excluded. The study was approved by the local Institutional Review Board, and patients signed an informed consent before they were enrolled into the study. Urodynamic study All patients underwent a multichannel videourodynamic study before RT as well as 3 and 18 months post-rt. The urodynamic study was carried out according to the recommendations of the International Continence Society (6). The result was analyzed and interpreted by one of the authors (S.H.), an urologist with expertise in this field. Figure 2 shows a schematic illustration of multichannel videourodynamic study. A patient was catheterized with two 8-French catheters, one for the measurement of filling pressure and the other for intravesical pressure (Pves). A 10-French balloon-tipped rectal catheter was also introduced to measure intra-abdominal pressure (Pabd). Detrusor pressure is the difference between intravesical and intra-abdominal pressure (i.e., Pdet Pves Pabd). Contrast solution was instilled into the bladder at an average filling rate of 50 ml/min and fluoroscopy was used to image the study. Several parameters were measured during the filling and voiding phase of the bladder in both supine and upright position. With the patient in the supine position and the bladder being filled, pressures as well as volumes at first sensation, at desire to void, and at capacity were measured. Instability or decreased compliance was also assessed. The patient was then asked to cough and strain. If stress incontinence was demonstrated, Valsalva or cough leak pressure was recorded. The bladder was then emptied and refilled in the upright position with similar measures taken. Stress maneuvers were again carried out. After these measurements, the filling catheter was removed and the patient was asked to void to measure the voiding pressure and flow rates. IPSS and QoL questionnaire All patients completed the IPSS and QoL questionnaire (7), in conjunction with the urodynamic study, pre-rt and at 3 months and 18 months post-rt. The IPSS is an instru-

3 292 I. J. Radiation Oncology Biology Physics Volume 53, Number 2, 2002 Fig. 2. Schematic description of a urodynamic study. ment designed to evaluate lower urinary tract symptoms (LUTS) in men with benign prostatic hypertrophy. IPSS scores of 7, 8 19, and 20 correspond to very mild, intermediate, and severe LUTS respectively (7). The application of the IPSS has been validated for the evaluation of LUTS in patients treated with permanent source interstitial brachytherapy (8) and external beam RT (9) for clinically localized prostate cancer. Other evaluations at pre-rt, 3 months post-rt, and 18 months post-rt At the time of the urodynamic study, all patients underwent physical examination and provided a detailed medical history including previous urological or pelvic surgery, spinal cord injury, neurologic illness, diabetes mellitus, and concomitant medications that might have an impact on the urodynamics. Urine was analyzed and tested for culture and sensitivity to rule out urinary tract infection. Baseline biochemical tests included blood count (CBC), urea, creatinine, serum prostate-specific antigen (PSA), prostate alkaline phosphatase, liver function profiles, and random glucose. Radiotherapy All patients received external beam RT using a four-field box technique and high-energy photons (18 or 23 MV). Conformally shaped fields were used with a multileaf collimator. Patients were treated in the supine position and advised to keep their bladder full before RT. The clinical target volume (CTV) was limited to the prostate and periprostatic tissue with known extent of tumor. Regional pelvic lymph nodes were not included in the CTV. A uniform 15 mm was added to the CTV to determine the planning target volume (PTV). All patients underwent computerized tomography (CT) planning to obtain the CTV and PTV. The bladder volume and the proportion of bladder volume within the 100%, 80%, and 50% radiation isodoses were calculated with AcQ Sim CT planning software. RT dose and fractionation ranged from 66 Gy/33 fractions (f) to 70 Gy/35 f with the majority receiving 66 Gy/33 f. RT was delivered 5 days a week in 2 Gy daily fractions. Dose was prescribed at the International Commission on Radiation Units and Measurements reference point (ICRU Report 50, 1993). Statistical methods Because of the exploratory and invasive nature of this study, the accrual was limited to 17 patients. Moreover, this project was considered as a pilot study from which a future, more rigorous study could be developed. Statistical analysis was done with SAS (Version 8; SAS Institute Inc., Cary, NC). RESULTS A total of 17 patients were accrued for this pilot study. One patient was excluded from analysis because he had a syncopal episode during the baseline urodynamic study, resulting in incomplete evaluation. Another patient, who underwent the urodynamic study pre-rt and 3 months post-rt, died of metastatic lung carcinoma before his 18- month urodynamics study. Thus, a total of 15 patients were the basis for this report examining the effect of RT on urodynamics at 18 months post-rt. The change in urodynamics at 3 months post-rt, which reflects more acute effect of RT, was not included in this report and will be addressed separately. The median age of the cohort was 72 years (range: 56 77). All underwent the computed tomographic (CT) scan of abdomen and pelvis and bone scan before RT and had no evidence of metastatic disease. Of the 15 patients,

4 Urodynamic findings at 18 months post-rt R. CHOO et al. 293 Table 1. Change of self-assessed urinary function measured by International Prostate Symptom Score (IPSS), Quality of Life assessment index (QoL), and urinary frequency over 24 h from pre-rt baseline to 18 months post-rt Mean change Standard error p value* IPSS QoL Urinary frequency over 24 h *From paired t test. one had a history of diabetes mellitus and another had transurethral resection of the prostate (TURP) before the diagnosis of prostate cancer. None had pelvic or urological surgery, spinal cord injury, neurologic illness, or other major medical illness during the time period between baseline and 18 months post-rt. Also there was no major change of medications such as the addition of an -adrenergic receptor blocker that could affect the urodynamic function of the lower urinary tract. The median pretreatment PSA was 8.55 ng/ml (range: , Hybritech assay). Gleason score ranged from 6 to 8 with a median of 7. The clinical T-stage distribution was as follows: 2 patients with T1C, 12 with T2, and 1 with T3. The proportions of bladder volume receiving 100%, 80%, and 50% of the total radiation dose were calculated with AcQ Sim CT planning software. The median percentage of bladder volume within 100% radiation isodose was 0.9% with the mean calculated volume of 4.1 ml (range: ). The median bladder volumes receiving 80% and 50% of the prescribed dose were 81.7 ml (range: ) and ml (range: ) respectively. These corresponded to 30.6% and 60.6% of the total bladder volume respectively. IPSS, QoL questionnaire, and urinary functional inquiry Median urinary frequency over 24 h, IPSS, and QoL at baseline were 8.5 times (range: 4 14), 7 (range: 1 22), 1.5 (range: 0 5) respectively, compared with 9 times (range: 4 18), 7 (range: 0 28), and 1 (range: 0 5) at 18 months post-rt. There was no statistically significant change in self-assessed urological symptoms at 18 months post-rt compared to pre-rt baseline, assessed by the three parameters (IPSS, QoL, and urinary frequency over 24 h). In our cohort, the mean changes from the baseline to 18 months post-rt were 0.4 for IPSS, 0 for QoL, and 0.67 for urinary frequency over 24 h (Table 1). Of 9 patients with urinary urgency at baseline, 6 had persistent urgency at 18 months post- RT whereas 3 had resolution of urinary urgency. Of 6 patients with no evidence of urgency at baseline, 5 had urgency at 18 months post-rt. Three patients with urge incontinence at baseline remained unchanged at 18 months post-rt. Of 12 patients with no evidence of urge incontinence at baseline, 3 had urge incontinence at 18 months post-rt. However, these changes in urinary urgency and urge incontinence were not statistically significant (Table 2). Urodynamic study Figure 3 represents the change of individual patients bladder volumes at capacity in the supine position from pre-rt baseline to 18 months post-rt. At 18 months post- RT, mean bladder capacity decreased from ml (range: ) to ml (range: ) in supine position and from ml (range: ) to ml (39 578) in upright position. Table 2 summarizes the results of urodynamic studies. There was statistically significant reduction in bladder capacity at 18 months post-rt compared to that at pre-rt Table 2. Change of urodynamic parameters from pre-rt baseline to 18 months post-rt Mean change Standard error P value* Supine position Mean change in residual volume (ml) Mean change in volume at first sensation (ml) Mean change in pressure at first sensation (cm H 2 O) Mean change in volume at desire to void (ml) Mean change in pressure at desire to void (cm H 2 O) Mean change in volume at capacity (ml) Mean change in pressure at capacity (cm H 2 O) Upright position Mean change in volume at first sensation (ml) Mean change in pressure at first sensation (cm H 2 O) Mean change in volume at desire to void (ml) Mean change in pressure at desire to void (cm H 2 O) Mean change in volume at capacity (ml) Mean change in pressure at capacity (cm H 2 O) Mean change in voiding pressure (cm H 2 O) Mean change in maximum flow rate (ml/s) Mean change in voided volume (ml) *From paired t test.

5 294 I. J. Radiation Oncology Biology Physics Volume 53, Number 2, 2002 Fig. 3. Change of individual patients bladder volumes at capacity in the supine position from pre-rt baseline to 18 months post-rt (sorted in order of baseline volume). baseline in both the supine and upright position. The mean reduction was 100 ml in the supine position (standard error [SE] 20, p ) and 54 ml in the upright position (SE 23, p 0.035). Other parameters that showed statistically significant changes were reduction in bladder volume at first sensation in both the supine and upright position, and decrease in bladder volume at desire to void in the supine position (Table 2). No statistically significant change was observed in other parameters including detrusor pressure at capacity as well as pressures at first sensation and at desire to void. Furthermore, there were no statistically significant changes in maximum flow rate, voiding pressure, voided volume, or postvoid residual volume. Table 3 summarizes the changes observed at 18 months post-rt in patients with or without preexisting decreased bladder compliance, bladder instability, and bladder outlet obstruction. Of 2 patients with decreased bladder compliance at baseline, 1 continued to have a characteristic urodynamic pressure volume curve consistent with decreased bladder compliance at 18 months post-rt. Of 13 patients with normal bladder compliance at baseline, 4 had decreased bladder compliance at 18 months post-rt. Eight patients had bladder instability at baseline; of these, 7 showed persistent bladder instability at 18 months post-rt. Of 7 patients with normal stable bladder at baseline, 2 developed bladder instability at 18 months post-rt. Twelve patients were interpreted as having bladder outlet obstruction at baseline. In this group, 3 patients were judged to have improvement in bladder outlet obstruction at 18 months post-rt whereas 9 patients were scored as unchanged. Three patients had no bladder obstruction at baseline and remained Table 3. Change of bladder compliance, bladder instability, bladder outlet obstruction, urgency, and urge incontinence from pre-rt baseline to 18 months post-rt Status at baseline and 18-month post RT Y-Y Y-N N-N N-Y p value* Decreased bladder compliance, n Bladder instability, n Bladder outlet obstruction, n Urgency, n Urge incontinence, n *Comparison using McNemar s test. Abbreviations: Y-Y presence of condition at baseline and remains present at follow-up; Y-N presence of condition at baseline and returns to normal at follow-up; N-N absence of condition at baseline and remains absent at follow-up; N-Y absence of condition at baseline but abnormal at follow-up.

6 Urodynamic findings at 18 months post-rt R. CHOO et al. 295 normal at 18 months post-rt. None of these changes were statistically significant and, overall, there was no significant change in bladder compliance, bladder instability, or bladder outlet obstruction from baseline to 18 months post-rt. Due to the small sample size of our series, a detailed evaluation of the relationship between the proportion of bladder volume receiving 100%, 80%, and 50% of the prescribed dose and the magnitude of reduction in bladder capacity was not feasible. Nevertheless, we examined the potential correlation of the proportion of bladder volume receiving 100%, 80%, and 50% of prescribed dose with those urodynamic parameters that showed statistically significant changes at 18 months post-rt (i.e., bladder volumes at capacity, at first sensation, and at desire to void) and the magnitude of change of self-assessed parameters (IPSS, QoL, and urinary frequency over 24 h). There was no significant correlation between these factors except a positive association between the proportion of bladder volume receiving 100% and 80% of prescribed dose and the change in bladder volume at capacity in the supine position (r 0.75, p and r 0.69, p 0.013, respectively). DISCUSSION Treatment-related sequel is an important aspect to consider for the evaluation of the therapeutic efficacy of any treatment modality. External beam RT is not an exception to this rule, and its potential morbidity has always been a concern to physicians and patients. In particular, in the context of a generally elderly population of prostate cancer patients, potential morbidity of external beam RT and its effect on the quality of life have always been a contentious issue when the therapeutic efficacy of external beam RT is addressed. Moreover, radiation dose has been steadily escalated for localized prostate cancer in recent years as there has been increasing evidence for a dose response relationship in tumor control. Although this dose escalation improves the probability of local tumor control, it is inherently associated with corresponding increase in the risk of acute and late morbidity of RT. Thus, proper evaluation and management of potential morbidity of RT has been increasingly important. Up to now, all studies evaluating RT-related urinary morbidity in prostate cancer patients have been qualitative in nature. A qualitative instrument such as the RTOG morbidity grading system has been very useful and practical, as it is user-friendly, noninvasive, and relevant to a patient s day-to-day functional aspect. However, these qualitative tools have limitation in that they do not provide any information relating to objective physiologic change in the lower urinary tract caused by RT. To quantify the effect of external beam RT on the lower urinary tract, our current series utilized the urodynamic study, which is a gold standard test for the evaluation of the lower urinary tract function. It provides not only detailed quantitative parameters such as pressure, volumes, and flow rate, but also information pertaining to the overall function of the lower urinary tract such as bladder compliance, bladder instability, and the presence or absence of bladder outlet obstruction. This objective quantitative evaluation further assists physicians in understanding the relationship between the change observed in a self-assessed qualitative assessment and that of quantitative parameters measured by the urodynamic study. There are several limitations in our current series. The main shortcoming is the small sample size of our study. The small sample size resulted in large confidence intervals for parameters estimated, and could potentially lead to falsepositive or false-negative conclusions. Another factor to consider is that the urodynamic changes observed at 18 months post-rt do not necessarily represent the long-term urological effect of RT, which may continue to evolve over a much longer period of time. Also, the evaluation of bladder compliance and instability as well as the presence or absence of urinary obstruction depends on, in some degree, a subjective interpretation of urodynamic study. For example, there has been no uniform method of calculating bladder compliance that is consistently used in the urology community. Bladder compliance is defined as the ratio of the change of volume to the change in pressure (10). It can be calculated as a static event at a single point on the pressure volume curve. However, because the selection of a single point is arbitrary, this approach is susceptible to an oversimplified, misleading, or erroneous conclusion (11). Compliance may also be determined by means of the best-fit curve technique or the reciprocal of the slope along numerous points of the cystometrogram curve. In our study, bladder compliance was evaluated subjectively by examining the entire pressure volume curve. Despite the aforementioned limitations, this is, to our knowledge, the first quantitative study that attempts prospectively to evaluate the effect of RT on urodynamics in prostate cancer patients receiving definitive external beam RT. To examine the magnitude and the nature of quantitative change in the lower urinary tract caused by RT, urodynamic study was conducted and compared before and 18 months after RT. Also assessed was whether there would be any correlation between these quantitative changes and those observed in self-assessed qualitative tools. The statistically significant changes at 18 months post-rt compared with baseline were reduction in bladder capacity and bladder volume at first sensation both in the supine and in the upright position, and decrease in bladder volume at desire to void in the supine position. These changes may be related to decreased bladder expansibility secondary to radiation fibrosis of the irradiated portion of the bladder. Despite the decrease in these parameters at 18 months post-rt, we did not observe any major change in selfassessed urological function, assessed by three parameters (IPSS, QoL, and urinary frequency over 24 h). Furthermore, there was no statistically significant change in other urodynamic parameters including postvoid residual volume, bladder pressure, voided volume, or maximum flow rate. Neither was any statistically significant adverse effect observed on bladder compliance, bladder instability, or bladder outflow obstruction. These results confirm the notion that most

7 296 I. J. Radiation Oncology Biology Physics Volume 53, Number 2, 2002 prostate cancer patients generally tolerate RT very well and the risk of serious urinary morbidity of RT is low. If there is a significant radiation-induced fibrosis in the bladder, one would expect decreased bladder compliance with some characteristic urodynamic findings, including reduced bladder capacity and persistently elevated bladder pressure. In our study, although a reduction in bladder capacity was demonstrated, there was no statistically significant increase in bladder pressure. This may be due to either a small sample size that does not allow one to detect a minimal change in bladder pressure, or the possibility that a longer follow-up beyond 18 months is needed to observe the change in bladder pressure. Another possible explanation is that the proportion of the bladder affected by radiation fibrosis has not reached a threshold at which a significant increase in detrusor pressure occurs. Urodynamic studies assessing the effect of RT have been reported for patients with cervical cancer. The urodynamic findings after RT for cervical carcinoma have varied widely. They included reduced bladder compliance (12, 13), decreased bladder capacity (14, 15), reduced mean volume of first bladder sensation, decreased maximal urethral closure pressure and functional profile length, and increased mean filling detrusor pressure (15). Abnormal bladder sensation, voiding problem (13), and urinary incontinence (12 14) could also accompany these abnormal objective findings. Farquharson et al. reported that bladder compliance was significantly reduced in patients receiving more than 30 Gy to the entire bladder and suggested that radiation dose to the bladder was one of the important predictive factors for post-rt bladder compliance (13). The relationship between the proportion of bladder volume receiving 100%, 80%, and 50% of the prescribed dose and the urodynamic parameters shown to have statistically significant changes at 18 months post-rt was explored. The only statistically significant finding was a positive correlation between the proportion of bladder volume receiving 100% and 80% of the prescribed dose and the change in bladder volume at capacity in the supine position. This implies the higher the proportion of bladder volume receiving 100% and 80% of the prescribed dose, the smaller the decrease in bladder capacity at 18 months post-rt. This correlation could not be well explained by our current understanding of the pathophysiological effect of RT on the bladder. It could be false-positive due to our small sample size. Further prospective study with larger sample size would be needed to validate this correlation. CONCLUSION In summary, our series represents the first study attempting to quantify the effect of external beam RT on urodynamics in prostate cancer patients undergoing definitive RT. The statistically significant changes at 18 months post-rt compared to baseline were the reduction in bladder volume at capacity, reduction in bladder volume at first sensation, and decrease in bladder volume at desire to void. These changes were more pronounced in the supine position. The reduction in these parameters may be explained by radiation fibrosis. Despite the decrease in these parameters, there was no statistically significant adverse effect of RT on bladder compliance, bladder stability, or bladder outlet flow. This observation corresponds well with no significant change in IPSS, QoL, or urinary frequency over 24 h. Furthermore, these results confirm the notion that most prostate cancer patients generally tolerate RT very well. REFERENCES 1. Millikan R, Logothetis C. 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