ERECTILE DYSFUNCTION (ED) is the persistent
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1 Transplantation Treatment of Erectile Dysfunction With Sildenafil Citrate in Renal Allograft Recipients: A Randomized, Double-Blind, Placebo-Controlled, Crossover Trial Raj K. Sharma, FASN, Narayan Prasad, DM, Amit Gupta, DNB, and Rakesh Kapoor, MCh Background: Erectile dysfunction (ED) is observed frequently in patients with end-stage renal disease, hemodialysis patients, and renal allograft recipients. There are few studies of sildenafil use in renal allograft recipients. Methods: The study is designed as a randomized, double-blind, placebo-controlled, crossover trial. Efficacy was assessed by using the self-administered International Index of Erectile Function (IIEF), a 15-question validated measure of ED, and a global efficacy question (Did the treatment improve your erection?). Results: Thirty-two eligible renal transplant recipients were included in this study. After treatment with sildenafil citrate, patients had significantly better scores in 13 of 15 questions, except for questions 11 (desire frequency; P 0.39) and 12 (desire level; P 0.61). Treatment efficacy assessed through questions 3 (penetration ability; P < 0.001) and 4 (maintenance frequency; P < 0.001) was significantly better after sildenafil therapy. There were no significant differences between baseline and post placebo treatment scores, except for question 13 (relationship satisfaction). Patients treated with sildenafil had significantly better scores in 4 domains compared with baseline, but a difference was not observed in the sexual desire domain (P 0.32). There were no significant differences in scores between placebo and baseline in any domain. On the global efficacy question, 81.3% of patients showed improvement compared with 18.7% with placebo. There were no differences in areas under the curve and maximum cyclosporine concentrations before and after sildenafil therapy. No patient discontinued the drug because of side effects except for 1 patient with visual hallucination. Conclusion: Treatment with sildenafil in renal transplant recipients is a valid option with an effective response. Am J Kidney Dis 48: by the National Kidney Foundation, Inc. INDEX WORDS: Erectile dysfunction; renal transplant recipient; sildenafil. ERECTILE DYSFUNCTION (ED) is the persistent inability to achieve a sustained erection sufficient for satisfactory sexual performance. The mental stress resulting from ED affects patients interactions with family and others. 1 ED is observed frequently in patients with end-stage renal disease and patients on hemodialysis therapy, and the estimated prevalence is between 71% and 82% in these patients. 2,3 Only up to 75% of these patients recover from ED after renal transplantation. 4 ED From the Departments of Nephrology and Urology, Sanjay Gandhi Post Graduate Institute of Medical Sciences, Lucknow, India. Received December 27, 2005; accepted in revised form April 10, Originally published online as doi: /j.ajkd on May 24, Support: Zydus Cadila provided placebo and sildenafil tablets. Potential conflicts of interest: None. Address reprint requests to Raj K. Sharma, FASN, Professor and Head, Department of Nephrology, Sanjay Gandhi Post Graduate Institute of Medical Sciences, Raebareli Rd, Lucknow , India. rksharma@sgpgi.ac.in 2006 by the National Kidney Foundation, Inc /06/ $32.00/0 doi: /j.ajkd also may occur in up to a third of patients receiving a double transplant with vascular anastomosis to the hypogastric artery because of reduced arterial flow to the penis. 5 Treatment options for men with ED include psychosexual therapy, drug therapy, transurethral or intracavernosal therapy, treatment with vacuum constriction devices, and surgical treatment. 6 Sildenafil citrate is a selective inhibitor of phosphodiesterase type 5, which is the predominant isozyme interacting with cyclic guanosine monophosphate in corpus cavernosum and results in increased smooth muscle relaxation and improved erection. Recently, sildenafil was shown to be an effective, safe, and well-tolerated drug for men with ED 7 and end-stage renal disease and maintenance hemodialysis patients with ED There are few either nonrandomized or uncontrolled studies on the use of sildenafil in renal allograft recipients There have been no double-blind placebo-controlled studies with sildenafil in renal allograft recipients. The area under the curve (AUC) of cyclosporine before and after sildenafil therapy was not compared in any of these studies Therefore, we conducted a randomized, double-blind, placebocontrolled, crossover study to establish the safety 128 American Journal of Kidney Diseases, Vol 48, No 1 (July), 2006: pp
2 SILDENAFIL CITRATE IN RENAL ALLOGRAFT RECIPIENT 129 and efficacy of sildenafil in renal transplant recipients with ED. METHODS The study is designed as a randomized, double-blind, placebo-controlled, crossover trial. Inclusion criteria for patients were renal transplant recipients who: (1) had stable graft function in the last 6 months, (2) were 18 years and older, (3) had medically documented ED as defined by the National Institute of Health Consensus Panel, 1 and (4) were in a stable relationship with a female partner in the last 6 months. All patients were subjected to a detailed medical history and physical examination that included blood pressure, pulse rate, 12-lead electrocardiogram, cyclosporine A level by means of enzyme multiplied immunoassay method, and standard biochemistry (blood urea nitrogen, serum creatinine) and hematologic tests (hemoglobin, total and differential leukocyte count, and platelet count) at baseline and after each crossover. Exclusion criteria included the following: (1) penile anatomic deformities, (2) history of recent stroke, (3) myocardial infarction in the previous 6 months, (4) proliferative diabetic retinopathy, (5) severe autonomic neuropathy, (6) regular treatment with nitrates and androgens, and (7) spinal cord injury. At week 0, each eligible patient was given a randomization number that followed a randomization table generated by the method of random permuted blocks. The system generating the randomization assignment was operationally independent from study investigators who executed the randomization assignment and conducted the study. Renal allograft recipients with ED were divided into 2 groups, the placebo group and sildenafil group, by randomization and then crossed over to another group after 8 weeks in a double-blind manner. The washout period of 2 weeks was ensured in each patient during crossover from 1 group to the other by the investigator. Patients were instructed to take a single dose of study medication in a day, not more than once daily. The initial dose was 50 mg of sildenafil citrate or placebo of identical appearance. Based on the investigator s judgment of efficacy and tolerability, the dose could be increased to 100 mg or decreased to 25 mg of sildenafil or placebo. The initial dose of the drug was taken 1 hour before sexual intercourse, avoiding heavy meals or excessive alcohol intake. All patients completed the International Index of Erectile Function (IIEF) and a diary card to record response to the drug and the occurrence of side effects. Efficacy was assessed by using the self-administered IIEF, a 15-question validated measure of ED, 17,18 and a global efficacy question (Did the treatment improve your erection?). 19 The IIEF system is used for clinical assessment of ED and treatment outcome in clinical studies. It evaluates several aspects of sexual performance, rating each answer from 0 to 5, with 0 meaning no sexual activity/no attempt at sexual intercourse, 1 meaning the worst response (almost never/ never), and 5 meaning the best response (almost always/ always). Total score ranges from 5 to 75. Treatment efficacy was assessed through the answer to questions 3 (penetration ability) and 4 (maintenance frequency). Efficacy also was evaluated through the score for the 5 separate response domains of male sexual function of the IIEF: erectile function (questions 1 to 5 and 15; total score, 1 to 30), intercourse satisfaction (questions 6 to 8; total score, 0 to 15), orgasmic function (questions 9 and 10; total score, 0 to 10), sexual desire (questions 11 and 12; total score, 2 to 10), and overall satisfaction (questions 13 and 14; total score, 2 to 10). The final score of each domain is the sum of scores for individual questions in that domain. Patients with a score of 26 or higher on the erectile function domain were considered to have no ED and were excluded from analysis. In a selected group of 5 patients with normal graft function, cyclosporine level was estimated at 0-, 0.5-, 1-, 2-, 3-, 4-, and 6-hour intervals with and without sildenafil, and the AUC of cyclosporine level was estimated to see the effect of sildenafil on cyclosporine level. AUC was estimated by using a linear trapezoid rule. The study was conducted at Sanjay Gandhi Post Graduate Institute of Medical Sciences, Lucknow, India, a tertiarycare academic institute. Informed consent was obtained from all patients included in the study. Both sildenafil and placebo of identical aspect were provided by Zydus Cadila (Ahmedabad, India) free of charge. The authors received no other support from the drug and placebo provider to avoid any conflict of interest. Statistical Analysis Mean SD was calculated for each IIEF question or domain. Results of the placebo and sildenafil groups were compared by using t-test and Mann-Whitney U test for parametric and nonparametric data, respectively. Comparison of basal and final results in each group was performed by using paired t-test and Wilcoxon test for parametric and nonparametric data, respectively. RESULTS Thirty-two eligible renal transplant recipients were included in this study. Mean age was 40 8 years. Mean duration of the transplant was years, duration of ED was months, and duration of dialysis therapy was months. All patients had undergone living-related transplantations. No patient in our study had a vascular anastomosis to both the internal iliac artery and hypogastric artery. Of these patients, 14 patients had chronic glomerulonephritis, 8 patients had chronic interstitial nephritis, 7 patients had diabetic nephropathy, and 3 patients had other basic diseases. No patient had autonomic neuropathy at time of enrollment into this study. At baseline, mean hemoglobin level was g/dl ( g/l), mean blood urea nitrogen level was mg/dl ( mmol/l), and creatinine level was mg/dl ( mol/l). In total, 32 tablets of sildenafil or placebo were offered to
3 130 SHARMA ET AL Table 1. IIEF Scores in Patients at Baseline and After Placebo and Sildenafil Treatment IIEF Question Baseline Post Placebo Treatment Post Sildenafil Treatment P, Baseline v Placebo P, Baseline v Sildenafil Erection frequency Erection firmness Penetration ability Maintenance frequency Maintenance ability Intercourse frequency Intercourse satisfaction Intercourse enjoyment Ejaculation frequency Orgasm frequency Desire frequency Desire level Overall satisfaction Relationship satisfaction Erection confidence NOTE. Data expressed as mean SD. patients during the study period. At end of the study, mean numbers of tablets of sildenafil and placebo taken by patients were and , respectively (P 0.49). Table 1 lists scores for each of the 15 IIEF questions. After treatment with sildenafil, patients administered sildenafil had highly significantly better scores in 13 of 15 questions. The only questions for which differences were not significant were questions 11 (desire frequency; P 0.39) and 12 (desire level; P 0.61). Treatment efficacy assessed through questions 3 (penetration ability; P 0.001) and 4 (maintenance frequency; P 0.001) was significantly better after sildenafil therapy. Data show no significant differences between baseline and post placebo treatment scores, except for question 13 (relationship satisfaction), which was significantly better after placebo treatment. The 5 IIEF domains are listed in Table 2. No significant differences between placebo and baseline scores were detected in any domain. Patients treated with sildenafil had better scores in 4 domains in comparison to the baseline score, but no difference was observed in the sexual desire domain (P 0.32). On analyzing the outcome of efficacy of sildenafil on the global efficacy question (whether treatment showed an improvement), 26 of 32 patients (81.3%) showed improvement in the sildenafil group, whereas only 6 patients (18.7%) showed improvement with placebo (P 0.01). On analyzing AUC and maximum concentration (C max ) of cyclosporine in 5 selected patients, mean AUC and C max were not different with and without sildenafil. Mean AUC of cyclosporine was 7,454 1,483 ng/h/ml with sildenafil compared with 7,460 1,480 ng/h/ml without sildenafil. Mean C max also was similar: 1,605 ng/ml with sildenafil compared with 1,604 ng/ml without sildenafil. Table 2. IIEF Domain Scores at Baseline and After Placebo and Sildenafil Treatment IIEF Domain Baseline Placebo Sildenafil P, Baseline v Placebo P, Baseline v Sildenafil Erectile function Orgasmic function Sexual desire Intercourse satisfaction Overall satisfaction NOTE. Data expressed as mean SD.
4 SILDENAFIL CITRATE IN RENAL ALLOGRAFT RECIPIENT 131 Table 3. Biochemical Parameters Pre and Post Sildenafil Treatment Pre Sildenafil Treatment Post Sildenafil Treatment P Blood urea nitrogen (mg/dl) Not significant Creatinine (mg/dl) Not significant Hemoglobin (g/dl) Not significant Cyclosporine trough level (ng/ml) Not significant NOTE. Data expressed as mean SD. To convert hemoglobin in g/dl to g/l, multiply by 10; blood urea nitrogen in mg/dl to mmol/l, multiply by 0.357; creatinine in mg/dl to mol/l, multiply by As listed in Table 3, there were no significant differences between biochemical parameters pre and post sildenafil treatment. Serum creatinine and blood urea nitrogen levels were not significantly different in the pre and post sildenafil treatment period. Five patients developed headache, 2 patients developed rhinorrhea and flushing, and 1 patient each developed generalized body ache and typical bluish visual hallucination with sildenafil, whereas only 2 patients developed headache with placebo. No patient discontinued the drug, except for the 1 patient with visual hallucination. DISCUSSION This study shows that sildenafil is safe and effective for the treatment of ED in renal allograft recipients. This is the first randomized, placebo-controlled, crossover study to show the efficacy of sildenafil in renal transplant recipients. sildenafil has an efficacy similar to that in other nontransplantation patients with ED sildenafil significantly improved erectile function score, although it did not improve desire level and sexual frequency as expected (Table 1) and also reported in other studies. 9,19 These results are similar to previous results in patients with diabetes, 19 hemodialysis patients, 8-11 and renal transplant recipients with ED. Treatment efficacy assessed through questions 3 (penetration ability) and 4 (maintenance frequency) was significantly better in these renal transplant recipients (P 0.001), similar to other patients with ED in another study. 19 In this study, all IIEF domain scores improved significantly after sildenafil, except for the sexual desire domain, whereas IIEF domain score did not improve after placebo (Table 2). Similar results were reported in patients with ED with diabetes 19 and hemodialysis patients. 9 Studies focusing on the use of sildenafil in renal transplant recipients showed a satisfactory response in 60% to 81% of transplant patients with ED ,20 However, in our study, the response rate was 81.3%, on the higher side of the range. Recently, Zhang et al 13 also showed a response in 81.5% of patients, similar to our study. This higher response rate may be caused by a shorter duration of dialysis therapy (mean, 3 months; range, 1 to 5.5 months) before transplantation in our patients. Prieto Castro et al 12 showed a satisfactory response in 60% of transplant recipients, with a mean time on dialysis therapy of 23 months in patients with a satisfactory response, compared with 43 months in patients for whom the drug was not effective. We do not have a maintenance hemodialysis program, and only patients with a renal transplantation prospect are accepted for hemodialysis therapy. The drug is more effective in patients who have less time on dialysis therapy before transplantation because penile vascular disease is less advanced. 12 A greater prevalence of ED usually is seen in patients with a longer duration of maintenance hemodialysis. 2,3 In a large experience of 22 years of ED in renal transplant recipients, Lasaponara et al 16 reported that ED is an important problem in male renal transplant recipients, and cultural resistance to treatment is common. However, sildenafil is an accepted mode of treatment. They also showed that more renal transplant patients are reporting ED (78%) after 1998, after the invention of sildenafil, compared with 45% before Russo et al 14 showed improvement in IIEF domain scores in 20 renal transplant recipients with ED with the use of sildenafil. This study was designed more to show the effect of renal transplantation on ED, rather than the effect of sildenafil. 14
5 132 Chatterjee et al 21 also showed a good response to combined testosterone and sildenafil therapy in all patients, but only 8 of 12 patients were renal transplant recipients and 4 patients were on hemodialysis therapy in this pilot study with a different design. Therefore, the response rate to combined sildenafil and testosterone therapy cannot be compared with the response rate of sildenafil alone in our renal transplant recipients. Sildenafil and cyclosporine are metabolized through cytochrome P-450 isoform 3A4, and there is concern of a drug interaction between the 2 drugs. However, AUC and C max were not changed after use of sildenafil, and this may have been caused by highly selective action on phosphodiesterase type 5 and the short half-life (60 to 90 minutes) of sildenafil. No change in drug dosing of cyclosporine is required, which was shown in other studies ,20,22 However, only the trough level of cyclosporine was compared in these studies. We are the first to compare the AUC of cyclosporine before and after sildenafil therapy. Blood urea nitrogen and serum creatinine levels were not changed significantly after the use of sildenafil in our study. Similar observations were seen in other studies An increase in glomerular filtration rate was seen in kidney transplant recipients after use of sildenafil. 23,24 However, a slight increase in serum creatinine levels between the inclusion visit and study end was observed in a study, but there was no evidence of a causal relationship between this increase and sildenafil administration in this study. 15 In the present study, side effects were reported in both the placebo and sildenafil groups. Headache was the most common side effect. No patient, except for the 1 patient with bluish visual hallucination, discontinued the drug. Similar sideeffect profiles were reported in other studies. 9,12,15,19 However, such visual changes similar to those of our patient also are reported in the literature of patients administered sildenafil. 25 In conclusion, treatment with sildenafil citrate in selected renal transplant recipients with ED is a valid option with an effective response. Although the same metabolic degradation pathway is used for sildenafil as for cyclosporine, no change is required in the initial dose of immunosuppression. SHARMA ET AL REFERENCES 1. National Institutes of Health Consensus Development Panel on Impotence: Impotence. JAMA 270:83-90, Turk S, Karalezli G, Tonbul HZ, et al: Erectile dysfunction and the effects of sildenafil treatment in patients on haemodialysis and continuous ambulatory peritoneal dialysis. Nephrol Dial Transplant 16: , Rosas SE, Joffe M, Franklin E, et al: Prevalence and determinants of erectile dysfunction in hemodialysis patients. Kidney Int 59: , Salvatierra JR, Fortman JL, Belzar FO: Sex function of males before and after renal transplantation. Urology 5:64-66, Gittes RF, Waters WB: Sexual impotence: The overlooked complication of a second renal transplant. J Urol 121: , Lue TF: Erectile dysfunction. N Engl J Med 342: , Goldstein I, Lue TF, Padma-Nathan H, Rosen RC, Steers WD, Wicker PA, for the Sildenafil Study Group: Oral sildenafil in the treatment of erectile dysfunction. N Engl J Med 338: , Paul HR, McLeish D, Rao TKS, Friedman EA: Initial experience with sildenafil for erectile dysfunction in maintenance hemodialysis (MD) patients. J Am Soc Nephrol 11: 222A, 1999 (abstr) 9. Seibel I, Eduardo Poli De Figueiredo C, Teloken C, Feliz Moraes J: Efficacy of oral sildenafil in hemodialysis patients with erectile dysfunction. J Am Soc Nephrol 13: , Rosas SE, Wasserstein A, Kobrin S, Feldman HI: Preliminary observation of sildenafil treatment for erectile dysfunction in dialysis patients. Am J Kidney Dis 37: , Chen J, Mabjeesh NJ, Greenstein A, Nadu A, Matzkin H: Clinical efficacy of sildenafil in patients on chronic dialysis. J Urol 165: , Prieto Castro RM, Anglada Curado FJ, Regueiro Lopez JC, et al: Treatment with sildenafil citrate in renal transplant patients with erectile dysfunction. Br J Urol Int 88: , Zhang Y, Guan DL, Ou TW, et al: Sildenafil citrate treatment for erectile dysfunction after kidney transplantation. Transplant Proc 37: , Russo D, Musone D, Alteri V, et al: Erectile dysfunction in kidney transplanted patients: Efficacy of sildenafil. J Nephrol 17: , Barrou B, Cuzin B, Malavaud B, et al: Early experience with sildenafil for the treatment of erectile dysfunction in renal transplant recipients. Nephrol Dial Transplant 18: , Lasaponara F, Paradiso M, Milan MG, et al: Erectile dysfunction after kidney transplantation: Our 22 years of experience. Transplant Proc 36: , Rosen RC, Riley A, Wagner G, Osterloh IH, Kirkpatrick J, Mishra A: The International Index of Erectile Function (IIEF): A multidimensional scale for assessment of erectile dysfunction. Urology 49: , 1997
6 SILDENAFIL CITRATE IN RENAL ALLOGRAFT RECIPIENT Cappelleri JC, Rosen RC, Smith MD, Mishra A, Osterloh IH: Diagnostic evaluation of the erectile function domain of the International Index of Erectile Function. Urology 54: , Rendell MS, Rajfer J, Wicker PA, Smith MD: Sildenafil for treatment of erectile dysfunction in men with diabetes: A randomized controlled trial. JAMA 281: , Sklar GN: Sildenafil citrate in the transplant recipient with erectile dysfunction. Int J Impotence Res 11:S70A, 1999 (suppl 1) 21. Chatterjee R, Wood S, McGarrigle HH, Lees WR, Ralph DJ, Neild GH: A novel therapy with testosterone and sildenafil for erectile dysfunction in patients on renal dialysis or after renal transplantation. J Fam Plann Reprod Health Care 30:88-90, Cuellar DC, Hamilton JP, Sklar GN: Sildenafil citrate in the transplant recipient with erectile dysfunction. J Urol 163: , Rostaing L, Tran Van T, Alder JL: Increased glomerular filtration rate in kidney transplant recipients who take sildenafil. N Engl J Med 342:1679, 2000 (letter) 24. Malavaud B, Rostaing L, Tran-Van T, Tack I, Ader JL: Transient renal effects of sildenafil in male kidney transplant recipients. Transplantation 15: , Vobig MA, Klotz T, Saak M, Bartz Schmidt KV, Engelmann U, Walter P: Retinal side-effects of sildenafil. Lancet 353:375, 1999
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