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Efficacy of testosterone gel in the treatment of erectile dysfunction in hypogonadal hemodialysis patients: a pilot study

Abstract

End-stage renal disease (ESRD) affects sexual function. The etiology of sexual dysfunction in ESRD is multifactorial and hypogonadism is not uncommon. In a cohort of 96 men with ESRD, scores on International Index of Erectile Function (IIEF) correlated with bioavailable testosterone (T; P<0.01). We further evaluated the effects of administration of T on ED in hypogonadal men on hemodialysis. Nine men with ED and hypogonadism (baseline bioavailable T <3.82 nmol l−1), received 5 g T-gel (1% (10 mg g−1) per day treatment for 6 months. The IIEF and frequency of sexual intercourse per week were used to assess treatment efficacy. T administration significantly increased serum T levels to the normal range, and was associated with statistically significant improvements of the scores of the IIEF domains (erectile function from 7.6±8.0 to 12.8±7.8; intercourse satisfaction from 3.4±4.5 to 4.8±3.1; orgasmic function from 4.8±3.1 to 3.4±2.9; sexual desire from 3.4±2.9 to 4.4±0.6; overall sexual satisfaction from 2.6±1.3 to 3.8±1.0). But scores of the IIEF did not normalize. Frequency of weekly sexual intercourse increased from 0.4±0.4 to 1.1±0.8 (P<0.05) after 6 months. There were no adverse effects. We conclude that restoring T levels to normal in men with ESRD improved scores on the IIEF and frequency of weekly sexual intercourse.

Introduction

Erectile dysfunction is a frequent occurrence in men with end-stage renal disease (ESRD).1, 2 Studies of patients with ESRD on hemodialysis (HD) have found that 57.9–88% of men have complaints of ED.3, 4, 5 This shows that despite the improvements in the treatment of ESRD over the past decade, prevalence of ED remains high. Sexual dysfunction and hypogonadism begin before patients reach ESRD and are not corrected by HD therapy.6

Hypogonadism leads not only to sexual dysfunction but also anemia, loss of lean body mass and altered bone metabolism.2, 7, 8, 9 It has been shown in men treated with HD that testosterone (T) concentrations inversely correlate with all-cause-related mortality, including cardiovascular disease.10 So there are reasons to believe that low T levels affect general health of patients with ESRD.

There have been a few studies addressing administration of T in HD patients.7, 11, 12 Remarkably, in the study of Brockenbrough et al.7 T administration of 100 mg of topical 1% T-gel for 6 months did not increase serum T levels and there was no effect on sexual function scores. But another study has shown that T transdermally administered daily as gel or patch resulted in a significant increase in serum T levels.13 Lawrence et al. studied the effectiveness of T replacement with depot T injections in men with biochemically proven hypogonadism.11 Only 3 of 27 patients benefited from T administration and the others had to use vacuum tumescence therapy to improve erectile function (EF).

So, there is limited information on the efficacy of administration of T only in men on HD with lower-than-normal serum T levels. The aim of this study was to evaluate the efficacy of administration of T on ED to hypogonadal ESRD patients on HD.

Methods

This study prospectively evaluated 102 male patients with ESRD receiving HD treatment between March 2008 and October 2008. Patients were treated in a teaching hospital and in a private HD center. Patients were on chronic HD and had received treatment (mean of 12 dialysis hours per week with polysulphone membranes) for at least 6 months. Six patients were unwilling to participate or there were other factors making them unsuitable for this study. The inclusion criteria were having ED (assessed with the International Index of Erectile Function (IIEF)–erectile function domain) and hypogonadism (based on levels of bioavailable T, as levels of sex hormone-binding globulin were strongly elevated). Patients who had undergone urogenital surgery or who had been treated with T earlier were excluded. Age, dialysis history and the number of weekly dialysis sessions of the patients were recorded. Coexisting diseases, use of medical drugs, urological complaints, were recorded. As another measure of sexual functioning the frequency of sexual intercourse per week was recorded as well. Each patient was asked to report the frequency of sexual intercourse per week in the last 4 weeks before the start of T treatment for baseline assessment and on days 30, 90 and 180 of the study.

A total of 96 patients with a median age of 48 years (18–81 years) were initially considered eligible for the study. The patients were receiving HD treatment for ESRD for a median period of 4 years (6 months to 16 years). The etiology of the ESRD was glomerulonephritis, hypertensive nephropathy, diabetes mellitus, obstructive nephropathy and polycystic kidney disease in 22, 10, 9, 4 and 2 patients, respectively. Alport syndrome, amyloidosis and familial Mediterranean fever were the etiology in the other three patients. None of these patients had used or was using PDE5 inhibitors because of listlessness and lack of sexual appetite.

Following physical examination, all patients were requested to fill out IIEF form of 15 questions (Qs).14 The IIEF has five domains: EF (Q1–Q5 and Q15, total score 1–30), intercourse satisfaction (Q6–Q8, total score 0–15), orgasmic function (Q9 and Q10, total score 0–10), sexual desire (Q11 and Q12, total score 2–10) and overall sexual satisfaction (Q13 and Q14, total score 2–10). The EF domain consists of six questions (erection frequency, Q1; erection firmness, Q2; penetration ability, Q3; maintenance frequency, Q4; maintenance ability, Q5 and erection confidence, Q15). Subjects who scored <26 in this domain were considered to have ED. The score for each item ranges from 0 to 5 for questions 1–10, 0 meaning no sexual activity/no attempt to have sexual intercourse, and from 1 to 5 for questions 11–15. The severity of ED was classified using five categories: no ED (EF score: 26–30), mild (EF score: 22–25), mild to moderate (EF score: 17–21), moderate (EF score: 11–16) and severe (EF score: 6–10).15

At baseline complete blood count, serum creatinine, albumin, PSA, alanine aminotransferase and serum hormone levels including follicle-stimulating hormone (FSH), luteinizing hormone (LH), prolactin (PRL), total and free T, sex hormone binding globulin (SHBG) and intact parathyroid hormone were measured.

Blood samples (8 ml) were obtained between 0800 and 0900 hours to minimize the confounding effects of diurnal variations in serum T. Serum (1 ml) from the blood taken from each sample was stored frozen at −18 °C until analyzed for measurement of SHBG. Autoanalyzer Immulite 2000 (DPC Diagnostic Products Corporation, Los Angeles, CA, USA) was used by using appropriate kit. Chemiluminescence was used as a method to measure levels of SHBG, LH, FSH, T, PSA and PRL.

The SHBG-bound fraction of T is biologically virtually inactive because of the high binding affinity of SHBG for T, and therefore, bioavailable T, which includes free and weakly bound T to albumin, was calculated. Calculated bioavailable T levels were assessed using the formula presented by the International Society for the Study of the Aging Male (available at www.issam.ch).

Patients with bioavailable T levels at screening of 3.82 nmol l−1 or less were considered hypogonadal. Of the 96 men initially selected for the study, 10 men eventually met the selection criteria of bioavailable T levels at screening of 3.82 nmol l−1 or less, and they were eligible for treatment with T-gel. However, before start of the T treatment, one patient suffered cardiovascular problems and had to be excluded from the prospective treatment group. So, nine men completed the research protocol.

They had a stable relationship with a female sexual partner. As safety measures, patients with an abnormal digital rectal examination and/or a PSA level >2.5 ng ml−1) were excluded. Hematocrit levels <45 were a requirement for inclusion in the study.

In addition to the monthly complete blood count and assessment of renal function variables, T levels were measured every month and SHBG and PSA levels were measured every 3 months. The patients were evaluated during monthly visits. To evaluate the potential changes in sexual functions, we requested the patients to fill out IIEF form on days 30, 90 and 180 of the study.

After baseline measurements, each patient applied 5 g T-gel (1% (10 mg g−1 T), Testogel; Bayer Schering Pharma, Montrouge Cedex, France) per day to different application sites (right and left upper arm/shoulder and hairless abdominal area). Application sites alternated throughout the study. After application of the gel to the skin, the gel dried within a few minutes. Patients washed their hands thoroughly with soap and water after gel application.

Main outcome measures

The scores on the different domains of the IIEF were used for assessment of sexual functioning of the hypogonadal ESRD patients before and after T-gel treatment. Also the frequency of weekly sexual intercourse was recorded and hormonal and hematological results in relation to bioavailable T were also recorded.

Statistical analysis

SPSS (Chicago, IL, USA) for Windows 10.0 statistics package program was used for statistical analysis of the data. Analysis of variance, Bonferroni test, Wilcoxon tests and Pearson's correlation analysis were used to analyze repeated measurements and P<0.05 was considered statistically significant.

This clinical study was carried out in an academic institution and was approved by the institutional ethical review board. All patients gave informed consent in writing before participating in the study.

Results

Based on the IIEF scores,15 ED was present in 90 of the total 96 patients initially selected for the study. The degree of ED was determined as mild, mild to medium, medium and severe in 15.70, 41.65, 18.70 and 17.70% of patients, respectively. In six (6.25%) patients, there was no ED. The weekly sexual intercourse average was 1 (0–4) and was lower in men with more severe degrees of ED.

There was no clear relationship of the degree of ED with respect to the various etiologies of ESRD. But in all of the diabetic patients medium and severe degrees of ED were found. On comparing of 86 men whose serum T was >3.82 nmol l−1 with the men with serum T 3.82 nmol l−1, it was found that all domains of the IIEF and frequency of sexual intercourse were significantly better in the first group than in the latter group (Table 1; P<0.001). There was a statistically significant correlation between serum T levels and scores on the IIEF (P<0.01). The creatinine and hematocrit levels were not different.

Table 1 Comparison of scores on IIEF between eugonadal and hypogonadal men with ESRD

Hypogonadism, defined as bioavailable T levels (3.82 nmol l−1), was found in 10 of the 90 patients with ED. The results of hypogonadal patients showed that there was a weak negative correlation between total T and age (r=−0.296; P<0.01). Various degrees of ED were seen in these patients. The average weekly frequency of sexual intercourse per week 0.4±0.4 (once per 2.5 weeks) before T treatment in this group.

In the patients defined as hypogonadal, IIEF–sexual desire score (P<0.05) and the weekly sexual intercourse frequency (0.4±0.4) were significantly lower (P<0.05), compared with HD patients without hypogonadism (1.0±0.4).

There was a weak positive correlation between the total of IIEF scores and the bioavailable T levels of the hypogonadal patients (r=0.406; P<0.05). There was also a weak positive correlation between the IIEF–sexual desire scores and the bioavailable T levels of the hypogonadal patients (r=0.338; P<0.05).

Using the methods described, 9 of the above 10 patients were eligible to be treated with T-gel in the study. Median HD period of the patients was 1.0±0.3 year. All nine patients completed the 6-month study. After the first month, the T levels of the patients had increased to reference levels (Table 1). In the follow-up period, the T level of one patient exceeded (total T: 41.2 nmol l−1) normal physiological T values. In the evaluation of this patient, 1 week later, it was found that the T level was normal. It may well be that in this patient venous blood sampling occurred in an area where T-gel had been applied. This was also encountered in other studies administering T-gel.16 No side effects requiring discontinuation of treatment were seen in any of the patients. None of the nine patients used any kind of PDE5 inhibitors.

International Index of Erectile Function scores and the number of weekly sexual intercourse increased significantly over the first month (P<0.05; Table 2) and then reached a plateau. Scores of IIEF at 3 months were not different from those at 1 month, and scores of IIEF at 6 were not different from scores at 3 months or at 1 month. Although it would seem that IIEF–sexual desire scores had declined at 6 months, the value at 6 months remained significantly higher than at baseline. Plasma levels of SHBG decreased profoundly on T administration. The levels of FSH and LH, which were higher than normal in the beginning, decreased significantly (P<0.05).

Table 2 IIEF and laboratory data of hypogonadal ESRD male patients (n=9) before and 1, 3 and 6 months after T-gel treatment

The average PRL level in the treatment group was 62.78 ng ml−1 (normal: 2.5–17 ng ml−1). PRL levels were not different between the total population of patients and the treatment group. There was no statistical significant relation between the PRL level and IIEF scores. There was no statistically significant change in PRL levels with the T replacement treatment (P>0.05).

Hematocrit levels had increased with an average of 4.9% at the end of 6 months (Table 2). In one of the patients in the study group, a clinically relevant increase in PSA was detected. The pathological examination of the prostate biopsy performed on this patient showed no signs of malignancy.

Discussion

This study found that men with ESRD requiring HD have an impairment of sexual functioning. We found that there was a strong correlation between IIEF scores and bioavailable T in the whole cohort of 96 men, potentially suggesting that T levels are a factor in sexual dysfunction in men with ESRD. This correlation was weaker in the men with serum T in the hypogonadal range.

We then analyzed the effects of administration of T to men treated with HD who had baseline levels of bioavailable T <3.82 nmol l−1 and IIEF scores qualifying them as having ED. Application of T-gel daily (5 mg per 24 h) consistently raised average serum total, free and bioavailable T concentrations to values in the mid-range for healthy young men. Normalization of serum T resulted in a significant increase in total and erectile function domain of IIEF scores. Then scores reached a plateau after 1 month and there were no significant further improvements when assessments were performed 3 and 6 months after initiation of T administration. Although the IIEF scores increased significantly in all patients, none of them attained an IIEF score of 26, regarded as normal erectile function. More importantly, T treatment led also to an increased sexual performance as shown by the significant increase in frequency of weekly intercourse.

The pathogenesis of ED in ESRD patients is manifold and includes hormonal disturbances, zinc deficiency, medications, peripheral neuropathy, peripheral vascular disease and biochemical disturbances not corrected by HD.1, 6, 8, 17 Normal levels of T are of major significance for normal male sexual behavior and potency.18, 19, 20 T monotherapy for the treatment of ED is very efficacious in men with hypogonadism when it is the sole cause of ED, but it is increasingly clear that it may also be beneficial in hypogonadal men with ED who have other pathologies, such as vascular disease and neuropathy.20, 21 In animal experimentation, experimental T deficiency caused significant reduction in trabecular smooth muscle and significant increase in connective tissue deposition concomitant with loss of erectile function.20, 22 These histological changes were partly reversible on normalization of T levels (for review see Saad et al.18 and Shabsigh et al.23). It is not clear in how far normalization of circulating T may be able to restore the histological damage to the corpus cavernosum in patients with ESRD.1, 24

In the ultrastructure of the corpora cavernosa in patients with ESRD treated with chronic HD, there are major changes in the structure of smooth muscle cells, with a reduction of dense bodies in the cytoplasm, and an increase of interstitial collagen fibers.24 Apart from the impairment of the anatomical substrate of erection in patients with ESRD there are endocrine factors. Testosterone deficiency may have impact on endothelial dysfunction and therewith being an etiological factor in ED.25

To elucidate the molecular mechanisms of hypogonadism in men with ESRD, Dunkel et al.26 tested the capacity of serum from ESRD patients to inhibit recombinant human LH receptor activity. Using a cell line expressing functional human LH receptors, they found that adenosine 3′5′-monophosphate production was markedly inhibited by sera from the patients, compared to sera from healthy subjects.26 However, the etiology of gonadal dysfunction remains largely unclear. A combination of primary testicular failure and secondary pituitary–hypothalamic dysfunction has been implicated.6, 27 There is no evidence that low serum T concentrations in men on HD can be explained by clearance during HD.13

Our patients had not tried PDE5 inhibitors. An earlier study indicated that is it rather sexual listlessness than lack of erectile function that prevents patients with ESRD from engaging in sexual activities.28 But PDE5 inhibitors have been used to treat patients with ED on HD.29 Seibel et al.30 evaluated the efficacy and tolerance to oral sildenafil to treat ED in ESRD in patients on HD. An improvement in the score of all questions and domains of the IIEF was found except those related to sexual desire.30 For the latter effect, addition of T might have been useful because sexual desire is exquisitely sensitive to the action of T.31 Indeed, in a study using combination therapy of sildenafil with T for ED in patients on HD or after renal transplantation, all patients had a good response to the combination of T and sildenafil, particularly hypogonadal patients.12

Our study restoring circulating plasma T to mid-normal levels was reasonably successful. In the study by Lawrence et al.11 administering depot injections, sexual function was fully restored in only three men (11.1%), and two gradually lost the response over 18 months. A total of 19 patients (70.3%) had partial responses, varying from an increased sense of well-being alone to restored sexual function apart from an impairment of the duration of penile erection. The patients in our study remained on HD for shorter time (1.0±0.3 years) than the participants of the study by Lawrence et al. (2.00±0.40 years).

In our study the hematocrit level increased on average by 4.9% after 6 months. This might have led to a better general condition thus improving sexual functioning as well. This boost may be helpful in cases of severe anemia and may lead to a reduction in the use of erythropoietin. In this study this was, however, not the case.

There are limitations to the design of our study that should be considered. The design was not double blind and placebo controlled and, therefore, it cannot be excluded that the effects of the T-gel were secondary to placebo effect. Further limitations of the study stem from the small number of participants, and relatively short follow-up period. We regard this study as a pilot study that hopefully leads to more studies including larger numbers of participants and longer duration.

In conclusion, normalization of serum T levels after administration of T-gel was an effective treatment for ED in the present sample of nine hypogonadal patients with ESRD on HD. Scores on the IIEF did, however, not normalize and combination with PDE5 inhibitors might achieve better results. Longer-term studies with a larger number of participants are required to measure the effects of normalization of serum T levels in men with subnormal T receiving HD for ESRD. The assessment should also measure parameters of general vitality, mood and fatigue, which might be elements in the improvement of sexual functioning as well.

Conflict of interest

SHBG kits (L2KSH2) were provided free of charge by Bayer Schering Pharma. No further disclosures to be made.

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Cangüven, Ö., Aykose, G., Albayrak, S. et al. Efficacy of testosterone gel in the treatment of erectile dysfunction in hypogonadal hemodialysis patients: a pilot study. Int J Impot Res 22, 140–145 (2010). https://doi.org/10.1038/ijir.2009.55

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Keywords

  • end-stage renal disease
  • erectile dysfunction
  • hypogonadism
  • testosterone

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