Sexual dysfunction in chronic renal failure

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1 QUALITY OF LIFE JNEPHROL 2008; 21 (suppl 13): S113-S Sexual dysfunction in chronic renal failure Guido Bellinghieri, Domenico Santoro, Agostino Mallamace, Vincenzo Savica Division of Nephrology, University of Messina, Messina - Italy ABSTRACT Recent studies have shown that testosterone is involved in the pathogenesis of cardiovascular diseases. Moreover, in observational studies blood testosterone concentrations, resulted consistently lower, not only among men with cardiovascular disease but also in men with uremia. In order to correlate the blood level of testosterone with the degree of erectile dysfunction (ED) and chronic renal failure (CRF) (stage I-V) we selected a group of patients with renal failure on conservative treatment, who attended our nephrology outpatients clinic. All the patients had stage II and III renal failure, respectively with a creatinine clearance between and ml/m. The sexual evaluation was done using a 15- item questionnaire, i.e. the International Index of Erectile Function (IIEF). Mean score of patients with ED were significantly lower than mean scores for healthy controls for all 15 questions (all p values <0.01). Preliminary results show a direct correlation between -IIEF and gromerular filtration rate (GFR) (R2 0.08); an inverse correlation between testosterone and cholesterol (R ); a higher number of diabetic patients with lower levels of testosterone, at level 3 of CRF; low levels of testosterone for smokers especially in stage II (GFR). These data confirm the direct correlation between ED and renal failure, and the role of diabetes and smoking in hypotestosteronemia, in patients with different degrees of renal insufficiency. Further prospective studies are needed in order to correlate cardiovascular morbidity and mortality in patients with CRF and blood levels of testosterone. Key words: Testosterone, Erectile dysfunction, Uremia, Cardiovascular disease INTRODUCTION Sexual disturbances and in particular, erectile dysfunction (ED) are common and often distressing side effects of renal failure with 40% of male dialysis patients and 55% of female dialysis patients reporting difficulty in achieving orgasm (1). In the uremic population, many patients report symptoms that include erectile dysfunction, decreased libido, and marked declines in the frequency of intercourse (2). With the starting of dialysis some of these symptoms may improve but without achieving the norm. Indeed in our dialysis population the prevalence of impotence, assessed by the international index of erectile function questionnaire, proposed by Rosen, was of 85% (3). On the other hand, in transplant population, a wellfunctioning kidney can restore sexual activity, even though some of the symptoms, relatively to the reproductive function may remain impaired, particularly reduced libido and erectile dysfunction (4). Sexual dysfunction has been related to several disturbances. In females, for example, a delay in sexual development, amenorrhea, and reduction of libido are frequently observed, while conception is rare (spontaneous abortion is a common eventuality). In males, we found a delay in sexual development, reduction in sexual drive, reduced frequency of sexual intercourse, partial or total impotency, decreased nocturnal penile tumescence, gynecomastia, testicular atrophy, oligospermia or azospermia (5). It is also possible to find an increased frequency of these disturbances among kidney transplant patients. The pathogenesis of these disturbances has been attributed to several factors, but to none of them conclusively. It has been linked to depression, zinc deficiency, autonomic dysfunction, cavernous body muscle dysfunction, and to alterations of the hormones of the hypothalamus-pituitary-gonad axis, secondary hyperparathyroidism, and antihy- S113

2 Bellinghieri et al: Erectile dysfunction in uremia pertensive therapy, such as beta-blockers, thiazide diuretics, clonidine, etc. (1). ED is associated with lower quality of life (QOL) scores, and it is a risk factor for the development of depression (6). Since penile erection requires an integral neurovascular structure, vascular disease, including hyperlipidemia, atherosclerosis, diabetes mellitus can interfere with the vascular mechanism underlying normal erection. Moreover, patients with sexual dysfunction have a likely comorbidity of cardiovascular disease and depression, as well as the potential increased risk for cardiac morbidity and mortality (7). ENDOCRINE PROBLEMS The endocrine abnormalities in men with chronic kidney disease best fit with impaired gonadal function. The alterations of the testicular system are mainly due to impaired spermatogenesis and are characterized by the decreased volume of ejaculate, low or complete azospermia, low percentage of motility and infertility. Elevated levels of prolactin hormone are frequently noted in patients with renal disease and are responsible for reduced libido. Since there is a negative correlation between renal function and prolactin levels, almost 80% of dialysis patients have hyperprolactinemia (8). Moreover, hyperparathyroidism stimulates prolactin synthesis and hyperprolactinemia is also associated with secondary hypogonadism. Increased plasma luteinizing hormone (LH) levels, are due to a reduced renal clearance rate of LH and also to stimulation of the pituitary by the diminished release of testosterone (9). FSH secretion is increased in patients with chronic kidney disease. Indeed there is damage to the seminiferous tubule and Sertoli cells with reduction of inhibin secretion which regulates FSH secretion, via a negative feedback loop (10) Modification of androgen synthesis and metabolism begins to appear early in the course of chronic kidney disease. Reduction of testosterone levels has been related to Leydig cell dysfunction (11). In spite of low plasma testosterone levels and impaired spermatogenesis, the levels of LH and FSH are elevated suggesting that the feedback mechanism between Leydig cells and the pituitary continues to operate (11). Today there is a new field of interest, represented by the molecular mechanism of testosterone and the role exerted in the pathogenesis of cardiovascular diseases. Observational studies show that blood testosterone concentrations are consistently lower among men with cardiovascular disease, as in the uremic men, suggesting a possible preventive role for testosterone therapy (12). Moreover, in observational studies, blood testosterone concentrations, resulted consistently lower not only among men with cardiovascular disease but also in men with uremia. Men with low testosterone levels are at increased risk of coronary artery disease: an antiinflammatory effect of normal physiological levels of sex hormones may, therefore, be important in athero-protection (13). A meta-analysis clearly indicates that gender is an important factor influencing the progression of some nondiabetic chronic renal diseases. However, it was not possible to determine whether the presence of testosterone or the absence of estrogen is a determining factor. Despite the reduction in androgens that occurs with aging, men progress to chronic renal failure at a more rapid rate than do women, even for similar levels of blood pressure (14, 15). Experimental studies showed that in aging rats, serum testosterone levels also decrease with age as found in men. It was reported that normotensive and hypertensive males present a more rapid progression of renal failure and more renal injury with age than do females (16). However, the degree of renal morphologic damage could not explain the reduction in GFR. Recent studies have been carried out in order to correlate the blood level of testosterone in patients with ED and different degrees of chronic renal failure (CRF) (stage I-V). For this reason we enrolled a group of patients on conservative treatment, who were attending our nephrology out patient clinic. Ninty-three patients with renal failure and ED, mean age 72+ years old (+8 SD) were selected. All the patients had stage II and III renal failure, with a creatinine clearance between and ml/m respectively. The evaluation was done using a 15-item sexual function questionnaire: International Index of Erectile Function (IIEF). Mean score of patients with ED were significantly lower than mean scores for healthy controls for all 15 questions (p values <0.01). A physician, expert in sexual problems, took the history and did a physical examination The arterial blood pressure, sexual hormone pattern, cholesterol and some other parameters related to life style were collected. Preliminary results show a direct correlation between IIEF and GFR (Fig. 1), an inverse correlation between testosterone and cholesterol (Fig. 2). Moreover, the number of S114

3 JNEPHROL 2008; 21 (suppl 13): S113-S117 Fig. 1 - Relation between IIEF score and renal function (GFR). Fig. 2 - Relation between testosterone and renal function (GFR). Fig. 3 - Diabetes and level of testosterone in patients with level 2 and 3 of CRF. diabetic patients hypotestorenemic increases in the group with level 3 of CRF (Fig. 3). These preliminary data require critical evaluation by further prospective studies. Among the various factors playing a role in the pathogenesis of sexual dysfunction in uremia, atherosclerosis represents an important cause. These patients prematurely suffer from atherosclerosis (to the point that it is generally recognized that an epidemic of cardiovascular incidents is present in this population), which is also the major contributing factor of the high mortality. Traditional risk factors, or those typical of uremia, cannot explain this increased mortality. It is obvious that the internal iliac artery, or the pelvic or pudenda artery can be the target of an atherosclerotic process, with consequent sexual dysfunction (1). In uremic patients on chronic dialysis vascular damage is frequently observed and it is probable that disturbances in fibrinolytic activity and endothelial dysfunction play an important role in peripheral vascular damage of which ED represents a pathological consequence. S115

4 Bellinghieri et al: Erectile dysfunction in uremia The integrity of the autonomic nervous system is essential for normal sexual activity (17, 18). Autonomic neuropathy can interfere with the complex neurological axis that is necessary for the achievement of an adequate erection. Anemia, which is a common complication of chronic kidney disease has been linked with a reduction of libido and erectile dysfunction. Some authors have shown that after correction of anemia with recombinant human erythropoietin (19, 20), there was improvement in oxygen delivery to the corpora cavernosa and amelioration of sex hormone abnormalities. Recent studies show that hyperhomocysteinemia is an important independent predictor of mortality and of cardiovascular events in hemodialysis patients (21). Hyperhomocysteinemia is present with a high prevalence in the uremic population. Indeed, this prevalence is estimated to be 60% in patients under conservative therapy and 90% in those on hemodialysis. High levels of homocysteinemia is also seen in transplant patients. Since it has been shown that hyperhomocysteinemia has a proatherogenic effect on the endothelium, it is possible that it may represent another risk factor for sexual dysfunction in uremia and in kidney transplantation. Men have higher levels of oxidative stress than do agematched women, despite the reduction in androgen levels in aging men (22). Renal hemodynamics in aging males is directly connected with nitric oxide (NO) system. Indeed, GFR and renal plasmatic flow (RPF) decreased to a much greater extent and glomerular capillary pressure almost doubled in aging males compared with young males after treatment with NO- synthase inhibitors (23). The identification of NO as the primary neurotransmitter of penile erection is well established and led to the development of oral agents for the treatment of ED. Some studies reported that insulin growth factor-1 (IGF-1) may contribute to the regulation of vascular tone mediated by NO (24). In chronic renal failure it has been shown alteration of the expression of NO-synthase (NOS) with concomitant changes in IGF-1. Since IGF-1 can selectively dilate vascular beds, leading to a decrease in regional blood flow and its action is mediated by NO, it is clear that circulating inhibitors factors that depress the activity of NOS, may decrease, at the same time, IGF-1 gene expression in penil tissue thus leading to a disturbance in sexual function (25). In conclusion, ED increases progressively with age but is not an inevitable consequence of aging. Current therapies for ED and other sexual dysfunction are safe and effective in the large majority of patients with or without cardiovascular disease, although the contraindications for sildenafil in patients taking nitrates should always be observed. Contrary to current public and professional opinion, many cases can be successfully managed with appropriate selected therapy. In particular we proposed a new algorithm according to the new insights in the treatment of impotence in the uremic population (5). Physicians need to be aware of the high incidence of ED among patients with CVD, because ED represents a symptom originating from damage to the vascular endothelium. The risk becomes more pronounced with increasing age, and for this reason all patients presenting with complaints of ED should be carefully assessed for the presence of cardiovascular risk factors (e.g., obesity, hypertension, hyperlipidemia). Conflict of interest statement: None declared. Address for correspondence: Prof. Guido Bellingheri Division of Nephrology and Dialysis University of Messina Policlinico Universitario Viale Gazzi Messina, Italy gbellinghieri@hotmail.com S116

5 JNEPHROL 2008; 21 (suppl 13): S113-S117 REFERENCES 1. Massry SG, Bellinghieri G. Sexual dysfunction. Textbook of Nephrology. 3rd ed. Baltimore: Williams and Wilkins; Feldman HA, Johannes CB, Derby CA, et al. Erectile dysfunction and coronary risk factors: prospective results from the Massachusetts male aging study. Prev Med. 2000;30: 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. J Urol. 1997;49: Shamsa A, Motavalli SM, Aghdam B. Erectile function in end-stage renal disease before and after renal transplantation. Transplant Proc. 2005;37: Bellinghieri G, Santoro D, Lo Forti B, Mallamace A, De Santo RM, Savica V. Erectile dysfunction in uremic dialysis patient: Diagnostic evaluation in the sildenafil era. Am J Kidney Dis. 2001;38(suppl 1):S Rosas SE, Joffe M, Franklin E, et al. Association of decreased quality of life and erectile dysfunction in hemodialysis patients. Kidney Int. 2003;64: Goldstein I. The mutually reinforcing triad of depressive symptoms, cardiovascular disease, and erectile dysfunction. Am J Cardiol. 2000;86:41F-45F. 8. Palmer BF. Sexual dysfunction in uremia. J Am Soc Nephrol. 1999;10: Schmidt A, Luger A, Horl WH. Sexual hormone abnormalities in male patients with renal failure. Nephrol Dial Transplant. 2002;17: Holdsworth S, Atkins RC, de Kretser DM. The pituitary-testicular axis in men with chronic renal failure. N Engl J Med. 1977;296: Tourkantonis A, Spiliopoulos A, Pharmakiotis A, Settas L. Haemodialysis and hypothalamo-pituitary-testicular axis. Nephron. 1981;27: Liu PY, Death AK, Handelsman DJ. Androgens and cardiovascular disease. Endocr Rev. 2003;24: Malkin CJ, Pugh PJ, Jones RD, Jones TH, Channer KS. Testosterone as a protective factor against atherosclerosis-- immunomodulation and influence upon plaque development and stability. J Endocrinol. 2003;178: Holley JL. The hypothalamic-pituitary axis in men and women with chronic kidney disease. Adv Chronic Kidney Dis. 2004;11: Neugarten J, Acharya A, Silbiger SR. Effect of gender on the progression of nondiabetic renal disease: a meta-analysis. J Am Soc Nephrol. 2000;11: Baylis C. Age-dependent glomerular damage in the rat. Dissociation between glomerular injury and both glomerular hypertension and hypertrophy. Male gender as a primary risk factor. J Clin Invest. 1994;94: Vita G, Bellinghieri G, Trusso A, et al. Uremic autonomic neuropathy studied by spectral analysis of heart rate. Kidney Int. 1999;56: Campese VM. Autonomic nervous system dysfunction in uraemia. Nephrol Dial Transplant. 1990;5(suppl 1):S Lawrence IG, Price DE, Howlett TA, Harris KP, Feehally J, Walls J. Erythropoietin and sexual dysfunction. Nephrol Dial Transplant. 1997;12: Schaefer F, van Kaick B, Veldhuis JD, et al. Changes in the kinetics and biopotency of luteinizing hormone in hemodialyzed men during treatment with recombinant human erythropoietin. J Am Soc Nephrol. 1994;5: Massy ZA, Chadefaux-Vekemans B, Chevalier A, et al. Hyperhomocysteinemia: a significant risk factor for cardiovascular disease in renal transplant recipients. Nephrol Dial Transplant. 1994;9: Ide T, Tsutsui H, Ohashi N, et al. Greater oxidative stress in healthy young men compared with premenopausal women. Arterioscler Thromb Vasc Biol. 2002;22: Reckelhoff JF, Manning RD Jr. Role of endothelial-derived nitric oxide in the control of the renal microvasculature in aging male rats. Am J Physiol Regul Integr Comp Physiol 1993;265:R Tsukahara H, Gordienko DV, Toushoff B, Gelato MC, Goligorski MS. Direct demonstration of insulin growth factor-1 induced nitric oxide production by endothelial cells. Kidney Int. 1994;45: Abdel Gawad M, Huynh H, Brock GB. Experimental chronic renal failure-associated erectile dysfunction: molecular alterations in nitric oxide synthase pathway and IGF-1 system. Mol Urol. 1999;3: Received: March 08, 2007 Revised: June 20, 2007 Accepted: July 16, 2007 Società Italiana di Nefrologia S117

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