ORIGINAL ARTICLE Hypogonadism is associated with overt depression symptoms in men with erectile dysfunction

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1 (2008) 20, & 2008 Nature Publishing Group All rights reserved /08 $ ORIGINAL ARTICLE Hypogonadism is associated with overt depression symptoms in men with erectile dysfunction AA Makhlouf 1, MA Mohamed 2, AD Seftel 3 and C Neiderberger 4 1 Department of Urologic Surgery, University of Minnesota, Minneapolis, MN, USA; 2 Urology Department El-Minia University Hospital, El-Minia, Egypt; 3 Department of Urology, Case Western Reserve University, University Hospitals of Cleveland, Cleveland, OH, USA and 4 Department of Urology, University of Illinois at Chicago, Chicago, IL, USA Depression and hypogonadism are associated with erectile dysfunction (ED). We evaluated the prevalence of both conditions in men presenting to an ED specialty clinic, and tested whether hypogonadism correlated with the presence of depressive symptoms using a validated questionnaire. From July 2001 to June 2003, 157 men referred to an ED specialty clinic prospectively filled the Center for Epidemiologic Studies Depression Scale (CES-D), the abbreviated International Index of Erectile Function (IIEF-5) and had testosterone serum levels drawn. Median age was 53 (range ¼ years). Hypogonadism, defined as serum T (testosterone)o300 mg/dl, was present in 36% of patients. This proportion was higher in men over the median age compared to younger patients (45 and 26%, respectively, P ¼ 0.002). Overt depression symptoms, defined as a CES-DX22, were found in 24% of men. Mean age of men with overt depression was years vs years for those with CES-Do22 (P ¼ 0.02). Hypogonadal men were more likely to have overt depression scores compared to eugonadal counterparts (35 vs 18%, P ¼ 0.02). This association was statistically stronger after correcting for age in a multivariate linear model (P ¼ 0.005). The relative risk of having overt depression was 1.94 times higher in men with hypogonadal testosterone level (95% confidence interval: 1.13 to 3.7). We conclude that in an ED referral population, symptoms of hypogonadism and depression symptoms are fairly prevalent, and that overt depression symptoms are strongly associated with hypogonadism. Clinicians should consider testosterone measurements in all men with high depression symptom scores. (2008) 20, ; doi: /sj.ijir ; published online 16 August 2007 Keywords: depression; testosterone; erectile dysfunction; hypogonadism; diagnosis; IIEF Introduction Testosterone levels decline gradually in aging men, with about 20% of men over 60 years having total testosterone levels dip below the accepted normal threshold. 1 This drop in androgen levels parallels an increase in the prevalence of erectile dysfunction (ED). 2 Testosterone supplementation has been shown to improve erectile function and rescue sildenafil failures. 3,4 Thus, there is a clear incentive for urologists to identify men with hypogonadism. Correspondence: Dr AA Makhlouf, Department of Urologic Surgery, University of Minnesota, 420 Delaware St SE MMC 394, Minneapolis, MN 55455, USA. makhl001@umn.edu Received 18 November 2006; revised 3 March 2007; accepted 1 May 2007; published online 16 August 2007 Depression was associated with 1.8-fold increase in the prevalence of ED in the Massachussetts Male Aging Study independent of age or the traditional organic comorbidities associated with ED. 2,5 The prevalence of depression in large epidemiological studies of ED has been reported as ranging from 11 to 25%. 6,7 Even higher rates (25 55%) were reported in men attending andrology clinics. 8,9 Furthermore, Shabsigh et al. 8 found that patients with ED and concomitant depression were more likely to discontinue therapy, making assessment of depression symptoms an important aspect of ED evaluation. There is an overlap between symptoms of hypogonadism and depression. One study has found that men with hypogonadal testosterone values are at higher risk of developing depression, 10 while others have not. 5,11 In this paper, we examine the correlation between depression symptoms and hypogonadsim in men attending an ED clinic. We specifically determine if men with hypogonadism

2 158 and depression form an overlapping sub-population of ED patients. Table 1 Summary data for all patients in the study Mean Median Range Methods Total serum testosterone levels were obtained from 185 consecutive patients presenting to an andrology specialty clinic with a chief complaint of ED between July 2001 and June Samples were drawn in the morning hours in most patients with rare exceptions. The Center of Epidemiologic Study Depression questionnaire (CES-D) and the fivequestion International Index of Erectile Function (IIEF-5) was administered as measures of depression and erectile function, respectively. The CES-D is an inventory of 20 questions on a 4-point scale, with a score of suggestive of mild or reactive depression, whereas a score of 22 or higher corresponding to signs of overt depression. 12,13 The IIEF-5 is widely used and validated measure of erectile function. 7 Men with incomplete data and those already on testosterone therapy were excluded, leaving a total of 157 to form the basis of this analysis. Of these, six patients had previously failed sildenafil oral therapy, and four had a diagnosis of depression or were taking anti-depressant medication. The number of men excluded because they were on testosterone was 11, with a mean CES-D score of Statistical analysis was performed with the R statistical package. 14 Age (years) IIEF CES-D Testosterone (ng/dl) Abbreviations: BPH, benign prostatic hyperplasia; CAD, coronary artery disease; CES-D, Center for Epidemiologic Studies Depression Scale; HTN, hypertension; IIEF-5, International Index of Erectile Function-5. Major comorbidites by patient-self report: diabetes, 21; Peyronie s, 4; BPH, 3; depression, 3; CAD, 2; HTN, 2; prostate cancer, 1. Proportion with T<300 ng/dl Hypogonadism by Age Group * Results The median age of men in the cohort was 53 (range ¼ years) with a mean of years (mean7s.d.). Mean IIEF-5 score was Mean testosterone was ng/dl (Table 1). Diabetes mellitus was the most common co-morbidity reported by 21% of patients (Table 1). Hypogonadism, defined as testosterone level below 300 ng/dl, was found in 57 men or 36%. It was less prevalent in men under the median age of 53 years compared to men aged 53 years or above (26 vs 45%, respectively, P ¼ 0.02; Figure 1). Seventy-one men, or just under half the cohort, had symptoms suggestive of at least mild depression (CES-D415). Of these, 38 men (24% of total) had a CES-D score above 21, a cutoff suggesting the presence of overt depression. Compared to the other men, patients with overt depression symptoms tended to be younger (mean age ¼ vs years for those with CES-D under 22; P ¼ 0.019). To examine the correlation between hypogonadism and overt depression symptoms, a 2 2 contingency table was created (Table 2). This shows that overt depression symptoms are 1.9 times more likely to be present if testosterone values were 0 below 300 ng/dl. In contrast, mild or reactive depression scores did not correlate at all with hypogonadism (Figure 2). Because both hypogonadism and depression varied with age, we corrected for age influence in a multivariate logistic regression model (Table 3). Correction for age increased the statistical significance of hypogonadism in predicting depression (P ¼ after correction). Discussion All Under and older Age Group Figure 1 Proportion of patients with hypogondal values of testosterone (o300 ng/dl) divided between those below the median age of 53 years and those above it. *Po0.05 vs under 53 group. Androgen deficiency is associated with depression, 10 and both conditions are associated with ED. 3,6 The present study shows that both conditions

3 are fairly prevalent in an ED clinic population, and that there is increased likelihood of finding depression among men with hypogonadism. Table contingency table showing the correlation of hypogonadism with presence or absence of overt depression symptoms. Mild or no depression symptoms (CES-D p21; n ¼ 117) Overt Sxs (CES-D 421; n ¼ 38) Normal T 82 (82%) 18 (18%) Low T 37 (65%) 20 (35%) (o300 ng/dl) Abbreviations: CES-D, Center for Epidemiologic Studies Depression Scale; CI, confidence intervals; T, testosterone. The relative risk of having overt depression if hypogonadal group is 1.95 higher than in eugonadal men (95% CI: ). P ¼ 0.02 by w 2 test. Proportion of patients None (CES-D<15) Normal T T < 300 ng/dl Mild CES-D Depression Symptoms p < 0.05 Overt CES-D 22 Figure 2 Comparison of depression symptom classification in eugonadal and hypogonadal men. Odds of having overt depression scores in hypogonadal men were significantly higher compared to eugonadal men (P ¼ 0.02 by w 2 test). Androgen deficiency is associated with a variety of symptoms in aging men. 15 In addition to physical signs such as loss of muscle mass and bone density, low testosterone values are associated with forgetfulness, insomnia, depressed mood and low sex drive. 15 Androgen blockade in prostate cancer patients leads to a rise in depression and anxiety symptoms and weakening of verbal memory. 16,17 In contrast, testosterone supplementation leads to an improvement in the sense of well being and a rise in libido. 18 Because of the effects of mood and libido on sexual performance, we determined the rate of hypogonadism in an ED referral population. Using a sensitive cutoff of 300 ng/dl, we found testosterone deficiency in 36% of men, while a more stringent cutoff of 200 ng/dl gave a rate of 9.5%. Regardless of cutoff, hypogonadism was more common in men over the median age. Total testosterone levels did not correlate with severity of ED as measured by the IIEF-5, even after correction for age (data not shown). This agrees with Shabsigh et al., 3 who did not find a correlation between Sexual Health Inventory for Men (SHIM) score and testosterone level in men supplemented with testosterone for ED. Overall, our rate of hypogonadism was higher than that reported for community men in general. 1 Recognition of testosterone deficiency is important since testosterone supplementation can rescue sildenafil failures. 3 This effect of testosterone is likely due to stabilization of neuronal nitric oxide synthase expression, 19 although other mechanisms such as prevention of smooth muscle cell loss through apoptosis have been proposed. 20 Previous epidemiological studies have found a strong correlation between the presence of ED and depression. In a multinational survey of over men, Rosen et al. 21 found depression to be twice as common in men with ED than in their potent counterparts. Conversely, the presence of depression correlated with a high prevalence of ED (25%), similar to the prevalence in men with hypertension or dyslipidemia, and much higher than in men without comorbidities (10%). 21 Seftel et al. 6 reported the incidence of depression to be 11.1% in men identified with ED in a managedcare claims database, and found that this prevalence was higher in the younger age groups, in agreement 159 Table 3 Effect of age, hypogonadism and IIEF-5 score on the probability of having overt depression symptoms in a multi-variate logistic regression model. Variable Coefficient Odds ratio P-value Intercept Age (years) (per additional year) ** Hypogonadism (yes/no) (if hypogonadal) ** IIEF-5 score (points) (per additional point) * Abbreviation: IIEF-5, International Index of Erectile Function-5. **Po0.001, *Po0.05 calculated for null hypothesis that coefficient is equal to zero. Negative coefficient means likelihood of depression decreases with increasing age and increasing IIEF-5 score. Presence of hypogonadism increases odds of overt depression.

4 160 with the present findings. These large epidemiological surveys have been borne out in studies of men attending ED specialty clinics. Shabsigh et al. 8 reported that 55% of men presenting to an ED clinic had significant depression symptoms as measured by the Beck Depression Inventory. Finally, treatment of ED with phosphodiesterase 5 (PDE5) inhibitors has been shown to improve depressive symptoms in two randomized controlled trials. 22,23 It should be noted that the prevalence of depressive symptoms in our cohort was significantly higher than that found in epidemiological surveys. 5,6 In the Massachusetts Male Aging Study (MMAS) sample, the overall prevalence of depressive symptoms defined as CES-D416 was 12%, much lower than in our study. 5 This can be explained by two factors. First, in the MMAS sample, the presence of depression increased the odds of ED twofold. Therefore, the prevalence of depressive symptoms among the ED subgroup of the MMAS is necessarily higher than 12%. Second, not all men with ED in the MMAS sought treatment for ED, and one would expect patients presenting to a clinic to be more distressed about ED and therefore score was higher on the CES-D. This is supported by the fact that another study of ED in an andrology clinic setting revealed similarly high prevalence of depressive symptoms. 8 Still, we cannot discount the possibility that our cohort represents a slightly skewed population of severe or refractory cases, especially that the clinic is a known tertiary referral center. Thus, one should be careful in generalizing our findings to a non-ed clinic population, such as one presenting for screening at a health fair or for an unrelated problem at a primary care clinic. Since both depression and hypogonadism are associated with ED, and since men with hypogonadal testosterone levels are at threefold increased risk of developing depression symptoms, 10 we examined the possibility that men with depression and low testosterone form a single subgroup in ED patients. We found that hypogonadal men were almost twice as likely to have high depression scores. Mild elevations on the depression scale, however, were not good correlates of hypogonadism. The relationship of depression and hypogonadism is even more striking considering that they vary in inverse ways with aging (hypogonadism more common in older men, while depression is less). This is borne out by the fact that correction for age improved the statistical strength of our conclusion. This agrees with the results reported by Shores et al., again stressing the need to evaluate both gonadal status and mood in men with ED. In fact, we have previously shown that depression scores can be used as a clinical aid to predict hypogonadism using an artificial neural network model. 24 The present study lends further support to this concept. Some limitations in the current study should be pointed out however. First, it did not address the question of whether depression contributes to the development of ED, or whether depression itself is the result of organic ED. Similarly, it does not establish a cause effect relationship between hypogonadism and depression. In fact, Schmidt et al. 25 have found that experimental androgen deprivation leads to depression in only a minority of men, while Seidman et al. 26 found no benefit to testosterone injections in treating depression in a small trial of men with concomitant major depression and low testosterone. Both studies therefore cast some doubt on the hypogonadism-depression linkage. Second, the present study is limited by the accuracy of the CES-D in diagnosing clinically relevant depression. The CES-D was designed as a population screening tool and not a diagnostic instrument in a clinical setting, and the optimal cutoff of the CES-D varies according to the population at hand. Unfortunately, the criterion validity of the CES-D in a population similar to ours (clinic-based, middle-aged, North American males with ED) has not been established. Studies of other populations have found the optimal cut point to be higher than the traditional value of 16, with most being between 18 and ,27 31 In the present work, we analyzed the data using both the traditional cutoff of 16, as well as the more stringent cutoff of 22 recommended by Haringsma et al., 13 and found an association of hypogonadism with the more overt depression scores. This finding agrees in part only with that of Delhez et al., 32 who also found that hypogonadism was associated with depressive scores, but reported that this association was strongest in men with mild depression symptoms, as opposed to pathological cases. Because the two studies used different questionnaires, a direct comparison is not possible in the absence of clinician-verified diagnosis of depression. In conclusion, depression symptoms and low testosterone are prevalent in ED patients referred to specialized clinics. Although limited in some respects, the present study shows a significant association between the two conditions, and suggests that men with hypogonadism and depression form a distinct subgroup of ED patients. References 1 Harman SM, Metter EJ, Tobin JD, Pearson J, Blackman MR. Baltimore Longitudinal Study of Aging. Longitudinal effects of aging on serum total and free testosterone levels in healthy men. Baltimore Longitudinal Study of Aging. J Clin Endocrinol Metab 2001; 86: Feldman HA, Goldstein I, Hatzichristou DG, Krane RJ, McKinlay JB. Impotence and its medical and psychosocial correlates: results of the Massachusetts Male Aging Study. J Urol 1994; 151: Shabsigh R, Kaufman JM, Steidle C, Padma-Nathan H. Randomized study of testosterone gel as adjunctive therapy to sildenafil in hypogonadal men with erectile dysfunction who do not respond to sildenafil alone. J Urol 2004; 172:

5 4 Rosenthal BD, May NR, Metro MJ, Harkaway RC, Ginsberg PC. Adjunctive use of AndroGel (testosterone gel) with sildenafil to treat erectile dysfunction in men with acquired androgen deficiency syndrome after failure using sildenafil alone. Urology 2006; 67: Araujo AB, Durante R, Feldman HA, Goldstein I, McKinlay JB. The relationship between depressive symptoms and male erectile dysfunction: cross-sectional results from the Massachusetts Male Aging Study. Psychosom Med 1998; 60: Seftel AD, Sun P, Swindle R. The prevalence of hypertension, hyperlipidemia, diabetes mellitus and depression in men with erectile dysfunction. J Urol 2004; 171(6 Part 1): Rosen RC, Cappelleri JC, Smith MD, Lipsky J, Pena BM. Development and evaluation of an abridged, 5-item version of the International Index of Erectile Function (IIEF-5) as a diagnostic tool for erectile dysfunction. Int J Impot Res 11; 319: Shabsigh R, Klein LT, Seidman S, Kaplan SA, Lehrhoff BJ, Ritter JS. Increased incidence of depressive symptoms in men with erectile dysfunction. Urology 1998; 52: Mallis D, Moysidis K, Nakopoulou E, Papaharitou S, Hatzimouratidis K, Hatzichristou D. Psychiatric morbidity is frequently undetected in patients with erectile dysfunction. J Urol 2005; 174: Shores MM, Sloan KL, Matsumoto AM, Moceri VM, Felker B, Kivlahan DR. Increased incidence of diagnosed depressive illness in hypogonadal older men. Arch Gen Psychiatry 2004; 61: Seidman SN, Araujo AB, Roose SP, McKinlay JB. Testosterone level, androgen receptor polymorphism, and depressive symptoms in middle-aged men. Biol Psychiatry 2001; 50: Radloff L. The CES-D scale: a self-report depression scale for use in the general population. Appl Psychol Measure 1; 385: Haringsma R, Engels GI, Beekman AT, Spinhoven P. The criterion validity of the Center for Epidemiological Studies Depression Scale (CES-D) in a sample of self-referred elders with depressive symptomatology. Int J Geriatr Psychiatry 2004; 19: R Development Core Team and the R Foundation for Statistical Computing. R: A Language and Environment for Statistical Computing. Vienna, Austria Wald M, Meacham RB, Ross LS, Niederberger CS. Testosterone replacement therapy for older men. J Androl 2006; 27: Almeida OP, Waterreus A, Spry N, Flicker L, Martins RN. One year follow-up study of the association between chemical castration, sex hormones, beta-amyloid, memory and depression in men. Psychoneuroendocrinology 2004; 29: Beer TM, Bland LB, Bussiere JR, Neiss MB, Wersinger EM, Garzotto M et al. Testosterone loss and estradiol administration modify memory in men. J Urol 2006; 175: Wang C, Swerdloff RS, Iranmanesh A, Dobs A, Snyder PJ, Cunningham G et al. Testosterone Gel Study Group. Transdermal testosterone gel improves sexual function, mood, muscle strength, and body composition parameters in hypogonadal men. J Clin Endocrinol Metab 2000; 85: Baba K, Yajima M, Carrier S, Morgan DM, Nunes L, Lue TF et al. Delayed testosterone replacement restores nitric oxide synthase-containing nerve fibres and the erectile response in rat penis. BJU Int 2000; 85: Traish AM, Munarriz R, O Connell L, Choi S, Kim SW, Kim NN et al. Effects of medical or surgical castration on erectile function in an animal model. J Androl 2003; 24: Rosen RC, Fisher WA, Eardley I, Niederberger C, Nadel A, Sand M. Men s Attitudes to Life Events and Sexuality (MALES) Study. The multinational Men s Attitudes to Life Events and Sexuality (MALES) study: I. Prevalence of erectile dysfunction and related health concerns in the general population. Curr Med Res Opin 2004; 20: Seidman SN, Roose SP, Menza MA, Shabsigh R, Rosen RC. Treatment of erectile dysfunction in men with depressive symptoms: results of a placebo-controlled trial with sildenafil citrate. Am J Psychiatry 2001; 158: Rosen R, Shabsigh R, Berber M, Assalian P, Menza M, Rodriguez-Vela L et al. Vardenafil Study Site Investigators. Efficacy and tolerability of vardenafil in men with mild depression and erectile dysfunction: the depression-related improvement with vardenafil for erectile response study. Am J Psychiatry 2006; 163: Kshirsagar A, Seftel A, Ross L, Mohamed M, Niederberger C. Predicting hypogonadism in men based upon age, presence of erectile dysfunction, and depression. Int J Impot Res 2006; 18: Schmidt PJ, Berlin KL, Danaceau MA, Neeren A, Haq NA, Roca CA et al. The effects of pharmacologically induced hypogonadism on mood in healthy men. Arch Gen Psychiatry 2004; 61: Seidman SN, Spatz E, Rizzo C, Roose SP. Testosterone replacement therapy for hypogonadal men with major depressive disorder: a randomized, placebo-controlled clinical trial. J Clin Psychiatry 2001; 62: Hedayati SS, Bosworth HB, Kuchibhatla M, Kimmel PL, Szczech LA. The predictive value of self-report scales compared with physician diagnosis of depression in hemodialysis patients. Kidney Int 2006; 69: Lyness JM, Noel TK, Cox C, King DA, Conwell Y, Caine ED. Screening for depression in elderly primary care patients. A comparison of the Center for Epidemiologic Studies-Depression Scale and the Geriatric Depression Scale. Arch Intern Med 1997; 157: Murrell SA, Himmelfarb S, Wright K. Prevalence of depression and its correlates in older adults. Am J Epidemiol 1983; 117: Wada K, Tanaka K, Theriault G, Satoh T, Mimura M, Miyaoka H et al. Validity of the Center for Epidemiologic Studies Depression Scale as a screening instrument of major depressive disorder among Japanese workers. Am J Ind Med 2007; 50: Beekman AT, Deeg DJ, Van Limbeek J, Braam AW, De Vries MZ, Van Tilburg W. Criterion validity of the Center for Epidemiologic Studies Depression scale (CES-D): results from a community-based sample of older subjects in The Netherlands. Psychol Med 1997; 27: Delhez M, Hansenne M, Legros JJ. Andropause and psychopathology: minor symptoms rather than pathological ones. Psychoneuroendocrinology 2003; 28:

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