http://orcid.org/0000-0002-2791-8028
Abstract
Objectives: Determination of the potential effect of metabolic syndrome (MetS) on erectile function in Egyptian men and description of the sociodemographic characteristics of these men.
Materials and methods: A cohort of 615 patients presenting to urology department aged between 30 and 75 years were prospectively assessed and divided into two groups. Group I (n = 325) diagnosed with MetS and mean age of 56.07 ± 8.51 years. Group II (n = 290) subjects with no MetS and mean age 54.97 ± 8.14 years. Patients filled the IIEF questionnaire, medical, personal history, and BMI data were tabulated. Metabolic syndrome was determined when three or more of the five risk factors were present according to the NCEP.
Results: In Group I (79.4%) of the patients had erectile dysfunction (ED). Of these, 20.3% had mild, 22.5% had moderate, and 36.6% had severe ED and 30% of patients without MetS had ED. Of these, 17.2% had mild, 5.9% had moderate, and 6.9% had severe ED (p < .001; odds ratio 5.549; 95% CI 3.101–9.928). Patients with metabolic syndrome had lower IIEF-EF domain scores. Logistic regression analysis revealed that DM, dyslipidemia, age, and HTN were the most important criteria for ED in the MetS group (p < .01). While in the group without MetS, DM, HTN, HDL, and age were the most important risk factors (p < .01), and TG and BMI were less important.
Conclusions: MetS is a potential risk factor for ED in Egyptian men. Patients with MetS should be questioned about ED. The diabetic patients are most risky for ED.
Introduction
Erectile dysfunction (ED) is a benign disorder, but it can have a significant impact on the quality of life of sufferers, partners, and families [Citation1]. ED is defined as the persistent inability to achieve or maintain penile erection sufficient for satisfactory sexual performance [Citation2]. A period of persistence of ED over 3 months has been suggested as a reasonable clinical guideline [Citation2,Citation3].
Erection depends on a delicate balance of signals from central and peripheral nervous systems affecting the neurotransmitters leading to arterial and venous changes resulting in erection.
The National Institutes of Health (NIH) recommended the use of ED as it is a more precise term, because sexual desire and ability to have an orgasm and ejaculate may well be intact despite the inability to achieve or maintain an erection [Citation2].
Erectile dysfunction is a common medical problem, its incidence differ according to age, the prevalence of ED was 1–10% in men younger than 49 years, 20–40% among men in 60–69 years range and 50–100% in men older than 70 years [Citation4].
The etiology of ED may be categorized as psychogenic, organic, or mixed according to the presence of the offending cause. Metabolic syndrome is one of the diseases that cause ED [Citation5,Citation6]. It generally refers to a constellation of interrelated cardiac risk factors consisting of insulin resistance (IR), abdominal (central) obesity, atherogenic dyslipidemia, endothelial dysfunction, and systemic inflammation [Citation7]. MetS increases the risk of developing cardiovascular disease, particularly heart failure and diabetes [Citation8].
Aim of the work
The objective of the present study was to determine the prevalence of ED in a sample of Egyptian men; as ED is neither well documented nor studied in Egyptian male population, and determine the effect of MetS on ED incidence and compare this data to ED prevalence in other nationalities.
Patients and methods
This prospective randomized study was conducted on a total of 615 consecutive married men patients who attended the urology outpatient clinics in Alexandria University Hospital.
History covering personal, medical, socio-demographic, and life style data was obtained from all patients. The level of education was graded as low if it was lower than senior high school, middle if finishing the senior high school, and high if it was involving university education.
The presence of MetS was determined according to the NCEP ATP-III guideline [Citation9]. When a patient had three or more risk factors, he was assumed to have MetS. These risk factors include: waist circumference (WC)> 102 cm; BP ≥ 130/85 mmHg; FBG ≥ 110 mg/dL; HDL-cholesterol < 40 mg/dL, and TG ≥ 150 mg/dL.
The patients were asked to answer the abridged five-item version of the IIEF [Citation10] to determine the presence of ED. The IIEF-5 allowed classification of ED as severe (1–7), moderate (8–11), mild to moderate (12–16), mild (17–21), and no ED (22–25). The individuals filled the Arabic version of IIEF questionnaire by themselves [Citation11].
All individuals underwent physical examination including measurement of height, weight, blood pressure, and supine waist circumference (WC) measured at the level of umbilicus with the person breathing silently.
Overnight fasting venous blood specimens were collected between 8 am and 11 am from all subjects for serum triglycerides (TG), high-density lipoprotein (HDL) cholesterol, and fasting blood sugar (FBS) analysis.
The ethics committee at faculty of medicine approved this study. Patients were previously informed of the research details and they agreed to participate in the study. Informed consent was obtained at the interview.
Data were analyzed using IBM SPSS software package version 20.0 (IBM SPSS Statistics, Armonk, NY). Qualitative data were described using number and percent. Quantitative data were described using range (minimum and maximum), mean, standard deviation, and median. The comparison between different groups was tested using Chi-square test and Fisher’s exact test or the Monte-Carlo correction. The distributions of quantitative variables were tested for normality using the Kolmogorov–Smirnov test, Shapiro–Wilk test, and D'Agstino test; also, histogram and QQ plot were used for vision test. If it reveals normal data distribution, parametric tests were applied. If the data were abnormally distributed, non-parametric tests were used. For normally distributed data, independent t-test was used. For abnormally distributed data, Mann–Whitney test was used.
Correlations and partial correlation between two quantitative variables were assessed using Spearman’s coefficient. Odds ratio (OR) and 95% confidence interval were used to calculate the ratio of the odds of an event occurring in one patient group to the odds of it occurring in the control group.
Subjects were divided, according to the duration of ED suffering, into three categories, <5 years, 5–10 years, and >10 years. The comparison was done using Chi-square, Monte-Carlo, and Spearman coefficient tests.
Results
The patients in the current study (n = 615) were divided into two groups according to the presence of MetS. Group I included patients diagnosed with metabolic syndrome, 325 (53%) while Group II included normal individuals, 290 (47%).
The data were collected from December 2013 to September 2014. The mean age for men with MetS was matched with the mean age for men in the control group (56.07 ± 8.51 vs. 54.97 ± 8.14 years, respectively). Subjects included in the study were from three governorates (Alexandria 70%, El-Behera 20%, and Kafr El-Shiekh 10%).
Demographics and laboratory findings in both study groups
Individuals with MetS were insignificantly older than the individuals without MetS (p > .05). Compared with the control group, the patients with MetS had decreased IIEF-5 scores (13.56 ± 7.35 vs. 21.54 ± 5.32), p < .001 ().
Table 1. Comparison between different parameters of the two studied groups.
Mean scores for all metabolic risk factors were higher in individuals with MetS than individuals without MetS except mean score of HDL (p < .001).
ED prevalence and severity
With regard to IIEF-5, 258 (79.4%) patients with MetS and 87 (30%) patients without MetS had the diagnosis of ED. A significant association was determined between the presence of MetS and ED (p < .001; OR, 8.985; 95% CI 6.220–12.980), as well as the prevalence of severe ED was significantly higher in patients with MetS than patients without MetS (36.6% vs. 5.9%; p < .001; OR → 21.209; 95% CI → 11.894–37.818) ().
Table 2. Comparison between patients with MetS and patients without MetS according to ED prevalence and severity.
The relationship between the MetS components and ED
The result of univariate analysis in the MetS group showed that all metabolic risk factors had statistically significant correlations with ED (p < .05) (), except WC and BMI which were statistically insignificant when correlated to ED. It was noted that the total MetS patients with WC >102 cm were 283 (87%) individuals, in whom 227 (69.8%) had ED while 31(9.5%) of MetS patients with WC ≤102 cm had ED.
Table 3. Association of metabolic risk factors and ED in MetS.
The result of univariate analysis for ED in the group without MetS showed associations between qualitative variables and ED, revealing that the frequencies of ED was significantly greater in patients with the quantitative variables like DM, HT, HDL, TG (p < .05), while no significant correlation was noted with WC.
Patients with MetS were classified according to the number of metabolic risk factors into three groups. IIEF-5 scores significantly decreased as the number of metabolic risk factors increased (p < .001). For example, the total patients who had five metabolic risk factors were 86 in whom 81 had ED (p < .001) ().
The logistic regression analysis was repeated with continuous variables which revealed that DM, dyslipidemia, age, and HTN were the most important criteria for ED in the MetS group (p < .01) (). While in the group without MetS, logistic regression analysis revealed that DM, HTN, HDL, and age were the most important risk factors (p < .01) and TG and BMI were less important (p > .05) ().
Table 4. Multivariate analysis Binary logistic regression for ED in thecontrol group.
Out of 160 MetS patients with known history of hypercholesterolemia, 137 (85.6%) had ED and 23 (14.4%) had no ED (p < .05). ED was common in men with known CAD and myocardial infarction (MI) (94.7% and 100%), respectively. In another relation, it was noticed that ED has frequently coexisted in the MetS group with chronic renal failure (81.3%).
In both groups, the prevalence of ED was significantly correlated with aging. The effect of aging on the prevalence of ED in the MetS group was higher than the control group ().
Figure 1. Association of ED prevalence and the age in MetS and control groups.
There was a significant correlation between duration of ED and its severity (determined by IIEF-5). The table also shows that severe ED was the most prevalent in all ED duration groups ().
Table 5. Relation between duration of ED and severity of ED in MetS group.
The mean age of ED patients in both groups was nearly similar. Although the majority of the patients in both groups were smokers, the smoking risk factor was not associated significantly with ED.
Discussion
In recent years, MetS has received substantial attention and is considered as the main threat for public health in the twenty-first century [Citation12]. MetS refers to a cluster of metabolic abnormalities related to a state of insulin resistance (IR), predisposing to an increased risk of developing metabolic and CVD [Citation8]. MetS was initially described by a committee of experts from the World Health Organization in 1998 [Citation13]. Few years later, NCEP-ATP III created an operational definition of the syndrome [Citation9]. In this classification, abdominal obesity, high blood pressure (BP), high fasting blood glucose (FBG), high triglyceride (TG), and decreased high-density lipoprotein (HDL) cholesterol are suggested as risk factors of MetS. The existence of any three out of these factors is defined as MetS [Citation9]. In the current study, MetS patients were described according to the NCEP ATP III criteria because of their simplicity.
The high prevalence of ED among MetS group in the study group confirms the strong pathogenic effect of MetS [Citation14,Citation15]. These results were consistent with the previous results in the literature reported from different nationalities; Austrian, Turkish, Italian, and American which had shown that MetS is strongly associated with ED [Citation5,Citation16–18]. The relation between MetS and ED was first described by Gündüz et al. [Citation19]. In a study by Heidler et al. [Citation20], on 2371 men aged 30 to 69 years reported that MetS in men older than 50 years was significantly associated with a higher proportion 48% of severe ED. Recently, Gorgel et al. [Citation21] reported in his study on 1300 Turkish individuals that 70% of individuals with MetS and 45% of individuals without MetS had ED (p < .001). The mean domain scores of IIEF of the individuals with and without metabolic syndrome were 15.3 ± 6.4 and 20.4 ± 4.8, respectively (p < .001).
In the current study, the logistic regression analysis in the MetS group, demonstrated that all metabolic risk factors were significant elements related to ED, except abnormal WC. The current work has also showed that abnormal FBG was in particular the most significant metabolic components for ED (p = .01, OR = 8.73, 95% CI: 3.74–20.37). This was consistent with results given by Demir et al. [Citation22], Bal et al. [Citation16], and Lee et al. [Citation23].
The present study showed that DM, abnormal WC, and HTN were the common metabolic features among men with MetS. Moreover, it revealed that 258 (79.4%) of MetS patients had ED. Of those ED patients, 72.5% had both DM and HTN, 19% had DM but no HTN, 6.5% had HTN but no DM and 2% had no DM or HT (p < .001). The existence of DM and HTN together in the same patient with MetS, therefore, increases the risk of developing ED.
Besides that MetS components had significant impact on ED prevalence and severity, Esposito et al. [Citation5] and Demir et al. [Citation22] reported that ED prevalence increases as the number of components of the MetS increases. In the study of Lee et al. [Citation23], prevalence of ED among the patients with 3 to 4 metabolic risk factors was 76.1 and 100% in those with five risk factors (p < .01). The present study also proved that severity of ED is associated with increasing the number of metabolic risk factors. In between the patients with three, four, and five metabolic risk factors, prevalence of ED were 62.6 vs. 86.2% vs. 94.2%, respectively, p < .001.
Gunduz et al. [Citation19], Demir et al. [Citation22], Bal et al. [Citation16], and Gorgel et al. [Citation21], all reported that WC was an independent metabolic risk factor for ED in most of the published reports. While abnormal WC in the multivariate analysis of the study by Lee et al. [Citation23] was insignificant (p = .25, OR =1.29, 95% CI: 0.84–2.00). In the present study, abnormal WC was statistically insignificant in univariate and multivariate analysis in both groups, although a higher percentage of ED patients was among obese men.
In the present study, there is a significant correlation between age factor and ED prevalence and severity in both groups. In the group with MetS, ED prevalence was 4.3% in men younger than 45 years ,27.1% among men between 45 and 55 years, and it reached the highest rate in men older than 55 years (48%). In the group without MetS, prevalence of ED was 1.4% in men younger than 45 years, 10% among men between 45 and 55 years, and 18.6% in men older than 55 years (p < .01). The cause of higher incidence of ED related to the age in the MetS group than non-MetS group, in the present study, might be due to either coexistence of MetS or medication used in its treatment. Furthermore, it was noticed that with long history of ED, severe ED is more predominant than mild or moderate ED (p < .001).
The relationship between MetS and CVD has been established by Wilson et al. [Citation24] and Yassin et al. [Citation25], and Sanchez et al. [Citation26]. Cross-sectional studies have documented a concordance between the causes of ED and causes of CVD, that is, elements common to the MetS [Citation20,Citation27–29]. Men with CVD or MetS often have ED, probably because of shared factors impairing hemodynamic mechanisms in both the penile and systemic vascular beds [Citation30]. Similarly, in the present study, we found that ED was common in men with known CAD and MI (94.7% and 100%), respectively. This may support the hypothesis of the artery size which has been used to explain how ED acts as a silent marker of vascular diseases elsewhere in the body, and particularly as a marker of CVD [Citation25,Citation30–32].
Conclusions
Metabolic syndrome seems to be a potential risk factor for ED.
Abnormal FBG, dyslipidemia, hypertension, and aging are the most independent predictors for ED.
The current results consolidated the idea that individuals with metabolic syndrome should be screened for ED.
The relation between ED and metabolic syndrome in consistent among different nationalities.
Disclosure statement
No potential conflict of interest was reported by the authors.
References
- San Martin C, Simonelli C, Sonksen J, et al. Perceptions and opinions of men and women on a man's sexual confidence and its relationship to ED: results of the European Sexual Confidence Survey [Research Support, Non-U.S. Gov't]. Int J Impot Res. 2012;24:234–241.
- NIH Consensus Conference. Impotence. NIH Consensus Development Panel on Impotence [Consensus Development Conference Consensus Development Conference, NIH Review]. JAMA. 1993;270:83–90.
- Feldman HA, Goldstein I, Hatzichristou DG, et al. Impotence and its medical and psychosocial correlates: results of the Massachusetts Male Aging Study. J Urol. 1994;151:54–61.
- Lewis R, Fugl-Meyer K, Corona G, et al. Definitions/epidemiology/risk factors for sexual dysfunction. J Sex Med. 2010;7:1598–1607.
- Esposito K, Giugliano F, Martedi E, et al. High proportions of erectile dysfunction in men with the metabolic syndrome. Diabetes Care. 2005;28:1201–1203.
- Corona G, Forti G, Maggi M. Why can patients with erectile dysfunction be considered lucky? The association with testosterone deficiency and metabolic syndrome. Aging Male. 2008;11:193–199.
- Huang PL. A comprehensive definition for metabolic syndrome [Review]. Disease Models Mech 2009;2:231–237.
- Grundy SM. Metabolic syndrome: a multiplex cardiovascular risk factor [Review]. J Clin Endocrinold Metab. 2007;92:399–404.
- Adult Treatment Panel (III) [Guideline Practice Guideline]. Executive summary of the third report of The National Cholesterol Education Program (NCEP) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults. JAMA. 2001;285:2486–2497.
- Rosen R, Cappelleri J, Smith M, et al. 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. 1999;11:319–326.
- Shamloul R, Ghanem H, Abou-zeid A. Validity of the Arabic version of the sexual health inventory for men among Egyptians. Int J Impot Res. 2004;16:452–455.
- Taskinen M. Is metabolic syndrome the main threat to human health in the twenty-first century? Arterioscler Thromb Vasc Biol. 2007;27:2275.
- Alberti KG, Zimmet PZ. Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus provisional report of a WHO consultation [Research Support, Non-U.S. Gov't]. Diabetic Med. 1998;15:539–553.
- Esposito K, Giugliano D. Obesity, the metabolic syndrome, and sexual dysfunction in men [Review]. Clin Pharmacol Ther. 2011;90:169–173.
- Yassin A, Nettleship J, Almehmadi Y, et al. Is there a relationship between the severity of erectile dysfunction and the comorbidity profile in men with late onset hypogonadism? Arab J Urol. 2015;13:162–168.
- Bal K, Öder M, Şahin AS, et al. Prevalence of metabolic syndrome and its association with erectile dysfunction among urologic patients: metabolic backgrounds of erectile dysfunction. Urology. 2007;69:356–360.
- Demir O, Akgul K, Akar Z, et al. Association between severity of lower urinary tract symptoms, erectile dysfunction and metabolic syndrome. Aging Male. 2009;12:29–34.
- Kaplan S, Meehan A, Shah A. The age related decrease in testosterone is significantly exacerbated in obese men with the metabolic syndrome. What are the implications for the relatively high incidence of erectile dysfunction observed in these men? J Urol. 2006;176:1524–1528.
- Gündüz M, Gümüs B, Sekuri C. Relationship between metabolic syndrome and erectile dysfunction. Asian J Androl. 2004;6:355–358.
- Heidler S, Temml C, Broessner C, et al. Is the metabolic syndrome an independent risk factor for erectile dysfunction? J Urol. 2007;177:651–654.
- Gorgel SN, Gorgel A, Sefik E. Sexual function in male patients with metabolic syndrome and effective parameters on erectile dysfunction. Int Braz j Urol. 2014;40:56–61.
- Demir T, Demir O, Kefi A, et al. Prevalence of erectile dysfunction in patients with metabolic syndrome [Comparative Study]. Int J Urol. 2006;13:385–388.
- Lee YC, Liu CC, Huang CN, et al. The potential impact of metabolic syndrome on erectile dysfunction in aging Taiwanese males [Research Support, Non-U.S. Gov't]. J Sex Med. 2010;7:3127–3134.
- Wilson PW, Kannel WB, Silbershatz H, et al. Clustering of metabolic factors and coronary heart disease [Research Support, U.S. Gov't, P.H.S.]. Arch Intern Med. 1999;159:1104–1109.
- Yassin AA, Saad F, Haider A, et al. The role of the urologist in the prevention and early detection of cardiovascular disease [Review]. Arab J Urol. 2011;9:57–62.
- Sanchez E, Pastuszak AW, Khera M. Erectile dysfunction, metabolic syndrome, and cardiovascular risks: facts and controversies [Review]. Transl Androl Urol. 2017;6:28–36.
- Corona G, Mannucci E, Schulman C, et al. Psychobiologic correlates of the metabolic syndrome and associated sexual dysfunction [Research Support, Non-U.S. Gov't]. Eur Urol. 2006;50:595–604.
- Ho CH, Wu CC, Chen KC, et al. Erectile dysfunction, loss of libido and low sexual frequency increase the risk of cardiovascular disease in men with low testosterone. Aging Male. 2016;19:96–101.
- Smith M, Goltz HH, Ahn S, et al. Correlates of chronic disease and patient-provider discussions among middle-aged and older adult males: implications for successful aging and sexuality. Aging Male. 2012;15:115–123.
- Jackson G. The metabolic syndrome and erectile dysfunction: multiple vascular risk factors and hypogonadism [Comment Editorial]. Eur Urol. 2006;50:426–427.
- Inman BA, Sauver JL, Jacobson DJ, et al. A population-based, longitudinal study of erectile dysfunction and future coronary artery disease [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't]. Mayo Clinic Proceed. 2009;84:108–113.
- Leoni LA, Fukushima AR, Rocha LY, et al. Physical activity on endothelial and erectile dysfunction: a literature review [Review]. Aging Male. 2014;17:125–130.