Prevalence and factors associated with erectile dysfunction in a cohort of HIV-infected patients

Abstract

To determine the prevalence of erectile dysfunction and its associated factors we conducted an observational study on a consecutive cohort of asymptomatic HIV-positive men. All the patients completed a questionnaire to evaluate erectile dysfunction based on the International Index of Erectile Function, a validated survey for the diagnosis of anxiety and depression (self-administered HAD), and a questionnaire about cardiovascular risk factors. Epidemiological, clinical, and analytical data were collected. In all, 158 men, participated: mean age 46.0 years, 96.2% on antiretroviral therapy (91.3% undetectable viral load), and the mean CD4 count was 534 cells/mL. Erectile dysfunction was present in 106 (67.1%) patients, and associated factors were age (OR 4.5 for each 5 years; 95% CI 4.3−4.7; p = 0.0001) and anxiety (OR 8.2, 95% CI 2.2−30.4; p = 0.002). The prevalence of erectile dysfunction is high in men living with HIV, even in those with good immunovirological control. It is related to increasing age and anxiety, both of which are important factors within our HIV cohort.

Keywords

HIV AIDS erectile dysfunction prevalence men cardiovascular risk anxiety disorder endocrine disorder

Introduction

Erectile dysfunction (ED) is defined as the inability to achieve or maintain an erection during sexual intercourse.¹ Sexual dysfunction is a broader term that as well as ED includes the waning of libido and alterations in ejaculation.² This problem increases with age although it is also related to multiple factors such as cardiovascular disease or other chronic diseases; medicines; and neurological, psychological, and hormonal disorders.³ Patients with HIV infection have a higher prevalence of ED than that of the general population,^2,4–6 reaching 61.4% in some series.⁵ The pathogenesis of sexual dysfunction in these subjects is not clear. Not only do factors traditionally related to this pathology have to be considered^2,5,7,8 but consideration must also be given to the role played by the HIV infection itself and its treatment, with the few data available being controversial.^2,4,6 The importance of this problem resides not only in the psychosocial and emotional sphere of the patients but it can also reflect or be the first symptom of endothelial dysfunction at the systemic level.⁸

The objective of this study was to determine the prevalence of ED in a cohort of men with HIV infection and analyse the associated factors.

Patients and methods

We undertook an observational study on a consecutive cohort of males with asymptomatic HIV infection under regular follow-up by the Infectious Diseases Unit of our centre and who attended the office between April and July 2011. All the patients were ≥18 years old, they were informed of the nature of the study and asked for their consent to participate in it. The study was approved by the Ethics and Research Committee of our centre.

All the patients completed a questionnaire to evaluate ED based on the International Index of Erectile Function (IIEF).⁹ The IIEF 5 is a validated questionnaire consisting of five questions, each scored from 0 to 5, and in which a global score below 21 is considered significant for ED. The patients also completed a validated survey for the diagnosis of anxiety and depression (self-administered HAD).¹⁰ This scale is composed of fourteen questions, seven of which measure anxiety and seven depression. A score above eleven is considered indicative of a case, between eight and eleven doubtful, and below seven absence of disorder. They also completed another questionnaire about cardiovascular risk factors, recreational drug use, medication, and family history of cardiovascular disease. They all underwent a complete physical examination, including measurements of weight, height, waist circumference, and blood pressure. Data recorded concerning HIV included the transmission route, time since diagnosis, AIDS event, viral load, nadir and current CD4 lymphocytes, antiretroviral therapy (ART) and its duration, and coinfection with hepatitis B virus (HBV) and hepatitis C virus (HCV). In all cases, the plasma testosterone concentration was also determined.

The qualitative variables were expressed in percentages and the association contrasts were analysed with the Chi square test (χ²) or Fischer's exact test when necessary. The quantitative variables were expressed as the mean and interquartile range (IQR) and the differences were analysed by the Student t test after confirming that the quantitative variables followed a normal distribution (Kolmogorov-Smirnov test). Comparison between more than two groups was done with one- or multi-way analysis of variance (ANOVA). The multivariate analysis for variables related to ED was done using the Cox proportional hazards model. The odds ratios and the 95% confidence intervals for significant variables were calculated. In all cases, the contrasts were done bilaterally and significance was set at a p < 0.05. The statistical analysis was carried out using the SPSS 17.0.0 program (SPSS, Inc., Chicago, IL, USA).

Results

Of the 196 individuals invited to participate, 158 (80.6%) accepted. The mean age was 46.0 years and the mean duration of HIV infection was 111.7 months. Of the 158, 150 (96.2%) were on ART; 91.3% of these had undetectable viral load and the global mean CD4 lymphocyte count was 534 cells/mL. The testosterone concentrations were below 3 ng/mL in 20 (12.6%) patients. ED was present in 106 patients, giving a prevalence of 67.1%. In the univariate analysis, ED was related with age, not being a smoker or consumer of other drugs, hypertension, dyslipidaemia, anxiety, depression, hypogonadism, having AIDS, and with the CD4 lymphocyte nadir (Table 1). The only factors that were still associated after the multivariate analysis were age (OR 4.5 for each 5 years; 95% CI 4.3–4.7; p = 0.0001) and anxiety (OR 8.2, 95% CI 2.2–30.4; p = 0.002).

Table 1.

Contrast of patients with and without erectile dysfunction (ED) (univariate analysis).

ED (n = 106)	No ED (n = 52)	p
Age (years)	47.04 (42.7, 54.2)	42.59 (32.2, 48.6)	0.000
Smoking	53 (50%)	35 (67.3%)	0.043
Alcohol	24 (22.6%)	13 (25%)	0.842
Drugs	12 (11.32%)	13 (25%)	0.036
HCV	24 (22.6%)	12 (23.0%)	1.000
HBV	3 (2,8)	2 (3,8)	0.66
Liver fibrosis F4	5 (4,7)	1 (1,9)	0.64
BMI (kg/m²)	24.47 (22.5, 27.4)	23.55 (21.9, 26.5)	0.162
Obesity	19 (17.9%)	6 (11.5%)	0.360
Diabetes	10 (9.4%)	2 (3.8%)	0.339
Hypertension	27 (25.5%)	3 (5.8%)	0.004
Hyperlipidaemia	29 (27.4%)	5 (9.8%)	0.013
Anxiety	31 (29.5%)	3 (5.8%)	0.000
Depression	13 (12.3%)	1 (1.9%)	0.037
Testosterone (ng/mL)	5.30 (3.42, 6.51)	5.51 (4.25, 6.76)	0.473
Hypogonadism^a	18 (16.9)	2 (3.8)	0.02
HIV risk	0.742
PDA	18 (16.9%)	11 (21.1%)
HMX	64 (60.4%)	28 (53.8%)
HTX	23 (21.7%)	13 (25%)
AIDS	36 (34.0%)	9 (17.3%)	0.039
Nadir CD4 (cells/µL)	169 (75.5, 292.0)	228 (133.0, 322.7)	0.013
Current CD4 (cells/µL)	485 (305.5, 671.5)	591 (393.7, 771.5)	0.089
HAART	102 (96.2%)	48 (92.3%)	0.393
HAART regimen	0.285
PI	41 (40.2%)	23 (47.9%)
NNRTI	58 (56.9%)	22 (45.8%)
HIV VL < 50 cop/ml^b	93 (91.2%)	44 (91.7%)	0.622

BMI: body mass index; HCV: coinfection with hepatitis C virus; PDA: parenteral drug abuser; HMX: homosexuals; HTX: heterosexuals; HAART: highly active antiretroviral therapy; PI: protease inhibitors; NNRTI: non-nucleoside reverse-transcriptase inhibitors; HIV VL: HIV viral load.

Hypogonadism: testosterone < 3 ng/mL.

In patients with HAART.

Discussion

In this series of asymptomatic men with HIV infection and a good immunovirological status, the prevalence of ED was high and greater than in other series of HIV-infected patients.^4–6,11,12 Age is a factor classically related with ED, as observed in this study, which is of great importance given the increasing age of HIV cohorts worldwide. Psychological factors, such as depression and anxiety, which were quite frequent in our series, are clearly related to ED.¹³ In HIV-infected patients, these factors, together with pharmacological and hormonal factors and comorbidities, have been the factors most related to sexual dysfunction.² Feelings of guilt from having acquired HIV via sexual transmission may be a mental factor that negatively influences the sexual response. This psychological factor may explain some reports of higher rates of sexual dysfunction in homosexual and bisexual men^14,15 and may also explain the high prevalence in our series, in which there was a predominance of homosexual men. Depression is one of the most important mental factors associated with sexual dysfunctions.¹⁶ A study of 300 HIV-infected men found that older age and depression were associated positively with ED, and higher CD4 cell counts were associated negatively; thus, a higher CD4 was considered protective regarding ED.⁵ Depression and anxiety were both related to ED in our patients, though only anxiety maintained the association after the multivariate analysis. No association was found with the clinical or immunovirological condition nor with highly active antiretroviral treatment (HAART). Several studies have found an association between antiretrovirals, particularly protease inhibitors, and sexual dysfunction,^4,14,17–20 though others have not.^{5,11,12,21–23} The differences found in the various studies may be explained by their different designs, the study populations involved, and the tools used to evaluate ED. Therefore, the possible relationship between HAART and the development of sexual disturbances in HIV-infected patients remains unresolved because of the inconsistency of the results of the different studies. Hypogonadism was one of the most frequent causes of sexual dysfunction before HAART. The prevalence of hypogonadism has been lowered with the introduction of HAART, particularly in patients on HAART in a good clinical condition, who may have even higher testosterone levels than naive patients,²⁴ though it still remains the most common endocrine disorder of HIV-infected men.²⁵ Despite being a cohort of asymptomatic patients, most on ART and in a good immunovirological condition, we nevertheless observed a high prevalence of hypogonadism, higher in those with ED. Lastly, several co-morbid conditions are common in HIV-infected individuals, some of which are often associated with sexual dysfunction, such as liver disease, diabetes, hyperlipidaemia, hypertension, vascular disease, and alcohol dependence.^2,3,7,8 However, none of these was related to ED in our study.

Although the study has a few limitations, mainly the cross-sectional design and the lack of a control group, the sample was large, and included the type of persons who nowadays make up any cohort of HIV-infected patients, and the results contribute relevant information on a frequent problem, of multifactorial aetiology and scarcely analysed in this population.

In summary, the prevalence of ED is high in HIV-infected men in a good immunovirological condition. Furthermore, this condition will increase as the patients grow older. Special attention should be paid to the psychological factors, such as depression and anxiety, so frequent in the HIV-infected population. This study demonstrates the importance of enquiring about ED during routine HIV consultations.

Footnotes

Conflict of Interest

The authors declare no conflict of interest.

Funding

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

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