Erectile dysfunction prevalence and associated factors in men living with HIV from Western Turkey: A cross-sectional study

Abstract

Background

The majority of people living with HIV in our country are younger men. However, limited data exist for the sexual health of these patients. Knowledge of the epidemiology in this population may improve health outcomes across the continuum of HIV care. The aim of this study was to determine the prevalence of erectile dysfunction (ED) and its association with some clinical and laboratory factors.

Methods

A cross-sectional study was conducted using random sampling in men living with HIV (MLWH) at a tertiary hospital in Turkey. Patients were asked to fill out the five-item International Index of Erectile Function (IIEF-5), and blood was collected for HIV viral load, CD4⁺ T lymphocyte count, lipids and hormone levels to assess biological aspects at the same clinical visit.

Results

A total of 107 MLWH were recruited. Mean age was 40.4 ± 12.4 years. ED was found in 73.8% (n = 79) of the participants. Severe ED was found in 6.3%, moderate in 5.1%, mild-moderate 35.4%, mild 53.2% of the participants, respectively. The mean age of men with erectile dysfunction was 42.5 ± 12.5 years, while those without erectile dysfunction were 34.5 ± 10 years (p:0.00). ED was detected more frequently in cases with high Low Density Lipoprotein (LDL) levels (p:0.003). There was no statistically significant difference between ED presence and having hormone abnormality. There was a moderate, negative correlation between age and ED score (r: −0.440, p < 0.001). A negative and low correlation was found between triglyceride level and ED score (r: −0.233, p:0.02). The only predictive variable was age in the multivariate analysis [B: −0.155 (95% CI -0.232 to −0.078), p: <0.001].

Conclusions

Our study revealed a high prevalence of ED in the MLWH cohort. Age was found to be the only factor associated with ED. HIV clinicians should consider routine ED screening with validated measures as a part of the follow-up scheme to improve integrated wellbeing in MLWH.

Keywords

HIV AIDS erectile dysfunction sexual dysfunction sexual health men living with HIV

Background

According to the national formal annual health reports, nearly 35,000 cases of HIV were confirmed in Turkey by November 2022. More than 80% were male, and the majority of the cases are in 25–29 and 30–34 age groups.¹ Since antiretroviral therapy is easily accessible, life expectancy of people living with HIV has increased, and HIV treatment has evolved from simple antimicrobial management to a broad and complex approach, including co-occurred chronic conditions management. Understanding the sexual health-related issues of men living with HIV (MLWH) is one of the imperative factors in improving health outcomes across the continuum of HIV care. Many MLWH express their concerns about unmet needs related to sexual health after their HIV diagnosis.² In contrast, sexual functioning is not adequately and systematically screened in clinic settings. Erectile dysfunction (ED) is the inability to achieve or maintain an erection of the penis that is sufficient for sexual intercourse. Several studies revealed that erectile dysfunction is the most frequent sexual functioning problem, with a prevalence of 30–50% in the general population and expectedly more significant in the MLWH.^3–5 Moreover, in some series, the ED rate in the MLWH is reaching 61%.⁶ Along with being a medical condition, ED has a detrimental impact on intimate relationships, psychological mood, and overall quality of life. Many men with sexual dysfunction usually struggle with depressed moods and anxiety regarding sexual performance. Like a vicious cycle, depression and ED reinforce each other.⁷ The past negative experiences regarding ED may lead to avoidance of future sexual intercourse, which results in prolonged distress, anxiety and potential relationship difficulties. Above all, erectile dysfunction is no longer just a sexual concern; it can also be an indication of systemic endothelial dysfunction.⁸ The penile arteries are relatively smaller than coronary vessels; the same amount of endothelial dysfunction significantly reduces blood flow in erectile tissues than those in the coronary circulation.⁹ Therefore, diagnosing erectile dysfunction could be an early marker to recognize men at increased risk of major cardiovascular disease, as it frequently precedes cardiovascular events.¹⁰ However, when it comes to the MLWH population, we come across a more complex situation; since HIV is a highly stigmatized chronic infection associated with mental and sexual problems. The causes of erectile dysfunction in MLWH could be broadly classified into two groups - psychosocial and pathophysiological. Grief and depressive reactions following HIV infection are examples of psychosocial causes, whereas physio-pathological causes could include HIV-related vasculopathies, endocrinopathies, neuropathies, or wasting associated with the advanced stage of AIDS. The majority of studies on sexual dysfunction in men living with HIV have been conducted in developed countries.^3–5 However, more information is needed to comprehensively assess the sexual functioning of men living with HIV in other parts of the world due to the wide variety of sexual behaviour in different cultures. Similarly, there is a limited supply of literature on this subject in our country. Therefore, this study aimed to assess erectile dysfunction and associated factors in men living with HIV attending an outpatient clinic in Turkey.

Methods

This cross-sectional study was carried out between September 2021 and March 2022 in MLWH at the HIV/AIDS clinic of a tertiary hospital in Turkey. Inclusion criteria for the study were being biologically male-sex, having confirmed HIV diagnosis, and being older than 18 years of age.

The study population was male individuals living with HIV in Izmir province, but the total number of cases is unknown. In a population-based erectile dysfunction prevalence study conducted in our country, the frequency was found to be 69.2%.¹¹ According to this, the minimum sample size was estimated to be 83 patients, assuming expected prevalence of 69% and the absolute precision of 10% with 95% confidence level using OpenEpi (sample size proportion section) program. The sample size was then inflated by 40% for possible non-response bias. The sample of 116 patients was then selected using a systematic sampling method from the HIV/AIDS patients list of our hospital (n:483).

The participants were informed and written consent was obtained. Patients were asked to fill out a patient information form and the 5-item simplified version of the International Index of Erectile Function (IIEF).¹² The patient information form consisted of the questions about age, marital status, and educational level. A Turkish validity study of IIEF-5 was conducted by Turunc et al.¹³ In this study, Cronbach’s alpha coefficient was 0.959. Cronbach’s alpha for questions 1, 2, 3, 4, 5 were 0.96, 0.94, 0.95, 0.94, 0.95, respectively. The coefficient correlation was r = 0.96. According to this, patients were categorized as; severe (score 5–7), moderate (score 8–11), mild-moderate (score 12–16), mild (score 17–21) and, no ED (score 22–25).

Blood was collected for HIV viral load, CD4⁺ T lymphocyte count, lipids and hormone levels at the same clinical visits after filling out the questionnaires. Serum FSH, LH, prolactin, and free testosterone were estimated by immunoassay testing using Beckman Coulter Access Immunoassay Systems. Standard laboratory reference values for hormones were used in the study. The cut-off values for follicle stimulating hormone (FSH), luteinizing hormone (LH), prolactin, testosterone are 1–12 U/L, 1.24–8.62 U/L, 5–10 μg/L, 300–1200 ng/dL, respectively. According to blood hormone levels, participants were categorized in the normal or abnormal range. Clinically related information such as HIV diagnosis duration and antiretroviral treatment status was obtained from electronic patient files.

The dependent variable of the study was erectile dysfunction presence; the independent variables were sociodemographic characteristics of the participants, HIV diagnosis and treatment duration, blood lipid and hormone levels, CD4⁺ T lymphocyte count and HIV viral load level. Descriptive statistics were given as numbers and percentages for categorical variables. Normality of continuous variables was examined visually (histogram and probability graphs) and statistical methods (Kolmogorov-Smirnov/Shapiro-Wilk tests). The Shapiro–Wilk test was used when the sample size is less than 50. The normality decision was based on all processes of checking for normality. If continuous variables fit the normal distribution, the mean and standard deviation were given, if not, the median and 25th–75th percentile were used. Comparison of categorical variables with each other was done with Pearson chi-square or Fisher’s exact test. Student’s t test (two groups) or one-way ANOVA test (more than two groups) in independent groups for comparison of continuous variables with normal distribution, if not, Mann Whitney U test (two groups) or Kruskal-Wallis (more than two groups) tests were used. Bonferroni correction was made for comparison when the result was statistically significant in Kruskal Wallis and ANOVA tests by making a pairwise comparison of groups.

Correlation coefficients were calculated by Pearson or Spearman tests according to normal distribution, and partial correlation test. The variables “age, triglyceride, HDL, LDL, total cholesterol, HIV diagnosis duration, and HIV treatment duration” were used in correlation tests. A multiple regression model was created to predict the erectile dysfunction score. Firstly, independent variables that correlated with the ED score and were found to be statistically significant in univariate analysis were included in the model. Backward elimination method was used for multivariate regression analysis. Analysis was performed using SPSS 22.0 (IBM Corporation, Armonk, New York, United States), and p-value <0.05 was considered statistically significant.

The study was carried out in accordance with the Declaration of Helsinki. Clearance was obtained from the Turkish Ministry of Health, University of Health Sciences, Izmir Tepecik Education and Research Hospital Ethical Committee before initiation of the study with the file number of 2021/08-15 on the date of 16/08/2021.

Results

A total of 107 MLWH were recruited for the study. The mean age of the participants was 40.4 ± 12.4 (min: 18–max: 71); all of those were white males. The median time for the duration of having HIV diagnosis and antiretroviral treatment is 36 months (21–60.5) (min: 3–max: 180) and 17 months (7–27.5) (min: 1–max: 82), respectively. The median CD4⁺ T lymphocytes count was 560 cell/mm³ (380–720) (min: 8–max: 1.697). Sixty-four (68.1%) of patients’ HIV RNA level was undetectable (<50 copies/mL). Socio-demographic, clinical, laboratory findings, and severity of ED are shown in Table 1.

Table 1.

Socio-demographic, clinical and laboratory findings of the cases.

Marital status	N (%)
Single	61 (58.7)
Married	40 (38.5)
Widow	3 (2.9)
Total	104 (100)
Education status
Primary school	46 (44.2)
Secondary school	11 (10.6)
High school	23 (22.1)
University or higher	24 (23.1)
Total	104 (100)
Erectile dysfunction diagnose
Yes	79 (73.8)
No	28 (26.2)
Total	107 (100)
Erectile dysfunction severity
No	28 (26.2)
Mild	42 (39.3)
Mild - moderate	28 (26.2)
Moderate	4 (3.7)
Severe	5 (4.7)
Total	107 (100)
FSH Level
Normal	90 (95.7)
High	4 (4.3)
Total	94 (100)
LH level
Normal	86 (91.5)
High	8 (8.5)
Total	94 (100)
Prolactin level
Normal	49 (92.5)
High	4 (7.5)
Total	53 (100)
Testosterone level
Normal	92 (98.9)
Low	1 (1.1)
Total	98 (100)

The IIEF-5 questionnaire identified 73.8% (n = 79) prevalence of erectile dysfunction. Mild erectile dysfunction was the most common score with the proportion of 39.3% (n: 42) in the study group, while severe ED was observed in 4.7% (n = 5) of them.

The mean age of men with erectile dysfunction was 42.5 ± 12.5 years, while those without erectile dysfunction were 34.5 ± 10 years (p:0.00). There was no statistically significant difference in the frequency of ED between the educational status groups (p:0.06), but it was observed that the frequency decreased as the education level increased (p trend:0.02). There was also no significant difference between tenofovir disoproxil fumarate (TDF) and tenofovir alafenamide (TAF) including regimens, (p:0.83). ED was detected more frequently in cases with high LDL levels (p:0.003). There was no statistically significant difference between ED presence and having hormone abnormality. Demographic and laboratory findings of patients with and without ED are shown in Table 2.

Table 2.

Demographic and laboratory findings of patients with and without Erectile Dysfunction.

Parameter	Erectile dysfunction		p value
Parameter	Yes	No	p value
Mean age (±SD)	42.5 ± 12.5	34.5 ± 10	0.00
HIV diagnosis duration (month) Median (IQR)	36.5 (21.5–60)	26.3 (19.7–63)	0.42
HIV treatment duration (month) Median (IQR)	15.8 (6.6–28.2)	18 (9.2–24.9)	0.88
CD4⁺ T cell count (mm³) Median (IQR)	560 (396–712)	566 (302–725)	0.99
	n (%)	n (%)
HIV RNA level
<50 copies/mL	46 (71.9)	18 (28.1)
>50 copies/mL	22 (73.3)	8 (26.7)	0.88
Marital status
Married	29 (72.5)	11 (27.5)	0.77
Single/Widow	48 (75)	16 (25)
Educational status
Primary/Secondary school	47 (82.5)	10 (17.5)	0.06 (p trend:0.02)
High school	16 (69.6)	7 (30.4)
University	14 (58.3)	10 (41.7)
Age
18–35	23 (59)	16 (41)	0.02 (p trend:0.006)
36–54	42 (79.2)	11 (20.8)
55–71	15 (92.9)	1 (7.1)
Tenofovir based regimen
TAF	27 (73)	10 (27)	0.83
TDF	27 (71)	11 (28)
FSH Level
Normal	65 (72.2)	25 (27.8)	1
High	3 (75)	1 (25)
LH level
Normal	63 (73.3)	23 (26.7)	0.68
High	5 (62.5)	3 (37.5)
Prolactin level
Normal	37 (75.5)	12 (24.5)	1
High	3 (75)	1 (25)
Total testosterone level
Normal	67 (72.8)	25 (27.2)	1
Low	1 (100)	0 (0)
Total cholesterole level
Normal	35 (64.8)	19 (35.2)	0.05
High	33 (82.5)	7 (17.5)
LDL level
Normal	35 (64.8)	19 (35.2)	0.03
High	30 (85.7)	5 (14.3)
Triglyceride level
Normal	42 (75)	14 (25)	0.48
High	26 (68.4)	12 (31.6)
HDL level
Normal	43 (71.7)	17 (28.3)	0.84
Low	25 (73.5)	9 (26.5)

A statistically significant difference was found between erectile dysfunction scores with increasing age (p:0.02; p trend:0.006). The significant difference between the groups was observed between the cases aged 61–71 years and those aged 18–30 years, and cases aged 61–71 years and cases aged 31–40 years (p:0.003, p:0.002, respectively) (Figure 1). There was a moderate, negative correlation between age and ED score (r: −0.440, p < 0.001). A negative and low correlation was found between triglyceride level and ED score (r: −0.233, p:0.02). No correlation was found between HIV diagnosis time, duration of treatment, HDL, LDL and cholesterol levels (r:−0.08, r:− 0.06, r:0.08, r:−0.08, r:−0.12 respectively, p > 0.2 in all) after age adjustment.

Figure 1.

Erectile dysfunction scores by age groups. *Score between 61–71 years and 18–30 years old p:0.003. ** Score between 61–71 years old and 31–40 years p:0.002. Among other age groups, p > 0.05.

Age, triglyceride, and total cholesterol regression coefficients were statistically significant in the univariate regression analysis performed to examine the variables predicting the ED score. However the only predictive variable was age in the multivariate analysis [B: −0.155 (95% CI −0.232 to −0.078), p: <0.001] (Table 3).

Table 3.

Association between erectile dysfunction score and other variables by univariate and multivariate multipl regression models.

	Univariate		Multivariate**
	Unstandardized coefficient* (95% CI)	p-value	Unstandardized coefficient (95% CI)	p-value
Age	−0.169 (−0.237; −0.100)	<0.001	−0.155 (−0.232; −0.078)	<0.001
Triglyceride	−0.013 (−0.023; −0.002)	0.01	−0.007 (−0.017; 0.006)	0.18
Total cholesterol	−0.030 (−0.051; −0.008)	0.007	−0.015 (−0.035; 0.003)	0.15
LDL (low-density lipoprotein)	−0.025 (−0.052; 0.001)	0.06
HDL (high-density lipoprotein)	−0.025 (−0.070; 0.120)	0.59
HIV diagnosis duration	−0.017 (−0.042; 0.008)	0.18
HIV treatment duration	−0.024 (−0.081; 0.033)	0.40

*Regression coefficent (B).

**Adjusted for age, triglyceride and total cholesterole

Discussion

The purpose of this study was to assess erectile dysfunction as a part of sexual dysfunction among individuals living with HIV and identify the prevalence and severity as well as the associated socio-demographic and clinic factors. Our MLWH outpatient cohort in Turkey revealed a high prevalence of erectile dysfunction. In addition, age was observed to be associated factor for erectile dysfunction in the multivariate analysis. Our study outcomes are consistent with the common literature showing a high erectile dysfunction prevalence. Different studies from various settings point out a higher prevalence of erectile dysfunction in men living with HIV than those who are negative.^5,14,15 Even though sexual dysfunction is common in MLWH, sexual behaviours are overlooked to be monitored among all other clinical issues. But ignoring and undermanaging sexual health would deteriorate the overall life quality of MLWH, who already struggle with the burden of stigma and HIV related co-morbidities. As indicated in our study, erectile dysfunction prevalence is much higher in lower educated individuals. Therefore, clinicians should empower the patients to talk about their sexuality and provide educational talks with a professional approach to break down the barriers with MLWHG from a lower educational background. Sexual behaviour should be tailored by educational status since people with different education levels may have different barriers and challenges. It is not rare to lose interest in sex or avoid sexual intercourse after being diagnosed with HIV. For instance, a clinical study conducted in Turkey revealed that nearly 70% of the people living with HIV expressed that their frequency of sexual interaction had been decreased after the diagnosis.² Likewise, another study among MLWH reported that 69% of the participants have one or more sexual dysfunction problems. In the same study, 51% of the participants stated that erectile dysfunction appears in the context of trying to use condoms.¹⁶ Using adequate barrier protection during sexual intercourse is strongly advisable for those without virological control. Instead of this, patients who wish to remain sexually active could be encouraged to undergo sufficient antiretroviral therapy to be in an undetectable virological status. If we disregard using a condom for other sexually transmitted diseases rather than HIV, in that case, patients under antiretroviral treatment and in an undetectable status can be directly referred to the “Undetectable = Untransmittable” protocol to have a thorough intimate relationship with their partners.^17,18 The results of the “PARTNER” study published in 2016 led to a groundbreaking step about the low transmissibility of condomless sex among undetectable individuals.¹⁷

Our study outcome shows a clear relationship between age and erectile dysfunction. It has been demonstrated that the frequency of erectile dysfunction increases with rising age. Compared our results of 42 years of age as the mean age of the ED group to results from previous studies in the general population, our findings among men living with HIV indicate that erectile dysfunction could be present at a relatively younger age.^7,9,14 Thus, clinicians should also involve young-middle aged individuals living with HIV in terms of sexual dysfunction management. However, could the HIV status be an independent factor in erectile dysfunction? A study from Italy demonstrates a clear link between erectile dysfunction and HIV, regardless of age. This finding was attributed to the peculiar clinical hallmark of HIV as confirming premature ageing in HIV.¹⁴ Furthermore, MLWH has peculiar factors related to HIV itself, such as fear of transmission to partner, changes in body image, stigma-related stress may all influence sex behaviours and could result in erectile dysfunction. Thus, clinicians should be concerned about erectile dysfunction in regular admissions of MLWH, even whether patients are young or aged.

An association between erectile dysfunction and sexual hormone level imbalance has long been recognized, but it is not straightforward in the MLWH setting. In particular, those with advanced immunosuppression might be faced with secondary hypogonadism related erectile dysfunction issues.¹⁹ Furthermore, low serum testosterone levels are associated with poor health status in MLWH, implying that low testosterone levels may be an adaptive response to chronic illness and reflect ongoing inflammation.²⁰ In our study, outcomes did not indicate any hormonal abnormalities. Since all our participants are under treatment, this could be attributed to the immune regulatory response of antiretroviral drugs, which are a protective factor against hypogonadism.¹⁶ However, there is a well-known connection between erectile dysfunction and endocrinological disorders; therefore, individuals with erectile dysfunction should be considered to have a comprehensive systemic approach.^6,19,20 In order to clarify this, we believe that hormonal assessment needs to be broader, including systemic hormones such as thyroid hormones. Thus, this point could be presented as a limitation of our study. The participants in this study mostly consisted of young and middle-aged males in whom frequency of erectile dysfunction found to be as high as 73.8%.

There are some limitations of our study. The study was conducted in a single centre, therefore the results of the study can not generalizable. Although there was no difference between the ED groups in terms of the frequency of sex hormone abnormalities, the etiology of ED in the group with abnormal test results could not be evaluated with further investigations. Due to the private content of the questions, patients may not have answered the questions correctly, and this may have caused information bias. In this study, an association was found between erectile dysfunction and age. However, the direct effect of HIV on ED could not be evaluated. Lastly, lack of psychosocial measurements in our study is another limitation.

Conclusion

Prevalence of erectile dysfunction increases with rising age and lower education levels. Clinicians should bear in mind that ED can manifest at earlier ages in men living with HIV. As a result, addressing sexuality and sexual dysfunction within routine follow-ups could encourage patients to adhere to comprehensive HIV care and improve overall wellbeing. In order to evaluate the direct effect of HIV on ED, controlled studies including the HIV-negative population should be performed.

Footnotes

Author contributions

Medical Practices: SA, HAU, DC, EA, HA, GK. Concept: SA, HAU, DC, EA, HA, GK. Design: SA, HAU, DC, EA, HA, GK. Data Collection or Processing: SA, HAU, DC, EA, HA, GK. Analysis or Interpretation: SA, HAU, DC, EA, HA, GK. Literature Search: SA, HAU, DC, EA, HA, GK. Writing: SA, HAU, DC, EA, HA, GK.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iDs

Hazal Albayrak Ucak

Derya Caglayan

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