Prevalence and Determinant of Erectile Dysfunction in Type II Diabetes Mellitus and Healthy Men

Erectile dysfunction is currently a growing health concern and one of the most prevalent sexual dysfunctions in men worldwide. Diabetes mellitus is considered a risk factor for developing ED. Therefore, this SHIM study was designed to assess the prevalence, severity and determinant of erectile dysfunction in type II diabetes mellitus patients and healthy men. This hospital-based cross-sectional study was conducted on 132 diabetic male patients and 66 healthy men at the Nkenkaasu hospital, Offinso North, Ghana between January-June, 2019. A pre-structured questionnaire and patients’ medical records were used to document relevant information. Erectile function was assessed using Sexual health inventory for men questionnaire. Data were analyzed using SPSS version 22.0. Chi-square test, binary and multivariable logistic regression analysis were used appropriately. The mean age of study participants was 57.94 ± 9.79 years. The overall mean score on the SHIM test was 12.42 ± 8.15 (range: 1–25), mean of 9.59±7.83 for the type II diabetics and 18.08±5.39 for non-diabetic men. The total erectile dysfunction (ED) prevalence was 81.8% (95% CI: 0.757, 0.869). ED was common in diabetics (70.4%) compared with healthy men (29.6%). Severe ED was 93.7% and 6.3% in the diabetic and non-diabetic men respectively. Multivariate logistic regression revealed that diabetic men with poor health-related quality of life had 3.48 times likelihood of having ED compared to their non-diabetic counterparts (AOR= 3.48, 95% CI; 1.284, 9.453). Very high erectile dysfunction was observed in our study participants. This is worrisome owing to the profound negative impact of ED on the quality of life and fertility of men. It is recommended that periodic assessment of erectile function should form part of routine diabetes care, focusing attention on the modifiable risk factors in preventing, delaying progression, or reversing established ED in persons.


Introduction
Penile erection must be maintained for sexual intercourse to occur. Achieving and maintaining a penile erection is mediated multi-factorially: psychological, neurovascular and hormonal factors [1].

Erectile Dysfunction (ED) is
This humiliating and disturbing ailment does not only affect the men but also their intimate partner. It adversely affects the social and psychological well-being of both partners and contributes to marital tension [21]. It should also be noted that, ED is the most treatable complication of diabetes; over 95% of cases can be successfully treated, however, owing to its embarrassing nature and the shame felt by sufferers, diagnosing and treatment of ED is more challenging [22].
In the Ghanaian community, a man's self-image and identity are associated with his sexual virility. As such, Ghanaian men desire to stay sexually virile throughout their life [23]. Research has been found that medical practitioners do not often take sexual history in males with diabetes and the clients feel insecure and shy to report their current sexual inabilities with healthcare givers [24]. Also healthy men with the problem rarely discuss about the condition or seek help from their fellow men due to the associated stigma [3].
Despite the increasing demand for clinical services and the possible impact of ED and other sexual dysfunctions on interpersonal relationships and quality of life, epidemiological data are relatively limited [25]. This Sexual health inventory for men (SHIM) study was designed to assess the prevalence, severity and associated factors of erectile dysfunction in type II diabetes mellitus patients and healthy men to supplement existing literature. The findings would enhance awareness amongst persons with this condition and also amongst the primary care physicians attending to ED patients.

Study Site
This study was conducted at the diabetic clinic at Nkenkaasu district hospital in the Offinso North district, Ashanti region of Ghana. The hospital serves about 120,585 people and is a referral centre for twelve (12) different health facilities in the Municipality. Offinso North district is one of the twenty-seven (27) districts in the Ashanti Region of Ghana, carved out of Offinso Municipality to facilitate rapid development of the area. The total land area of the District is about 945.9 square kilometers and it lies between longitudes 10 60W and 10 45E and as well as latitudes 70 20N and 60 50S. Offinso North is a peri-urban area with a heterogeneous population with varied religious beliefs, varied political ideas, occupations and education levels [23].

Target/study Population
The clinical material for this present study comprised a total of 198 subjects. The study group consisted of men with type II diabetes mellitus, while the control group consisted of apparently healthy non-diabetic men. The type II diabetic group were patients who were diagnosed according to the current WHO diagnostic criteria of FBS≥7.0 mmol/l, [24] and had been referred for management at the hospital. The non-diabetic group consisted of apparently healthy men who visited the hospital to visit their relatives, blood donation or for routine check-up during the period of data collection. The criteria for type II diabetes exclusion among the healthy group were based on measurement of baseline fasting blood sugar and laboratory assessments confirmed through a physician's diagnosis.

Study Design
This comparative cross-sectional study involved 132 type II diabetic men between 40-70 years registered at the diabetic clinic of Nkenkaasu Government Hospital and 66 healthy men of the same age range. This study excluded patients on androgens, steroids medications, patients with history of chronic renal failure, prostate cancer, prostatectomy and castrated men.

Administration of Questionnaire
A pre-structured questionnaire and patients' medical records were used to document relevant demographic, lifestyle practices and clinical information like age, level of education, marital status, and cigarette smoking history, height, weight, glucose levels and quality of life.

Body mass index (BMI)
Participants were weighed using an electronic weighing scale, while wearing light clothing, to the nearest 0.1 kg. Height was measured using height rod to the nearest cm, without the subjects wearing shoes. BMI was computed by dividing the body weight (kg) by the square of the height in meters (m 2 ), BMI was categorized as: <18.5 (underweight); 18.5 to 24.9 (normal weight); 25 to 29.9 (overweight); and ≥30 (obese).

Physical activities
Leisure-time physical activity was measured based on alternatives to the question "How physically active are you during your leisure time?". Subjects were characterized as having; sedentary leisure time if they perform activities related to watching television, or other sedentary activity; light leisure-time physical activity if subjects engage in some walking, cycling, or other physical activity at least four hours per week; Moderate leisure-time physical activity if they perform any of the following activities running, , aerobic, heavier gardening, or similar physical activity during at least 2 hours a week; and lastly, Heavy leisure-time physical activity if engaged in heavy training or competitions in running, walking for a long distance, swimming, football, etc., which is performed regularly and several times a week [25].

Health-related quality of life questionnaire (EuroQoL group / EQ-5D questionnaire)
A basic health-related quality of life (HRQoL) questionnaire was completed by all subjects. Five questions were asked on mobility, self-care, usual activity, pain/discomfort and anxiety/depression, with three options each were provided for each item. [26] The overall score a participant could obtain ranged from 0 to 15. The median score was 9, hence those scoring greater than or equal to the median were considered to have good HRQoL and those scoring below the median mark were considered to have poor HRQoL. This questionnaire was chosen for its brevity and simplicity.

Sexual health inventory for men (SHIM) questionnaire
SHIM questionnaire is a basic 5-point questionnaire used to assess erectile dysfunction status. Each answer was graded from 0 (no sexual activity or attempts at intercourse) to 5 (very good sexual function). The maximum score patients could obtain was be 25, the minimum was 1. Based on the SHIM questionnaire patients were divided into groups has having: Severe ED=0-7; Moderate ED= 8-11; Mild to Moderate ED =12-16; Mild ED=17-21; and No ED=>22. This questionnaire was completed by all participants.

Statistical Analysis
Data were analyzed using Statistical Package for the Social Sciences (SPSS), version 22.0. Test for normality was done with box plot and Kolmogorov-Smirnoff test. Parametric data were presented as means ± standard deviation. Frequencies and percentages were calculated to enable comparison of characteristics between type II diabetes mellitus subjects and the healthy men. The Chi square (χ2) or Fishers exact test was used appropriately to test the descriptive statistics for the categorical variables. To establish the determinants of erectile dysfunction in the type II diabetic men and the non-diabetic men, binary logistic regression analysis was performed. All independent variables at p<0.20 were taken to multivariable logistic regression analysis. The statistical significance of variables at the final model was set at p<0.05 and 95% confidence level for the adjusted odds ratio. The Hosmer and Lemeshow statistics and deviance coefficient were used to check the goodness of fit of the model.

Ethical Consideration and Informed Consent
This study was conducted based on the Helsinki Declaration and study protocol, consent forms and participant information material were reviewed and approved by University of Ibadan/University Collage Hospital Ethics Committee (UI/EC/18/0621).
Written informed consent of individual participants was sought after the aims and objectives of the study had been thoroughly explained to them. Participants either signed or thumb-printed to give their consent, before the commencement of the study and they assured of the confidentiality of their data.

Results
A total of 198 male volunteers participated in this research study. The ratio of type II diabetics to healthy nondiabetic men was 2:1. There was a statistically significant difference between the type II diabetic and non-diabetic groups when categorized by occupation (p=0.004), Health-related quality of Life (HRQoL) (p<0.001) and leisure time activity (p=0.017). With reference to occupation, a statistically significant difference was observed between type II diabetic and non-diabetic subjects in relation to unemployment and farming. HRQoL was significantly different between both group. There was a significant difference between the type II diabetics men and non-diabetics men with respect to leisure time activities (Table 1). The overall mean score on the five-item version of Sexual Health Inventory for Men (SHIM) was 12.42 ± 8.15 (range: 1-25). The mean SHIM scores for the type II diabetics men and non-diabetics men was 9.59±7.83 and 18.08±5.39 (t= -8.92, p<0.001) respectively. The overall prevalence of erectile dysfunction in our study population was found to be 81.8% (95% CI: 0.757, 0.869). Erectile dysfunction was common among type II diabetic men than healthy men (70.4% vs. 29.6%: χ 2 =5.50, p=0.019). Severe erectile dysfunction was commonnest among type II diabetics (59/144, 93.7%) compared with 6.3% (4/48) of healthy men. The level of severity of erectile dysfunction was significantly associated with diabetes (χ 2 =70.66, p<0.001) ( Table 2). Nine and three independent variables were entered into the bivariate logistic regression (first model) and the multivariate logistic regression (second model) respectively. After controlling for confounders in the second model, only health-related quality of life was found to be significantly associated with erectile dysfunction in the study participants. Diabetic men with poor health-related quality of life between had 3.48 times likelihood of having erectile dysfunction compared to their non-diabetic counterparts (AOR= 3.48, 95% CI; 1.284, 9.453) ( Table 3).

Discussions
In this study, the mean age of the diabetic men was 58.62±9.88 years. Similar to epidemiological study from Finland suggests that, high exposure to unemployment double the risk of type II diabetes among men [27], most unemployed men in this study belonged to the type II diabetes group. The plausible explanation could be the detrimental effect of complications like retinopathy, nephropathy, stroke, hypertension and depression on job performance. Hu et al., (2001) reported that, overweight is the single most important determinant of type II diabetes, therefore, it was not surprising to observe that more of the diabetic men were overweight compared to the healthy men. Majority of the diabetic men had poor quality of life compared with the healthy men and this finding is supported by a study that observed prolonged stress and anxiety being causally linked to the onset of type II diabetes due to the over activity of hypothalamo-pituitary-adrenal (HPA) axis, cortisol production and behavioral factors [27,29].
About half of the diabetic men had a sedentary lifestyle, increased time spent in sedentary behaviour and decreased time spent in moderate-to-vigorous-intensity physical activities have been reported to be independently associated with type II diabetes [30,31]. Moderate alcohol consumption is linked with a decreased risk of type II diabetes [28], similarly, we found that more of the healthy men were consumers of alcoholic beverages compared the diabetic men.
It was surprising that compared to the type II diabetic men, the healthy men recorded the highest number of smokers. Although, cigarette smoking is associated with a small increase in the risk of type II diabetes [28], our study assessed current smoking habits, it is therefore likely that health education given to DM patients encourage them to give up cigarette smoking and excess alcohol consumption.
Diabetes has a strong and well established relationship with ED. About 50 percent of men with chronic diabetes mellitus have erectile dysfunction [1]. Diabetes either affects internal pudendal artery that supplies the majority of the blood flow to the penis through the cavernosal branches or the cavernous nerve terminals and endothelial cells, resulting in a deficiency of neurotransmitters like nitric oxide and intracellular cyclic guanosine monophosphate [32].
The present study showed that, ED was more common in the type II diabetics men than the healthy men. A hospital-based cross-sectional study conducted on male diabetic patients on follow-up at the diabetic clinic of Jimma Medical Center (JMC), Southwest Ethiopia, observed that, the majority, 212 (60.4%) of the diabetic patients had varying degrees of ED [22]. These findings are in accordance with other studies which recorded higher prevalence of ED in type II diabetic men ranging from 44-83% [19,33]. The overall prevalence of erectile dysfunction in our study population was found to be 81.8%, higher than the prevalence from the aforementioned these studies. The plausible explanation for that disparity may be because of the population-specific composition and the method applied for ED assessment. This study further assessed the severity of ED among the participants. It was observed that more than half of the diabetic subjects had severe ED. A previous study by Sondhi et al., (2018) reported that 21.4% of the diabetic males had no ED, 12.3% had mild ED, and 30.9% had mild to moderate ED. The implications of these findings are clear and that this study outcome should inform health care professionals to increase patient awareness about diabetes associated ED.
The current study revealed that health-related quality of life of participants is associated with high erectile dysfunction. Diabetic men with poor health had greater chance of having ED relative to the non-diabetic men. Similarly, a systematic review carried out by Thongtag and Seesawang, 2020 to assess the erectile dysfunction and quality of life among diabetic men revealed that, erectile dysfunction had a negative impact on QoL, with increased severity of ED correlating with a lower QoL [26]. ED results in a decline of QoL because of difficulty in intimate relationships, causing men to lose their self-esteem and self-efficacy. In addition, one study revealed that DED has a significant association with psychological, social relationships, and environmental domains of WHO-QoL-BREF [27].
This finding indicates that a more detailed health-related quality of life assessment should be incorporated in the routine evaluation of ED in diabetic men. Screening of such a high risk population may also help classify those who will benefit the most from interventions and improvements in their Health. A review of previous studies has shown that certain aspects of the demographic, environment and lifestyle, such as age, occupation, BMI, alcohol consumption, smoking and leisure time activities are important predictors of erectile dysfunction [34,35]. However, this our study found no association between these variable and erectile dysfunctions, likely due to the cross-sectional nature of the survey, difference in sample sizes and discrepancy of methodology data collection tool.
For instance, Seid et al. (2017) carried out amongst diabetic patients attending in hospitals of central and northwestern zone of Tigray, northern Ethiopia and observed that age, longer duration of diabetes and lower monthly income were independent predictors of ED. But their study had no control group and the researchers utilized chart, erectile function was assessed using abridged 5-item version of the International Index of Erectile Function (IIEF-5) and in-person interviews to probe further the responses elicited from some participants and this may have identified extra cases of ED and associated factors. Also, cigarette smoking is one of the well-recognized risk factors of ED in diabetic patients by accelerating atherosclerosis which is the main pathophysiologic pathway for vasculogenic ED [22]. However, our study failed to show such an association with smoking. This might be related to the relatively small number of participants who had ever smoked cigarette actively in our study population. This lower proportion of smokers might be due to a significant reduction in the number of smokers owing to continual campaign against smoking as part of lifestyle modification education programs in the diabetic clinics. Moreover, the use of questionnaires to assess smoking status may have a social desirability issue diminishing response rate.
It is also probable that individuals with prevalent erectile dysfunction and diabetes might have modified this lifestyle behaviour compared with the healthy men. Some studies have revealed that about one-third of men with ED display improvement in sexual function based on lifestyle interventions, such as diet, exercise, and weight loss, discontinuance of smoking, counseling, and suitable glycemic control through diet [4,37].
Findings of this study provided a baseline/preliminary data for further research and interventions in the Offinso North district and its environs. The data in this area could be useful evidence for the treatment of erectile dysfunction in both healthy and diabetes mellitus men, more especially among young diabetes mellitus men who would want to have children in the future. This study also increased our understanding of the roles of the factors contributing to the pathogenesis.

Conclusion
A high frequency of erectile dysfunction was observed in our study participants, irrespective of their sociodemographic, clinical and lifestyle characteristics. However, moderate to severe and severe erectile dysfunctions appeared to be more prevalent among type II diabetes men than healthy men. Our results confirmed that diabetes mellitus significantly contributes to the pathophysiology and manifestation of ED.
This high prevalence of ED among the study participants is worrisome, owing to the profound negative impact on the affected individuals. ED in patients highly threatens the wellbeing of clients by increased psychological distress, decreased quality of life, and increased risk of cardiovascular disease. The multivariate regression analysis also revealed that the prevalence of erectile dysfunction among the study participants increased with declining Healthrelated quality of life. This finding provide a scientific basis for a further understanding of the risk factors of ED in patients with DM and serve as a baseline for preventive strategies.
Health care providers should therefore provide psycho-educational interventions such as counseling to promote better QoL among ED patients, particularly those who ignore the complications resulting from ED such as stress or anxiety, unsatisfactory sex life, and relationship problems. Based on these findings, it is recommended that periodic assessment of erectile function should form part of routine diabetes care, focusing attention on the modifiable risk factors as this may go a long way in preventing ED, delaying its progression, or reversing established ED in persons with type II diabetes.

Funding
This study was funded by the African Union Commission and Pan African University, Institute of Life and Earth (PAULESI), University of Ibadan, Nigeria. The funder had no role in the study design, data collection and analysis, decision to publish or preparation of the manuscript.

Acknowledgements
Authors appreciate the efforts of the Medical Laboratory Scientists and Medical Superintendent of Nkenkaasu Hospital, Ghana.

Ethical Approval
This study was conducted based on the Helsinki Declaration and study protocol, consent forms and participant information material were reviewed and approved by University of Ibadan/University Collage Hospital Ethics Committee (UI/EC/18/0621).

Data Availability Statement
The data presented in this study are available on request from the corresponding author.

Conflict of Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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