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Assessment of erectile dysfunction and other sexual dysfunction in men with type 2 diabetes mellitus: A multicenter observational study in North India

Open AccessPublished:September 05, 2022DOI:https://doi.org/10.1016/j.cegh.2022.101136

      Abstract

      Background

      Type 2 diabetes mellitus (T2DM) is one of the major contributing factors of sexual dysfunction in males. Given the presence of limited literature on prevalence of T2DM associated sexual dysfunction in North Indian population, the following study was conducted with aim of investigating the prevalence of ED.

      Materials and methods

      A multicenter observational study was conducted across 11 centers in Lucknow, North India. A total of 460 patients were asked to fill a validated International Index of Erectile function (IIEF) Questionnaire, and sexual dysfunction was assessed based on scoring for erectile function, orgasmic function, sexual desire, intercourse satisfaction, and overall satisfaction over a period of 4 weeks. Chi-Square analysis was performed to form an association between ED or OFD and other confounding factors.

      Results

      ED and OFD were found to be prevalent in 32% and 43.3% of patients, respectively. Their presence correlated significantly with T2DM duration (ED, p = 0.0101; OFD, p = 002). In Indian context, the prevalence of ED was found to correlate with, presence of macrovascular complications and serum creatinine levels, whereas OFD significantly correlated with T2DM duration, macro– and microvascular complications among other factors.

      Conclusion

      The prevalence of ED and OFD in men suffering from T2DM is on significant rise, considerably impacting the lives of millions of men worldwide. Thus, the findings of this study highlight the significance of taking follow-up of sexual discomfort and disorders by the clinicians during the visits.

      Keywords

      2. Introduction

      Erectile dysfunction (ED) is a disorder characterized by the inability to attain and/or maintain an erection sufficient to allow satisfactory sexual intercourse.
      • Kouidrat Y.
      • Pizzol D.
      • Cosco T.
      • et al.
      High prevalence of erectile dysfunction in diabetes: a systematic review and meta-analysis of 145 studies.
      Globally, more than 150 million men are affected by ED, and this figure is expected to reach 322 million by 2025.
      • Azad A.K.
      • Setunge S.
      • Selim S.
      • et al.
      Dyslipidaemia as a risk factor for erectile dysfunction in type 2 diabetes mellitus patients.
      Type 2 diabetes mellitus (T2DM) is the major risk factor for the development of ED, and it has been observed that as compared to healthy men, diabetic men have a threefold higher risk of developing ED.
      • Kouidrat Y.
      • Pizzol D.
      • Cosco T.
      • et al.
      High prevalence of erectile dysfunction in diabetes: a systematic review and meta-analysis of 145 studies.
      ,
      • Castela Â.
      • Costa C.
      Molecular mechanisms associated with diabetic endothelial-erectile dysfunction.
      The latest epidemiological data states that the prevalence of ED in T2DM males could be anywhere between 20% and 71%,
      • Bahar A.
      • Elyasi F.
      • Moosazadeh M.
      • et al.
      Sexual dysfunction in men with type II diabetes.
      with huge differences among different studies. The DISCOVER study reported the prevalence of ED as low as 2.7% in diabetic patients from 38 countries all around the globe.
      • Kosiborod M.
      • Gomes M.B.
      • Nicolucci A.
      • et al.
      Vascular complications in patients with type 2 diabetes: prevalence and associated factors in 38 countries (the DISCOVER study program).
      As per epidemiological studies, men with both type 1 and type 2 DM are at an increased risk of ED, as compared to the general population.
      • Kamenov Z.A.
      A comprehensive review of erectile dysfunction in men with diabetes.
      However, 66% of people with T2DM have ED.
      • Cannarella R.
      • Barbagallo F.
      • Condorelli R.A.
      • et al.
      Erectile dysfunction in diabetic patients: from etiology to management.
      The incidence of ED in patients with DM is age-related, and ED occurs at a younger age with its incidence increasing with disease duration.
      • Kouidrat Y.
      • Pizzol D.
      • Cosco T.
      • et al.
      High prevalence of erectile dysfunction in diabetes: a systematic review and meta-analysis of 145 studies.
      ,
      • Castela Â.
      • Costa C.
      Molecular mechanisms associated with diabetic endothelial-erectile dysfunction.
      Although in general cases, ED is age related, it occurs 10–15 years early in men with diabetes. Moreover, ED in patients with DM is more severe and less responsive to conventional oral medication compared to general ED cases, thereby compromising the quality of life.
      • Kamenov Z.A.
      A comprehensive review of erectile dysfunction in men with diabetes.
      In 12–30% of men, ED is often the first sign of diabetes,
      • Kamenov Z.A.
      A comprehensive review of erectile dysfunction in men with diabetes.
      and ED is often one of the under-diagnosed and under-reported complications associated with.
      • Anwar Z.
      • Sinha V.
      • Mitra S.
      • et al.
      Erectile dysfunction: an underestimated presentation in patients with diabetes mellitus.
      The pathogenesis of DM-related ED is complex and multifactorial, the key factors being diabetic neuropathy, macrovascular arterial disease, structural remodeling of the corporeal tissue, psychogenic components, hypogonadism, and adverse drug reactions.
      • Gray M.
      • Zillioux J.
      • Khourdaji I.
      • et al.
      Contemporary management of ejaculatory dysfunction.
      The mechanisms of ED in men with DM include vascular diabetic complications, endothelial dysfunction, poor glycemic control, and longer disease duration. Other risk factors for type 2 diabetes mellitus (T2DM) patients include obesity, hypertension, hyperlipidemia, metabolic syndrome, and a sedentary lifestyle.
      • Kamenov Z.A.
      A comprehensive review of erectile dysfunction in men with diabetes.
      ,
      • Singh K.
      • Devi S.
      • Pankaj P.P.
      Diabetes associated male reproductive dysfunctions: prevalence, diagnosis, and risk factors.
      Orgasmic function defect (OFD) is another condition that is commonly associated with ED in patients with T2DM.
      • Singh K.
      • Devi S.
      • Pankaj P.P.
      Diabetes associated male reproductive dysfunctions: prevalence, diagnosis, and risk factors.
      OFD can be termed as incessant difficult or delay or absence of achieving orgasm post sufficient sexual stimulation leading to personal distress. OFD included delayed orgasms as well as anorgasmia. Anorgasmia is perceived absence of orgasm, independent of the presence of ejaculation. Delayed orgasm is defined as a noticeable delay in ejaculation/infrequent or absence of ejaculatory response in75%–100% of occasions of partnered sexual activity without the self-desiring of delay, which persists for at least 6 months. Patients with OFD may also have ejaculatory dysfunction including delayed ejaculations and premature ejaculation and anorgasmia.
      • Jenkins L.C.
      • Mulhall J.P.
      Delayed orgasm and anorgasmia.
      The prevalence of ejaculatory disturbance in diabetic males is estimated to be around 9%–31%, while that of orgasmic dysfunction is around 7%–8%.
      • Jakka N.R.
      • Ramesh J.
      A study of various factors associated with sexual dysfunction in males with type 2 diabetes mellitus.
      The main concern with orgasmic dysfunction in young males is the failure to inseminate, thereby leading to male infertility.
      • Jenkins L.C.
      • Mulhall J.P.
      Delayed orgasm and anorgasmia.
      Peripheral neurological interruptions as seen in diabetic neuropathy are one of the causes of OFD. Further poor glycemic controls are strongly associated with premature ejaculations in males with T2DM; however, the role of glycemic control in orgasmic dysfunction is not clearly understood.
      • Jakka N.R.
      • Ramesh J.
      A study of various factors associated with sexual dysfunction in males with type 2 diabetes mellitus.
      Endothelial dysfunction plays a key role in DM-associated ED. Alterations in the functionality of the penile endothelium, a specialized component of the vascular system, lead to complications such as ED. Endothelial dysfunction links ED and cardiovascular complications in such patients. Additionally, common comorbidities associated with DM, such as hypercholesterolemia, hypertension, and obesity, serve as independent risk factors for cardiovascular disease, endothelial dysfunction, and ED.
      • Castela Â.
      • Costa C.
      Molecular mechanisms associated with diabetic endothelial-erectile dysfunction.
      Accumulating pieces of evidence consider ED to be an independent risk factor for coronary artery disease (CAD), particularly in younger men with DM who are already at a higher risk of developing CAD.
      • Hackett G.I.
      Erectile dysfunction, diabetes, and cardiovascular risk.
      ED is also associated with poor glycemic control, which in turn is associated with microvascular and macrovascular complications in DM patients. Therefore, DM-associated ED has emerged as the major issue requiring serious attention in the male diabetic population.
      • Ugwu T.
      • Ezeani I.
      • Onung S.
      • et al.
      Predictors of erectile dysfunction in men with type 2 diabetes mellitus referred to a tertiary healthcare center.
      DM has become an epidemic over the last two decades, majorly T2DM, which constitutes 90%–95% of all DM cases.
      • Cannarella R.
      • Barbagallo F.
      • Condorelli R.A.
      • et al.
      Erectile dysfunction in diabetic patients: from etiology to management.
      Incidence of ED has been extensively associated with T2DM, with a 50% global prevalence in men with T2DM.
      • Carrillo-Larco R.M.
      • Luza-Dueñas A.C.
      • Urdániga-Hung M.
      • et al.
      Diagnosis of erectile dysfunction can be used to improve screening for type 2 diabetes mellitus.
      Despite the clinical importance of ED in men with DM, most clinicians do not enquire about ED, and the prevalence of patient-reported ED is generally very low.
      • Ugwu T.
      • Ezeani I.
      • Onung S.
      • et al.
      Predictors of erectile dysfunction in men with type 2 diabetes mellitus referred to a tertiary healthcare center.
      When questioned directly by clinicians, patients tend to hide ED and these factors are instrumental in rendering ED as an undiagnosed and underrated problem in male patients with DM.
      • Goyal A.
      • Singh P.
      • Ahuja A.
      Prevalence and severity of erectile dysfunction as assessed by IIEF-5 in North Indian type 2 diabetic males and its correlation with variables.
      Nevertheless, ED is a diabetic complication that can be prevented; approximately 95% of patients with T2DM-related ED can be treated successfully.
      • Nisahan B.
      • Kumanan T.
      • Rajeshkannan N.
      • et al.
      Erectile dysfunction and associated factors among men with diabetes mellitus from a tertiary diabetic center in Northern Sri Lanka.
      In this context, it has been observed that the use of validated questionnaires that are either administered by a third-party interviewer or in an anonymous neutral setting is preferred by patients, thereby aiding the early diagnosis of ED.
      • Goyal A.
      • Singh P.
      • Ahuja A.
      Prevalence and severity of erectile dysfunction as assessed by IIEF-5 in North Indian type 2 diabetic males and its correlation with variables.
      Given the attitude of the Indian society toward sexuality, along with the fact that men are usually embarrassed and reluctant to admit having ED, making precise estimates about the prevalence and severity of DM-associated ED in the country is difficult and warrants attention.
      • Nisahan B.
      • Kumanan T.
      • Rajeshkannan N.
      • et al.
      Erectile dysfunction and associated factors among men with diabetes mellitus from a tertiary diabetic center in Northern Sri Lanka.
      In this context, the present study aimed at determining the prevalence and risk factors of ED and OFD among men with T2DM at 11 centers in North India. We have included the factors such as sexual stimulation, sexual intercourse, ejaculation and orgasm as sexual dysfunction factors in our questionnaire. The study also assessed the association of ED and OFD with confounding factors such as age, age of onset of disease, duration of disease, the extent of diabetic control, DM-associated complications (microvascular and macrovascular), and also the use of any prescription drugs.

      3. Materials and methods

      3.1 Study design and participants

      This was a multicenter observational study conducted across 11 centers in Lucknow, North India. This study included sexually active male patients with DM, aged >18 years visiting the study centers for consultation between August 2018 and April 2019. The English and Hindi-translated (regional language) version of the International Index of Erectile Function (IIEF) Questionnaire was used in the study.
      Hindi translation was done initially by a qualified translator. Five questionnaires were then filled by subjects who were well versed in both English and Hindi. Changes were made accordingly. This was done 5 times. The fifth revision of the questionnaire was put to test on 50 healthy subjects and consistency was evaluated, which was found satisfactory. Certification for translation was obtained from an appropriate agency. Ethics committee clearance was obtained before the start of the study.
      In our study, we have utilized the IIEF-15 questionnaire with lower cut off values. The questionnaire was divided into three sub sections: 0–13 (severe), 14–24 (moderate to mild), 25–30 (without disorder). Based on our study, patients falling under the severe category of ED, that is, if their IIEF scores were less than or equal to 14 out of 30 (functional domain A; Erectile Dysfunction; see attached questionnaire in Supplementary File 1) were included for analysis. In functional domain B corresponding to Orgasmic Dysfunction, patients with a score less than or equal to 5 out of 10 were labeled as having primary orgasmic or ejaculatory dysfunction. Moreover, sexual desire, intercourse satisfaction and overall satisfaction were also included.
      During the initial consultation, we recorded patients’ demographic and clinical characteristics (age, weight, height, body mass index [BMI], abdominal circumference, and habits such as smoking, tobacco chewing, and alcohol consumption) along with a thorough medical history (for any known systemic diseases such as hypertension and hypothyroidism).
      We also collected data on various disease-related parameters, such as duration of T2DM, age of onset of the disease, degree of control of T2DM, medication details, history of hypoglycemia, and microvascular and macrovascular complications.
      Upon completion of the initial consultation, all the patients were asked to fill the questionnaire, and the filled copy was collected in a coded envelope to maintain confidentiality. Using the well-validated IIEF Questionnaire, we assessed ED and OFD based on scoring for erectile function, orgasmic function, sexual desire, intercourse satisfaction, and overall satisfaction in the past 4 weeks.
      The study protocol was approved by the ethical committee of the participating centers, and written informed consent was obtained from all the enrolled patients.

      3.2 Statistical analysis

      Descriptive statistics were used to present the baseline characteristics and the prevalence of OFD in T2DM patients. A chi-square test was used for evaluating the association between ED or OFD and other confounding factors. A p-value of <0.05 was considered statistically significant.

      3.3 Study outcomes

      The primary outcome was to assess the prevalence of ED and OFD in patients with T2DM, while the secondary outcome was to evaluate various parameters associated with these sexual dysfunctions.

      4. Results

      4.1 Baseline characteristics of the study population

      A total of 456 male diabetic patients were included in the study, out of which more than 99% were T2DM patients. No specific selection criteria were used related to the duration of the disease. The age of patients ranged from 22 to 72 years, while the mean age of the study population was 47.64 ± 9.59 years. The mean age (± standard deviation [SD]) of the onset of T2DM was 40.48 ± 10.53. About 38.48% of the study population had T2DM for about 1–5 years, while 25.43% of the patients reported T2DM for ≥5 up to 10 years duration. The majority of the participants did not have hypertension (56.74%) or a history of hypoglycemia (13.26%). Either microvascular or macrovascular complications were seen in 17.17% and 8.04%, respectively. The mean (±SD) HbA1c of the population was 8.49 ± 2.06. Details of the baseline characteristics of the study population have been represented in Table 1.
      Table 1Baseline characteristics of the study population.
      Patient CharacteristicsCategories/Mean/MedianValues
      Age (years)Mean ± SD47.64 ± 9.59
      Median47
      Smoking behaviorNonsmoker368 (80%)
      Smoker <1 pack91 (19.78%)
      Smoker >1 pack0 (0%)
      UNK1 (0.22%)
      Tobacco useYes116 (25.22%)
      No343 (74.57%)
      UNK1 (0.22%)
      Alcohol consumptionNonalcoholic350 (76.09%)
      Alcohol <100 g/week109 (23.70%)
      UNK1 (0.22%)
      Height (cm)Mean ± SD165.80 ± 8.76
      Weight (kg)Mean ± SD74.64 ± 13.21
      Waist circumference (cm)Mean ± SD97.06 ± 10.79
      BMI (kg/m2)Mean ± SD26.8 ± 3.97
      Pulse rate (bpm)N412
      Mean ± SD89.03 ± 12.28
      Median88
      Systolic blood pressure (mmHg)N442
      Mean ± SD131.76 ± 17.29
      Median130
      Diastolic blood pressure (mmHg)N442
      Mean ± SD81.44 ± 10.16
      Median80
      Duration of DMTotal456 (100%)
      1 = <1 year71 (15.43%)
      2 = 1–5 years177 (38.48%)
      3 = 5–10 years117 (25.43%)
      4 = >10 years91 (19.79%)
      Patients withT2DMTotal457 (100%)
      Patients with T2DM456 (99.13%)
      Age of onset (years)N456
      Mean ± SD40.48 ± 10.53
      Median40
      HypertensionYes197 (42.83%)
      No261 (56.74%)
      UNK2 (0.43%)
      HypothyroidYes58 (12.61%)
      No400 (86.96%)
      UNK2 (0.43%)
      Other endocrinological disordersYes19 (4.13%)
      No439 (95.43%)
      UNK2 (0.43%)
      HypoglycemiaYes61 (13.26%)
      No397 (86.30%)
      UNK2 (0.43%)
      HbA1c (%)N414
      Mean ± SD8.49 ± 2.06
      Median8.1
      Macrovascular complicationsYes37 (8.04%)
      No421 (91.52%)
      UNK2 (0.43%)
      Microvascular complicationsYes79 (17.17%)
      No379 (82.39%)
      UNK2 (0.43%)
      BMI: Body mass index; HbA1c: Hemoglobin A1C; SD: Standard deviation; T2DM: Type 2 diabetes mellitus; UNK: Unknown.

      4.2 Prevalence of ED and OFD in the study population

      The prevalence of ED was found to be 32.4%, while 43.3% reported OFD. About 27.8% had both ED and OFD, whereas a total of 48.4% of patients suffered from a sexual disorder, that is, having either ED or OFD (Table 2).
      Table 2Prevalence of erectile dysfunction and orgasmic function defect in the study population (N = 460).
      Condition TypeStatusPatient Number (N)Percentage (%)
      Erectile dysfunctionNormal erectile function30867.0%
      Erectile dysfunction14932.4%
      Unknown30.6%
      Orgasmic function defectYes19943.3%
      No25856.1%
      Unknown30.6%

      4.3 Association of ED and OFD with different variables

      We also evaluated the association of ED and OFD with different baseline variables. In the case of ED, a significant association was observed between the prevalence of ED and age category (p = 0.0006) and the age of diabetes onset (p = 0.0096), with ED prevalence gradually increasing with age (Fig. 1). There was also a positive association between the prevalence and the duration of T2DM (p = 0.0101) (Table 3).
      Fig. 1
      Fig. 1Prevalence of erectile dysfunction with age category and age of onset (N = 460).
      *p = 0.0006, #p = 0.0096.
      Table 3Association of erectile dysfunction and orgasmic function defect with the duration of T2DM.
      Duration of T2DMErectile DysfunctionOrgasmic Function Defect
      NoYesp-ValueNoYesp-Value
      1 (<1 year)45 (65.2%)24 (34.8%)0.010144 (63.8%)25 (36.2%)0.0002
      2 (1–5 years)136 (76.8%)41 (23.2%)117 (66.1%)60 (33.9%)
      3 (5–10 years)74 (63.8%)42 (36.2%)56 (48.3%)60 (51.7%)
      4 (>10 years)52 (57.8%)39 (42.2%)39 (42.9%)52 (57.1%)
      T2DM: Type 2 Diabetes mellitus.
      For OFD, the prevalence was found to increase significantly with age (p = 0.003) (Fig. 2) and the duration of T2DM (p = 0.0002) (Table 3), whereas no significant association was observed with the age of onset (p = 0.0553) (Fig. 2).
      Fig. 2
      Fig. 2Prevalence of orgasmic function defect with age category and age of onset (N = 460).
      *p = 0.003, #p = 0.0553.
      Among the other variables studied, the prevalence of ED was found to be significantly associated with that of macrovascular complications (p = 0.0032) and serum creatinine levels (p = 0.0141) as shown in Table 04Table 04Table 04, while there was no significant association with parameters such as hypertension, hypoglycemia, HbA1c levels, microvascular complications, and mean platelet volume (MPV). Among the medications studied, the prevalence of ED was found to be significantly associated with the use of beta-blocker (p = 0.0326) (Table 4). No significant association was observed between the prevalence of ED and other medications such as oral hypoglycemic agents, insulin, alpha-blockers, and antihypertensives.
      Table 4Association of erectile dysfunction and orgasmic function defect with different variables.
      VariablesErectile DysfunctionOrgasmic Function Defect
      YesNop-ValueYesNop-Value
      Hypertension
      Without hypertension75 (29.1%)183 (70.9%)0.0910100 (38.8%)158 (61.2%)0.0192
      p: Significant p-value; T2DM: Diabetes mellitus; HbA1c: Hemoglobin A1C.
      With hypertension72 (36.5%)125 (63.5%)98 (49.7%)99 (50.3%)
      Hypoglycemia
      Without hypoglycemia123 (31.2%)271 (68.8%)0.2066159 (40.4%)235 (59.6%)0.0005
      p: Significant p-value; T2DM: Diabetes mellitus; HbA1c: Hemoglobin A1C.
      With hypoglycemia24 (39.3%)37 (60.7%)39 (63.9%)22 (36.1%)
      Macrovascular complications
      Without macrovascular127 (30.4%)291 (69.6%)0.0032
      p: Significant p-value; T2DM: Diabetes mellitus; HbA1c: Hemoglobin A1C.
      172 (41.1%)246 (58.9%)0.0006
      p: Significant p-value; T2DM: Diabetes mellitus; HbA1c: Hemoglobin A1C.
      With macrovascular20 (54.1%)17 (45.9%)26 (70.3%)11 (29.7%)
      Microvascular complications
      Without macrovascular115 (30.6%)261 (69.4%)0.0865153 (40.7%)223 (59.3%)0.008
      p: Significant p-value; T2DM: Diabetes mellitus; HbA1c: Hemoglobin A1C.
      With macrovascular32 (40.5%)47 (59.5%)45 (57%)34 (43%)
      HbA1C
      ≤729 (28.7%)72 (71.3%)0.308434 (33.7%)67 (66.3%)0.0134
      p: Significant p-value; T2DM: Diabetes mellitus; HbA1c: Hemoglobin A1C.
      >7106 (34.2%)204 (65.8%)148 (47.7%)162 (52.3%)
      Creatinine
      ≤1.2127 (30.8%)285 (69.2%)0.0141
      p: Significant p-value; T2DM: Diabetes mellitus; HbA1c: Hemoglobin A1C.
      173 (42%)239 (58%)0.0425
      p: Significant p-value; T2DM: Diabetes mellitus; HbA1c: Hemoglobin A1C.
      >1.222 (48.9%)23 (51.1%)26 (57.8%)19 (42.2%)
      Beta-blocker
      Without beta-blocker118 (30.5%)269 (69.5%)0.0326
      p: Significant p-value; T2DM: Diabetes mellitus; HbA1c: Hemoglobin A1C.
      159 (41.1%)228 (58.9%)0.0008
      p: Significant p-value; T2DM: Diabetes mellitus; HbA1c: Hemoglobin A1C.
      With beta-blocker27 (44.3%)34 (55.7%)39 (63.9%)22 (36.1%)
      Statin
      Without statin62 (29.5%)148 (70.5%)0.204482 (39%)128 (61%)0.0433
      p: Significant p-value; T2DM: Diabetes mellitus; HbA1c: Hemoglobin A1C.
      With statin84 (35.1%)155 (64.9%)116 (48.5%)123 (51.5%)
      a p: Significant p-value; T2DM: Diabetes mellitus; HbA1c: Hemoglobin A1C.
      The prevalence of OFD was found to be significantly associated with almost all the variables studied, including hypertension (p = 0.0192), hypoglycemia (p = 0.0005), macrovascular (p = 0.0006) and microvascular (p = 0.008) complications, HbA1c (p = 0.0134) and creatinine (p = 0.0425) levels, beta-blocker (p = 0.0008), and statin (p = 0.0433) (Table 4).

      5. Discussion

      ED serves as one of the major complications of T2DM, yet its presence mostly goes unnoticed in routine clinical practice.
      • Anwar Z.
      • Sinha V.
      • Mitra S.
      • et al.
      Erectile dysfunction: an underestimated presentation in patients with diabetes mellitus.
      In the present study, around 32% and 43.3% of all patients with T2DM were found to suffer from ED and OFD, respectively, while 27.8% had both ED and OFD. A total of 48.4% of patients reported a sexual disorder, that is, having either ED or OFD.
      In general, the prevalence of ED among patients with T2DM mostly varies between 20% to 78% across different studies. In a recent cross-sectional study conducted in Northern Sri Lanka, 62.9% of diabetic patients were found to suffer from ED, while 22.4% had severe ED.
      • Nisahan B.
      • Kumanan T.
      • Rajeshkannan N.
      • et al.
      Erectile dysfunction and associated factors among men with diabetes mellitus from a tertiary diabetic center in Northern Sri Lanka.
      In a global meta-analysis involving 88,577 male DM patients, the overall prevalence of ED was found to be 59.1%.
      • Kouidrat Y.
      • Pizzol D.
      • Cosco T.
      • et al.
      High prevalence of erectile dysfunction in diabetes: a systematic review and meta-analysis of 145 studies.
      Several Indian studies have reported a prevalence of T2DM-associated ED in different study populations across the country. A cross-sectional study from Northern India reported ED in 67.4% of patients with diabetes, and 42.4% of them suffered from severe ED.
      • Anwar Z.
      • Sinha V.
      • Mitra S.
      • et al.
      Erectile dysfunction: an underestimated presentation in patients with diabetes mellitus.
      A study from Jaipur, India, reported a very high prevalence of ED (78%) in T2DM patients, while 36% of patients had severe ED.
      • Terrier J.E.
      • Mulhall J.P.
      • Nelson C.J.
      Exploring the optimal erectile function domain score cutoff that defines sexual satisfaction after radical prostatectomy.
      Another study from Jammu, North India, reported a 62.08% prevalence of ED in T2DM patients.
      • Langer R.
      • Sharma E.
      • Langer B.
      Erectile dysfunction: prevalence and determinants among T2DM men attending a tertiary care hospital in northern India.
      The divergent prevalence rates of ED among diabetic patients could be attributed to differences in study populations, including demographic characteristics, type of setting in which the study was done, study population size, severity and duration of T2DM, and presence of other comorbidities.
      • Ugwu T.
      • Ezeani I.
      • Onung S.
      • et al.
      Predictors of erectile dysfunction in men with type 2 diabetes mellitus referred to a tertiary healthcare center.
      We found an overall low prevalence of ED in our study group. A plausible explanation might be the low cut-off values used in our study. Studies have used a cut-off score of 24 as diagnostic criterion for ED,
      • Terrier J.E.
      • Mulhall J.P.
      • Nelson C.J.
      Exploring the optimal erectile function domain score cutoff that defines sexual satisfaction after radical prostatectomy.
      but IIEF-5 has demonstrated that values between 22-25 reflects no ED, and mild to moderate ED can only be present if the patient's score is between 12 to 16.
      • Rosen R.C.
      • Cappelleri J.C.
      • Smith M.D.
      • 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.
      Also, the original IIEF-15 questionnaire reported a mean cut-off score of 25.8 ± 7.6 for normal population and mean score of 10.7 ± 6.5 for ED patients; similarly, for orgasmic dysfunction, the cut-off value was 8.8 ± 2.9 in control group and 5.3 ± 3.2 for study population.
      • Rosen R.C.
      • Riley A.
      • Wagner G.
      • et al.
      The international index of erectile function (IIEF): a multidimensional scale for assessment of erectile dysfunction.
      So, based on these data, we had chosen a lower cut-off values as diagnostic criteria for ED in our patients, and patients with scoring of >14 were not considered to have ED and >5 were not considered to have orgasmic defect.
      A consistent risk factor for ED includes increasing age, in both the diabetic and general population.
      • Jakka N.R.
      • Ramesh J.
      A study of various factors associated with sexual dysfunction in males with type 2 diabetes mellitus.
      In the present study, a significant association was observed between age and prevalence of ED; the proportion of ED in diabetic patients increased with age, and the highest prevalence was observed in the >60-year age category (48.1%) and the lowest in the ≤30-year age category (0.00%). In another Indian study, the prevalence of ED was found to be 10.3% and 54.6% in <40-year and 40–59-year age-groups of patients, respectively.
      • Anwar Z.
      • Sinha V.
      • Mitra S.
      • et al.
      Erectile dysfunction: an underestimated presentation in patients with diabetes mellitus.
      A similar trend was reported by Garg et al., where the prevalence of ED was as low as 20% in the <40-year age category and increased to 100% in the >60-year age-group.
      • Garg S.
      • Rijhwani P.
      • Gupta D.
      • et al.
      Study of erectile dysfunction in type-2 diabetic patients.
      A study from Jordan reported that the prevalence of ED increased from 26.5% in patients aged <40 years to 91% in patients aged >70 years.
      • AlMogbel T.A.
      Erectile dysfunction and other sexual activity dysfunctions among Saudi type 2 diabetic patients.
      Again, Langer et al. reported a significant association of age with the prevalence of ED; the majority of ED cases belonged to the 40–60-year age-group.
      • Langer R.
      • Sharma E.
      • Langer B.
      Erectile dysfunction: prevalence and determinants among T2DM men attending a tertiary care hospital in northern India.
      This association between ED and increasing age could be attributed to the prevalence of several common risk factors for ED, such as atherosclerosis, hypertension, and hypogonadism, which become common with increasing age. Also, the presence of T2DM itself increases the risk of developing most of these factors.
      • Ugwu T.
      • Ezeani I.
      • Onung S.
      • et al.
      Predictors of erectile dysfunction in men with type 2 diabetes mellitus referred to a tertiary healthcare center.
      In addition to age, the present study also demonstrated the prevalence of ED to be significantly associated with the age of onset of T2DM; the later the age of onset of T2DM, the higher the prevalence of ED. In the study population, the highest prevalence of ED was observed in >60-year age of onset (66.7%), while the lowest prevalence was observed in the ≤30-year age of onset (21%). A similar observation was reported in a study by Anwar et al., showing that the severity of ED increases with a later age of onset of T2DM.
      • Anwar Z.
      • Sinha V.
      • Mitra S.
      • et al.
      Erectile dysfunction: an underestimated presentation in patients with diabetes mellitus.
      This could be attributed to the fact that, generally, patients with ED ignore their symptoms and delay treatment owing to embarrassment and ignorance.
      • Anwar Z.
      • Sinha V.
      • Mitra S.
      • et al.
      Erectile dysfunction: an underestimated presentation in patients with diabetes mellitus.
      Apart from the age of onset, several studies have documented a longer duration of T2DM as an independent risk factor for ED.
      • Ugwu T.
      • Ezeani I.
      • Onung S.
      • et al.
      Predictors of erectile dysfunction in men with type 2 diabetes mellitus referred to a tertiary healthcare center.
      ,
      • Goyal A.
      • Singh P.
      • Ahuja A.
      Prevalence and severity of erectile dysfunction as assessed by IIEF-5 in North Indian type 2 diabetic males and its correlation with variables.
      • Nisahan B.
      • Kumanan T.
      • Rajeshkannan N.
      • et al.
      Erectile dysfunction and associated factors among men with diabetes mellitus from a tertiary diabetic center in Northern Sri Lanka.
      • Anwar Z.
      • Sinha V.
      • Mitra S.
      • et al.
      Erectile dysfunction: an underestimated presentation in patients with diabetes mellitus.
      • Langer R.
      • Sharma E.
      • Langer B.
      Erectile dysfunction: prevalence and determinants among T2DM men attending a tertiary care hospital in northern India.
      ,
      • Garg S.
      • Rijhwani P.
      • Gupta D.
      • et al.
      Study of erectile dysfunction in type-2 diabetic patients.
      • Khatib F.A.
      • Jarrah N.S.
      • Shegem N.S.
      • et al.
      Sexual dysfunction among Jordanian men with diabetes.
      • AlMogbel T.A.
      Erectile dysfunction and other sexual activity dysfunctions among Saudi type 2 diabetic patients.
      Our data also confirmed this notion that a longer duration of T2DM increases the prevalence and severity of ED.
      • Khatib F.A.
      • Jarrah N.S.
      • Shegem N.S.
      • et al.
      Sexual dysfunction among Jordanian men with diabetes.
      While 43.3% of patients with >10-year duration of T2DM suffered from ED, 23.2% of patients with <5-year duration of T2DM had ED.
      None of the various lifestyle factors evaluated in this study, such as smoking, alcohol consumption, and BMI, were found to be significantly associated with ED. Although smoking is a risk factor for ED associated with T2DM,
      • Hackett G.I.
      Erectile dysfunction, diabetes, and cardiovascular risk.
      this was not observed in our study. Our findings are in line with other reports where smoking habit was not related to the prevalence of ED.
      • Ugwu T.
      • Ezeani I.
      • Onung S.
      • et al.
      Predictors of erectile dysfunction in men with type 2 diabetes mellitus referred to a tertiary healthcare center.
      ,
      • Khatib F.A.
      • Jarrah N.S.
      • Shegem N.S.
      • et al.
      Sexual dysfunction among Jordanian men with diabetes.
      While some studies have found alcohol consumption to be an independent risk factor for ED,
      • Nisahan B.
      • Kumanan T.
      • Rajeshkannan N.
      • et al.
      Erectile dysfunction and associated factors among men with diabetes mellitus from a tertiary diabetic center in Northern Sri Lanka.
      other studies did not find any such correlation,
      • Langer R.
      • Sharma E.
      • Langer B.
      Erectile dysfunction: prevalence and determinants among T2DM men attending a tertiary care hospital in northern India.
      similar to our observation. In some studies, as compared to non-ED cases, the BMI of patients with ED has been observed to be higher.
      • Carrillo-Larco R.M.
      • Luza-Dueñas A.C.
      • Urdániga-Hung M.
      • et al.
      Diagnosis of erectile dysfunction can be used to improve screening for type 2 diabetes mellitus.
      ,
      • Nisahan B.
      • Kumanan T.
      • Rajeshkannan N.
      • et al.
      Erectile dysfunction and associated factors among men with diabetes mellitus from a tertiary diabetic center in Northern Sri Lanka.
      However, our findings are congruent with several other studies where BMI was not associated with ED.
      • Kouidrat Y.
      • Pizzol D.
      • Cosco T.
      • et al.
      High prevalence of erectile dysfunction in diabetes: a systematic review and meta-analysis of 145 studies.
      ,
      • Langer R.
      • Sharma E.
      • Langer B.
      Erectile dysfunction: prevalence and determinants among T2DM men attending a tertiary care hospital in northern India.
      ,
      • Garg S.
      • Rijhwani P.
      • Gupta D.
      • et al.
      Study of erectile dysfunction in type-2 diabetic patients.
      ,
      • Khatib F.A.
      • Jarrah N.S.
      • Shegem N.S.
      • et al.
      Sexual dysfunction among Jordanian men with diabetes.
      Overall, our study did not reveal any association between lifestyle factors and the prevalence of ED.
      Among the various T2DM-associated complications, both microvascular and macrovascular complications have been associated with a high risk of ED. While microvascular complications include medical conditions such as diabetic neuropathy, nephropathy, and retinopathy, macrovascular complications include conditions such as CAD, peripheral vascular disease, and ischemic stroke.
      • Nisahan B.
      • Kumanan T.
      • Rajeshkannan N.
      • et al.
      Erectile dysfunction and associated factors among men with diabetes mellitus from a tertiary diabetic center in Northern Sri Lanka.
      Although the present study did not reveal any significant association between the prevalence of ED and microvascular complications, macrovascular complications were found to be significantly associated with the prevalence of ED. In a cross-sectional study on 376 T2DM patients, 81% of patients without ischemic heart disease (IHD) had ED, while 98% of patients with IHD suffered from ED (p < 0.01).
      • Garg S.
      • Rijhwani P.
      • Gupta D.
      • et al.
      Study of erectile dysfunction in type-2 diabetic patients.
      Another study on 988 diabetic men demonstrated that ED was concomitantly present in 80.2% of diabetic patients with CAD.
      • Khatib F.A.
      • Jarrah N.S.
      • Shegem N.S.
      • et al.
      Sexual dysfunction among Jordanian men with diabetes.
      These studies support our findings that macrovascular complications are significantly associated with ED.
      The findings of the study revealed that apart from macrovascular complications, the prevalence of ED was not associated with other medical conditions such as hypertension and a history of hypoglycemia. Hypertension in diabetic patients increases the risk of atherosclerosis that might affect penile arteries, leading to ED.
      • Nisahan B.
      • Kumanan T.
      • Rajeshkannan N.
      • et al.
      Erectile dysfunction and associated factors among men with diabetes mellitus from a tertiary diabetic center in Northern Sri Lanka.
      However, the present study did not reveal any significant association of ED with hypertension., but we found higher non-significant prevalence of ED in hypertensive patients. Similar observations have been reported by Ugwu et al. and Goyal et al., wherein hypertension was not found to be significantly associated with ED in patients with T2DM.
      • Ugwu T.
      • Ezeani I.
      • Onung S.
      • et al.
      Predictors of erectile dysfunction in men with type 2 diabetes mellitus referred to a tertiary healthcare center.
      ,
      • Goyal A.
      • Singh P.
      • Ahuja A.
      Prevalence and severity of erectile dysfunction as assessed by IIEF-5 in North Indian type 2 diabetic males and its correlation with variables.
      Other risk factors that were not found to be associated with ED in the study population included hypothyroidism, endocrinological disorders, and MPV. Even the extent of glycemic control (measured by HbA1c) was not associated with the prevalence of ED in the study population. However, some studies have found a positive correlation between poor glycemic control and the prevalence of ED.
      • Ugwu T.
      • Ezeani I.
      • Onung S.
      • et al.
      Predictors of erectile dysfunction in men with type 2 diabetes mellitus referred to a tertiary healthcare center.
      ,
      • Goyal A.
      • Singh P.
      • Ahuja A.
      Prevalence and severity of erectile dysfunction as assessed by IIEF-5 in North Indian type 2 diabetic males and its correlation with variables.
      ,
      • Anwar Z.
      • Sinha V.
      • Mitra S.
      • et al.
      Erectile dysfunction: an underestimated presentation in patients with diabetes mellitus.
      ,
      • Garg S.
      • Rijhwani P.
      • Gupta D.
      • et al.
      Study of erectile dysfunction in type-2 diabetic patients.
      ,
      • Khatib F.A.
      • Jarrah N.S.
      • Shegem N.S.
      • et al.
      Sexual dysfunction among Jordanian men with diabetes.
      The prevalence of ED has also been associated with creatinine levels and patients undergoing hemodialysis
      • Costa M.R.
      • Reis A.M.
      • Pereira B.P.
      • et al.
      Associated factors and prevalence of erectile dysfunction in hemodialysis patients.
      ; although we did not analyze the correlation between estimated glomerular filtration rate and ED in our study, a significant association was observed between creatinine levels and the prevalence of ED. Therefore, patients with chronic kidney disease and DM should be aware of early signs of ED.
      Several medications are known to affect sexual function owing to their long-term side effects.
      • AlMogbel T.A.
      Erectile dysfunction and other sexual activity dysfunctions among Saudi type 2 diabetic patients.
      While comparing the association between the type of medications used by the study population and the prevalence of ED, a significant association was observed with beta-blockers. This finding was similar to other studies that have shown beta-blockers to be risk factors for ED.
      • Nisahan B.
      • Kumanan T.
      • Rajeshkannan N.
      • et al.
      Erectile dysfunction and associated factors among men with diabetes mellitus from a tertiary diabetic center in Northern Sri Lanka.
      Nisahan et al. observed in a study on male diabetic patients that 13 out of 14 users of beta-blockers had ED (p = 0.019), thereby indicating that beta-blockers are potential factors for ED.
      • Nisahan B.
      • Kumanan T.
      • Rajeshkannan N.
      • et al.
      Erectile dysfunction and associated factors among men with diabetes mellitus from a tertiary diabetic center in Northern Sri Lanka.
      However, none of the other medications used by the patients, including statin, thiazides, alpha-blocker, insulin, oral hypoglycemic agents, and other antihypertensives, were found to be associated with ED. But in our study, we found a higher prevalence of ED in patients using statin therapy (35% vs. 29%; with statin vs. without statin). Future trials are warranted to assess this correlation further. Similarly, we found higher prevalence of ED in patients with hypoglycemia.
      In the present study, patients with T2DM also had a high prevalence of OFD. Assessing the orgasmic function is included as a domain in the IIEF questionnaire. The orgasmic function includes even the process of ejaculation. In our study, we observed that 43.3% of the study population was affected by OFD. Similar to the results of our study, Jakka and Ramesh had reported orgasmic dysfunction in about 38% of their study population, comprising males with T2DM.
      • Jakka N.R.
      • Ramesh J.
      A study of various factors associated with sexual dysfunction in males with type 2 diabetes mellitus.
      Further, the study by Malavige et al. reported premature ejaculation in 40% of patients with diabetes. They also reported a strong association between ED and premature ejaculation (odds ratio = 4.41; 95% confidence interval = 2.08–9.39) in patients with T2DM.
      • Malavige L.S.
      • Jayaratne S.D.
      • Kathriarachchi S.T.
      • et al.
      Erectile dysfunction among men with diabetes is strongly associated with premature ejaculation and reduced libido.
      The population-based study by Lindau et al. reported a high prevalence of orgasmic dysfunction in patients with diagnosed and undiagnosed diabetes. It was also noted that the rate of ED was not markedly elevated in men with undiagnosed diabetes and hence they reported that orgasmic dysfunction may actually precede ED and not always a consequence of ED.
      • Lindau S.T.
      • Tang H.
      • Gomero A.
      • et al.
      Sexuality among middle-aged and older adults with diagnosed and undiagnosed diabetes: a national, population-based study.
      Even in our study, we observed that more T2DM patients reported OFD compared to ED. Moreover, a significant association was observed between the prevalence of OFD and nearly all the variables studied, that is, age, duration of T2DM, microvascular and macrovascular complications, serum creatinine, HbA1c levels, hypertension, hypoglycemia, and use of beta-blockers and statin. Hence, OFD may be a preceding condition occurring before ED.

      5.1 Strengths and limitations of the study

      The key strengths of the study include the large sample size, multicenter location of the specific study group of T2DM, and the assessment of the association of a wide range of variables with ED and OFD. Being a multicenter study covering 11 centers in North India, the findings of this study depict a wide spectrum in subject selection, hence a better picture of the current scenario of ED and OFD prevalence in T2DM patients, compared to single-center studies that have wide variations in data owing to sociodemographic differences in the study populations. However, some of the limitations of the study include a lack of a healthy control group of individuals for better interpretation of the results and lack of information regarding the proportion of patients receiving treatment of ED and the type of treatment. Moreover, the study did not cover psychological parameters such as depression, which is known to be a contributing factor for ED.
      • Langer R.
      • Sharma E.
      • Langer B.
      Erectile dysfunction: prevalence and determinants among T2DM men attending a tertiary care hospital in northern India.
      Data on the association of ED or OFD with dyslipidemia were also not available for the current study. Lastly, we did not consider the influence of endocrine disorders which are a well-known contributing factor to ED. Findings in this regard should be interpreted with caution.

      6. Conclusion

      To conclude, about one-third and nearly half of our study population reported ED and OFD, respectively, which was significantly associated with higher age, longer duration of T2DM, macrovascular complications, and higher creatinine levels. As most patients suffer silently from ED and OFD, periodic screening for these sexual disorders among diabetic men is essential for early diagnosis and proper management.

      Disclosures

      All authors had full access to the articles reviewed in this manuscript, have read and reviewed the final draft of this manuscript, and take complete responsibility for the integrity and accuracy of this manuscript. The content published herein solely represents the views and opinions of the authors.

      Funding

      No funding or sponsorship was received for this study or publication of this article.

      Authorship

      All named authors meet the International Committee of Medical Journal Editors (ICMJE) criteria for authorship for this article, take responsibility for the integrity of the work as a whole, and have given their approval for this version to be published.

      Declaration of competing interest

      All authors declare that there is no conflict of interest.

      Acknowledgments

      We would like to thank BioQuest Solutions Pvt. Ltd., Bangalore, for providing proofreading and editorial support in the preparation of this manuscript.
      We would like to thank Crystal Language Services for translating the IIEF form into local languages.
      We acknowledge the support from our numerous research assistants who helped in data collection.
      Finally, we thank our families who bore the brunt of our involvement.

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