Erectile Dysfunction in Turkish Diabetics
Erectile Dysfunction in Turkish Diabetics
Soner Cander, MD,1 Soner Coban, MD,2 Sakir Altuner, MD,3 Ozen Oz Gul, MD,1
Zeynel Abidin Yetgin, MD,4 Aysen Akkurt, MD,5 Hakan Ucar, MD,4 and Ercan Tuncel, MD 5
Abstract
Objective: The aim of this study was to evaluate prevalence of erectile dysfunction (ED) in patients with type 2
diabetes mellitus (T2DM) in relation to vascular and neurogenic correlates.
Methods: A total of 116 males including T2DM patients [n = 68; mean age, 56.7 (5.8) years] and age-matched
healthy controls [n = 48; mean age, 57.0 (6.6) years] were included in this cross-sectional single-center study.
Data on anthropometrics, blood biochemistry, concomitant hypertension, hyperlipidemia, and coronary artery
disease (CAD) were recorded in each subject along with measurement of carotid artery intima media thickness
(CIMT) and evaluation of erectile dysfunction (ED) via International Index of Erectile Function (IIEF-5)
Questionnaire. A univariate analysis was performed to determine the relationship of cardiovascular risk factors
and diabetes-related complications to ED.
Results: Patient and control groups were similar in terms of percentage patients with hyperlipidemia (51.5%
and 39.6%, respectively) and CAD (33.8% and 22.9%, respectively), whereas concomitant hypertension was
more common (P = 0.05) and CIMT values were significantly higher (P = 0.020) in patients with T2DM
compared with controls. Polyneuropathy was noted in 46.2% of patients, nephropathy in 30.8%, and retinopathy
in 33.8%. ED scores were significantly lower in patients than controls [14.3 (7.3) vs. 18.2 (6.3), P = 0.004] with
a significantly higher percentage of patients than controls in the category of severe dysfunction (29.4 vs. 10.4%,
P = 0.014). Univariate analysis revealed that diabetic polyneuropathy was the only factor to be associated with
higher likelihood (93.3% in the presence and 60.0% in the absence of neuropathy) and severity (43.3% in the
presence and 14.3% in the absence of neuropathy) of ED (P = 0.004).
Conclusion: Findings from the present cross-sectional single-center study revealed the prevalence of ED to be
considerably higher in patients with T2DM than age-matched healthy controls, with identification of diabetic
polyneuropathy as the only risk factor associated with higher likelihood and more severe forms of ED.
1
Clinic of Endocrinology and Metabolism, 2Clinic of Urology, 3Clinic of Internal Medicine, and 4Clinic of Cardiology, Sevket Yilmaz
Training and Research Hospital, Bursa, Turkey.
5
Department of Endocrinology and Metabolism, Uludag University Faculty of Medicine, Bursa, Turkey.
1
2 CANDER ET AL.
Table 1. Basic Clinical Characteristics and Laboratory Findings in Patients and Control Subjects
Total (n = 116) Type 2 diabetes (n = 68) Control (n = 48) P value
Basic characteristics Mean (SD)
Age (years) 56.8 (6.1) 56.7 (5.8) 57.0 (6.6) 0.819
Duration of diabetes (years) 7.4 (6.9) 7.4 (6.9) — —
HbA1c (%) 8.6 (2.0) 8.6 (2.0) — —
Height (cm) 169.5 (6.2) 168.9 (6.6) 170.4 (5.5) 0.153
Weight (kg) 82.8 (12.8) 82.5 (13.8) 83.3 (11.3) 0.468
Body mass index (kg/m2) 28.8 (3.9) 28.8 (4.3) 28.6 (3.3) 0.775
Waist circumference (cm) 101.0 (10.6) 101.0(11.2) 100.8 (9.8) 0.927
Hip circumference (cm) 102.2 (7.1) 102.0 (7.6) 102.4 (6.4) 0.778
Fat % 24.0 (6.2) 24.6 (6.5) 23.2 (5.6) 0.247
Smoking, n(%) 27 (23.3) 15 (22.1) 12 (25.0) 0.824
Blood biochemistry
PSA (ng/mL) 1.5 (2.1) 1.5 (2.6) 1.4 (1.4) 0.227
fPSA (ng/mL) 0.4 (0.4) 0.4 (0.4) 0.4 (0.4) 0.453
T-test (ng/dL) 345.2 (121.7) 334.8 (120.9) 360.5 (122.6) 0.273
FSH (IU/mL) 7.6 (4.8) 8.7 (5.4) 6.0 (3.4) 0.003
LH (IU/mL) 5.7 (2.9) 6.5 (3.1) 4.6 (2.2) 0.001
Prolactin (ng/mL) 9.1 (10.5) 10.6 (13.4) 7.0 (2.5) 0.018
TSH (IU/L) 2.0 (3.0) 1.9 (2.3) 2.1 (3.7) 0.076
Fasting blood glucose (mg/dL) 156.2 (89.0) 197.8 (93.5) 93.5 (13.0) <0.001
Creatinine (mg/dL) 0.9 (0.3) 1.0 (0.3) 0.9 (0.2) 0.074
ALT (U/L) 27.0 (15.4) 27.0 (14.6) 27.0 (16.6) 0.875
AST (U/L) 22.2 (9.2) 21.0 (9.8) 24.1 (7.9) 0.004
Total cholesterol (mg/dL) 200.2 (40.3) 198.1 (41.6) 203.5 (38.7) 0.486
HDL (mg/dL) 44.6 (9.8) 45.6 (10.1) 43.1 (9.1) 0.076
Triglycerides (mg/dL) 165.3 (90.7) 173.0 (101.6) 153.8 (71.1) 0.630
BUN (mmol/dL) 5.3 (1.5) 5.0 (1.4) 5.9 (1.4) 0.001
Protein volume 42.3 (23.7) 40.1 (19.5) 45.5 (28.6) 0.532
Cardiological findings n (%)
CIMT (mm) Mean (SD) 0.6 (0.2) 0.7 (0.2) 0.6 (0.2) 0.020
Hypertension 41 (35.3) 29 (42.6) 12 (25) 0.0501
Hyperlipidemia 54 (46.6) 35 (51.5) 19 (39.6) 0.2061
Coronary artery disease 34 (29.3) 23 (33.8) 11 (22.9) 0.2041
Diabetes-related complications n (%)
Polyneuropathy 30 (46.2) 30 (46.2) — —
Nephropathy 20 (30.8) 20 (30.8) — —
Retinopathy 22 (33.8) 22 (33.8) — —
Erectile dysfunction
Total score Mean (SD) 15.9 (7.1) 14.3 (7.3) 18.2 (6.3) 0.004
n (%)
Severe (scores 5–7) 25 (21.6) 20 (29.4) 5 (10.4) 0.014
Moderate (scores 8–11) 13 (11.2) 10 (14.7) 3 (6.3) 0.1581
Mild to moderate (scores 12–16) 14 (12.1) 6 (8.8) 8 (16.7) 0.1983
Mild (scores 17–21) 28 (24.1) 15 (22.1) 13 (27.1) 0.5356
None (scores 22–25) 36 (31) 17 (25.0) 19 (39.6) 0.0941
Age, waist circumference, hip circumference, total testosterone, total cholesterol, blood urea nitrogen, fat % variables were analyzed via
the Student t-test.
All other continuous variables were not normally distributed and compared with Mann–Whitney U-test.
Figures in bold are statistically significant.
1
Chi-squared test.
HbA1c, glycated hemoglobin; PSA, prostate-specific antigen; fPSA, free PSA; T-test, total testosterone FSH, follicle-stimulating
hormone; LH, luteinizing hormone; TSH, thyroid-stimulating hormone; ALT, alanine aminotransferase; AST, aspartate aminotransferase;
HDL, high-density lipoprotein; BUN, blood urea nitrogen; CIMT, carotid intima media thickness; SD, standard deviation.
Fasting blood glucose (mg/dL, P < 0.001), follicle-stimulating respectively) and CAD (33.8% and 22.9%, respectively),
hormone (FSH; IU/mL, P = 0.003), luteinizing hormone (LH; whereas concomitant hypertension was more common among
IU/mL, P = 0.001), and prolactin (ng/mL, P = 0.018) levels were diabetic patients than controls (42.6% and 25.0%, P = 0.050)
significantly higher in patients with T2DM with control subjects. (Table 1).
Serum levels for aspartate aminotransferase (AST; U/L, P =
0.001) and blood urea nitrogen (BUN; mmol/dL, P = 0.004) Diabetes-related complications
were significantly higher in controls than patients (Table 1).
Patient and control groups were similar in terms of per- Polyneuropathy was noted in 46.2% of patients, ne-
centage patients with hyperlipidemia (51.5% and 39.6%, phropathy in 30.8%, and retinopathy in 33.8% (Table 1).
4 CANDER ET AL.
diabetic complications are more important risk factors for 5. Kaiser DR, Billups K, Mason C, et al. Impaired brachial
ED than macrovascular ones and the hypothesis that, in the artery endothelium-dependent and -independent vasodila-
complex pathogenesis of diabetic ED, diabetic neuropathy is tion in men with erectile dysfunction and no other clinical
at least an equal, if not more important, pathogenic causal cardiovascular disease. J Am Coll Cardiol 2004;43:
factor than macroangiopathy.29 179–184.
The present study has a number of limitations that should 6. Melman A, Gingell JC. The epidemiology and pathophys-
be taken into account in evaluating the results. First, rela- iology of erectile dysfunction. J Urol 1999;161:5–11.
tively low sample size might have prevented us from achiev- 7. Cartledge JJ, Eardley I, Morrison JF. Nitric oxide-mediated
ing the statistical significance concerning the correlates of ED corpus cavernosal smooth muscle relaxation is impaired in
as well as projecting results to the entire population. Second, ageing and diabetes. BJU Int 2001;87:394–401.
8. Montorsi P, Ravagnani PM, Galli S, et al. Association
the cross-sectional design made it impossible to establish any
between erectile dysfunction and coronary artery disease.
cause-and-effect relationships. Nevertheless given the likely
Role of coronary clinical presentation and extent of coro-
negative impact of cultural customs and social stigma on nary vessels involvement: The COBRA trial. Eur Heart J
patients’ willingness to discuss their symptoms about ED, our 2006;27:2632–2639.
findings emphasize the role of more comprehensive ques- 9. McCulloch DK, Campbell IW, Wu FC, et al. The preva-
tioning considering ED in male diabetic patients with neu- lence of diabetic impotence. Diabetalogia 1980;18:279–283.
ropathic complaints. 10. Saenz de Tejada I, Goldstein I, Azadzoi K, et al. Impaired
In conclusion, findings from the present cross-sectional neurogenic and endothelium-mediated relaxation of penile
single-center study revealed the prevalence of ED to be con- smooth muscle from diabetic men with impotence. N Engl J
siderably higher in patients with T2DM than in age-matched Med 1989;320:1025–1030.
healthy controls, with identification of diabetic polyneuro- 11. Ryan JG, Gajraj J. Erectile dysfunction and its association
pathy as the only risk factor associated with higher likeli- with metabolic syndrome and endothelial function among
hood and more severe forms of ED. Although our findings patients with type 2 diabetes mellitus. J Diabetes Compli-
emphasize that diabetic neuropathy is a more important cations 2012;26:141–147.
pathogenic factor than macroangiopathy and other micro- 12. Sullivan ME, Keoghane SR, Miller MA. Vascular risk
vascular diabetic complications, several mechanisms of ED factors and erectile dysfunction. BJU Int 2001;87:838–845.
have not yet been elucidated. There is a need for further 13. Kirby M, Jackson G, Simonsen U. Endothelial dysfunction
studies considering the particular nature of interrelated factors links erectile dysfunction to heart disease. Int J Clin Pract
in the pathogenesis of endothelial dysfunction-related ED in 2005;59:225–229.
T2DM. Given that ED was noted in three out of every four 14. Akkus E, Kadioglu A, Esen A, et al.; Turkish Erectile
diabetic patients in the present study, systematic screening for Dysfunction Prevalence Study Group. Prevalence and cor-
relates of erectile dysfunction in Turkey: A population-
ED in diabetic patients is strongly suggested so that the onset
based study. Eur Urol 2002;41:298–304.
of ED is not missed. ED marks the decisive aggravation stage
15. Rosen CR, Riley A, Wagner G, et al. The International
of diabetes and of its complications and offers a powerful Index of Erectile Function (IIEF): A multidimensional scale
motivator for patients to change their lifestyle and improve for assessment of erectile dysfunction. Urology 1997;49:
medication compliance. 822–830.
16. Rosen RC, Cappelleri JC, Gendrano N 3rd. The Interna-
Acknowledgments tional Index of Erectile Function (IIEF): A state-of-the-
We would like to acknowledge the reviewers for their science review. Int J Impot Res 2002;14:226–244.
helpful comments. We would also like to thank our col- 17. Turunc T, Deveci S, Guvel S, et al. The assessment of
Turkish validation with 5 question version of International
leagues at the Clinics of Endocrinology and Metabolism,
Index of Erectile Function (IIEF-5). Turkish J Urol 2007;
Clinics of Urology, Sevket Yilmaz Training and Research
33:45–49. [Article in Turkish]
Hospital. 18. Colson MH, Roussey G. Screening and managing erectile
dysfunction in diabetic patients. Sexologies 2013;22:e1–e8.
Author Disclosure Statement 19. Fedele D, Coscelli C, Santeusanio F, et al. Erectile dys-
The authors declare they have no conflict of interest. function in diabetic subjects in Italy. Gruppo Italiano Studio
Deficit Erettile nei Diabetici. Diabetes Care 1998;21:1973–
References 1977.
20. Feldman HA, Goldstein I, Hatzichristou DG, et al. Im-
1. NIH Consensus Development Panel on Impotence. JAMA potence and its medical and psychosocial correlates: Results
1993;270:83–90. of the Massachusetts Male Aging Study. J Urol 1994;151:
2. Phé V, Rouprêt M. Erectile dysfunction and diabetes: A 54–61.
review of the current evidence-based medicine and a syn- 21. Solomon H, Man JW, Wierzbicki AS, et al. Relation of
thesis of the main available therapies. Diabetes Metab erectile dysfunction to angiographic coronary artery dis-
2012;38:1–13. ease. Am J Cardiol 2003;91:230–231.
3. Dan A, Chakraborty K, Mondal M, et al. Erectile dysfunc- 22. Veves A, Webster L, Chen TF, et al. Aetiopathogenesis and
tion in patients with diabetes mellitus: Its magnitude, pre- management of impotence in diabetic males: Four year
dictors and their bio-psycho-social interaction: A study from experience from a combined clinic. Diabet Med 1995;12:
a developing country. Asian J Psychiatry 2013;7:58–65. 77–82.
4. Aslan Y, Sezgin T, Tuncel A, et al. Is type 2 diabetes 23. Romeo JH, Seftel AD, Madhun ZT, et al. Sexual function
mellitus a cause of severe erectile dysfunction in patients in men with diabetes type 2: Association with glycemic
with metabolic syndrome? Urology 2009;74:561–564. control. J Urol 2000;163:788–791.
6 CANDER ET AL.
24. Klein R, Klein BE, Lee KE, et al. Prevalence of self-re- 29. Kamenov ZA, Christov VG, Yankova TM. Erectile dys-
ported erectile dysfunction in people with long-term IDDM. function in diabetic men is linked more to microangiopathic
Diabetes Care 1996;19:135–141. complications and neuropathy than to macroangiopathic
25. Fedele D, Bortolotti A, Coscelli C, et al. Erectile dys- disturbances. JMHG 2007;4:64–73.
function in type 1 and type 2 diabetics in Italy. On behalf of
Gruppo Italiano Studio Deficit Erettile nei Diabetici. Int J
Epidemiol 2000;29:524–531. Address correspondence to:
26. Malavige LS, Levy JC. Erectile dysfunction in diabetes Soner Cander, MD
mellitus. J Sex Med 2009;6:1232–1247. Clinic of Endocrinology and Metabolism
27. Vinik AI, Maser RE, Mitchell BD, et al. Diabetic auto- Sevket Yilmaz Training and Research Hospital
nomic neuropathy. Diabetes Care 2003;26:1553–1579. 16230 Yildirim
28. Pegge NC, Twomey AM, Vaughton K, et al. The role of Bursa
endothelial dysfunction in the pathophysiology of erectile Turkey
dysfunction in diabetes and in determining response to
treatment. Diabet Med 2006;23:873–878. E-mail: drcander@gmail.com