Abstract
Erectile dysfunction (ED) due to androgen deficiency is rare in the young population. We retrospectively evaluated in this study men aged 18–40 years presenting with ED from 2015 to 2017. The International Index of Erectile Function-5 (IIEF-5) and Erection Hardness Grade Scores (EHGS) were used to assess erectile function. Total testosterone (TT), sex hormone-binding globulin (SHBG), lipid profile, and glycometabolic indicators were tested in fasting blood sample. TT and SHBG were detected by electrochemiluminescence immunoassay, and free (FT) and bio-available testosterone (BT) were calculated from a validated formula. Linear regression was used to analyze the data. In total, 140 cases (30.56 ± 4.81 years) with a mean TT levels of 6.15 ± 2.17 ng/ml were enrolled. Decreased levels of FT were associated with lower IIEF-5 scores(β = 0.176, P = 0.048) and EHGS (β = 0.198, P = 0.026) after adjustment for age, body mass index (BMI), smoking, comorbidities, high-sensitive C-reactive protein (hsCRP), uric acid, fructosamine, and quantitative insulin sensitivity check index (QUICKI). TT was only associated with EHGS in the crude model (β = 0.177, P = 0.037) and some single factor adjustment models, whereas BT and SHBG were not related with erectile function in any model. Low FT level, even in the presence of normal TT, is associated with ED severity in young men. FT levels should be screened in ED patient even with normal total testosterone.
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References
JAMA. Impotence: Nih consensus development panel on impotence. J Am Med Assoc. 1993;270:83–90.
Chew KK, Finn J, Stuckey B, Gibson N, Sanfilippo F, Bremner A, et al. Erectile dysfunction as a predictor for subsequent atherosclerotic cardiovascular events: Findings from a linked-data study. J Sex Med. 2010;7:192–202.
Ferrandis-Cortes C, Martinez-Jabaloyas JM, Diez-Calzadilla NA, Hernandez-Medina JA, Chuan-Nuez P. Cardiovascular risk assessment using high-sensitivity c-reactive protein in patients with erectile dysfunction. Urol Int. 2013;91:187–91.
Vlachopoulos C, Aznaouridis K, Ioakeimidis N, Rokkas K, Vasiliadou C, Alexopoulos N, et al. Unfavourable endothelial and inflammatory state in erectile dysfunction patients with or without coronary artery disease. Eur Heart J. 2006;27:2640–8.
Somani B, Khan S, Donat R. Screening for metabolic syndrome and testosterone deficiency in patients with erectile dysfunction: Results from the first uk prospective study. BJU Int. 2010;106:688–90.
Podlasek CA, Mulhall J, Davies K, Wingard CJ, Hannan JL, Bivalacqua TJ, et al. Translational perspective on the role of testosterone in sexual function and dysfunction. J Sex Med. 2016;13:1183–98.
Harman SM, Metter EJ, Tobin JD, Pearson J, Blackman MR. Longitudinal effects of aging on serum total and free testosterone levels in healthy men. Baltimore longitudinal study of aging. J Clin Endocrinol Metab. 2001;86:724–31.
Satkunasivam R, Ordon M, Hu B, Mullen B, Lo K, Grober E, et al. Hormone abnormalities are not related to the erectile dysfunction and decreased libido found in many men with infertility. Fertil Steril. 2014;101:1594–8.
Martinez-Jabaloyas JM, Queipo-Zaragoza A, Pastor-Hernandez F, Gil-Salom M, Chuan-Nuez P. Testosterone levels in men with erectile dysfunction. BJU Int. 2006;97:1278–83.
O’Connor DB, Lee DM, Corona G, Forti G, Tajar A, O’Neill TW, et al. The relationships between sex hormones and sexual function in middle-aged and older european men. J Clin Endocrinol Metab. 2011;96:2010–216.
Antonio L, Wu FC, O’Neill TW, Pye SR, Ahern TB, Laurent MR, et al. Low free testosterone is associated with hypogonadal signs and symptoms in men with normal total testosterone. J Clin Endocrinol Metab. 2016;101:2647–57.
Rastrelli G, O’Neill TW, Ahern T. Symptomatic androgen deficiency develops only when both total and free testosterone decline in obese men who may have incident biochemical secondary hypogonadism: prospective results from the EMAS. Clin Endocrinol (Oxf). 2018;89:459-69
Gades NM, Jacobson DJ, McGree ME, St Sauver JL, Lieber MM, Nehra A, et al. The associations between serum sex hormones, erectile function, and sex drive: The olmsted county study of urinary symptoms and health status among men. J Sex Med. 2008;5:2209–20.
Wong SY, Chan D, Hong A, Leung PC, Woo J. Depression and lower urinary tract symptoms: Two important correlates of erectile dysfunction in middle-aged men in hong kong, china. Int J Urol. 2006;13:1304–10.
Rosen RC, Cappelleri JC, Smith MD, Lipsky J, Pena BM. 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. Int J Impot Res. 1999;11:319–26.
Mulhall JP, Levine LA, Junemann KP. Erection hardness: a unifying factor for defining response in the treatment of erectile dysfunction. Urology. 2006;68:17–25.
Vermeulen A, Verdonck L, Kaufman JM. A critical evaluation of simple methods for the estimation of free testosterone in serum. J Clin Endocrinol Metab. 1999;84:3666–72.
Ly LP, Sartorius G, Hull L, Leung A, Swerdloff RS, Wang C, et al. Accuracy of calculated free testosterone formulae in men. Clin Endocrinol. 2010;73:382–8.
Wang C, Nieschlag E, Swerdloff R, Behre HM, Hellstrom WJ, Gooren LJ, et al. Investigation, treatment, and monitoring of late-onset hypogonadism in males: ISA, ISSAM, EAU, EAA, and ASA recommendations. J Androl. 2009;30:1–9.
Wu FC, Tajar A, Beynon JM, Pye SR, Silman AJ, Finn JD, et al. Identification of late-onset hypogonadism in middle-aged and elderly men. N Engl J Med. 2010;363:123–35.
Lee WC, Kim MT, Ko KT, Lee WK, Kim SY, Kim HY, et al. Relationship between serum testosterone and cardiovascular disease risk determined using the framingham risk score in male patients with sexual dysfunction. World J Men Health. 2014;32:139–44.
Salvatore N, Rosanna I, Vito B, Vincenzo E, Egle C, Mariaconcetta DP, et al. Erectile dysfunction is associated with low total serum testosterone levels and impaired flow-mediated vasodilation in intermediate risk men according to the framingham risk score. Atherosclerosis. 2015;238:415–9.
Liao M, Huang X, Gao Y, Tan A, Lu Z, Wu C, et al. Testosterone is associated with erectile dysfunction: a cross-sectional study in chinese men. PLoS ONE. 2012;7:21.
Rhoden EL, Teloken C, Sogari PR, Souto CA. The relationship of serum testosterone to erectile function in normal aging men. J Urol. 2002;167:1745–8.
Rhoden EL, Teloken C, Mafessoni R, Souto CA. Is there any relation between serum levels of total testosterone and the severity of erectile dysfunction? Int J Impot Res. 2002;14:167–71.
Kocoglu H, Alan C, Soydan H, Ates F, Adayener C, Eren AE, et al. Association between the androgen levels and erectile function, cognitive functions and hypogonadism symptoms in aging males. Aging Male. 2011;14:207–12.
Muezzinogu T, Gumus B, Temeltas G, Ari Z, Buyuksu C. A relationship of sex hormone levels and erectile dysfunction: which tests should be done routinely? Yonsei Med J. 2007;48:1015–9.
Corona G, Mannucci E, Mansani R, Petrone L, Bartolini M, Giommi R, et al. Aging and pathogenesis of erectile dysfunction. Int J Impot Res. 2004;16:395–402.
Corona G, Mannucci E, Ricca V, Lotti F, Boddi V, Bandini E, et al. The age-related decline of testosterone is associated with different specific symptoms and signs in patients with sexual dysfunction. Int J Androl. 2009;32:720–8.
Ahn HS, Park CM, Lee SW. The clinical relevance of sex hormone levels and sexual activity in the ageing male. BJU Int. 2002;89:526–30.
Basar MM, Aydin G, Mert HC, Keles I, Caglayan O, Orkun S, et al. Relationship between serum sex steroids and aging male symptoms score and international index of erectile function. Urology. 2005;66:597–601.
Tsujimura A, Matsumiya K, Matsuoka Y, Takahashi T, Koga M, Iwasa A, et al. Bioavailable testosterone with age and erectile dysfunction. J Urol. 2003;170:2345–7.
Yeh HC, Wang CJ, Lee YC, Hsiao HL, Wu WJ, Chou YH, et al. Association among metabolic syndrome, testosterone level and severity of erectile dysfunction. Kaohsiung J Med Sci. 2008;24:240–7.
Martínez-Jabaloyas JM, Queipo-Zaragozá A, Pastor-Hernández F, Gil-Salom M, Chuan-Nuez P. Testosterone levels in men with erectile dysfunction. BJU Int. 2010;97:1278–83.
Priskorn L, Jensen TK, Bang AK, Nordkap L, Joensen UN, Lassen TH, et al. Is sedentary lifestyle associated with testicular function? A cross-sectional study of 1,210 men. Am J Epidemiol. 2016;184:284–94.
Cao S, Gan Y, Dong X, Liu J, Lu Z. Association of quantity and duration of smoking with erectile dysfunction: a dose-response meta-analysis. J Sex Med. 2014;11:2376–84.
Shah NP, Cainzos-Achirica M, Feldman DI, Blumenthal RS, Nasir K, Miner MM, et al. Cardiovascular disease prevention in men with vascular erectile dysfunction: The view of the preventive cardiologist. Am J Med. 2016;129:251–9.
Russo GI, Cimino S, Fragala E, Privitera S, La Vignera S, Condorelli R, et al. Insulin resistance is an independent predictor of severe lower urinary tract symptoms and of erectile dysfunction: results from a cross-sectional study. J Sex Med. 2014;11:2074–82.
Huang YP, Chen B, Yao FJ, Chen SF, Ouyang B, Deng CH, et al. Weaker masturbatory erection may be a sign of early cardiovascular risk associated with erectile dysfunction in young men without sexual intercourse. J Sex Med. 2014;11:1519–26.
Chen S, Wu R, Huang Y, Zheng F, Ou Y, Tu X, et al. Insulin resistance is an independent determinate of ed in young adult men. PLoS ONE. 2013;8:e83951
Huang Y, Sun X, Liu G, Yao F, Zheng F, Dai Y, et al. Glycosylated serum protein may improve our ability to predict endothelial and erectile dysfunction in nonorganic patients. J Sex Med. 2011;8:840–50.
Laaksonen DE, Niskanen L, Punnonen K, Nyyssönen K, Tuomainen TP, Valkonen VP, et al. The metabolic syndrome and smoking in relation to hypogonadism in middle-aged men: a prospective cohort study. J Clin Endocrinol & Metab. 2005;90:712.
Jandikova H, Duskova M, Simunkova K, Racz B, Hill M, Kralikova E, et al. The steroid spectrum during and after quitting smoking. Physiol Res. 2015;64:S211. Suppl 2
Pardridge WM. Serum bioavailability of sex steroid hormones. Clin Endocrinol Metab. 1986;15:259–78.
Bhasin S, Brito JP, Cunningham GR, Hayes FJ, Hodis HN, Matsumoto AM, et al. Testosterone therapy in men with hypogonadism: an endocrine society clinical practice guideline. J Clin Endocrinol Metab. 2018;103:1715–44.
Esposito K, Giugliano F, Di Palo C, Giugliano G, Marfella R, D’Andrea F, et al. Effect of lifestyle changes on erectile dysfunction in obese men: a randomized controlled trial. JAMA. 2004;291:2978–84.
Acknowledgements
This study was funded by a grant from the National Natural Science Foundation of China (No. 81401196) and Incubating Program for Clinical Research and Innovation of Renji Hospital, School of Medicine, Shanghai Jiao Tong University (No. PYXJS16-009)
Author contributions:
Conception and design: BC, C-HD, and M-JL. Data analysis and drafting article: Y-PH, S-FC, WL, Y-DL. Final approval of the completed article: Y-PH, WL, S-FC, Y-DL, BC, C-HD, and M-JL.
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Huang, YP., Liu, W., Chen, SF. et al. Free testosterone correlated with erectile dysfunction severity among young men with normal total testosterone. Int J Impot Res 31, 132–138 (2019). https://doi.org/10.1038/s41443-018-0090-y
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DOI: https://doi.org/10.1038/s41443-018-0090-y
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