Low Prolactin Is Associated with Sexual Dysfunction and Psychological or Metabolic Disturbances in Middle-Aged and Elderly Men: The European Male Aging Study (EMAS)
Giovanni Corona MD
Sexual Medicine and Andrology Unit Department of Experimental, Clinical, and Biomedical Sciences, University of Florence, Florence, Italy
Endocrinology Unit, Medical Department, Azienda Usl Bologna Maggiore-Bellaria Hospital, Bologna, Italy
Search for more papers by this authorFrederick C. Wu MD
Department of Endocrinology, Manchester Royal Infirmary, The University of Manchester, Manchester, UK
Search for more papers by this authorGiulia Rastrelli MD
Sexual Medicine and Andrology Unit Department of Experimental, Clinical, and Biomedical Sciences, University of Florence, Florence, Italy
Search for more papers by this authorDavid M. Lee PhD
Epidemiology Unit, The University of Manchester, Manchester, UK
Search for more papers by this authorGianni Forti MD
Endocrinology Unit Department of Experimental, Clinical, and Biomedical Sciences, University of Florence, Florence, Italy
Search for more papers by this authorDaryl B. O'Connor PhD
Institute of Psychological Sciences, University of Leeds, Leeds, UK
Search for more papers by this authorTerence W. O'Neill MD
Epidemiology Unit, The University of Manchester, Manchester, UK
Search for more papers by this authorNeil Pendleton MD
Clinical Gerontology, The University of Manchester, Hope Hospital, Salford, UK
Search for more papers by this authorGyorgy Bartfai MD
Gynaecology and Andrology, Albert Szent-Gyorgy Medical University, Szeged, Hungary
Search for more papers by this authorSteven Boonen MD
Division of Gerontology and Geriatrics & Centre for Musculoskeletal Research, Department of Experimental Medicine, Katholieke Universiteit Leuven, Leuven, Belgium
Search for more papers by this authorFelipe F. Casanueva MD
Department of Medicine, Santiago de Compostela University, Complejo Hospitalario Universitario de Santiago (CHUS), Santiago de Compostela, Spain
CIBER de Fisiopatología Obesidad y Nutricion (CB06/03), Instituto Salud Carlos III, Santiago de Compostela, Spain
Search for more papers by this authorJoseph D. Finn BSc
Epidemiology Unit, The University of Manchester, Manchester, UK
Search for more papers by this authorIlpo T. Huhtaniemi MD
Department of Reproductive Biology, Imperial College London, Hammersmith Campus, London, UK
Search for more papers by this authorKrzysztof Kula MD
Department of Andrology and Reproductive Endocrinology, Medical University of Lodz, Lodz, Poland
Search for more papers by this authorMargus Punab MD
Andrology Unit, United Laboratories of Tartu University Clinics, Tartu, Estonia
Search for more papers by this authorDirk Vanderschueren MD
Department of Andrology and Endocrinology, Katholieke Universiteit Leuven, Leuven, Belgium
Search for more papers by this authorMartin K. Rutter MD
Cardiovascular Research Group, School of Biomedicine, The University of Manchester, Manchester, UK
Search for more papers by this authorMario Maggi MD
Sexual Medicine and Andrology Unit Department of Experimental, Clinical, and Biomedical Sciences, University of Florence, Florence, Italy
Search for more papers by this authorEMAS Study Group
The members of the European Male Aging Study (EMAS) group are listed in Appendix A.Search for more papers by this authorGiovanni Corona MD
Sexual Medicine and Andrology Unit Department of Experimental, Clinical, and Biomedical Sciences, University of Florence, Florence, Italy
Endocrinology Unit, Medical Department, Azienda Usl Bologna Maggiore-Bellaria Hospital, Bologna, Italy
Search for more papers by this authorFrederick C. Wu MD
Department of Endocrinology, Manchester Royal Infirmary, The University of Manchester, Manchester, UK
Search for more papers by this authorGiulia Rastrelli MD
Sexual Medicine and Andrology Unit Department of Experimental, Clinical, and Biomedical Sciences, University of Florence, Florence, Italy
Search for more papers by this authorDavid M. Lee PhD
Epidemiology Unit, The University of Manchester, Manchester, UK
Search for more papers by this authorGianni Forti MD
Endocrinology Unit Department of Experimental, Clinical, and Biomedical Sciences, University of Florence, Florence, Italy
Search for more papers by this authorDaryl B. O'Connor PhD
Institute of Psychological Sciences, University of Leeds, Leeds, UK
Search for more papers by this authorTerence W. O'Neill MD
Epidemiology Unit, The University of Manchester, Manchester, UK
Search for more papers by this authorNeil Pendleton MD
Clinical Gerontology, The University of Manchester, Hope Hospital, Salford, UK
Search for more papers by this authorGyorgy Bartfai MD
Gynaecology and Andrology, Albert Szent-Gyorgy Medical University, Szeged, Hungary
Search for more papers by this authorSteven Boonen MD
Division of Gerontology and Geriatrics & Centre for Musculoskeletal Research, Department of Experimental Medicine, Katholieke Universiteit Leuven, Leuven, Belgium
Search for more papers by this authorFelipe F. Casanueva MD
Department of Medicine, Santiago de Compostela University, Complejo Hospitalario Universitario de Santiago (CHUS), Santiago de Compostela, Spain
CIBER de Fisiopatología Obesidad y Nutricion (CB06/03), Instituto Salud Carlos III, Santiago de Compostela, Spain
Search for more papers by this authorJoseph D. Finn BSc
Epidemiology Unit, The University of Manchester, Manchester, UK
Search for more papers by this authorIlpo T. Huhtaniemi MD
Department of Reproductive Biology, Imperial College London, Hammersmith Campus, London, UK
Search for more papers by this authorKrzysztof Kula MD
Department of Andrology and Reproductive Endocrinology, Medical University of Lodz, Lodz, Poland
Search for more papers by this authorMargus Punab MD
Andrology Unit, United Laboratories of Tartu University Clinics, Tartu, Estonia
Search for more papers by this authorDirk Vanderschueren MD
Department of Andrology and Endocrinology, Katholieke Universiteit Leuven, Leuven, Belgium
Search for more papers by this authorMartin K. Rutter MD
Cardiovascular Research Group, School of Biomedicine, The University of Manchester, Manchester, UK
Search for more papers by this authorMario Maggi MD
Sexual Medicine and Andrology Unit Department of Experimental, Clinical, and Biomedical Sciences, University of Florence, Florence, Italy
Search for more papers by this authorEMAS Study Group
The members of the European Male Aging Study (EMAS) group are listed in Appendix A.Search for more papers by this authorAbstract
Introduction
We previously reported that in male patients consulting for sexual dysfunction, low prolactin (PRL) levels were associated with metabolic syndrome (MetS), arteriogenic erectile dysfunction, and incident major cardiovascular events.
Aim
The aim of this study is to assess the clinical associations of PRL levels in the European Male Ageing Study (EMAS).
Methods
EMAS is a prospective, observational cohort of community-dwelling men aged 40–79 years old (mean age 60 ± 11 years old). PRL was available for 2,948 men.
Main Outcome Measures
Different parameters were evaluated including the Short Form-36 questionnaire, Becks Depression Inventory, the Adverse Life Events Scale, the Physical Activity Scale for the Elderly, and the EMAS sexual function questionnaire (EMAS-SFQ).
Results
After the adjustment for confounders, PRL levels were inversely related with worsening of sexual function as compared with the previous year, as derived from change in sexual functioning domain of the EMAS-SFQ (adj. r = −0.043; P = 0.029). The strongest correlation (Wald = 6.840; P = 0.009) was observed between lower PRL levels and reduced enjoyment of orgasmic experiences. Furthermore, an inverse relationship between PRL levels and stressful life events or depressive symptoms was observed. Low PRL was also negatively associated with an unhealthy metabolic phenotype as well as with the MetS (Wald = 5.229; P = 0.022). In line with these data, low PRL was associated with a lower level of physical activity and feeling unhealthier.
Conclusions
Low PRL is related to several metabolic, psychological, and sexual unhealthy characteristics in European men. Checking PRL might be useful to stratify men for cardiovascular risk and to encourage appropriate lifestyle changes. Corona G, Wu FC, Rastrelli G, Lee DM, Forti G, O'Connor DB, O'Neill TW, Pendleton N, Bartfai G, Boonen S, Casanueva FF, Finn JD, Huhtaniemi IT, Kula K, Punab M, Vanderschueren D, Rutter MK, Maggi M, and the EMAS Study Group. Low prolactin is associated with sexual dysfunction and psychological or metabolic disturbances in middle aged and elderly men: The European Male Aging Study (EMAS). J Sex Med 2014;11:240–253.
References
- 1 Ben-Jonathan N, LaPensee CR, LaPensee EW. What can we learn from rodents about prolactin in humans? Endocr Rev 2008; 29: 1–41.
- 2 Sobrinho LG. Prolactin, psychological stress and environment in humans: Adaptation and maladaptation. Pituitary 2003; 6: 35–39.
- 3 Maggi M, Buvat J, Corona G, Guay A, Torres LO. Hormonal causes of male sexual dysfunctions and their management (hyperprolactinemia, thyroid disorders, GH disorders, and DHEA). J Sex Med 2013; 10: 661–677.
- 4 Buvat J, Maggi M, Gooren L, Guay AT, Kaufman J, Morgentaler A, Schulman C, Tan HM, Torres LO, Yassin A, Zitzmann M. Endocrine aspects of male sexual dysfunctions. J Sex Med 2010; 7(4 Pt 2): 1627–1656.
- 5 Bole-Feysot C, Goffin V, Edery M, Binart N, Kelly PA. Prolactin (PRL) and its receptor: Actions, signal transduction pathways and phenotypes observed in PRL receptor knockout mice. Endocr Rev 1998; 19: 225–268.
- 6 Buvat J. Hyperprolactinemia and sexual function in men: A short review. Int J Impot Res 2003; 15: 373–377.
- 7 Corona G, Mannucci E, Fisher AD, Lotti F, Ricca V, Balercia G, Petrone L, Forti G, Maggi M. Effect of hyperprolactinemia in male patients consulting for sexual dysfunction. J Sex Med 2007; 4: 1485–1493.
- 8 Corona G, Rastrelli G, Ricca V, Jannini EA, Vignozzi L, Monami M, Sforza A, Forti G, Mannucci E, Maggi M. Risk factors associated with primary and secondary reduced libido in male patients with sexual dysfunction. J Sex Med 2013; 10: 1074–1089.
- 9 Ciccarelli A, Guerra E, De Rosa M, Milone F, Zarrilli S, Lombardi G, Colao A. PRL secreting adenomas in male patients. Pituitary 2005; 8: 39–42.
- 10 Corona G, Mannucci E, Jannini EA, Lotti F, Ricca V, Monami M, Boddi V, Bandini E, Balercia G, Forti G, Maggi M. Hypoprolactinemia: A new clinical syndrome in patients with sexual dysfunction. J Sex Med 2009; 6: 1457–1466.
- 11 Corona G, Rastrelli G, Boddi V, Monami M, Melani C, Balzi D, Sforza A, Forti G, Mannucci E, Maggi M. Prolactin levels independently predict major cardiovascular events in patients with erectile dysfunction. Int J Androl 2011; 34: 217–224.
- 12 Haring R, Völzke H, Vasan RS, Felix SB, Nauck M, Dörr M, Wallaschofski H. Sex-specific associations of serum prolactin concentrations with cardiac remodeling: Longitudinal results from the Study of Health Pomerania (SHIP). Atherosclerosis 2012; 221: 570–576.
- 13 Lee DM, O'Neill TW, Pye SR, Silman AJ, Finn JD, Pendleton N, Bartfai G, Casanueva F, Forti G, Giwercman A, Huhtaniemi IT, Kula K, Punab M, Boonen S, Vanderschueren D, Wu FC; EMAS study group. The European Male Ageing Study: Design, methods and recruitment. Int J Androl 2009; 32: 11–24.
- 14 Corona G, Lee DM, Forti G, O'Connor DB, Maggi M, O'Neill TW, Pendleton N, Bartfai G, Boonen S, Casanueva FF, Finn JD, Giwercman A, Han TS, Huhtaniemi IT, Kula K, Lean ME, Punab M, Silman AJ, Vanderschueren D, Wu FC, EMAS Study Group. Age-related changes in general and sexual health in middle-aged and older men: Results from the European Male Ageing Study (EMAS). J Sex Med 2010; 7(4 Pt1): 1362–1380.
- 15 Corona G, Wu FC, Forti G, Lee DM, O'Connor DB, O'Neill TW, Pendleton N, Bartfai G, Boonen S, Casanueva FF, Finn JD, Giwercman A, Han TS, Huhtaniemi IT, Kula K, Lean ME, Punab M, Vanderschueren D, Jannini EA, Mannucci E, Maggi M, EMAS Study Group. Thyroid hormones and male sexual function. Int J Androl 2012; 35: 668–679.
- 16 Ware JE, Sherbourne CD. The MOS 36-item short form health survey (SF-36): Conceptual framework and item selection. Med Care 1992; 30: 473–483.
- 17 Beck AT, Steer RA, Brown GK. Manual for the beck depression inventory-II. San Antonio, TX: Psychological Corporation; 1996.
- 18 Brugha T, Bebbington P, Tennant C, Hurry J. The list of threatening experiences: A subset of 12 life event categories with considerable long-term contextual threat. Psychol Med 1985; 15: 189–194.
- 19 Washburn RA, Smith KW, Jette AM, Janney CA. The Physical Activity scale for the Elderly (PASE): Development and evaluation. J Clin Epidemiol 1993; 46: 153–162.
- 20 O'Connor DB, Corona G, Forti G, Tajar A, Lee DM, Finn JD, Bartfai G, Boonen S, Casanueva FF, Giwercman A, Huhtaniemi IT, Kula K, O'Neill TW, Pendleton N, Punab M, Silman AJ, Vanderschueren D, Wu FC. Assessment of sexual health in aging men in Europe: Development and validation of the European Male Ageing Study sexual function questionnaire. J Sex Med 2008; 5: 1374–1385.
- 21 O'Connor DB, Lee DM, Corona G, Forti G, Tajar A, O'Neill TW, Pendleton N, Bartfai G, Boonen S, Casanueva FF, Finn JD, Giwercman A, Han TS, Huhtaniemi IT, Kula K, Labrie F, Lean ME, Punab M, Silman AJ, Vanderschueren D, Wu FC, European Male Ageing Study Group. The relationships between sex hormones and sexual function in middle-aged and older European men. J Clin Endocrinol Metab 2011; 96: E1577–1587.
- 22 Huhtaniemi IT, Tajar A, Lee DM, O'Neill TW, Finn JD, Bartfai G, Boonen S, Casanueva FF, Giwercman A, Han TS, Kula K, Labrie F, Lean ME, Pendleton N, Punab M, Silman AJ, Vanderschueren D, Forti G, Wu FC, EMAS Group. Comparison of serum testosterone and estradiol measurements in 3174 European men using platform immunoassay and mass spectrometry; relevance for the diagnostics in aging men. Eur J Endocrinol 2012; 166: 983–991.
- 23 Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, Fruchart J-C, James WPT, Loria CM, Smith SC, Jr. Harmonizing the metabolic syndrome: A joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 2009; 120: 1640–1645.
- 24 Corona G, Rastrelli G, Vignozzi L, Mannucci E, Maggi M. Testosterone, cardiovascular disease and the metabolic syndrome. Best Pract Res Clin Endocrinol Metab 2011; 25: 337–353.
- 25 Smith SR. The endocrinology of obesity. Endocrinol Metab Clin North Am 1996; 25: 921–942.
- 26 Weaver JU, Noonan K, Kopelman PG, Coste M. Impaired prolactin secretion and body fat distribution in obesity. Clin Endocrinol (Oxf) 1990; 32: 641–646.
- 27 Donders SH, Pieters GF, Heevel JG, Ross HA, Smals AG, Kloppenborg PW. Disparity of thyrotropin (TSH) and prolactin responses to TSH-releasing hormone in obesity. J Clin Endocrinol Metab 1985; 61: 56–59.
- 28 Lala VR, Ray A, Jamias P, Te D, Orteza N, Fiscina B, Noto R. Prolactin and thyroid status in prepubertal children with mild to moderate obesity. J Am Coll Nutr 1988; 7: 361–366.
- 29 Röjdmark S, Rössner S. Decreased dopaminergic control of prolactin secretion in male obesity: Normalization by fasting. Metabolism 1991; 40: 191–195.
- 30 Steger RW, Rabe MB. The effect of diabetes mellitus on endocrine and reproductive function. Proc Soc Exp Biol Med 1997; 214: 1–11.
- 31 Sondermeijer BM, Klein Twennaar CF, Kastelein JJ, Franssen EJ, Hutten BA, Dallinga-Thie GM, Stroes ES, Fliers E, Twickler MT, Serlie MJ. Infusion of a lipid emulsion in healthy men decreases the serotonergic response. Neuroendocrinology 2012; 95: 325–331.
- 32 Van den Berghe G, de Zegher F, Veldhuis JD, Wouters P, Gouwy S, Stockman W, Weekers F, Schetz M, Lauwers P, Bouillon R, Bowers CY. Thyrotrophin and prolactin release in prolonged critical illness: Dynamics of spontaneous secretion and effects of growth hormone-secretagogues. Clin Endocrinol (Oxf) 1997; 47: 599–612.
- 33 Bondanelli M, Zatelli MC, Ambrosio MR, degli Uberti EC. Systemic illness. Pituitary 2008; 11: 187–207.
- 34 Langouche L, Princen L, Gunst J, Güiza F, Derde S, Van den Berghe G. Anterior pituitary morphology and hormone production during sustained critical illness in a rabbit model. Horm Metab Res 2013; 45: 277–282.
- 35 Arroba AI, Lechuga-Sancho AM, Frago LM, Argente J, Chowen JA. Cell-specific expression of X-linked inhibitor of apoptosis in the anterior pituitary of streptozotocin-induced diabetic rats. J Endocrinol 2007; 192: 215–227.
- 36 Torner L, Toschi N, Pohlinger A, Landgraf R, Neumann ID. Anxiolytic and anti-stress effects of brain prolactin: Improved efficacy of antisense targeting of the prolactin receptor by molecular modeling. J Neurosci 2001; 21: 3207–3214.
- 37 Torner L, Karg S, Blume A, Kandasamy M, Kuhn HG, Winkler J, Aigner L, Neumann ID. Prolactin prevents chronic stress-induced decrease of adult hippocampal neurogenesis and promotes neuronal fate. J Neurosci 2009; 29: 1826–1833.
- 38 Walker TL, Vukovic J, Koudijs MM, Blackmore DG, Mackay EW, Sykes AM, Overall RW, Hamlin AS, Bartlett PF. Prolactin stimulates precursor cells in the adult mouse hippocampus. PLoS ONE 2012; 7: e44371.
- 39 Mann JJ, McBride PA, Malone KM, DeMeo M, Keilp J. Blunted serotonergic responsivity in depressed inpatients. Neuropsychopharmacology 1995; 13: 53–64.
- 40 Keilp JG, Oquendo MA, Stanley BH, Burke AK, Cooper TB, Malone KM, Mann JJ. Future suicide attempt and responses to serotonergic challenge. Neuropsychopharmacology 2010; 35: 1063–1072.
- 41 Ely DL. Hypertension, social rank and aortic arteriosclerosis in CBA/J mice. Physiol Behav 1981; 26: 655–661.
- 42 Henry JP, Stephens PM, Ely DL. Psychosocial hypertension and the defence and defeat reactions. J Hypertens 1986; 4: 687–697.
- 43 Theorell T. Prolactin—A hormone that mirrors passiveness in crisis situations. Integr Physiol Behav Sci 1992; 27: 32–38.
- 44 Cruz-Casallas PE, Nasello AG, Hucke EE, Felicio LF. Dual modulation of male sexual behavior in rats by central prolactin: Relationship with in vivo striatal dopaminergic activity. Psychoneuroendocrinology 1999; 24: 681–693.
- 45 Drago F, Lissandrello CO. The “low-dose” concept and the paradoxical effects of prolactin on grooming and sexual behavior. Eur J Pharmacol 2000; 405: 131–137.
- 46 Gettler LT, McDade TW, Feranil AB, Kuzawa CW. Prolactin, fatherhood, and reproductive behavior in human males. Am J Phys Anthropol 2012; 148: 362–370.
- 47 Seo Y, Jeong B, Kim JW, Choi J. Plasma concentration of prolactin, testosterone might be associated with brain response to visual erotic stimuli in healthy heterosexual males. Psychiatry Investig 2009; 6: 194–203.
- 48 Redouté J, Stoléru S, Grégoire MC, Costes N, Cinotti L, Lavenne F, Le Bars D, Forest MG, Pujol JF. Brain processing of visual sexual stimuli in human males. Hum Brain Mapp 2000; 11: 162–177.
- 49 Haraguchi S, Koyama T, Hasunuma I, Vaudry H, Tsutsui K. In the rat, intracerebroventricular injection of ovine PRL increases not only sexual behavior, but also dopaminergic activity in striatal microdialysis perfusates. Endocrinology 2010; 151: 2211–2212.
- 50 Lindell SG, Suomi SJ, Shoaf S, Linnoila M, Higley JD. Salivary prolactin as a marker for central serotonin turnover. Biol Psychiatry 1999; 46: 568–572.
- 51 Yatham LN, Steiner M. Neuroendocrine probes of serotonergic function: A critical review. Life Sci 1993; 53: 447–463.
- 52 Coto E, Reguero JR, Alvarez V, Morales B, Batalla A, González P, Martín M, García-Castro M, Iglesias-Cubero G, Cortina A. 5-Hydroxytryptamine 5-HT2A receptor and 5-hydroxytryptamine transporter polymorphisms in acute myocardial infarction. Clin Sci (Lond) 2003; 104: 241–245.
- 53 Yuan X, Yamada K, Ishiyama-Shigemoto S, Koyama W, Nonaka K. Identification of polymorphic loci in the promoter region of the serotonin 5-HT2C receptor gene and their association with obesity and type II diabetes. Diabetologia 2000; 43: 373–376.
- 54 Rosmond R, Bouchard C, Björntorp P. Increased abdominal obesity in subjects with a mutation in the 5-HT(2A) receptor gene promoter. Ann N Y Acad Sci 2002; 967: 571–575.
- 55 Sussman N, Ginsberg DL, Bikoff J. Effects of nefazodone on body weight: A pooled analysis of selective serotonin reuptake inhibitor- and imipramine-controlled trials. J Clin Psychiatry 2001; 62: 256–260.
- 56 Daubresse JC, Kolanowski J, Krzentowski G, Kutnowski M, Scheen A, Van Gaal L. Usefulness of fluoxetine in obese non-insulin-dependent diabetics: A multicenter study. Obes Res 1996; 4: 391–396.
- 57 Muldoon MF, Mackey RH, Korytkowski MT, Flory JD, Pollock BG, Manuck SB. The metabolic syndrome is associated with reduced central serotonergic responsivity in healthy community volunteers. J Clin Endocrinol Metab 2006; 91: 718–721.
- 58 Muldoon MF, Mackey RH, Williams KV, Korytkowski MT, Flory JD, Manuck SB. Low central nervous system serotonergic responsivity is associated with the metabolic syndrome and physical inactivity. J Clin Endocrinol Metab 2004; 89: 266–271.
- 59 Muldoon MF, Mackey RH, Sutton-Tyrrell K, Flory JD, Pollock BG, Manuck SB. Lower central serotonergic responsivity is associated with preclinical carotid artery atherosclerosis. Stroke 2007; 38: 2228–2233.
- 60 Yatham LN, Steiner M. Neuroendocrine probes of serotonergic function: A critical review. Life Sci 1993; 53: 447–463.
- 61 Waldinger MD. The neurobiological approach to premature ejaculation. J Urol 2002; 168: 2359–2367.
- 62 Corona G, Jannini EA, Vignozzi L, Rastrelli G, Maggi M. The hormonal control of ejaculation. Nat Rev Urol 2012; 9: 508–519.
- 63 Corona G, Jannini EA, Lotti F, Boddi V, De Vita G, Forti G, Lenzi A, Mannucci E, Maggi M. Premature and delayed ejaculation: Two ends of a single continuum influenced by hormonal milieu. Int J Androl 2011; 34: 41–48.
- 64 Corona G, Mannucci E, Petrone L, Fisher AD, Balercia G, De Scisciolo G, Pizzocaro A, Giommi R, Chiarini V, Forti G, Maggi M. Psychobiological correlates of delayed ejaculation in male patients with sexual dysfunctions. J Androl 2006; 27: 453–458.
- 65 Boddi V, Corona G, Monami M, Fisher AD, Bandini E, Melani C, Balzi D, Sforza A, Patussi V, Forti G, Mannucci E, Maggi M. Priapus is happier with Venus than with Bacchus. J Sex Med 2010; 7: 2831–2841.