Erectile dysfunction as a cardiovascular risk factor in patients with diabetes

Endocrine

Volumn 43, Issue 2, 2013, Pages 285-292

  Gandaglia, Giorgio ^a   Salonia, Andrea ^a   Passoni, Niccolò ^a   Montorsi, Piero ^b   Briganti, Alberto ^a   Montorsi, Francesco ^a  

^a VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

Author keywords

Coronary artery disease; Diabetes; Erectile dysfunction

Indexed keywords

PHOSPHODIESTERASE V INHIBITOR; PLACEBO;

ANGINA PECTORIS; ARTERY DIAMETER; CARDIOVASCULAR DISEASE; CARDIOVASCULAR MORTALITY; CARDIOVASCULAR RISK; CLINICAL FEATURE; CORONARY ARTERY DISEASE; DIABETES MELLITUS; DISEASE ASSOCIATION; DISEASE MARKER; DRUG EFFECT; DRUG RESPONSE; ERECTILE DYSFUNCTION; HEART INFARCTION; HEART PROTECTION; HEART VENTRICLE HYPERTROPHY; HUMAN; PATIENT ASSESSMENT; PRACTICE GUIDELINE; PREVALENCE; PRIORITY JOURNAL; PROSPECTIVE STUDY; REVIEW; RISK ASSESSMENT; RISK FACTOR; SENSITIVITY ANALYSIS;

EID: 84879545227     PISSN: 1355008X     EISSN: 15590100     Source Type: Journal    
DOI: 10.1007/s12020-012-9780-2     Document Type: Review

References (79)

1. NIH Consensus Conference. Impotence. NIH Consensus Development Panel on Impotence. JAMA, 270, 83-90 (1993)
2. R.W. Lewis, K.S. Fugl-Meyer, G. Corona, R.D. Hayes, E.O. Laumann, E.D. Moreira Jr, A.H. Rellini, T. Segraves, Definitions/epidemiology/risk factors for sexual dysfunction. J. Sex. Med. 7, 1598-1607 (2010)
3. G. Corona, D.M. Lee, G. Forti, D.B. O'Connor, M. Maggi, T.W. O'Neill, N. Pendleton, G. Bartfai, S. Boonen, F.F. Casanueva, J.D. Finn, A. Giwercman, T.S. Han, I.T. Huhtaniemi, K. Kula, M.E. Lean, M. Punab, A.J. Silman, D. Vanderschueren, F.C. Wu, 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. 7, 1362-1380 (2010)
4. J. De Almeida Claro, O.G. Kaufmann, G. Alarcon, W. Aguiar, A. Nadozza Jr, V. Ortiz, M. Srougi, Could a rural lifestyle decrease the prevalence of erectile dysfunction? BJU Int. 99, 127-129 (2007)
5. N.M. Gades, A. Nehra, D.J. Jacobson, M.E. McGree, C.J. Girman, T. Rhodes, R.O. Roberts, M.M. Lieber, S.J. Jacobsen, Association between smoking and erectile dysfunction: a population-based study. Am. J. Epidemiol. 161, 346-351 (2005)
6. B.P. Gupta, M.H. Murad, M.M. Clifton, L. Prokop, A. Nehra, S.L. Kopecky, The effect of lifestyle modification and cardiovascular risk factor reduction on erectile dysfunction: a systematic review and meta-analysis. Arch. Intern. Med. 171, 1797-1803 (2011)
7. S.R. Fine, Erectile dysfunction and comorbid diseases, androgen deficiency, and diminished libido in men. J. Am. Osteopath. Assoc. 104, S9-S15 (2004)
8. C. Gazzaruso, S. Giordanetti, E. De Amici, G. Bertone, C. Falcone, D. Geroldi, P. Fratino, S.B. Solerte, A. Garzaniti, Relationship between erectile dysfunction and silent myocardial ischemia in apparently uncomplicated type 2 diabetic patients. Circulation 110, 22-26 (2004)
9. J. Hidalgo-Tamola, K. Chitaley, Review type 2 diabetes mellitus and erectile dysfunction. J. Sex. Med. 6, 916-926 (2009)
10. H.A. Feldman, I. Goldstein, D.G. Hatzichristou, R.J. Krane, J.B. McKinlay, Impotence and its medical and psychosocial correlates: results of the Massachusetts Male Aging Study. J. Urol. 151, 54-61 (1994)
11. F.A. Giuliano, A. Leriche, E.O. Jaudinot, A.S. de Gendre, Prevalence of erectile dysfunction among 7689 patients with diabetes or hypertension, or both. Urology 64, 1196-1201 (2004)
12. J.P. Burke, D.J. Jacobson, M.E. McGree, A. Nehra, R.O. Roberts, C.J. Girman, M.M. Lieber, S.J. Jacobsen, Diabetes and sexual dysfunction: results from the Olmsted County study of urinary symptoms and health status among men. J. Urol. 177, 1438-1442 (2007)
13. A. Al-Hunayan, M. Al-Mutar, E.O. Kehinde, L. Thalib, M. Al-Ghorory, The prevalence and predictors of erectile dysfunction in men with newly diagnosed with type 2 diabetes mellitus. BJU Int. 99, 130-134 (2007)
14. G. Yang, C. Pan, J. Lu, Prevalence of erectile dysfunction among Chinese men with type 2 diabetes mellitus. Int. J. Impot. Res. 22, 310-317 (2010)
15. R. Klein, B.E. Klein, K.E. Lee, S.E. Moss, K.J. Cruickshanks, Prevalence of self-reported erectile dysfunction in people with long-term IDDM. Diabetes Care 19, 135-141 (1996)
16. O. Kalter-Leibovici, J. Wainstein, A. Ziv, I. Harman-Bohem, H. Murad, I. Raz, Israel Diabetes Research Group (IDRG) Investigators, Clinical, socioeconomic, and lifestyle parameters associated with erectile dysfunction among diabetic men. Diabetes Care 28, 1739-1744 (2005)
17. W.B. Kannel, D.L. McGee, Diabetes and cardiovascular disease. The Framingham study. JAMA 241, 2035-2038 (1979)
18. S.M. Grundy, I.J. Benjamin, G.L. Burke, A. Chait, R.H. Eckel, B.V. Howard, W. Mitch, S.C. Smith Jr, J.R. Sowers, Diabetes and cardiovascular disease: a statement for healthcare professionals from the American Heart Association. Circulation 100, 1134-1146 (1999)
19. C.M. Alexander, P.B. Landsman, S.M. Teutsch, Diabetes mellitus, impaired fasting glucose, atherosclerotic risk factors, and prevalence of coronary heart disease. Am. J. Card. 86, 897-902 (2000)
20. R. Scognamiglio, C. Negut, A. Ramondo, A. Tiengo, A. Avogaro, Detection of coronary artery disease in asymptomatic patients with type 2 diabetes mellitus. J. Am. Coll. Cardiol. 47, 65-71 (2006)
21. F.J. Wackers, L.H. Young, S.E. Inzucchi, D.A. Chyun, J.A. Davey, E.J. Barrett, R. Taillefer, S.D. Wittlin, G.V. Heller, N. Filipchuk, S. Engel, R.E. Ratner, A.E. Iskandrian, Detection of ischemia in asymptomatic diabetics Investigators: detection of silent myocardial ischemia in asymptomatic diabetic subjects: the DIAD study. Diabetes Care 27, 1954-1961 (2004)
22. S. Stern, Symptoms other than chest pain may be important in the diagnosis of "silent ischemia," or "the sounds of silence". Circulation 111, e435-e437 (2005)
23. American Diabetes Association. Consensus development conference on the diagnosis of coronary heart disease in people with diabetes: 10-11 February 1998, Miami, Florida. Diabetes care 21, 1551-1559 (1998)
24. C. Gazzaruso, A. Coppola, T. Montalcini, C. Valenti, A. Garzaniti, G. Pelissero, F. Salvucci, P. Gallotti, A. Pujia, C. Falcone, S.B. Solerte, A. Giustina, Erectile dysfunction can improve the effectiveness of the current guidelines for the screening for asymptomatic coronary artery disease in diabetes. Endocrine 40, 273-279 (2011)
25. F.J. Wackers, Asymptomatic patients with diabetes mellitus should be screened for coronary artery disease. J. Nucl. Cardiol. 13, 609-615 (2006)
26. R.C. Ma, W.Y. So, X. Yang, L.W. Yu, A.P. Kong, G.T. Ko, C.C. Chow, C.S. Cockram, J.C. Chan, P.C. Tong, Erectile dysfunction predicts coronary heart disease in type 2 diabetes. J. Am. Coll. Cardiol. 51, 2045-2050 (2008)
27. K. García-Malpartida, R. Mármol, A. Jover, M.J. Gómez-Martínez, E. Solá-Izquierdo, V.M. Victor, M. Rocha, D. Sanmiguel, A. Hernández-Mijares, Relationship between erectile dysfunction and silent myocardial ischemia in type 2 diabetic patients with no known macrovascular complications. J. Sex. Med. 8, 2606-2616 (2011)
28. T.D. Miller, R.F. Redberg, F.J. Wackers, Screening asymptomatic diabetic patients for coronary artery disease: why not? J. Am. Coll. Cardiol. 48, 761-764 (2006)
29. G.A. Beller, Noninvasive screening for coronary atherosclerosis and silent ischemia in asymptomatic type 2 diabetic patients: is it appropriate and cost-effective? J. Am. Coll. Cardiol. 49, 1918-1923 (2007)
30. E. Faglia, M. Mantero, A. Quarantiello, M. Gino, V. Curci, M. Caminiti, R. Mattioli, A. Morabito, Risk reduction of cardiac events by screening of unknown asymptomatic coronary artery disease in subjects with type 2 diabetes mellitus at high cardiovascular risk: an open-label randomized pilot study. Am. Heart J. 149, e1-e6 (2005)
31. L.H. Young, F.J. Wackers, D.A. Chyun, J.A. Davey, E.J. Barrett, R. Taillefer, G.V. Heller, A.E. Iskandrian, S.D. Wittlin, N. Filipchuk, R.E. Ratner, S.E. Inzucchi, DIAD Investigators, Cardiac outcomes after screening for asymptomatic coronary artery disease in patients with type 2 diabetes: the DIAD study: a randomized controlled trial. JAMA 301, 1547-1555 (2009)
32. C. Gazzaruso, A. Coppola, T. Montalcini, C. Valenti, G. Pelissero, S.B. Solerte, F. Salvucci, P. Gallotti, A. Pujia, A. Garzaniti, A. Giustina, Screening for asymptomatic coronary artery disease can reduce cardiovascular mortality and morbidity in type 2 diabetic patients. Intern. Emerg. Med. 7, 257-266 (2012)
33. O.H. Franco, E.W. Steyerberg, F.B. Hu, J. Mackenbach, W. Nusselder, Associations of diabetes mellitus with total life expectancy and life expectancy with and without cardiovascular disease. Arch. Intern. Med. 167, 1145-1151 (2007)
34. M. Laakso, Hyperglycemia and cardiovascular disease in type 2 diabetes. Diabetes 48, 937-942 (1999)
35. K. Gu, C.C. Cowie, M.I. Harris, Mortality in adults with and without diabetes in a national cohort of the U.S. population, 1971-1993. Diabetes Care 21, 1138-1145 (1998)
36. S.M. Haffner, S. Lehto, T. Ronnemaa, K. Pyörälä, M. Laakso, Mortality from coronary heart disease in subjects with type 2 diabetes and in nondiabetic subjects with and without prior myocardial infarction. N. Engl. J. Med. 339, 229-234 (1998)
37. S. Yamagishi, Cardiovascular disease in recent onset diabetes mellitus. J. Cardiol. 57, 257-262 (2011)
38. W.D. Rosamond, L.E. Chambless, A.R. Folsom, L.S. Cooper, D.E. Conwill, L. Clegg, C.H. Wang, G. Heiss, Trends in the incidence of myocardial infarction and in mortality due to coronary heart disease, 1987 to 1994. N. Engl. J. Med. 339, 861-867 (1998)
39. J.H. Lee, R. Ngengwe, P. Jones, F. Tang, J.H. O'Keefe, Erectile dysfunction as a coronary artery disease risk equivalent. J. Nucl. Cardiol. 15, 800-803 (2008)
40. The Diabetes Control and Complications Trial Research Group. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N. Eng. J. Med. 329, 977-86 (1993)
41. P.J. Savage, Cardiovascular complications of diabetes mellitus: what we know and what we need to know about their prevention. Ann. Intern. Med. 124, 123-126 (1996)
42. M. Chiariello, C. Indolfi, M.R. Cotecchia, C. Sifola, M. Romano, M. Condorelli, Asymptomatic transient ST changes during ambulatory ECG monitoring in diabetic patients. Am. Heart J. 110, 529-534 (1985)
43. O. May, H. Arildsen, E.M. Damsgaard, H. Mickley, Prevalence and prediction of silent ischaemia in diabetes mellitus: a population-based study. Cardiovasc. Res. 34, 241-247 (1997)
44. P. Valensi, E. Cosson, It is not yet the time to stop screening diabetic patients for silent myocardial ischaemia. Diabetes Metab. 36, 91-96 (2010)
45. J.Y. Dong, Y.H. Zhang, L.Q. Qin, Erectile dysfunction and risk of cardiovascular disease: meta-analysis of prospective cohort studies. J. Am. Coll. Cardiol. 58, 1378-1385 (2011)
46. W. Guo, C. Liao, Y. Zou, F. Li, T. Li, Q. Zhou, Y. Cao, X. Mao, Erectile dysfunction and risk of clinical cardiovascular events: a meta-analysis of seven cohort studies. J. Sex. Med. 7, 2805-2816 (2010)
47. S.T. Chang, C.M. Chu, J.F. Hsiao, C.M. Chung, J.J. Shee, C.S. Chen, J.T. Hsu, Coronary phenotypes in patients with erectile dysfunction and silent ischemic heart disease: a pilot study. J. Sex. Med. 7, 2798-2804 (2010)
48. C. Gratzke, J. Angulo, K. Chitaley, Y.T. Dai, N.N. Kim, J.S. Paick, U. Simonsen, S. Uckert, E. Wespes, K.E. Andersson, T.F. Lue, C.G. Stief, Anatomy, physiology, and pathophysiology of erectile dysfunction. J. Sex. Med. 7, 445-475 (2010)
49. K.L. Billups, A.J. Bank, H. Padma-Nathan, S.D. Katz, R.A. Williams, Erectile dysfunction as a harbinger for increased cardiometabolic risk. Int. J. Impot. Res. 20, 236-242 (2008)
50. G. Jackson, P. Montorsi, M.A. Adams, T. Anis, A. El-Sakka, M. Miner, C. Vlachopoulos, E. Kim, Cardiovascular aspects of sexual medicine. J. Sex. Med. 7, 1608-1626 (2010)
51. F. Montorsi, A. Briganti, A. Salonia, P. Rigatti, A. Margonato, A. Macchi, S. Galli, P.M. Ravagnani, P. Montorsi, Erectile dysfunction prevalence, time of onset and association with risk factors in 300 consecutive patients with acute chest pain and angiographically documented coronary artery disease. Eur. Urol. 44, 360-364 (2003)
52. R.A. Kloner, S.H. Mullin, T. Shook, R. Matthews, G. Mayeda, S. Burstein, H. Peled, C. Pollick, R. Choudhary, R. Rosen, H. Padma-Nathan, Erectile dysfunction in the cardiac patient: how common and should we treat? J. Urol. 170, S46-S50 (2003)
53. P. Montorsi, P.M. Ravagnani, S. Galli, A. Salonia, A. Briganti, J.P. Werba, F. Montorsi, Association between erectile dysfunction and coronary artery disease: matching the right target with the right test in the right patient. Eur. Urol. 50, 721-731 (2006)
54. H. Solomon, J.W. Man, G. Jackson, Erectile dysfunction and the cardiovascular patient: endothelial dysfunction is the common denominator. Heart 89, 251-253 (2003)
55. J. Araña Rosaínz Mde, M.O. Ojeda, J.R. Acosta, L.C. Elías-Calles, N.O. González, O.T. Herrera, C.T. García Álvarez, E.M. Rodríguez, M.E. Báez, E.Á. Seijas, R.F. Valdés, Imbalanced low-grade inflammation and endothelial activation in patients with type 2 diabetes mellitus and erectile dysfunction. J. Sex. Med. 8, 2017-2030 (2011)
56. P. Montorsi, P.M. Ravagnani, S. Galli, F. Rotatori, A. Briganti, A. Salonia, P. Rigatti, F. Montorsi, The artery size hypothesis: a macrovascular link between erectile dysfunction and coronary artery disease. Am. J. Cardiol. 96, 19M-23M (2005)
57. I.M. Thompson, C.M. Tangen, P.J. Goodman, J.L. Probstfield, C.M. Moinpour, C.A. Coltman, Erectile dysfunction and subsequent cardiovascular disease. JAMA 294, 2996-3002 (2005)
58. A.B. Araujo, T.G. Travison, P. Ganz, G.R. Chiu, V. Kupelian, R.C. Rosen, S.A. Hall, J.B. McKinlay, Erectile dysfunction and mortality. J. Sex. Med. 6, 2445-2454 (2009)
59. G. Corona, M. Monami, V. Boddi, M. Cameron-Smith, F. Lotti, G. de Vita, C. Melani, D. Balzi, A. Sforza, G. Forti, E. Mannucci, M. Maggi, Male sexuality and cardiovascular risk. A cohort study in patients with erectile dysfunction. J. Sex. Med. 7, 1918-1927 (2010)
60. A. Ponholzer, C. Temml, R. Obermayr, C. Wehrberger, S. Madersbacher, Is erectile dysfunction an indicator for increased risk of coronary heart disease and stroke? Eur. Urol. 48, 512-518 (2005)
61. P. Montorsi, P.M. Ravagnani, S. Galli, F. Rotatori, F. Veglia, A. Briganti, A. Salonia, F. Dehò, P. Rigatti, F. Montorsi, C. Fiorentini, Association between erectile dysfunction and coronary artery disease. Role of coronary clinical presentation and extent of coronary vessels involvement: the COBRA trial. Eur. Heart J. 27, 2632-2639 (2006)
62. E. Chiurlia, R. D'Amico, C. Ratti, A.R. Granata, R. Romagnoli, M.G. Modena, Subclinical coronary artery atherosclerosis in patients with erectile dysfunction. J. Am. Coll. Cardiol. 46, 1503-1506 (2005)
63. C. Gazzaruso, S.B. Solerte, A. Pujia, A. Coppola, M. Vezzoli, F. Salvucci, C. Valenti, A. Giustina, A. Garzaniti, Erectile dysfunction as a predictor of cardiovascular events and death in diabetic patients with angiographically proven asymptomatic coronary artery disease: a potential protective role for statins and 5-phosphodiesterase inhibitors. J. Am. Coll. Cardiol. 51, 2040-2044 (2008)
64. G.D. Batty, Q. Li, S. Czernichow, B. Neal, S. Zoungas, R. Huxley, A. Patel, B.E. de Galan, M. Woodward, P. Hamet, S.B. Harrap, N. Poulter, J. Chalmers, ADVANCE Collaborative Group, Erectile dysfunction and later cardiovascular disease in men with type 2 diabetes: prospective cohort study based on the ADVANCE (Action in Diabetes and Vascular Disease: Preterax and Diamicron Modified-Release Controlled Evaluation) trial. J. Am. Coll. Cardiol. 56, 1908-1913 (2010)
65. R.J. Heruti, I. Uri, Y. Arbel, M. Swartzon, S. Galor, D. Justo, Erectile dysfunction severity might be associated with poor cardiovascular prognosis in diabetic men. J. Sex. Med. 4, 465-471 (2007)
66. B.L. Meena, D.K. Kochar, T.D. Agarwal, R. Choudhary, A. Kochar, Association between erectile dysfunction and cardiovascular risk in individuals with type-2 diabetes without overt cardiovascular disease. Int. J. Diabetes Dev. Ctries. 29, 150-154 (2009)
67. C. Gazzaruso, A. Pujia, S.B. Solerte, E.D. Amici, E. Emanuele, C. Falcone, D. Geroldi, A. Giustina, A. Garzaniti, Erectile dysfunction and angiographic extent of coronary artery disease in type II diabetic patients. Int. J. Impot. Res. 18, 311-315 (2006)
68. P.F. Cohn, Prognosis for patients with different types of silent coronary artery disease. Circulation 75, II33-II35 (1987)
69. M.K. Gaba, S. Gaba, L.T. Clark, Cardiovascular disease in patients with diabetes: clinical considerations. J. Assoc. Acad. Minor. Phys. 10, 15-22 (1999)
70. D.E. Price, J.C. Gingell, S. Gepi-Attee, K. Wareham, P. Yates, M. Boolell, Sildenafil: study of a novel oral treatment for erectile dysfunction in diabetic men. Diabet. Med. 15, 821-825 (1998)
71. K. Hatzimouratidis, E. Amar, I. Eardley, F. Giuliano, D. Hatzichristou, F. Montorsi, Y. Vardi, E. Wespes, European Association of Urology, Guidelines on male sexual dysfunction: erectile dysfunction and premature ejaculation. Eur. Urol. 57, 804-814 (2010)
72. I. Saenz de Tejada, Molecular mechanisms for the regulation of penile smooth muscle contractility. Int. J. Impot. Res. 14, S6-S10 (2002)
73. B.G. Schwartz, L.A. Levine, G. Comstock, V.J. Stecher, R.A. Kloner, Cardiac uses of phosphodiesterase-5 inhibitors. J. Am. Coll. Cardiol. 59, 9-15 (2012)
74. M. Jamnicki-Abegg, D. Weihrauch, P.C. Chiari, J.G. Krolikowski, P.S. Pagel, D.C. Warltier, J.R. Kersten, Diabetes abolishes sildenafil-induced cGMP-dependent protein kinase-I expression and cardioprotection. J. Cardiovasc. Pharmacol. 50, 670-676 (2007)
75. M. Madhani, A.R. Hall, F. Cuello, R.L. Charles, J.R. Burgoyne, W. Fuller, A.J. Hobbs, M.J. Shattock, P. Eaton, Phospholemman Ser69 phosphorylation contributes to sildenafil-induced cardioprotection against reperfusion injury. Am. J. Physiol. Heart Circ. Physiol. 299, H827-H836 (2010)
76. F.N. Salloum, A. Abbate, A. Das, J.E. Houser, C.A. Mudrick, I.Z. Qureshi, N.N. Hoke, S.K. Roy, W.R. Brown, S. Prabhakar, R.C. Kukreja, Sildenafil (Viagra) attenuates ischemic cardiomyopathy and improves left ventricular function in mice. Am. J. Physiol. Heart. Circ. Physiol. 294, H1398-H1406 (2008)
77. F.N. Salloum, Y. Takenoshita, R.A. Ockaili, V.P. Daoud, E. Chou, K. Yoshida, R.C. Kukreja, Sildenafil and vardenafil but not nitroglycerin limit myocardial infarction through opening of mitochondrial K(ATP) channels when administered at reperfusion following ischemia in rabbits. J. Mol. Cell. Cardiol. 42, 453-458 (2007)
78. S. Rosanio, Y. Ye, S. Atar, A.M. Rahman, S.Y. Freeberg, M.H. Huang, B.F. Uretsky, Y. Birnbaum, Enhanced cardioprotection against ischemia-reperfusion injury with combining sildenafil with low-dose atorvastatin. Cardiovasc. Drugs Ther. 20, 27-36 (2006)
79. K.K. Chew, J. Finn, B. Stuckey, N. Gibson, F. Sanfilippo, A. Bremner, P. Thompson, M. Hobbs, K. Jamrozik, Erectile dysfunction as a predictor for subsequent atherosclerotic cardiovascular events: findings from a linked-data study. J. Sex. Med. 7, 192-202 (2010)