Low serum testosterone is associated with atherosclerosis in postmenopausal women undergoing hemodialysis

Clinical and Experimental Nephrology

Volumn 18, Issue 3, 2014, Pages 499-506

  Shiraki, Nobuaki ^a   Nakashima, Ayumu ^a   Doi, Shigehiro ^a   Carrero, Juan Jesús ^b   Sugiya, Naoko ^c   Ueno, Toshinori ^a   Stenvinkel, Peter ^b   Kohno, Nobuoki ^d   Masaki, Takao ^a  

^a HIROSHIMA UNIVERSITY HOSPITAL   (Japan)

^b KAROLINSKA INSTITUTE   (Sweden)

^c Kure Kyosai Hospital   (Japan)

^d HIROSHIMA UNIVERSITY   (Japan)

Author keywords

Atherosclerosis; Hemodialysis; Postmenopausal woman; Testosterone

Indexed keywords

C REACTIVE PROTEIN; CALCIUM; ESTRADIOL; PARATHYROID HORMONE; PHOSPHATE; SEX HORMONE BINDING GLOBULIN; TESTOSTERONE; BIOLOGICAL MARKER;

AGE; AGED; ARTERIAL WALL THICKNESS; ARTICLE; ATHEROSCLEROSIS; CALCIUM BLOOD LEVEL; CARDIO ANKLE VASCULAR INDEX; CARDIOVASCULAR PARAMETERS; CARDIOVASCULAR RISK; CHRONIC KIDNEY DISEASE; CONTROLLED STUDY; DIABETES MELLITUS; DISEASE ASSOCIATION; FEMALE; HEMODIALYSIS; HUMAN; HYPOTHESIS; JAPANESE (PEOPLE); MAJOR CLINICAL STUDY; MEDICAL HISTORY; PERIPHERAL OCCLUSIVE ARTERY DISEASE; PHOSPHATE BLOOD LEVEL; POSTMENOPAUSE; TESTOSTERONE BLOOD LEVEL; TREATMENT DURATION; BLOOD; CASE CONTROL STUDY; JAPAN; MIDDLE AGED; RENAL INSUFFICIENCY, CHRONIC; RENAL REPLACEMENT THERAPY; RISK FACTOR; SEVERITY OF ILLNESS INDEX; STATISTICAL MODEL; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ATHEROSCLEROSIS; BIOLOGICAL MARKERS; CAROTID INTIMA-MEDIA THICKNESS; CASE-CONTROL STUDIES; FEMALE; HUMANS; JAPAN; LOGISTIC MODELS; MIDDLE AGED; RENAL DIALYSIS; RENAL INSUFFICIENCY, CHRONIC; RISK FACTORS; SEVERITY OF ILLNESS INDEX; TESTOSTERONE;

EID: 84903380159     PISSN: 13421751     EISSN: 14377799     Source Type: Journal    
DOI: 10.1007/s10157-013-0840-6     Document Type: Article

References (46)

1. Carrero JJ. Gender differences in chronic kidney disease: underpinnings and therapeutic implications. Kidney Blood Press Res. 2010;33:383-92.
2. Carrero JJ, Qureshi AR, Nakashima A, et al. Prevalence and clinical implications of testosterone deficiency in men with end-stage renal disease. Nephrol Dial Transplant. 2011;26:184-90.
3. Carrero JJ, Stenvinkel P. The vulnerable man: impact of testosterone deficiency on the uraemic phenotype. Nephrol Dial Transplant. 2012;27:4030-41.
4. Basaria S, Dobs AS. Hypogonadism and androgen replacement therapy in elderly men. Am J Med. 2001;110:563-72.
5. Maggio M, Basaria S. Welcoming low testosterone as a cardiovascular risk factor. Int J Impot Res. 2009;21:261-4.
6. Alexandersen P, Haarbo J, Christiansen C. The relationship of natural androgens to coronary heart disease in males: a review. Atherosclerosis. 1996;125:1-13. (Pubitemid 26267117)
7. Shapiro J, Christiana J, Frishman WH. Testosterone and other anabolic steroids as cardiovascular drugs. Am J Ther. 1999;6:167-74. (Pubitemid 29230541)
8. Jones RD, Pugh PJ, Jones TH, et al. The vasodilatory action of testosterone: a potassium-channel opening or a calcium antagonistic action? Br J Pharmacol. 2003;138:733-44. (Pubitemid 36390629)
9. Foresta C, Caretta N, Lana A, et al. Reduced number of circulating endothelial progenitor cells in hypogonadal men. J Clin Endocrinol Metab. 2006;91:4599-602. (Pubitemid 44833444)
10. Dalia S, Fortune K, Anat J, et al. Effects of gonadal steroids and their antagonists on DNA synthesis in human vascular cells. Hypertension. 1998;32:39-45.
11. Carrero JJ, Bárány P, Yilmaz MI, et al. Testosterone deficiency is a cause of anaemia and reduced responsiveness to erythropoiesis-stimulating agents in men with chronic kidney disease. Nephrol Dial Transplant. 2012;27:709-15.
12. Cigarran S, Pousa M, Castro MJ, et al. (2013) Endogenous testosterone, muscle strength and fat-free mass in men with chronic kidney disease. J Ren Nutr.
13. Yilmaz MI, Sonmez A, Qureshi AR, et al. Endogenous testosterone, endothelial dysfunction, and cardiovascular events in men with nondialysis chronic kidney disease. Clin J Am Soc Nephrol. 2011;6:1617-25.
14. Kyriazis J, Tzanakis I, Stylianu K, et al. Low serum testosterone, arterial stiffness and mortality in male hemodialysis patients. Nephrol Dial Transplant. 2011;26:2971-7.
15. Laughlin GA, Goodell V, Barrett-Connor E. Extremes of endogenous testosterone are associated with increased risk of incident coronary events in older women. J Clin Endocrinol Metab. 2010;95:740-7.
16. Sievers C, Klotsche J, Pieper L, et al. Low testosterone levels predict all-cause mortality and cardiovascular events in women: a prospective cohort study in German primary care patients. Eur J Endocrinol. 2010;163:699-708.
17. Creatsa M, Armeni E, Stamatelopoulos K, et al. Circulating androgen levels are associated with subclinical atherosclerosis and arterial stiffness in healthy recently menopausal women. Metabolism. 2012;61:193-201.
18. Patel SM, Ratcliffe SJ, Reilly MP, et al. Higher serum testosterone concentration in older women is associated with insulin resistance, metabolic syndrome, and cardiovascular disease. J Clin Endocrinol Metab. 2009;94:4776-84.
19. McKinlay SM, Brambilla DJ, Posner JG. The normal menopause transition. Maturitas. 1992;14:103-15.
20. Kramer HM, Curhan GC, Singh A, et al. Permanent cessation of menses and postmenopausal hormone use in dialysis-dependent women: the HELP study. Am J Kidney Dis. 2003;41:643-50. (Pubitemid 36278382)
21. Wendelhag I, Wiklund O, Wikstrand J. Atherosclerotic changes in the femoral and carotid arteries in familial hypercholesterolemia. Ultrasonographic assessment of intima-media thickness and plaque occurrence. Arterioscler Thromb. 1993;13:1404-11. (Pubitemid 23303392)
22. Shirai K, Utino J, Otsuka K, et al. A novel blood pressure-independent arterial wall stiffness parameter; cardio-ankle vascular index (CAVI). J Atheroscler Thromb. 2006;13:101-7.
23. Zoungas S, Cameron JD, Kerr PG, et al. Association of carotid intima-medial thickness and indices of arterial stiffness with cardiovascular disease outcomes in CKD. Am J Kidney Dis. 2007;50:622-30. (Pubitemid 47444462)
24. Shoji T, Maekawa K, Emoto M, et al. Arterial stiffness predicts cardiovascular death independent of arterial thickness in a cohort of hemodialysis patients. Atherosclerosis. 2010;210:145-9.
25. Payne RB, Little AJ, Williams RB, et al. Interpretation of serum calcium in patients with abnormal serum proteins. Br Med J. 1973;4:643-6.
26. Singh AB, Norris K, Modi N, et al. Pharmacokinetics of a transdermal testosterone system in men with end stage renal disease receiving maintenance hemodialysis and healthy hypogonadal men. J Clin Endocrinol Metab. 2001;86:2437-45. (Pubitemid 32545688)
27. Schmidt A, Luger A, Hörl WH. Sexual hormone abnormalities in male patients with renal failure. Nephrol Dial Transplant. 2002;17:368-71. (Pubitemid 34211129)
28. Carrero JJ, Kyriazis J, Sonmez A, et al. Prolactin levels, endothelial dysfunction, and the risk of cardiovascular events and mortality in patients with CKD. Clin J Am Soc Nephrol. 2012;7:207-15.
29. Strippoli GF. Collaborative depression and sexual dysfunction (CDS) in hemodialysis working group. Sexual dysfunction in women with ESRD requiring hemodialysis. Clin J Am Soc Nephrol. 2012;7:974-81.
30. Hladunewich M, Hercz AE, Keunen J, et al. Pregnancy in end stage renal disease. Semin Dial. 2011;24:634-9.
31. Golden SH, Maguire A, Ding J, et al. Endogenous postmenopausal hormones and carotid atherosclerosis: a case-control study of the atherosclerosis risk in communities cohort. Am J Epidemiol. 2002;155:437-45. (Pubitemid 34174155)
32. Montalcini T, Gorgone G, Gazzaruso C, et al. Role of endogenous androgens on carotid atherosclerosis in non-obese postmenopausal women. Nutr Metab Cardiovasc Dis. 2007;17:705-11. (Pubitemid 350103758)
33. Bernini GP, Sgro' M, Barlascini CO, et al. Endogenous androgens and carotid intimal-medial thickness in women. J Clin Endocrinol Metab. 1999;84:2008-12.
34. Yaron M, Greenman Y, Rosenfeld JB, et al. Effect of testosterone replacement therapy on arterial stiffness in older hypogonadal men. Eur J Endocrinol. 2009;160:839-46.
35. Dockery F, Bulpitt CJ, Donaldson M, et al. The relationship between androgens and arterial stiffness in older men. J Am Geriatr Soc. 2003;51:1627-32. (Pubitemid 37409599)
36. Hougaku H, Fleg JL, Najjar SS, et al. Relationship between androgenic hormones and arterial stiffness, based on longitudinal hormone measurements. Am J Physiol Endocrinol Metab. 2006;290:E234-42.
37. Montalcini T, Gorgone G, Gazzaruso C, et al. Endogenous testosterone and endothelial function in postmenopausal women. Coron Artery Dis. 2007;18:9-13. (Pubitemid 44973750)
38. Izuhara M, Shioji K, Kadota S, et al. Relationship of cardio-ankle vascular index (CAVI) to carotid and coronary arteriosclerosis. Circ J. 2008;72:1762-7.
39. Carrero JJ, Stenvinkel P, Cuppari L, et al. Etiology of the protein-energy wasting syndrome in chronic kidney disease: a consensus statement from the International Society of Renal Nutrition and Metabolism (ISRNM). J Ren Nutr. 2013;23:77-90.
40. Nettleship JE, Jones TH, Channer KS, et al. Physiological testosterone replacement therapy attenuates fatty streak formation and improves high-density lipoprotein cholesterol in the Tfm mouse: an effect that is independent of the classic androgen receptor. Circulation. 2007;116:2427-34. (Pubitemid 350145077)
41. Braunstein GD, Johnson BD, Stanczyk FZ, et al. Relations between endogenous androgens and estrogens in postmenopausal women with suspected ischemic heart disease. J Clin Endocrinol Metab. 2008;93:4268-75. (Pubitemid 352789521)
42. Foresta C, Zuccarello D, De Toni L, et al. Androgens stimulate endothelial progenitor cells through an androgen receptor-mediated pathway. Clin Endocrinol (Oxf). 2008;68:284-9.
43. Liu D, Dillon JS. Dehydroepiandrosterone stimulates nitric oxide release in vascular endothelial cells: evidence for a cell surface receptor. Steroids. 2004;69:279-89. (Pubitemid 38748724)
44. Webb CM, Elkington AG, Kraidly MM, et al. Effects of oral testosterone treatment on myocardial perfusion and vascular function in men with low plasma testosterone and coronary heart disease. Am J Cardiol. 2008;101:618-24. (Pubitemid 351625084)
45. Malkin CJ, Jones RD, Jones TH, et al. Effect of testosterone on ex vivo vascular reactivity in man. Clin Sci (Lond). 2006;111:265-74. (Pubitemid 44599873)
46. Ros S, Carrero JJ. Endocrine alterations and cardiovascular risk in CKD: is there a link? Nefrologia. 2013;33:181-7.