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• W2094418908 abstract "Related Article, p. 367 Related Article, p. 367 Several endocrine abnormalities that arise as a direct consequence of chronic kidney disease (CKD) traditionally have been considered “innocent” consequences of uremia and received scarce attention.1Ros S. Carrero J.J. Endocrine alterations and cardiovascular risk in CKD: is there a link?.Nefrologia. 2013; 33: 181-187PubMed Google Scholar However, in recent years, evidence is mounting that testosterone deficiency is common in men with CKD and that this condition consistently associates with various cardiometabolic complications. In this issue of AJKD, Khurana et al2Khurana K.K. Navaneethan S.D. Arrigain S. Schold J.D. Nally Jr., J.V. Shoskes D.A. Serum testosterone levels and mortality in men with CKD stages 3-4.Am J Kidney Dis. 2014; 64: 367-374Google Scholar report the largest study to date on the association between serum testosterone level and mortality in men with non–dialysis-dependent CKD. The authors performed careful data extraction using electronic records from a tertiary-care center and identified 2,419 eligible men with CKD stages 3-4 who had undergone testosterone measurements. Hypogonadism is a very common finding in men with CKD, with a reported prevalence of approximately 50%-75% among contemporary dialysis cohorts.3Carrero J.J. Stenvinkel P. The vulnerable man: impact of testosterone deficiency on the uraemic phenotype.Nephrol Dial Transplant. 2012; 27: 4030-4041Crossref PubMed Scopus (60) Google Scholar Its pathogenesis is explained by the advanced age of CKD onset and by direct consequences of kidney failure (eg, inhibition of luteinizing hormone signaling and prolactin retention), which inhibit gonadotropin secretion.4Dousdampanis P, Trigka K, Fourtounas C, Bargman JM. Role of testosterone in the pathogenesis, progression, prognosis and comorbidity of men with chronic kidney disease [published online ahead of print September 30, 2013]. Ther Apher Dial. http://dx.doi.org/10.1111/1744-9987.12101.Google Scholar, 5Iglesias P. Carrero J.J. Diez J.J. Gonadal dysfunction in men with chronic kidney disease: clinical features, prognostic implications and therapeutic options.J Nephrol. 2012; 25: 31-42Crossref PubMed Scopus (77) Google Scholar, 6Carrero J.J. 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: 207-215Crossref PubMed Scopus (74) Google Scholar This is evidenced in this study by the strong multivariate inverse association observed between kidney function and testosterone deficiency. Typical risk factors for CKD, as well as common drugs (Fig 1), further suppress testosterone secretion. The clinical diagnosis of hypogonadism in CKD must rely mainly on measurements of testosterone, given that typical symptoms and signs of hypogonadism (such as decreased bone mineral density and muscle mass/strength, anemia, frailty, depression, apathy, or decreased libido) clearly overlap with those of CKD. This overlap may justify why only 11.8% of the patients in the study by Khurana et al2Khurana K.K. Navaneethan S.D. Arrigain S. Schold J.D. Nally Jr., J.V. Shoskes D.A. Serum testosterone levels and mortality in men with CKD stages 3-4.Am J Kidney Dis. 2014; 64: 367-374Google Scholar were tested for clinical indications, but 54% of those tested were found to have low testosterone levels (6.4% of the entire cohort). It is notable that of hypogonadal men in the study, only 31.6% were ever on testosterone replacement therapy. Whether this is a consequence of unawareness of the problem or disbelief regarding the need to correct this endocrine deficiency cannot be assessed. However, uremic hypogonadism likely is underappreciated by nephrologists, and the low proportion of treated hypogonadal men is very much in line with previous reports from dialysis populations.7Yilmaz M.I. Sonmez A. Qureshi A.R. et al.Endogenous testosterone, endothelial dysfunction, and cardiovascular events in men with nondialysis chronic kidney disease.Clin J Am Soc Nephrol. 2011; 6: 1617-1625Crossref PubMed Scopus (83) Google Scholar, 8Bello A.K. Stenvinkel P. Lin M. et al.Serum testosterone levels and clinical outcomes in male hemodialysis patients.Am J Kidney Dis. 2014; 63: 268-275Abstract Full Text Full Text PDF PubMed Scopus (38) Google Scholar, 9Carrero J.J. Qureshi A.R. Nakashima A. et al.Prevalence and clinical implications of testosterone deficiency in men with end-stage renal disease.Nephrol Dial Transplant. 2011; 26: 184-190Crossref PubMed Scopus (108) Google Scholar, 10Cigarran S. Pousa M. Castro M.J. et al.Endogenous testosterone, muscle strength, and fat-free mass in men with chronic kidney disease.J Ren Nutr. 2013; 23: e89-e95Abstract Full Text Full Text PDF PubMed Scopus (45) Google Scholar, 11Gungor O. Kircelli F. Carrero J.J. et al.Endogenous testosterone and mortality in male hemodialysis patients: is it the result of aging?.Clin J Am Soc Nephrol. 2010; 5: 2018-2023Crossref PubMed Scopus (58) Google Scholar Hypogonadism may not be just an innocent consequence of decreased kidney function or a simple matter of libido. Testosterone is a potent anabolic hormone with implications for various and important cardiometabolic pathways. Observational studies from around the world consistently link testosterone deficiency in male patients with CKD with adverse outcomes (Fig 1). In dialysis populations, low testosterone level has been linked to anemia and erythropoiesis-stimulating agent hyporesponsiveness,12Carrero J.J. Barany P. Yilmaz M.I. 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: 709-715Crossref PubMed Scopus (60) Google Scholar, 13Ekart R, Taskovska M, Hojs N, Bevc S, Hojs R. Testosterone and hemoglobin in hemodialysis male and female patients [published online ahead of print November 21, 2013]. Artif Organs. http://dx.doi.org/10.1111/aor.12218.Google Scholar arterial stiffness,14Kyriazis J. Tzanakis I. Stylianou K. et al.Low serum testosterone, arterial stiffness and mortality in male haemodialysis patients.Nephrol Dial Transplant. 2011; 26: 2971-2977Crossref PubMed Scopus (63) Google Scholar low muscle mass,15Kojo G. Yoshida T. Ohkawa S. et al.Association of serum total testosterone concentration with skeletal muscle mass in men under hemodialysis.Int Urol Nephrol. 2014; 46: 985-991Crossref PubMed Scopus (9) Google Scholar poor quality of life,8Bello A.K. Stenvinkel P. Lin M. et al.Serum testosterone levels and clinical outcomes in male hemodialysis patients.Am J Kidney Dis. 2014; 63: 268-275Abstract Full Text Full Text PDF PubMed Scopus (38) Google Scholar and (cardiovascular) death.8Bello A.K. Stenvinkel P. Lin M. et al.Serum testosterone levels and clinical outcomes in male hemodialysis patients.Am J Kidney Dis. 2014; 63: 268-275Abstract Full Text Full Text PDF PubMed Scopus (38) Google Scholar, 9Carrero J.J. Qureshi A.R. Nakashima A. et al.Prevalence and clinical implications of testosterone deficiency in men with end-stage renal disease.Nephrol Dial Transplant. 2011; 26: 184-190Crossref PubMed Scopus (108) Google Scholar, 14Kyriazis J. Tzanakis I. Stylianou K. et al.Low serum testosterone, arterial stiffness and mortality in male haemodialysis patients.Nephrol Dial Transplant. 2011; 26: 2971-2977Crossref PubMed Scopus (63) Google Scholar, 16Carrero J.J. Qureshi A.R. Parini P. et al.Low serum testosterone increases mortality risk among male dialysis patients.J Am Soc Nephrol. 2009; 20: 613-620Crossref PubMed Scopus (138) Google Scholar In kidney transplant recipients, low testosterone level is reported to predict both increased death risk and decreased transplant survival.17Shoskes DA, Kerr H, Askar M, Goldfarb DA, Schold J. Low testosterone at time of transplant is independently associated with poor patient and graft survival in male renal transplant recipients [published online ahead of print April 1, 2014]. J Urol. http://dx.doi.org/10.1016/j.juro.2014.03.102.Google Scholar In patients with non–dialysis-dependent CKD, hypogonadism has been linked to impaired cognitive function and depression,18Afsar B. Relationship between total testosterone, cognitive function, depressive behavior, and sleep quality in chronic kidney disease patients not on dialysis.Clin Exp Nephrol. 2013; 17: 59-65Crossref PubMed Scopus (11) Google Scholar low muscle mass and strength,10Cigarran S. Pousa M. Castro M.J. et al.Endogenous testosterone, muscle strength, and fat-free mass in men with chronic kidney disease.J Ren Nutr. 2013; 23: e89-e95Abstract Full Text Full Text PDF PubMed Scopus (45) Google Scholar endothelial dysfunction,7Yilmaz M.I. Sonmez A. Qureshi A.R. et al.Endogenous testosterone, endothelial dysfunction, and cardiovascular events in men with nondialysis chronic kidney disease.Clin J Am Soc Nephrol. 2011; 6: 1617-1625Crossref PubMed Scopus (83) Google Scholar increased risk of cardiovascular events,7Yilmaz M.I. Sonmez A. Qureshi A.R. et al.Endogenous testosterone, endothelial dysfunction, and cardiovascular events in men with nondialysis chronic kidney disease.Clin J Am Soc Nephrol. 2011; 6: 1617-1625Crossref PubMed Scopus (83) Google Scholar and death.19Haring R. Nauck M. Volzke H. et al.Low serum testosterone is associated with increased mortality in men with stage 3 or greater nephropathy.Am J Nephrol. 2011; 33: 209-217Crossref PubMed Scopus (41) Google Scholar The report of Khurana et al2Khurana K.K. Navaneethan S.D. Arrigain S. Schold J.D. Nally Jr., J.V. Shoskes D.A. Serum testosterone levels and mortality in men with CKD stages 3-4.Am J Kidney Dis. 2014; 64: 367-374Google Scholar further expands on the association between testosterone and mortality in a large population of individuals with non–dialysis-dependent CKD. Their results first show that the clinical guideline–based cutoff for testosterone deficiency (<350 ng/dL) does not discriminate individuals at increased risk of death; this may not be surprising if CKD per se renders low testosterone values.3Carrero J.J. Stenvinkel P. The vulnerable man: impact of testosterone deficiency on the uraemic phenotype.Nephrol Dial Transplant. 2012; 27: 4030-4041Crossref PubMed Scopus (60) Google Scholar, 4Dousdampanis P, Trigka K, Fourtounas C, Bargman JM. Role of testosterone in the pathogenesis, progression, prognosis and comorbidity of men with chronic kidney disease [published online ahead of print September 30, 2013]. Ther Apher Dial. http://dx.doi.org/10.1111/1744-9987.12101.Google Scholar, 5Iglesias P. Carrero J.J. Diez J.J. Gonadal dysfunction in men with chronic kidney disease: clinical features, prognostic implications and therapeutic options.J Nephrol. 2012; 25: 31-42Crossref PubMed Scopus (77) Google Scholar It is possible that lower clinical cutoffs must be applied in testosterone-suppressing diseases such as CKD, an issue that has not been considered sufficiently to date in endocrinology guidelines.20Bhasin S. Cunningham G.R. Hayes F.J. et al.Testosterone therapy in adult men with androgen deficiency syndromes: an Endocrine Society clinical practice guideline.J Clin Endocrinol Metab. 2006; 91: 1995-2010Crossref PubMed Scopus (765) Google Scholar However, in the work by Khurana et al,2Khurana K.K. Navaneethan S.D. Arrigain S. Schold J.D. Nally Jr., J.V. Shoskes D.A. Serum testosterone levels and mortality in men with CKD stages 3-4.Am J Kidney Dis. 2014; 64: 367-374Google Scholar when testosterone levels were studied as continuous variables or per quintiles of distribution, increased hazards of death were observed in patients with lower testosterone levels irrespective of confounders and comorbid conditions. This finding expands and agrees with all previous studies7Yilmaz M.I. Sonmez A. Qureshi A.R. et al.Endogenous testosterone, endothelial dysfunction, and cardiovascular events in men with nondialysis chronic kidney disease.Clin J Am Soc Nephrol. 2011; 6: 1617-1625Crossref PubMed Scopus (83) Google Scholar, 8Bello A.K. Stenvinkel P. Lin M. et al.Serum testosterone levels and clinical outcomes in male hemodialysis patients.Am J Kidney Dis. 2014; 63: 268-275Abstract Full Text Full Text PDF PubMed Scopus (38) Google Scholar, 9Carrero J.J. Qureshi A.R. Nakashima A. et al.Prevalence and clinical implications of testosterone deficiency in men with end-stage renal disease.Nephrol Dial Transplant. 2011; 26: 184-190Crossref PubMed Scopus (108) Google Scholar, 14Kyriazis J. Tzanakis I. Stylianou K. et al.Low serum testosterone, arterial stiffness and mortality in male haemodialysis patients.Nephrol Dial Transplant. 2011; 26: 2971-2977Crossref PubMed Scopus (63) Google Scholar, 16Carrero J.J. Qureshi A.R. Parini P. et al.Low serum testosterone increases mortality risk among male dialysis patients.J Am Soc Nephrol. 2009; 20: 613-620Crossref PubMed Scopus (138) Google Scholar except one,11Gungor O. Kircelli F. Carrero J.J. et al.Endogenous testosterone and mortality in male hemodialysis patients: is it the result of aging?.Clin J Am Soc Nephrol. 2010; 5: 2018-2023Crossref PubMed Scopus (58) Google Scholar in which age adjustment abrogated the association between testosterone level and mortality in young Turkish hemodialysis patients. Interestingly, testosterone levels in Japanese postmenopausal women undergoing hemodialysis also were reported to be abnormally low and associated with features of atherosclerosis.21Shiraki N. Nakashima A. Doi S. et al.Low serum testosterone is associated with atherosclerosis in postmenopausal women undergoing hemodialysis.Clin Exp Nephrol. 2014; 18: 499-506Crossref PubMed Scopus (9) Google Scholar The strengths of this study include a large sample size, the use of time-dependent analysis, and consideration of both testosterone levels and medication. However, the study is not exempt from limitations, the main ones being patient selection by indication, the inability to account for over-the-counter testosterone supplements (a practice that is becoming increasingly common), and the lack of information on circadian variation. The latter may have introduced important bias because testosterone values vary 20%-30% during the course of the day, and a random inspection of 40 cases in this study revealed that about half the patients had their blood samples obtained in the afternoon. In addition, because a large case-control study including more than 10,000 men with newly diagnosed nonmetastatic prostate cancer demonstrated that androgen deprivation therapy increases the risk of acute kidney injury,22Lapi F. Azoulay L. Niazi M.T. Yin H. Benayoun S. Suissa S. Androgen deprivation therapy and risk of acute kidney injury in patients with prostate cancer.JAMA. 2013; 310: 289-296Crossref PubMed Scopus (79) Google Scholar it could be speculated that hypogonadism may represent a risk factor for kidney failure. While this hypothesis is worth testing, because kidney failure and death are mutually exclusive events, a competing-risk Cox analysis may be a more appropriate statistical analysis. This study nevertheless is the largest to date documenting adverse outcomes in hypogonadal patients with CKD. Whether these associations are causal cannot be inferred from observational designs. Although this and past cohort studies have attempted to adjust for comorbid conditions, there may be residual confounding by unmeasured factors that account for this excess mortality risk. For this particular study, reliance on International Classification of Diseases, Ninth Revision codes, missing information on sex hormone binding globulin and inflammatory biomarkers, or the use of body mass index categories may have introduced error. It certainly is plausible that low testosterone levels are just a marker of poor health, reflecting both CKD severity and pre-existing diseases. However, it also is plausible that low testosterone levels resulting from pre-existing diseases and/or uremia may themselves contribute to other complications leading to adverse outcomes. Such hypothesis is not jejune because experimental evidence and well-designed randomized controlled trials clearly indicate a benefit for testosterone replacement therapy in atherosclerosis regression, prevention of cardiac failure, anemia, and muscle synthesis, to mention a few (reviewed in3Carrero J.J. Stenvinkel P. The vulnerable man: impact of testosterone deficiency on the uraemic phenotype.Nephrol Dial Transplant. 2012; 27: 4030-4041Crossref PubMed Scopus (60) Google Scholar). With regard to clinical practice, this and previous observational studies cannot provide any guidelines but have 2 important findings: uremic hypogonadism is highly prevalent in male patients with CKD and it possibly may be implicated in uremia-associated cardiometabolic complications. The first underlines the need for increased awareness of the problem among nephrologists and renewed efforts toward adequate screening of hypogonadism in men with CKD. The second requires better understanding of the possible risks and benefits of testosterone replacement therapy. Regretfully, very few interventional studies have addressed correction of testosterone deficiency in individuals with manifest CKD. One from 1998 reported that testosterone replacement improved libido and sexual function.23Lawrence I.G. Price D.E. Howlett T.A. Harris K.P. Feehally J. Walls J. Correcting impotence in the male dialysis patient: experience with testosterone replacement and vacuum tumescence therapy.Am J Kidney Dis. 1998; 31: 313-319Abstract Full Text Full Text PDF PubMed Scopus (60) Google Scholar Although most studies show that supraphysiologic testosterone supplementation improves anemia and reduces erythropoiesis-stimulating agent needs,24Gaughan W.J. Liss K.A. Dunn S.R. et al.A 6-month study of low-dose recombinant human erythropoietin alone and in combination with androgens for the treatment of anemia in chronic hemodialysis patients.Am J Kidney Dis. 1997; 30: 495-500Abstract Full Text PDF PubMed Scopus (75) Google Scholar, 25Ballal S.H. Domoto D.T. Polack D.C. Marciulonis P. Martin K.J. Androgens potentiate the effects of erythropoietin in the treatment of anemia of end-stage renal disease.Am J Kidney Dis. 1991; 17: 29-33Abstract Full Text PDF PubMed Scopus (100) Google Scholar the only trial addressing this issue in frankly hypogonadal men failed to show an effect, attributed by the authors to the low bioavailability of transdermal patches.26Brockenbrough A.T. Dittrich M.O. Page S.T. Smith T. Stivelman J.C. Bremner W.J. Transdermal androgen therapy to augment EPO in the treatment of anemia of chronic renal disease.Am J Kidney Dis. 2006; 47: 251-262Abstract Full Text Full Text PDF PubMed Scopus (63) Google Scholar Hypogonadal men are more likely to show signs of wasting and muscle catabolism.10Cigarran S. Pousa M. Castro M.J. et al.Endogenous testosterone, muscle strength, and fat-free mass in men with chronic kidney disease.J Ren Nutr. 2013; 23: e89-e95Abstract Full Text Full Text PDF PubMed Scopus (45) Google Scholar, 15Kojo G. Yoshida T. Ohkawa S. et al.Association of serum total testosterone concentration with skeletal muscle mass in men under hemodialysis.Int Urol Nephrol. 2014; 46: 985-991Crossref PubMed Scopus (9) Google Scholar, 27Carrero J.J. 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: 77-90Abstract Full Text Full Text PDF PubMed Scopus (459) Google Scholar Although no studies have addressed the impact of testosterone replacement on muscle wasting in hypogonadal patients, supraphysiologic administration of androgenic steroids in nonhypogonadal men and women undergoing dialysis consistently have been shown to result in improvements in muscle anabolism and insulin sensitivity.28Aramwit P. Kobpipat N. Satirapoj B. Kopple J.D. Supasyndh O. Oxymetholone ameliorates insulin sensitivity in maintenance hemodialysis patients: a randomized controlled trial.Clin Nephrol. 2009; 71: 413-422Crossref PubMed Scopus (4) Google Scholar, 29Supasyndh O. Satirapoj B. Aramwit P. et al.Effect of oral anabolic steroid on muscle strength and muscle growth in hemodialysis patients.Clin J Am Soc Nephrol. 2013; 8: 271-279Crossref PubMed Scopus (31) Google Scholar, 30Johansen K.L. Painter P.L. Sakkas G.K. Gordon P. Doyle J. Shubert T. Effects of resistance exercise training and nandrolone decanoate on body composition and muscle function among patients who receive hemodialysis: a randomized, controlled trial.J Am Soc Nephrol. 2006; 17: 2307-2314Crossref PubMed Scopus (288) Google Scholar, 31Johansen K.L. Mulligan K. Schambelan M. Anabolic effects of nandrolone decanoate in patients receiving dialysis: a randomized controlled trial.JAMA. 1999; 281: 1275-1281Crossref PubMed Scopus (210) Google Scholar In my opinion, the issue at stake is the correction of endocrine deficiencies, and not supraphysiologic administration. The frequency of adverse events related to physiologic testosterone administration is low.32Fernandez-Balsells M.M. Murad M.H. Lane M. et al.Clinical review 1: adverse effects of testosterone therapy in adult men: a systematic review and meta-analysis.J Clin Endocrinol Metab. 2010; 95: 2560-2575Crossref PubMed Scopus (544) Google Scholar However, safety concerns have been raised following the publication of 2 retrospective observational studies suggesting that the use of testosterone increases the risk of cardiovascular events in men (without known CKD) older than 65 years or with pre-existing heart disease.33Vigen R. O'Donnell C.I. Baron A.E. et al.Association of testosterone therapy with mortality, myocardial infarction, and stroke in men with low testosterone levels.JAMA. 2013; 310: 1829-1836Crossref PubMed Scopus (704) Google Scholar, 34Finkle W.D. Greenland S. Ridgeway G.K. et al.Increased risk of non-fatal myocardial infarction following testosterone therapy prescription in men.PLoS One. 2014; 9: e85805Crossref PubMed Scopus (521) Google Scholar Although the interpretation of these observational studies currently is a matter of active debate in the scientific community, both the US Food and Drug Administration and the European Medicines Agency have launched separate reviews of safety concerns of testosterone-containing medicines.35European Medicines Agency. Testosterone-containing medicines. http://www.ema.europa.eu/ema/index.jsp?curl=pages/medicines/human/referrals/Testosterone-containing_medicines/human_referral_prac_000037.jsp&mid=WC0b01ac05805c516f. Accessed June 11, 2014.Google Scholar, 36US Food and Drug Administration. FDA Drug Safety Communication: FDA evaluating risk of stroke, heart attack and death with FDA-approved testosterone products. http://www.fda.gov/Drugs/DrugSafety/ucm383904.htm. Accessed June 11, 2014.Google Scholar All in all, although the study by Khurana et al2Khurana K.K. Navaneethan S.D. Arrigain S. Schold J.D. Nally Jr., J.V. Shoskes D.A. Serum testosterone levels and mortality in men with CKD stages 3-4.Am J Kidney Dis. 2014; 64: 367-374Google Scholar provides yet another convincing indication that hypogonadism in men with CKD may be linked to poor outcomes, whether testosterone replacement would yield benefits to this vulnerable group of patients warrants investigation. I thank my colleagues for never ending support and enthusiasm toward research curiosity. Support: This editorial was produced without direct funding. Dr Carrero acknowledges grant support from the Swedish Research Council. Financial Disclosure: Dr Carrero reports having received speaking fees from Bayer Pharmaceuticals (the manufacturer of Nebido) in 2013 and participates in an investigator-driven randomized controlled trial on testosterone replacement therapy in hypogonadal men undergoing dialysis at Karolinska Institutet (Principal Investigator, P. Stenvinkel). This trial is partly supported by Bayer Pharmaceuticals . Serum Testosterone Levels and Mortality in Men With CKD Stages 3-4American Journal of Kidney DiseasesVol. 64Issue 3PreviewHypogonadism in men (total testosterone < 350 ng/dL) is associated with higher risk of cardiovascular disease and mortality in men on dialysis therapy. We evaluated the association of hypogonadism with all-cause mortality in men with non–dialysis-dependent chronic kidney disease (CKD). Full-Text PDF" @default.
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• W2094418908 title "Testosterone Deficiency at the Crossroads of Cardiometabolic Complications in CKD" @default.
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