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Rapid recovery of hypogonadism in male patients with end stage renal disease after renal transplantation

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Abstract

Purpose

End stage renal disease (ESRD) in male patients is associated with a high prevalence of hypogonadism. After renal transplantation (RTx) an improvement in gonadal function is often observed. However, the time course of changes in pituitary-gonadal axis after RTx and the influence of renal function, age and anthropometric parameters are not well characterized. We prospectively evaluated pituitary-gonadal axis in male patients with ESRD before and after RTx for up to 1 year.

Methods

Ninety-seven male patients with ESRD were consecutively investigated on day of surgery and 1, 3, 6, and 12 months after RTx. Time course of changes in sex hormones (total testosterone ((TT)), calculated free testosterone ((cfT)), estradiol (E2), LH, FSH and prolactin), and interdependence with renal function, age, anthropometric factors, cause of ERDS, time on dialysis, and transplant associated factors were analyzed.

Results

Hypogonadism (TT < 8 nmol/l) was present in 40% of pts prior to RTX and in only 18% at 1 year after RTX. Recovery from hypogonadism was significantly higher in pts < 50 years and occurred within 3 months. RTx resulted in a decrease in E2/T ratio starting at 1 month and suggesting a shift from estrogen to testosterone production. BMI and waist circumference had the similar impact on T levels after successful RTx compared to patients without renal disease. No specific impact on recovery of hypogonadism was found for time on dialysis prior to RTx and living or cadaver transplantation.

Conclusions

Successful RTx is associated with a rapid recovery from hypogonadism within 3 months preceeded by improvement in renal function particularly in patients younger than 50 years.

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References

  1. J.J. Carrero, P. Stenvinkel, The vulnerable man: impact of testosterone deficiency on the uraemic phenotype. Nephrol. Dial. Transplant. 27, 4030–4041 (2012). https://doi.org/10.1093/ndt/gfs383

    Article  CAS  PubMed  Google Scholar 

  2. D.J. Handelsman, Hypothalamic–pituitary gonadal dysfunction in renal failure, dialysis and renal transplantation. Endocr. Rev. 6, 151–182 (1985)

    Article  CAS  PubMed  Google Scholar 

  3. A.K. Bello, P. Stenvinkel, M. Lin, B. Hemmelgarn, R. Thadhani, S. Klarenbach, C. Chan, D. Zimmerman, G. Cembrowski, G. Strippoli, J.J. Carrero, M. Tonelli, Serum testosterone levels and clinical outcomes in male hemodialysis patients. Am. J. Kidn Dis. 63, 268–275 (2014). https://doi.org/10.1053/j.ajkd.2013.06.010

    Article  CAS  Google Scholar 

  4. J.J. Carrero, A.R. Qureshi, P. Parini, S. Arver, B. Lindholm, P. Bárány, O. Heimbürger, P. Stenvinkel, Low serum testosterone increases mortality risk among male dialysis patients. J. Am. Soc. Nephrol. 20, 613–620 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. J. Kyriazis, I. Tzanakis, K. Stylianou, I. Katsipi, D. Moisiadis, A. Papadaki, V. Mavroeidi, S. Kagia, N. Karkavitsas, E. Daphnis, Low serum testosterone, arterial stiffness and mortality in male haemodialysis patients. Nephrol. Dial. Transplant. 26, 2971–2977 (2011). https://doi.org/10.1093/ndt/gfq847

    Article  CAS  PubMed  Google Scholar 

  6. D.A. Shoskes, H. Kerr, M. Askar, D.A. Goldfarb, J. Schold, Low testosterone at time of transplantation is independently associated with poor patient and graft survival in male renal transplant recipients. J. Urol. 192, 1168–1171 (2014). https://doi.org/10.1016/j.juro.2014.03.102

  7. M. Grossmann, R. Hoermann, M. Ng Tang Fui, J.D. Zajac, F.L. Ierino, M.A. Roberts, Sex steroids levels in chronic kidney disease and kidney transplant recipients: associations with disease severity and prediction of mortality. Clin. Endocrinol. 82, 767–775 (2015). https://doi.org/10.1111/cen

  8. J. Bao, Q. Yu, H. Yu, J. Hao, J. Liu, J. Yao, W. Yuan, Erectile dysfunction in male hemodialysis patients in China--one center experience. Clin. Nephrol. 75, 135–140 (2011)

    Article  CAS  PubMed  Google Scholar 

  9. D. Eckersten, A. Giwercman, A. Christensson, Male patients with terminal renal failure exhibit low serum levels of antimullerian hormone. J. Androl. 17, 149–153 (2015). https://doi.org/10.4103/1008-682X.135124

    CAS  Google Scholar 

  10. M.T. Saha, H.H. Saha, L.K. Niskanen, K.T. Salmela, A.I. Pasternack, Time course of serum prolactin and sex hormones following successful renal transplantation. Nephron 92, 735–737 (2002)

    Article  CAS  PubMed  Google Scholar 

  11. E. Samojlik, M.A. Kirschner, S. Ribot, E. Szmal, Changes in the hypothalamic-pituitary-gonadal axis in men after cadaver kidney transplantation and cyclosporine therapy. J. Androl. 13, 332–336 (1992)

    CAS  PubMed  Google Scholar 

  12. J.D. Veldhuis, A. Iranmanesh, M.J. Wilkowski, E. Samojlik, Neuroendocrine alterations in the somatotropic and lactotropic axes in uremic men. Eur. J. Endocrinol. 131, 489–498 (1994)

    Article  CAS  PubMed  Google Scholar 

  13. S. Yi, E. Selvin, S. Rohrmann, S. Basaria, A. Menke, N. Rifai, E. Guallar, E.A. Platz, B. Astor, Endogenous sex steroid hormones and measures of chronic kidney disease (CKD) in a nationally representative sample of men. Clin. Endocrinol. 71, 246–252 (2009). https://doi.org/10.1111/j.1365-2265.2008.03455

    Article  CAS  Google Scholar 

  14. F. Albaaj, M. Sivalingham, P. Haynes, G. McKinnon, R.N. Foley, S. Waldek, D.J. O’Donoghue, P.A. Kalra, Prevalence of hypogonadism in male patients with renal failure. Postgrad. Med. J. 82, 693–696 (2006)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. M.G. Park, H.S. Koo, B. Lee, Characteristics of testosterone deficiency syndrome in men with chronic kidney disease and male renal transplant recipients: a cross-sectional study. Transplant. Proc. 45, 2970–2974 (2013). https://doi.org/10.1016/j.transproceeding

    Article  CAS  PubMed  Google Scholar 

  16. R. Peces, M. de la Torre, J.M. Urra, Pituitary-testicular function in cyclosporin-treated renal transplant patients. Nephrol. Dial. Transplant. 9, 1453–1455 (1994)

    CAS  PubMed  Google Scholar 

  17. A.R. Prem, S.V. Punekar, M. Kalpana, A.R. Kelkar, V.N. Acharya, Male reproductive function in uraemia: efficacy of haemodialysis and renal transplantation. Brit J. Urol. 78, 635–638 (1996)

    Article  CAS  PubMed  Google Scholar 

  18. V. Tondolo, F. Citterio, N. Panocchia, G. Nanni, E. Favi, A. Brescia, M. Castagneto, Gonadal function and immunosuppressive therapy after renal transplantation. Transpl. Proc. 37, 1915–1917 (2005). https://doi.org/10.1016/j.transproceed.2005.04.004

  19. R. Yadav, S.N. Mehta, A. Kumar, S. Guleria, V. Seenu, S.C. Tiwari, A prospective analysis of testicular androgenic function in recipients of a renal allograft. Int. J. Urolol. Nephrol. 40, 397–403 (2008). https://doi.org/10.1007/s11255-007-9277-8

    Article  CAS  Google Scholar 

  20. H. Colak, I. Sert, Y. Kurtulmus, C. Karaca, H. Toz, S. Kursat, The relation between serum testosterone levels and cardiovascular risk factors in patients with kidney transplantation and chronic kidney disease. Saudi J. Kid Dis. Transplant. 25, 951–959 (2014)

    Article  Google Scholar 

  21. L. Tauchmanovà, R. Carrano, M. Sabbatini, M. De Rosa, F. Orio, S. Palomba, T. Cascella, G. Lombardi, S. Federico, A. Colao, Hypothalamic-pituitary-gonadal axis function after successful kidney transplantation in men and women. Hum. Reprod. 19, 867–873 (2004). https://doi.org/10.1093/humrep/deh192

    Article  PubMed  Google Scholar 

  22. W. Reinhardt, D. Patschan, F. Pietruck, T. Philipp, O.E. Janssen, K.I. Mann, F. Jockenhoevel, O. Witzke, Free androgen index is superior to total testosterone for short-term assessment of the gonadal axis after renal transplantation. Horm. Res. 64, 248–252 (2005). https://doi.org/10.1159/000089292

    CAS  PubMed  Google Scholar 

  23. A. Vermeulen, L. Verdonck, J.M. Kaufman, A critical evaluation of simple methods for the estimation of free testosterone in serum. J. Clin. Endocrinol. Metab. 84, 3666–3672 (1999)

    Article  CAS  PubMed  Google Scholar 

  24. A.S. Levey, L. Inker, J. Coresh, GFR estimation from physiology to public health. Am. J. Kidn. Dis. 63, 820–834 (2014)

  25. C. Wang, E. Nieschlag, R. Swerdloff, H.M. Behre, W.J. Hellstrom, L.J. Gooren, J.M. Kaufman, J.J. Legros, B. Lunenfeld, A. Morales, J.E. Morley, C. Schulman, I.M. Thompson, W. Weidner, F.C. Wu, Investigation, treatment and monitoring of late-onset hypogonadism in males: ISA, ISSAM, EAU, EAA and ASA recommendations. Eur. J. Endocrinol. 159, 507–514 (2008). https://doi.org/10.1530/EJE-08-0601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. R. Blake, S. Rajguru, G. Nolan, B. Ahluwalia, Dexamethasone suppresses sex-hormone binding globulin. Fertil. Steril. 49, 66–70 (1988)

    Article  CAS  PubMed  Google Scholar 

  27. V.S. Lim, V.S. Fang, Gonadal dysfunction in uremic men. A study of the hypothalamo-pituitary-testicular axis before and after renal transplantation. Am. J. Med. 58, 655–662 (1975)

    Article  CAS  PubMed  Google Scholar 

  28. D.J. Handelsman, B. Yeap, L. Flicker, S. Martin, G.A. Wittert, L.P. Ly, Age-specific population centiles for androgen status in men. Eur. J. Endocrinol. 173, 809–817 (2015). https://doi.org/10.1530/EJE-15-0380

    Article  CAS  PubMed  Google Scholar 

  29. B. Lapauw, S. Goemaere, H. Zmierczak, I. Van Pottelbergh, A. Mahmoud, Y. Taes, D. De Bacquer, S. Vansteelandt, J.M. Kaufman, The decline of serum testosterone levels in community-dwelling men over 70 years of age: descriptive data and predictors of longitudinal changes. Eur. J. Endocrinol. 159, 459–468 (2008). https://doi.org/10.1530/EJE-07-0873

    Article  CAS  PubMed  Google Scholar 

  30. E. Orwoll, L.C. Lambert, L.M. Marshall, K. Phipps, J. Blank, E. Barrett-Connor, J. Cauley, K. Ensrud, S. Cummings, Testosterone and estradiol among older men. J. Clin. Endocrinol. Metab. 91, 1336–1344 (2006)

    Article  CAS  PubMed  Google Scholar 

  31. J.S. Brand, I. van der Tweel, D.E. Grobbee, M.H. Emmelot-Vonk, Y.T.Testosterone van der Schouw, Sex hormone-binding globulin and the metabolic syndrome: a systematic review and meta-analysis of observational studies. Int. J. Epidemiol. 40, 189–207 (2011). https://doi.org/10.1093

    Article  PubMed  Google Scholar 

  32. L. Vandenput, D. Mellström, M.K. Karlsson, E. Orwoll, F. Labrie, O. Ljunggren, C. Ohlsson, Serum estradiol is associated with lean mass in elderly Swedish men. Eur. J. Endocrino1 62, 737–745 (2010). https://doi.org/10.1530/EJE-09-0696

    Article  Google Scholar 

  33. G. Kantarci, S. Sahin, A.R. Uras, H. Ergin, Effects of different calcineurin inhibitors on sex hormone levels in transplanted male patients. No difference CyA vs Tacrolimus. Transpl. Proc. 361, 78–79 (2004)

    Google Scholar 

  34. J.A. Talbot, R.S. Rodger, W.R. Robertson, Pulsatile bioactive luteinizing hormone secretion in men with chronic renal failure and following renal transplantation. Nephron 56, 66–72 (1990)

    Article  CAS  PubMed  Google Scholar 

  35. A. Vermeulen, J.M. Kaufman, S. Goemaere, I. van Pottelberg, Estradiol in elderly men. Aging Male. 5, 98–102 (2002)

    Article  CAS  PubMed  Google Scholar 

  36. S.R. Holdsworth, D.M. de Kretser, R.C. Atkins, A comparison of hemodialysis and transplantation in reversing the uremic disturbance of male reproductive function. Clin. Nephrol. 10, 146–150 (1978)

    CAS  PubMed  Google Scholar 

  37. M.C. Fung, G.C. Wah, W.D. Odell, Effect of prolactin on luteinizing hormone–stimulated testosterone in isolated perfused rat testis. J. Androl. 10, 37–42 (1989)

    Article  CAS  PubMed  Google Scholar 

  38. G.D. Sievertsen, V.S. Lim, C. Nakawatase, L.A. Frohman, Metabolic clearance and secretion rates of human prolactin in normal subjects and in patients with chronic renal failure. J. Clin. Endocrinol. Metab. 50, 846–852 (1980)

    Article  CAS  PubMed  Google Scholar 

  39. R. Peces, C. Horcajada, J.M. López-Novoa, M.A. Frutos, S. Casado, L. Hernando, Hyperprolactinemia in chronic renal failure: impaired responsiveness to stimulation and suppression. Normalization after transplantation. Nephron 28, 11–16 (1981)

    Article  CAS  PubMed  Google Scholar 

  40. I.T. Huhtaniemi, A. Tajar, D.M. Lee, T.W. O’Neill, J.D. Finn, G. Bartfai, S. Boonen, F.F. Casanueva, A. Giwercman, T.S. Han, K. Kula, F. Labrie, M.E. Lean, N. Pendleton, M. Punab, A.J. Silman, D. Vanderschueren, G. Forti, F.C. Wu; 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. 166, 983–991 (2012)

    Article  CAS  PubMed  Google Scholar 

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Reinhardt, W., Kübber, H., Dolff, S. et al. Rapid recovery of hypogonadism in male patients with end stage renal disease after renal transplantation. Endocrine 60, 159–166 (2018). https://doi.org/10.1007/s12020-018-1543-2

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  • DOI: https://doi.org/10.1007/s12020-018-1543-2

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