Table of Contents Author Guidelines Submit a Manuscript
International Journal of Endocrinology
Volume 2014, Article ID 496948, 9 pages
http://dx.doi.org/10.1155/2014/496948
Research Article

Progressive Improvement of T-Scores in Men with Osteoporosis and Subnormal Serum Testosterone Levels upon Treatment with Testosterone over Six Years

1Private Urology Practice, 27570 Bremerhaven, Germany
2Department of Orthopedics, Wesermuende Hospital, 27607 Langen, Germany
3Departments of Biochemistry and of Urology, Boston University School of Medicine, Boston, MA 02118, USA
4Bayer Pharma, Global Medical Affairs Andrology, 13353 Berlin, Germany
5Gulf Medical University School of Medicine, Ajman, UAE
6Department of Biostatistics, Boston University School of Public Health, Boston, MA 02118, USA
7Endocrine Section, Department of Internal Medicine, VU University Medical Center, 1081 HV Amsterdam, The Netherlands
8Chiang Mai 50220, Thailand

Received 27 November 2013; Accepted 31 December 2013; Published 13 February 2014

Academic Editor: Antonio Aversa

Copyright © 2014 Ahmad Haider et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. Laurent, E. Gielen, F. Claessens, S. Boonen, and D. Vanderschueren, “Osteoporosis in older men: recent advances in pathophysiology and treatment,” Best Practice & Research Clinical Endocrinology & Metabolism, vol. 27, no. 4, pp. 527–539, 2013. View at Publisher · View at Google Scholar
  2. P. N. Kannegaard, S. van der Mark, P. Eiken, and B. Abrahamsen, “Excess mortality in men compared with women following a hip fracture. National analysis of comedications, comorbidity and survival,” Age and Ageing, vol. 39, no. 2, pp. 203–209, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. T. G. Travison, A.-H. Nguyen, V. Naganathan et al., “Changes in reproductive hormone concentrations predict the prevalence and progression of the frailty syndrome in older men: the concord health and ageing in men project,” The Journal of Clinical Endocrinology & Metabolism, vol. 96, no. 8, pp. 2464–2474, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. F. Callewaert, M. Sinnesael, E. Gielen, S. Boonen, and D. Vanderschueren, “Skeletal sexual dimorphism: relative contribution of sex steroids, GH-IGF1, and mechanical loading,” Journal of Endocrinology, vol. 207, no. 2, pp. 127–134, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. H. A. Fink, S. K. Ewing, K. E. Ensrud et al., “Association of testosterone and estradiol deficiency with osteoporosis and rapid bone loss in older men,” The Journal of Clinical Endocrinology & Metabolism, vol. 91, no. 10, pp. 3908–3915, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. S. P. Tuck and R. M. Francis, “Testosterone, bone and osteoporosis,” Frontiers of Hormone Research, vol. 37, pp. 123–132, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. S. Bhasin, M. Pencina, G. K. Jasuja et al., “Reference ranges for testosterone in men generated using liquid chromatography tandem mass spectrometry in a community-based sample of healthy nonobese young men in the framingham heart study and applied to three geographically distinct cohorts,” The Journal of Clinical Endocrinology & Metabolism, vol. 96, no. 8, pp. 2430–2439, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. E. Nieschlag, “Klinefelter syndrome: the commonest form of hypogonadism, but often overlooked or untreated,” Deutsches Ärzteblatt International, vol. 110, no. 20, pp. 347–353, 2013. View at Publisher · View at Google Scholar
  9. D. G. Jo, H. S. Lee, Y. M. Joo, and J. T. Seo, “Effect of testosterone replacement therapy on bone mineral density in patients with Klinefelter syndrome,” Yonsei Medical Journal, vol. 54, no. 6, pp. 1331–1335, 2013. View at Publisher · View at Google Scholar
  10. A. Ferlin, M. Schipilliti, C. Vinanzi et al., “Bone mass in subjects with Klinefelter syndrome: role of testosterone levels and androgen receptor gene CAG polymorphism,” The Journal of Clinical Endocrinology & Metabolism, vol. 96, no. 4, pp. E739–E745, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. A. Bojesen, N. Birkebæk, K. Kristensen et al., “Bone mineral density in Klinefelter syndrome is reduced and primarily determined by muscle strength and resorptive markers, but not directly by testosterone,” Osteoporosis International, vol. 22, no. 5, pp. 1441–1450, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. A. E. Oostlander, N. Bravenboer, E. Sohl et al., “Histomorphometric analysis reveals reduced bone mass and bone formation in patients with quiescent Crohn's disease,” Gastroenterology, vol. 140, no. 1, pp. 116–123, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. A. E. Oostlander, V. Everts, T. Schoenmaker et al., “T cell-mediated increased osteoclast formation from peripheral blood as a mechanism for Crohn's disease-associated bone loss,” Journal of Cellular Biochemistry, vol. 113, no. 1, pp. 260–268, 2012. View at Publisher · View at Google Scholar · View at Scopus
  14. A. E. Oostlander, N. Bravenboer, H. W. van Essen et al., “Bone cells from patients with quiescent Crohn's disease show a reduced growth potential and an impeded maturation,” Journal of Cellular Biochemistry, vol. 113, no. 7, pp. 2424–2431, 2012. View at Publisher · View at Google Scholar
  15. A. Haider, W. Kurtz, E. J. Giltay, L. J. Gooren, and F. Saad, “Administration of testosterone to elderly hypogonadal men with Crohn’s disease improves their Crohn’s disease activity index: a pilot study,” Hormone Molecular Biology and Clinical Investigation, vol. 2, no. 3, pp. 287–292, 2010. View at Publisher · View at Google Scholar
  16. D. B. Maurel, N. Boisseau, C. L. Benhamou, and C. Jaffre, “Alcohol and bone: review of dose effects and mechanisms,” Osteoporosis International, vol. 23, no. 1, pp. 1–16, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. C. E. Kiserud, A. Fosså, T. Bjøro, H. Holte, M. Cvancarova, and S. D. Fosså, “Gonadal function in male patients after treatment for malignant lymphomas, with emphasis on chemotherapy,” British Journal of Cancer, vol. 100, no. 3, pp. 455–463, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. J. J. Carrero and P. Stenvinkel, “The vulnerable man: impact of testosterone deficiency on the uraemic phenotype,” Nephrology Dialysis Transplantation, vol. 27, no. 11, pp. 4030–4041, 2012. View at Publisher · View at Google Scholar
  19. E. Martin Ritzén, A. Bergh, R. Bjerknes et al., “Nordic consensus on treatment of undescended testes,” Acta Paediatrica, vol. 96, no. 5, pp. 638–643, 2007. View at Publisher · View at Google Scholar · View at Scopus
  20. L. A. Heinemann, “Aging Males' Symptoms scale: a standardized instrument for the practice,” Journal of Endocrinological Investigation, vol. 28, no. 11, pp. 34–38, 2005. View at Google Scholar · View at Scopus
  21. R. C. Rosen, J. C. Cappelleri, and N. Gendrano III, “The International Index of Erectile Function (IIEF): a state-of-the-science review,” International Journal of Impotence Research, vol. 14, no. 4, pp. 226–244, 2002. View at Publisher · View at Google Scholar · View at Scopus
  22. P. J. Snyder, H. Peachey, P. Hannoush et al., “Effect of testosterone treatment on body composition and muscle strength in men over 65 years of age,” The Journal of Clinical Endocrinology & Metabolism, vol. 84, no. 8, pp. 2647–2653, 1999. View at Google Scholar · View at Scopus
  23. G. Caminiti, M. Volterrani, F. Iellamo et al., “Effect of long-acting testosterone treatment on functional exercise capacity, skeletal muscle performance, insulin resistance, and baroreflex sensitivity in elderly patients with chronic heart failure: a double-blind, placebo-controlled, randomized study,” Journal of the American College of Cardiology, vol. 54, no. 10, pp. 919–927, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. A. A. Ferrando, M. Sheffield-Moore, C. W. Yeckel et al., “Testosterone administration to older men improves muscle function: molecular and physiological mechanisms,” American Journal of Physiology, vol. 282, no. 3, pp. E601–E607, 2002. View at Publisher · View at Google Scholar · View at Scopus
  25. J. K. Amory, N. B. Watts, K. A. Easley et al., “Exogenous testosterone or testosterone with finasteride increases bone mineral density in older men with low serum testosterone,” The Journal of Clinical Endocrinology & Metabolism, vol. 89, no. 2, pp. 503–510, 2004. View at Publisher · View at Google Scholar · View at Scopus
  26. C. Wang, R. S. Swerdloff, A. Iranmanesh et al., “Effects of transdermal testosterone gel on bone turnover markers and bone mineral density in hypogonadal men,” Clinical Endocrinology, vol. 54, no. 6, pp. 739–750, 2001. View at Publisher · View at Google Scholar · View at Scopus
  27. L. Katznelson, J. S. Finkelstein, D. A. Schoenfeld, D. I. Rosenthal, E. J. Anderson, and A. Klibanski, “Increase in bone density and lean body mass during testosterone administration in men with acquired hypogonadism,” The Journal of Clinical Endocrinology & Metabolism, vol. 81, no. 12, pp. 4358–4365, 1996. View at Publisher · View at Google Scholar · View at Scopus
  28. H. M. Behre, S. Kliesch, E. Leifke, T. M. Link, and E. Nieschlag, “Long-term effect of testosterone therapy on bone mineral density in hypogonadal men,” The Journal of Clinical Endocrinology & Metabolism, vol. 82, no. 8, pp. 2386–2390, 1997. View at Publisher · View at Google Scholar · View at Scopus
  29. P. J. Snyder, H. Peachey, P. Hannoush et al., “Effect of testosterone treatment on bone mineral density in men over 65 years of age,” The Journal of Clinical Endocrinology & Metabolism, vol. 84, no. 6, pp. 1966–1972, 1999. View at Publisher · View at Google Scholar · View at Scopus
  30. A. Aversa, R. Bruzziches, D. Francomano et al., “Effects of long-acting testosterone undecanoate on bone mineral density in middle-aged men with late-onset hypogonadism and metabolic syndrome: results from a 36 months controlled study,” The Aging Male, vol. 15, no. 2, pp. 96–102, 2012. View at Publisher · View at Google Scholar
  31. J. Rodriguez-Tolra, J. Torremade, S. di Gregorio, L. del Rio, and E. Franco, “Effects of testosterone treatment on bone mineral density in men with testosterone deficiency syndrome,” Andrology, vol. 1, no. 4, pp. 570–575, 2013. View at Publisher · View at Google Scholar
  32. A. Aminorroaya, S. Kelleher, A. J. Conway, L. P. Ly, and D. J. Handelsman, “Adequacy of androgen replacement influences bone density response to testosterone in androgen-deficient men,” European Journal of Endocrinology, vol. 152, no. 6, pp. 881–886, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. G. Corona, L. Vignozzi, A. Sforza, and M. Maggi, “Risks and benefits of late onset hypogonadism treatment: an expert opinion,” The World Journal of Men's Health, vol. 31, no. 2, pp. 103–125, 2013. View at Publisher · View at Google Scholar
  34. G. Corona, G. Rastrelli, and M. Maggi, “Diagnosis and treatment of late-onset hypogonadism: systematic review and meta-analysis of TRT outcomes,” Best Practice & Research Clinical Endocrinology & Metabolism, vol. 27, no. 4, pp. 557–579, 2013. View at Publisher · View at Google Scholar
  35. R. Kacker, W. Conners, J. Zade, and A. Morgentaler, “Bone mineral density and response to treatment in men less than fifty years with testosterone deficiency and sexual dysfunction or infertility,” The Journal of Urology, 2013. View at Publisher · View at Google Scholar
  36. F. Saad, L. J. Gooren, A. Haider, and A. Yassin, “A dose-response study of testosterone on sexual dysfunction and features of the metabolic syndrome using testosterone gel and parenteral testosterone undecanoate,” Journal of Andrology, vol. 29, no. 1, pp. 102–105, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. E. J. Giltay, A. Haider, F. Saad, and L. J. Gooren, “C-reactive protein levels and ageing male symptoms in hypogonadal men treated with testosterone supplementation,” Andrologia, vol. 40, no. 6, pp. 398–400, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. F. Saad, A. Haider, G. Doros, and A. Traish, “Long-term treatment of hypogonadal men with testosterone produces substantial and sustained weight loss,” Obesity, vol. 21, no. 10, pp. 1975–1981, 2013. View at Publisher · View at Google Scholar
  39. A. Haider, L. J. G. Gooren, P. Padungtod, and F. Saad, “Improvement of the metabolic syndrome and of non-alcoholic liver steatosis upon treatment of hypogonadal elderly men with parenteral testosterone undecanoate,” Experimental and Clinical Endocrinology & Diabetes, vol. 118, no. 3, pp. 167–171, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. F. Saad, L. Gooren, A. Haider, and A. Yassin, “An exploratory study of the effects of 12 month administration of the novel long-acting testosterone undecanoate on measures of sexual function and the metabolic syndrome,” Archives of Andrology, vol. 53, no. 6, pp. 353–357, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. F. Saad, L. Gooren, A. Haider, and A. Yassin, “Effects of testosterone gel followed by parenteral testosterone undecanoate on sexual dysfunction and on features of the metabolic syndrome,” Andrologia, vol. 40, no. 1, pp. 44–48, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. S. J. Jacobsen, C. J. Girman, H. A. Guess, T. Rhodes, J. E. Oesterling, and M. M. Lieber, “Natural history of prostatism: longitudinal changes in voiding symptoms in community dwelling men,” The Journal of Urology, vol. 155, no. 2, pp. 595–600, 1996. View at Publisher · View at Google Scholar · View at Scopus
  43. J. B. Anderson, C. G. Roehrborn, J. A. Schalken, and M. Emberton, “The progression of benign prostatic hyperplasia: examining the evidence and determining the risk,” European Urology, vol. 39, no. 4, pp. 390–399, 2001. View at Publisher · View at Google Scholar · View at Scopus
  44. A. Haider, L. J. Gooren, P. Padungtod, and F. Saad, “Concurrent improvement of the metabolic syndrome and lower urinary tract symptoms upon normalisation of plasma testosterone levels in hypogonadal elderly men,” Andrologia, vol. 41, no. 1, pp. 7–13, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Haider, L. J. G. Gooren, P. Padungtod, and F. Saad, “A safety study of administration of parenteral testosterone undecanoate to elderly men over minimally 24 months,” Andrologia, vol. 42, no. 6, pp. 349–355, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. A. Morgentaler, “Testosterone and prostate cancer: what are the risks for middle-aged men?” Urologic Clinics of North America, vol. 38, no. 2, pp. 119–124, 2011. View at Publisher · View at Google Scholar · View at Scopus