World Journal of Urology

, Volume 31, Issue 2, pp 275–280 | Cite as

Preoperative sex steroids are significant predictors of early biochemical recurrence after radical prostatectomy

  • Andrea Salonia
  • Firas Abdollah
  • Umberto Capitanio
  • Andrea Gallina
  • Nazareno Suardi
  • Alberto Briganti
  • Giuseppe Zanni
  • Matteo Ferrari
  • Fabio Castiglione
  • Maria Chiara Clementi
  • Patrizio Rigatti
  • Francesco Montorsi
Original Article

Abstract

Purpose

We sought the association of preoperative serum total testosterone (tT), hypogonadism, 17β estradiol (E2), and sex hormone-binding globulin (SHBG) with early biochemical recurrence (BCR) after radical prostatectomy (RP).

Methods

Sex steroids were assessed the day before surgery (7–11 a.m.) in a cohort of 605 patients with a median follow-up of 24 months following RP. Cox regression models tested the association between predictors [including age, body mass index (BMI), prostate-specific antigen (PSA), clinical stage, biopsy Gleason scores, tT, hypogonadism, E2, and SHBG] and early BCR (defined as a PSA ≥ 0.1 ng/ml that occurred within 24 months after RP).

Results

Early BCR was found in 34 (5.6 %) patients. Patients with BCR did not differ in terms of age, BMI, serum PSA, tT, E2, and SHBG levels, rate of hypogonadism, and clinical stage as compared with those without BCR (all p ≥ 0.05). Conversely, patients with BCR showed a greater prevalence of biopsy Gleason scores ≥4 + 3 (all p ≤ 0.001). At multivariable Cox regression analysis, tT [hazard ratio (HR): 1.43; p = 0.03] E2 (HR: 1.05; p = 0.04), SHBG (HR: 1.29; p = 0.02), and biopsy Gleason scores equal to 4 + 3 (HR: 3.37; p = 0.04) and ≥8 (HR: 20.06; p < 0.001) achieved independent predictor status for early BCR. Conversely, no significant associations were found for all the other predictors.

Conclusions

Current findings show that preoperative serum sex steroids are independent predictors of early BCR in a homogeneous, large cohort of nonscreened patients treated with RP.

Keywords

Prostate cancer Radical prostatectomy Biochemical recurrence Testosterone 17β Estradiol Sex hormone-binding globulin 

Notes

Acknowledgments

The authors thank Dragonfly Editorial for reviewing the language in this manuscript.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Boorjian SA, Thompson RH, Tollefson MK, Rangel LJ, Bergstralh EJ, Blute ML, Karnes RJ (2011) Long-term risk of clinical progression after biochemical recurrence following radical prostatectomy: the impact of time from surgery to recurrence. Eur Urol 59:893–899. doi:10.1016/j.eururo.2011.02.026 PubMedCrossRefGoogle Scholar
  2. 2.
    Lughezzani G, Budäus L, Isbarn H, Sun M, Perrotte P, Haese A, Chun FK, Schlomm T, Steuber T, Heinzer H, Huland H, Montorsi F, Graefen M, Karakiewicz PI (2010) Head-to-head comparison of the three most commonly used preoperative models for prediction of biochemical recurrence after radical prostatectomy. Eur Urol 57:562–568. doi:10.1016/j.eururo.2009.12.003 PubMedCrossRefGoogle Scholar
  3. 3.
    D’Amico AV, Whittington R, Malkowicz SB, Schultz D, Blank K, Broderick GA, Tomaszewski JE, Renshaw AA, Kaplan I, Beard CJ, Wein A (1998) Biochemical outcome after radical prostatectomy, external beam radiation therapy, or interstitial radiation therapy for clinically localized prostate cancer. JAMA 280:969–974. doi:10.1001/jama.280.11.969 PubMedCrossRefGoogle Scholar
  4. 4.
    Stephenson AJ, Scardino PT, Eastham JA, Bianco FJ Jr, Dotan ZA, Fearn PA, Kattan MW (2006) Preoperative nomogram predicting the 10-year probability of prostate cancer recurrence after radical prostatectomy. J Natl Cancer Inst 98:715–717. doi:10.1093/jnci/djj190 PubMedCrossRefGoogle Scholar
  5. 5.
    Escaff S, Fernández JM, González LO, Suárez A, González-Reyes S, González JM, Vizoso FJ (2011) Collagenase-3 expression by tumor cells and gelatinase B expression by stromal fibroblast-like cells are associated with biochemical recurrence after radical prostatectomy in patients with prostate cancer. World J Urol 29:657–663. doi:10.1007/s00345-010-0595-6 PubMedCrossRefGoogle Scholar
  6. 6.
    Aufderklamm S, Hennenlotter J, Todenhoefer T, Gakis G, Schilling D, Vogel U, Kuehs U, Dlugosch J, Knapp J, Merseburger A, Gerber V, Ordelheide A, Hevler J, Stenzl A, Schwentner C (2011) XPA-210: a new proliferation marker determines locally advanced prostate cancer and is a predictor of biochemical recurrence. World J Urol [Epub ahead of print] doi:10.1007/s00345-011-0768-y
  7. 7.
    Isbarn H, Pinthus JH, Marks LS, Montorsi F, Morales A, Morgentaler A, Schulman C (2009) Testosterone and prostate cancer: revisiting old paradigms. Eur Urol 56:48–56. doi:10.1016/j.eururo.2009.03.088 PubMedCrossRefGoogle Scholar
  8. 8.
    Ellem SJ, Risbridger GP (2010) Aromatase and regulating the estrogen:androgen ratio in the prostate gland. J Steroid Biochem Mol Biol 118:246–251. doi:10.1016/j.jsbmb.2009.10.015 PubMedCrossRefGoogle Scholar
  9. 9.
    Røder MA, Christensen IJ, Berg KD, Gruschy L, Brasso K, Iversen P (2011) Serum testosterone level as a predictor of biochemical failure after radical prostatectomy for localized prostate cancer. BJU Int [Epub ahead of print] doi:10.1111/j.1464-410X.2011.10335.x
  10. 10.
    Li R, Wheeler T, Dai H, Frolov A, Thompson T, Ayala G (2004) High level of androgen receptor is associated with aggressive clinicopathologic features and decreased biochemical recurrence-free survival in prostate: cancer patients treated with radical prostatectomy. Am J Surg Pathol 28:928–934PubMedCrossRefGoogle Scholar
  11. 11.
    Yamamoto S, Yonese J, Kawakami S, Ohkubo Y, Tatokoro M, Komai Y, Takeshita H, Ishikawa Y, Fukui I (2007) Preoperative serum testosterone level as an independent predictor of treatment failure following radical prostatectomy. Eur Urol 52:696–701. doi:10.1016/j.eururo.2007.03.052 PubMedCrossRefGoogle Scholar
  12. 12.
    Bhasin S, Cunningham GR, Hayes FJ, Matsumoto AM, Snyder PJ, Swerdloff RS, Montori VM, Task Force Endocrine Society (2010) Testosterone therapy in men with androgen deficiency syndromes: an endocrine Society clinical practice guideline. J Clin Endocrinol Metab 95:2536–2559. doi:10.1210/jc.2009-2354 PubMedCrossRefGoogle Scholar
  13. 13.
    Isbarn H, Wanner M, Salomon G, Steuber T, Schlomm T, Köllermann J, Sauter G, Haese A, Heinzer H, Huland H, Graefen M (2010) Long-term data on the survival of patients with prostate cancer treated with radical prostatectomy in the prostate-specific antigen era. BJU Int 106:37–43. doi:10.1111/j.1464-410X.2009.09134.x PubMedCrossRefGoogle Scholar
  14. 14.
    Mottet N, Bellmunt J, Bolla M, Joniau S, Mason M, Matveev V, Schmid HP, Van der Kwast T, Wiegel T, Zattoni F, Heidenreich A (2011) EAU guidelines on prostate cancer. Part II: treatment of advanced, relapsing, and castration-resistant prostate cancer. Eur Urol 59:572–583. doi:10.1016/j.eururo.2011.01.025 PubMedCrossRefGoogle Scholar
  15. 15.
    Morgentaler A (2009) Testosterone therapy in men with prostate cancer: scientific and ethical considerations. J Urol 181:972–979. doi:10.1016/j.juro.2008.11.031 PubMedCrossRefGoogle Scholar
  16. 16.
    Massengill JC, Sun L, Moul JW, Wu H, McLeod DG, Amling C, Lance R, Foley J, Sexton W, Kusuda L, Chung A, Soderdahl D, Donahue T (2003) Pretreatment total testosterone level predicts pathological stage in patients with localized prostate cancer treated with radical prostatectomy. J Urol 169:1670–1675. doi:10.1097/01.ju.0000062674.43964.d0 PubMedCrossRefGoogle Scholar
  17. 17.
    Xylinas E, Ploussard G, Durand X, Fabre A, Salomon L, Allory Y, Vordos D, Hoznek A, Abbou CC, de la Taille A (2011) Low pretreatment total testosterone (<3 ng/mL) predicts extraprostatic disease in prostatectomy specimens from patients with preoperative localized prostate cancer. BJU Int 107:1400–1403. doi:10.1111/j.1464-410X.2010.09816.x PubMedCrossRefGoogle Scholar
  18. 18.
    Salonia A, Gallina A, Briganti A, Abdollah F, Suardi N, Capitanio U, Colombo R, Freschi M, Rigatti P, Montorsi F (2011) Preoperative hypogonadism is not an independent predictor of high-risk disease in patients undergoing radical prostatectomy. Cancer 117:3953–3962. doi:10.1002/cncr.25985 PubMedCrossRefGoogle Scholar
  19. 19.
    Tajar A, Forti G, O’Neill TW, Lee DM, Silman AJ, Finn JD, Bartfai G, Boonen S, Casanueva FF, Giwercman A, Han TS, Kula K, Labrie F, Lean ME, Pendleton N, Punab M, Vanderschueren D, Huhtaniemi IT, Wu FC, EMAS Group (2010) Characteristics of secondary, primary, and compensated hypogonadism in aging men: evidence from the European Male Ageing Study. J Clin Endocrinol Metab 95:1810–1818 doi:10.1210/jc.2009-1796 Google Scholar
  20. 20.
    Bonkhoff H, Berges R (2009) The evolving role of oestrogens and their receptors in the development and progression of prostate cancer. Eur Urol 55:533–542. doi:10.1016/j.eururo.2008.10.035 PubMedCrossRefGoogle Scholar
  21. 21.
    Salonia A, Gallina A, Briganti A, Suardi N, Capitanio U, Abdollah F, Bertini R, Freschi M, Rigatti P, Montorsi F (2011) Circulating estradiol, but not testosterone, is a significant predictor of high-grade prostate cancer in patients undergoing radical prostatectomy. Cancer 117:5029–5038. doi:10.1002/cncr.26136 PubMedCrossRefGoogle Scholar
  22. 22.
    Lee SE, Chung JS, Han BK, Park CS, Moon KH, Byun SS, Choe G, Hong SK (2008) Preoperative serum sex hormone-binding globulin as a predictive marker for extraprostatic extension of tumor in patients with clinically localized prostate cancer. Eur Urol 54:1324–1332. doi:10.1016/j.eururo.2008.02.032 PubMedCrossRefGoogle Scholar
  23. 23.
    Alenda O, Ploussard G, Mouracade P, Xylinas E, de la Taille A, Allory Y, Vordos D, Hoznek A, Abbou CC, Salomon L (2011) Impact of the primary Gleason pattern on biochemical recurrence-free survival after radical prostatectomy: a single-center cohort of 1,248 patients with Gleason 7 tumors. World J Urol 29:671–676. doi:10.1007/s00345-010-0620-9 PubMedCrossRefGoogle Scholar
  24. 24.
    Bechis SK, Carroll PR, Cooperberg MR (2011) Impact of age at diagnosis on prostate cancer treatment and survival. J Clin Oncol 29:235–241. doi:10.1200/JCO.2010.30.2075 PubMedCrossRefGoogle Scholar
  25. 25.
    Barlow LJ, Badalato GM, Bashir T, Benson MC, McKiernan JM (2010) The relationship between age at time of surgery and risk of biochemical failure after radical prostatectomy. BJU Int 105:1646–1649. doi:10.1111/j.1464-410X.2009.08977.x PubMedCrossRefGoogle Scholar
  26. 26.
    Freedland SJ, Aronson WJ, Kane CJ, Presti JC Jr, Amling CL, Elashoff D, Terris MK (2004) Impact of obesity on biochemical control after radical prostatectomy for clinically localized prostate cancer: a report by the Shared Equal Access Regional Cancer Hospital database study group. J Clin Oncol 22:446–453. doi:10.1200/JCO.2004.04.181 PubMedCrossRefGoogle Scholar
  27. 27.
    Kok DE, van Roermund JG, Aben KK, van de Luijtgaarden MW, Karthaus HF, van Vierssen Trip OB, Kampman E, Alfred Witjes J, Kiemeney LA (2011) Body mass index is not a predictor of biochemical recurrence after radical prostatectomy in Dutch men diagnosed with prostate cancer. World J Urol 29:695–701. doi:10.1007/s00345-010-0629-0 PubMedCrossRefGoogle Scholar
  28. 28.
    Magheli A, Gonzalgo ML, Su LM, Guzzo TJ, Netto G, Humphreys EB, Han M, Partin AW, Pavlovich CP (2011) Impact of surgical technique (open vs laparoscopic vs robotic-assisted) on pathological and biochemical outcomes following radical prostatectomy: an analysis using propensity score matching. BJU Int 107:1956–1962. doi:10.1111/j.1464-410X.2010.09795.x PubMedCrossRefGoogle Scholar
  29. 29.
    Walz J, Chun FK, Klein EA, Reuther A, Saad F, Graefen M, Huland H, Karakiewicz PI (2009) Nomogram predicting the probability of early recurrence after radical prostatectomy for prostate cancer. J Urol 181:601–607. doi:10.1016/j.juro.2008.10.033 PubMedCrossRefGoogle Scholar
  30. 30.
    Kwon T, Jeong IG, You D, Park MC, Hong JH, Ahn H, Kim CS (2010) Effect of prostate size on pathological outcome and biochemical recurrence after radical prostatectomy for prostate cancer: is it correlated with serum testosterone level? BJU Int 106:633–638. doi:10.1111/j.1464-410X.2009.09182.x PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Andrea Salonia
    • 1
  • Firas Abdollah
    • 1
  • Umberto Capitanio
    • 1
  • Andrea Gallina
    • 1
  • Nazareno Suardi
    • 1
  • Alberto Briganti
    • 1
  • Giuseppe Zanni
    • 1
  • Matteo Ferrari
    • 1
  • Fabio Castiglione
    • 1
  • Maria Chiara Clementi
    • 1
  • Patrizio Rigatti
    • 1
  • Francesco Montorsi
    • 1
  1. 1.Department of UrologyUniversity Vita-Salute San RaffaeleMilanItaly

Personalised recommendations