Preoperative low serum testosterone levels are associated with tumor aggressiveness in radical prostatectomy treated cancer patients

Hormone Molecular Biology and Clinical Investigation

Volumn 2, Issue 1, 2010, Pages 191-201

  Botto, Henry ^a   Neuzillet, Yann ^a   Lebret, Thierry ^a   Camparo, Philippe ^a   Molinie, Vincent ^b   Raynaud, Jean Pierre ^c,d  

^a FOCH HOSPITAL   (France)

^b SAINT JOSEPH HOSPITAL   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d NONE   (France)

Author keywords

aggressiveness; Gleason pattern; prostate cancer; testosterone

Indexed keywords

PROSTATE SPECIFIC ANTIGEN; TESTOSTERONE;

ADULT; AGE; AGED; ANDROGEN DEFICIENCY; ARTICLE; BODY MASS; CANCER PATIENT; CANCER SURGERY; CONTROLLED STUDY; GLEASON SCORE; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; PRIORITY JOURNAL; PROSTATE BIOPSY; PROSTATE CANCER; PROSTATECTOMY; RADIOIMMUNOASSAY; SURGICAL MARGIN; TESTOSTERONE BLOOD LEVEL; TUMOR AGGRESSIVENESS; TUMOR BIOPSY;

EID: 80052265228     PISSN: 18681883     EISSN: 18681891     Source Type: Journal    
DOI: 10.1515/HMBCI.2010.023     Document Type: Article

References (69)

1. Liverman CT., Blazer DG., editors. Institute of Medicine report on testosterone and aging. Washington., DC: National Academies Press., 2004.
2. Rhoden EL., Morgentaler A. Risks of testosterone replacement therapy and recommendations for monitoring. N Engl J Med 2004;350:482-92.
3. Bhasin S., Cunningham GR., Hayes FJ., Matsumoto AM., Snyder PJ., Swerdloff RS., Montori VM. Testosterone therapy in adult men with androgen deficiency syndromes: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab 2006;91: 1995-2010.
4. Wang C., Nieschlag E., Swerdloff RS., Behre H., Hellstrom WJ., Gooren LJ., Kaufman JM., Legros JJ., Lunenfeld B., Morales A., Morley JE., Schulman C., Thompson IM., Weidner W., Wu F. ISA., ISSAM., EAU., EAA., and ASA recommendations: investigation., treatment and monitoring of late-onset hypogonadism in males. Eur J Endocrinol 2008;159:507-14.
5. Huggins C., Hodges CV. Studies on prostate cancer. I. The effect of castration., of estrogen and of androgen injection on serum phosphatases in metastatic carcinoma of the prostate. Cancer Res 1941;1:293-7.
6. Huggins C., Stevens RE Jr., Hodges CV. Studies on prostate cancer. II. The effects of castration on advanced carcinoma of the prostate gland. Arch Surg 1941;43:209-23.
7. Ferreira U., Leitao VA., Denardi F., Matheus WE., Stopiglia RM., Netto NR Jr. Intermittent androgen replacement for intense hypogonadism symptoms in castrated patients. Prostate Cancer Prostatic Dis 2006;9:39-41.
8. Imamoto T., Suzuki H., Yano M., Kawamura K., Kamiya N., Araki K., Komiya A., Nihei N., Naya Y., Ichikawa T. The role of testosterone in the pathogenesis of prostate cancer. Int J Urol 2008;15:472-80.
9. Isbarn H., Pinthus JH., Marks LS., Montorsi F., Morales A., Morgentaler A., Schulman C. Testosterone and prostate cancer: revisiting old paradigms. Eur Urol 2009;56:48-56.
10. Morgentaler A. Testosterone therapy in men with prostate cancer: scientific and ethical considerations. J Urol 2009;181: 972-9.
11. Raynaud JP. Testosterone deficiency syndrome: treatment and cancer risk. J Steroid Biochem Mol Biol 2008;109:168-76.
12. Morgentaler A. Testosterone therapy and prostate cancer. Urol Clin N Am 2007;34:555-63.
13. Basaria S., Muller DC., Carducci MA., Egan S., Dobs AS. Hyper-glycemia and insulin resistance in men with prostate carcinoma who receive androgen-deprivation therapy. Cancer 2006;106: 581-8.
14. Lage MJ., Barber BL., Markus RA. Association between andro-gen-deprivation therapy and incidence of diabetes among males with prostate cancer. Urology 2007;70:1104-8.
15. Laughlin GA., Barrett-Connor E., Bergstrom J. Low serum testosterone and mortality in older men. J Clin Endocrinol Metab 2008;93:78-85.
16. Khera M., Lipshultz LI. The role of testosterone replacement therapy following radical prostatectomy. Urol Clin N Am 2007; 34:549-53.
17. Khaw KT., Dowsett M., Folkerd V., Bingham S., Wareham N., Luben R., Welch A., Day N. Endogenous testosterone and mortality due to all causes., cardiovascular disease., and cancer in men. Circulation 2007;116:2694-701.
18. Caminiti G., Volterrani M., Marazzi G., Massaro R., Miceli M., Mammi C., Piepoli M., Fini M., Rosano GMC. 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. J Am Coll Cardiol 2009;54:919-27.
19. Rhoden EL., Morgentaler A. Testosterone replacement therapy in hypogonadal men at high risk for prostate cancer: results of 1 year of treatment in men with prostatic intraepithelial neopla-sia. J Urol 2003;170:2348-51.
20. Rhoden EL., Averbeck MA., Teloken PE. Androgen replacement in men undergoing treatment for prostate cancer. J Sex Med 2008;5:2202-8.
21. Kaufman JM., Graydon RJ. Androgen replacement after curative radical prostatectomy for prostate cancer in hypogonadal men. J Urol 2004;172:920-2.
22. Agarwal PK., Oefelein MG. Testosterone replacement therapy after primary treatment for prostate cancer. J Urol 2005;173: 533-6.
23. Sarosdy MF. Testosterone replacement for hypogonadism after treatment of early prostate cancer with brachytherapy. Cancer 2007;109:536-41.
24. Morales A., Black AM., Emerson LE. Testosterone administration to men with testosterone deficiency syndrome after external beam radiotherapy for localized prostate cancer: preliminary observations. BJU Int 2009;103:62-4.
25. Gann PH., Hennekens CH., Ma J., Longcope C., Stampfer MJ. Prospective study of sex hormone levels and risk of prostate cancer. J Natl Cancer Inst 1996;88:1118-26.
26. Vatten LJ., Ursin G., Ross RK., Stanczyk FZ., Lobo RA., Harvei S., Jellum E. Androgens in serum and the risk of prostate cancer; a nested case-control study from the Janus serum bank in Norway. Cancer Epidemiol Boimarkers Prev 1997;6:967-9.
27. Stattin P., Lumme S., Tenkanen L., Alfthan H., Jellum E., Hallmans G., Thorensen S., Hakulinen T., Luostarinen T., Lehtinen M., Dill-ner J., Stenman UH., Hakama M. High levels of circulating testosterone are not associated with increased prostate cancer risk: a pooled prospective study. Int J Cancer 2004;108:418-24.
28. Severi G., Morris HA., MacInnis RJ., English DR., Tilley W., Hopper JL., Boyle P., Giles G. Circulating steroid hormones and the risk of prostate cancer. Cancer Epidemiol Biomarkers Prev 2006;15:86-91.
29. Shaneyfelt T., Husein R., Bubley G., Montzoros CS. Hormonal predictors of prostate cancer: a meta-analysis. J Clin Oncol 2000;98:847-53.
30. Rosner W., Auchus RJ., Azziz R., Sluss PM., Raff H. Utility., limitations., and pitfalls in measuring testosterone; an Endocrine Society position statement. J Clin Endocrinol Metab 2007;92: 405-11.
31. Hoffman MA., deWolf WC., Morgentaler A. Is low serum free testosterone a maker for high grade prostate cancer. J Urol 2000;63:824-7.
32. Schatzl G., Madersbacher S., Thurridl T., Waldmüller J., Kramer G., Haitel A., Marberger M. High-grade prostate cancer is associated with low serum testosterone levels. Prostate 2001;47: 52-8.
33. Lackner JE., Maerk I., Koller A., Bieglmayer C., Marberger M., Kratzik C., Schatzl G. Serum inhibin-not a cause of low testosterone levels in hypogonadal prostate cancer. Urology 2008;72: 1121-4.
34. Imamoto T., Suzuki H., Fukasawa S., Shimbo M., Inahara M., Komiya A., Ueda T., Shiraishi T., Ichikawa T. Pretreatment serum testosterone level as a predictive factor of pathological stage in localized prostate cancer treated with radical prostatectomy. Eur Urol 2005;47:308-12.
35. Isom-Batz G., Bianco FJ., Kattan MW., Mulhall JP., Lilja H., East-ham JA. Testosterone as a predictor of pathological stage in clinically localized prostate cancer. J Urol 2005;173:1935-7.
36. 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. Pretreatment total testosterone level predicts pathological stage in patients with localized prostate cancer treated with radical prostatectomy. J Urol 2003;169:1670-5.
37. Teloken C., Teodosio Da Ros C., Caraver F., Weber FA., Caval-heiro AP., Meyer Graziottin T. Low serum testosterone levels are associated with positive surgical margins in radical retropubic prostatectomy: hypogonadism represents bad prognosis in prostate cancer. J Urol 2005;174:2178-80.
38. Giton F., Fiet J., Guechot J., Ibrahim F., Bronsard F., Chopin D., Raynaud JP. Serum bioavailable testosterone: assayed or calculated? Clin Chem 2006;52:474-81.
39. Giton F., Urien S., Born C., Tichet J., Guechot J., Callebert J., Bronsard F., Raynaud JP., Fiet J. Determination of bioavailable testosterone [non-sex hormone-binding globulin (SHBG)-bound testosterone] in a population of healthy French men: influence of androstenediol on testosterone binding to SHBG. Clin Chem 2007;53:474-81.
40. Epstein JI., Allsbrook WC., Amin MB., Egevad LL and the ISUP Grading Committee. The 2005 International Society of Urolo-gical Pathology (ISUP) consensus conference on Gleason grading of prostate carcinoma. Am J Surg Pathol 2005;29:1228-42.
41. Molinié V., Sibony M., Fromont G., de Fromont M., Aillet G., Balaton A., Bernadette A., Peneau M., Soulié M. Les membres du sous comité prostate du Comité de cancérologie de l-'Association francaise d'urologie. Fiche compte rendu standardise et prostatectomie radicale. Ann Pathol 2008;28:467-73.
42. Srigley JR., Amin MB., Epstein JI., Grignon DJ., Humphrey PA., Renshaw AA., Wheeler TM for the Members of the Cancer Committee., College of American Pathologists. Updated protocol for the examination of specimens from patients with carcinomas of the prostate gland. Arch Pathol Lab Med 2006;130:936-46.
43. Srigley JR. Key issues in handling and reporting radical prostatectomy specimens. Arch Pathol Lab Med 2006;130:303-17.
44. Gleason DF., Mellinger GT. The Veterans Administration Cooperative Urological Research Group. Prediction of prognosis for prostate adenocarcinoma by combined histological grading and clinical staging. J Urol 1974;111:58-64.
45. Gleason DF. Histological grading and clinical staging of pro-static carcinoma. In: Tannenbaum M., editor. Urologic pathology: the prostate. Philadelphia: Lea & Feibiger., 1977:171-98.
46. Grignon DJ., Bostwick DG., Civantos F., Garnick MB., Gaudin P., Srigley JR. Pathologic handling and reporting of prostate tissue specimens in patients receiving neoadjuvant hormonal therapy: report of the pathology committee. Mol Urol 1999;3:193-8.
47. Rhoden EL., Riedner CE., Morgentaler A. The ratio of serum testosterone-to-prostate specific antigen predicts prostate cancer in hypogonadal men. J Urol 2008;179:1741-5.
48. Ide H., Yasuda M., Nishio K., Isotani S., Kamiyama Y., Muto S., Horie S. Development of a nomogram for predicting high-grade prostate cancer on biopsy: the significance of serum testosterone levels. Anticancer Res 2008;28:2487-92.
49. Molinie V. Le score de Gleason en 2008. Ann Pathol 2008;28: 350-3.
50. Amin MB., Grignon DJ., Humphrey PA., Srigley JR. Gleason grading of prostate cancer. A contemporary approach. Philadelphia., PA: Lippincott Williams & Wilkins., 2004.
51. Sakr WA., Tefilli MV., Grignon DJ., Banerjee M., Dey J., Gheiler EL., Tiguert R., Powell IJ., Wood DP. Gleason score 7 prostate cancer: a heterogeneous entity? Correlation with pathologic parameters and disease-free survival. Urology 2000;56:730-4.
52. Wright JL., Salinas CA., Lin DW., Kolb S., Koopmeiners J., Feng Z., Stanford JL. Prostate cancer specific mortality and Gleason 7 disease differences in prostate cancer outcomes between cases with Gleason 4+3 and Gleason 3+4 in tumors in a population based cohort. J Urol 2009;182:2702-7.
53. Stark JR., Perner S., Stampfer MJ., Sinnott JA., Finn S., Eisenstein AS., Ma J., Fiorentino M., Kurth T., Loda M., Giovannucci EL., Rubin MA., Mucci LA. Gleason score and lethal prostate cancer: does 3+4=4+3? J Clin Oncol 2009;27:3459-64.
54. Rosner W. Plasma steroid-binding proteins. Endocrinol Metab Clin North Am 1991;20:697-720.
55. Rosner W. Errors in the measurement of plasma free testosterone. J Clin Endocrinol Metab 1997;82:2014-5.
56. Winters SJ., Kelley DE., Goodpaster B. The analog free testosterone assay: Are the results in men clinically useful? Clin Chem 1998;44:2178-82.
57. Wierman ME., Basson R., Davis SR., Khosla S., Miller KK., Ros-ner W., Santoro N. Androgen therapy in women: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab 2006;91:3697-710.
58. Swerdloff RS., Wang C. Free testosterone measurement by the analog displacement direct assay: old concerns and new evidence. Clin Chem 2008;54:458-60.
59. Vermeulen A., Verdonck L., Kaufman JM. A critical evaluation of simple methods for the estimation of free testosterone in serum. J Clin Endocrinol Metab 1999;84:3666-7.
60. Mazer NA. A novel spreadsheet method for calculating the free serum concentrations of testosterone., dihydrotestosterone., estra-diol., estrone and cortisol: with illustrative examples from male and female populations. Steroids 2009;74:512-9.
61. Manni A., Pardridge WM., Cefalu W., Nisula BC., Bardin CW., Santner SJ., Santen RJ. Bioavailability of albumin-bound testosterone. J Clin Endocrinol Metab 1985;61:705-10.
62. Wang C., Catlin DH., Demers LM., Starcevic B., Swerdloff RS. Measurement of total testosterone in adult men: comparison of current laboratory methods versus liquid chromatography-tandem mass spectrometry. J Clin Endocrinol Metab 2004;89: 534-43.
63. Crawford DE., Barqawi AB., O'Donnell C., Morgentaler A. The association of time of day and serum testosterone concentration in a large screening population. BJU Int 2007;100:509-13.
64. American Association of Clinical Endocrinologists. Medical guidelines for clinical practice for the evaluation and treatment of hypogonadism in adult male patients-2002 update. Endocr Pract 2002; 8:440-56.
65. Mearini L., Constantini E., Zucchi A., Mearini E., Bini V., Cottini E., Porena M. Testosterone levels in benign prostatic cancer. Urol Int 2008;80:134-40.
66. Mulligan T., Frick MF., Zuraw QC., Stemhagen A., McWhirter C. Prevalence of hypogonadism in males aged at least 45 years. The HIM study. Int J Clin Pract 2006;60:762-9.
67. Roddam AW., Allen NE., Appleby P., Key TJ., for the Endogenous Hormones and Prostate Cancer Collaborative Group. Endogenous sex hormones and prostate cancer: a collaborative analysis of 18 prospective studies. J Natl Cancer Inst 2008;100:170-83.
68. Hsing AW., Chu LW., Stanczyk FZ. Androgen and prostate cancer: Is the hypothesis dead? Cancer Epidemiol Biomarkers Prev 2008;17:2525-30. 69. Marks LS., Mazer NA., Mostaghel E., Hess DL., Dorey FL., Epstein JI., Veltri RW., Makarov DV., Partin AW., Bostwick DG., Macairan ML., Nelson PS. Effect of testosterone replacement therapy on prostate tissue hormone in men with late-onset hypo-gonadism. J Am Med Assoc 2006;296:2351-61.
69. Behre HM., Boymeyer J., Nieschlag E. Prostate volume in testosterone-treated and untreated hypogonadal men in comparison to age-matched controls. Clin Endocrinol 1994;40:341-9.