© 1996 by Oxford University Press
Journal of the National Cancer Institute, Vol. 88, No. 16, 1118-1126,
August 21, 1996
© 1996 Oxford University Press
Prospective Study of Sex Hormone Levels and Risk of Prostate Cancer
Division of Preventive Medicine and Channing Laboratory, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA Department of Preventive Medicine, Northwestern University Medical School, Chicago, IL
Division of Preventive Medicine and Channing Laboratory, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School and Department of Ambulatory Care and Prevention, Brigham and Women's Hospital, Harvard Medical School; Department of Epidemiology, Harvard School of Public Health Boston
Channing Laboratory, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School
Department of Obstetrics and Gynecology, Department of Medicine, University of Massachusetts Medical Center Worcester
Channing Laboratory, and Departments of Epidemiology and Nutrition, Harvard School of Public Health
Correspondence to: Peter H. Gann, M.D., Department of Preventive Medicine, Northwestern University Medical School, 680 N. Lake Shore Dr., Suite 1102, Chicago, IL 60611.
BACKGROUND:: Sex steroids, particularly androgens, have been implicated in the pathogenesis of prostate cancer. Data from previous studies comparing circulating hormone levels in men with and without prostate cancer are difficult to interpret, since the studies were limited in size, hormone levels were analyzed in blood drawn after the diagnosis of cancer, nonrepresentative control subjects were used, and hormone and hormone-binding protein levels were not simultaneously adjusted.
PURPOSE:: We conducted a prospective, nested case-control study to investigate whether plasma hormone and sex hormone-binding globulin (SHBG) levels in healthy men were related to the subsequent development of prostate cancer.
METHODS:: Among participants in the Physicians' Health Study who provided plasma samples in 1982, we identified 222 men who developed prostate cancer by March 1992. Three hundred ninety control subjects, matched to the case patients on the bases of age, smoking status, and length of follow-up, were also identified. Immunoassays were used to measure the levels of total testosterone, dihydrotestosterone (DHT), 3
-androstanediol glucuronide (AAG), estradiol, SHBG, and prolactin in the stored (at –82 °C) plasma samples. Correlations between individual hormone levels and between hormone levels and SHBG in the plasma of control subjects were assessed by use of Spearman correlation coefficients (r). Odds ratios (ORs) and 95% confidence intervals (CIs) specifying the prostate cancer risk associated with quartile levels of individual hormones, before and after adjustment for other hormones and SHBG, were calculated by use of conditional logistic regression modeling. Reported P values are two-sided.
RESULTS:: No clear associations were found between the unadjusted levels of individual hormones or SHBG and the risk of prostate cancer. However, a strong correlation was observed between the levels of testosterone and SHBG (r = .55), and weaker correlations were detected between the levels of testosterone and the levels of both estradiol (r = .28) and DHT (r = .32) (all P<.001). When hormone and SHBG levels were adjusted simultaneously, a strong trend of increasing prostate cancer risk was observed with increasing levels of plasma testosterone (ORs by quartile = 1.00, 1.41, 1.98, and 2.60 [95% CI = 1.34–5.02]; P for trend = .004), an inverse trend in risk was seen with increasing levels of SHBG (ORs by quartile = 1.00, 0.93, 0.61, and 0.46 [95% CI = 0.24–0.89]; P for trend = .01), and a nonlinear inverse association was found with increasing levels of estradiol (ORs by quartile = 1.00, 0.53, 0.40, and 0.56 [95% CI = 0.32–0.98]; P for trend = .03). No associations were detected between the levels of DHT or prolactin and prostate cancer risk; for AAG, a marker of 5-reductase activity, only suggestive evidence of a positive association was found. The results were essentially unchanged when case patients diagnosed within 4 years of plasma collection, case patients diagnosed with localized (i.e., nonaggressive) disease, or control subjects with elevated prostate serum antigen levels (>2.5 ng/mL) were excluded from the analyses.
CONCLUSIONS:: High levels of circulating testosterone and low levels of SHBG—both within normal endogenous ranges—are associated with increased risks of prostate cancer. Low levels of circulating estradiol may represent an additional risk factor. Circulating levels of DHT and AAG do not appear to be strongly related to prostate cancer risk. [J Natl Cancer Inst 1996;88:1118–26]
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H. A. Feldman, C. Longcope, C. A. Derby, C. B. Johannes, A. B. Araujo, A. D. Coviello, W. J. Bremner, and J. B. McKinlay Age Trends in the Level of Serum Testosterone and Other Hormones in Middle-Aged Men: Longitudinal Results from the Massachusetts Male Aging Study J. Clin. Endocrinol. Metab., February 1, 2002; 87(2): 589 - 598. [Abstract] [Full Text] [PDF]
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 A. M. Matsumoto Andropause: Clinical Implications of the Decline in Serum Testosterone Levels With Aging in Men J. Gerontol. A Biol. Sci. Med. Sci., February 1, 2002; 57(2): M76 - 99. [Full Text]
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 A. Mifsud, A. T. Choon, D. Fang, and E.L. Yong Prostate-specific antigen, testosterone, sex-hormone binding globulin and androgen receptor CAG repeat polymorphisms in subfertile and normal men Mol. Hum. Reprod., November 1, 2001; 7(11): 1007 - 1013. [Abstract] [Full Text] [PDF]
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 F. Modugno, J. L. Weissfeld, D. L. Trump, J. M. Zmuda, P. Shea, J. A. Cauley, and R. E. Ferrell Allelic Variants of Aromatase and the Androgen and Estrogen Receptors: Toward a Multigenic Model of Prostate Cancer Risk Clin. Cancer Res., October 1, 2001; 7(10): 3092 - 3096. [Abstract] [Full Text] [PDF]
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M. J. M. Dirx, P. A. van den Brandt, R. A. Goldbohm, and L. H. Lumey Energy Restriction in Childhood and Adolescence and Risk of Prostate Cancer: Results from the Netherlands Cohort Study Am. J. Epidemiol., September 15, 2001; 154(6): 530 - 537. [Abstract] [Full Text] [PDF]
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M. E. Taplin and S.-M. Ho The Endocrinology of Prostate Cancer J. Clin. Endocrinol. Metab., August 1, 2001; 86(8): 3467 - 3477. [Full Text] [PDF]
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C. A. Haiman, M. J. Stampfer, E. Giovannucci, J. Ma, N. E. Decalo, P. W. Kantoff, and D. J. Hunter The Relationship between a Polymorphism in CYP17 with Plasma Hormone Levels and Prostate Cancer Cancer Epidemiol. Biomarkers Prev., July 1, 2001; 10(7): 743 - 748. [Abstract] [Full Text] [PDF]
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K. A. Rosenblatt, K. G. Wicklund, and J. L. Stanford Sexual Factors and the Risk of Prostate Cancer Am. J. Epidemiol., June 15, 2001; 153(12): 1152 - 1158. [Abstract] [Full Text] [PDF]
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A. Vermeulen Androgen Replacement Therapy in the Aging Male--A Critical Evaluation J. Clin. Endocrinol. Metab., June 1, 2001; 86(6): 2380 - 2390. [Full Text] [PDF]
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T. W.-M. Boileau, S. K. Clinton, S. Zaripheh, M. H. Monaco, S. M. Donovan, and J. W. Erdman Jr. Testosterone and Food Restriction Modulate Hepatic Lycopene Isomer Concentrations in Male F344 Rats J. Nutr., June 1, 2001; 131(6): 1746 - 1752. [Abstract] [Full Text]
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 Z. Weihua, S. Makela, L. C. Andersson, S. Salmi, S. Saji, J. I. Webster, E. V. Jensen, S. Nilsson, M. Warner, and J.-A. Gustafsson A role for estrogen receptor beta in the regulation of growth of the ventral prostate PNAS, May 22, 2001; 98(11): 6330 - 6335. [Abstract] [Full Text] [PDF]
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A. H. Wu, A. S. Whittemore, L. N. Kolonel, F. Z. Stanczyk, E. M. John, R. P. Gallagher, and D. W. West Lifestyle Determinants of 5{{alpha}}-Reductase Metabolites in Older African-American, White, and Asian-American Men Cancer Epidemiol. Biomarkers Prev., May 1, 2001; 10(5): 533 - 538. [Abstract] [Full Text]
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A. M. Kenny, K. M. Prestwood, C. A. Gruman, K. M. Marcello, and L. G. Raisz Effects of Transdermal Testosterone on Bone and Muscle in Older Men With Low Bioavailable Testosterone Levels J. Gerontol. A Biol. Sci. Med. Sci., May 1, 2001; 56(5): 266M - 272. [Abstract] [Full Text]
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C. Rodriguez, A. V. Patel, E. E. Calle, E. J. Jacobs, A. Chao, and M. J. Thun Body Mass Index, Height, and Prostate Cancer Mortality in Two Large Cohorts of Adult Men in the United States Cancer Epidemiol. Biomarkers Prev., April 1, 2001; 10(4): 345 - 353. [Abstract] [Full Text]
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D. J. George, T. F. Shepard, J. Ma, E. Giovannucci, P. W. Kantoff, and M. J. Stampfer PTEN Polymorphism (IVS4) Is Not Associated with Risk of Prostate Cancer Cancer Epidemiol. Biomarkers Prev., April 1, 2001; 10(4): 411 - 412. [Full Text]
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C. Nagata, N. Takatsuka, H. Shimizu, H. Hayashi, T. Akamatsu, and K. Murase Effect of Soymilk Consumption on Serum Estrogen and Androgen Concentrations in Japanese Men Cancer Epidemiol. Biomarkers Prev., March 1, 2001; 10(3): 179 - 184. [Abstract] [Full Text]
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N. E. Allen, M. S. Forrest, and T. J. Key The Association between Polymorphisms in the CYP17 and 5{{alpha}}-Reductase (SRD5A2) Genes and Serum Androgen Concentrations in Men Cancer Epidemiol. Biomarkers Prev., March 1, 2001; 10(3): 185 - 189. [Abstract] [Full Text]
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P. Stattin, S. Söderberg, G. Hallmans, A. Bylund, R. Kaaks, U.-H. Stenman, A. Bergh, and T. Olsson Leptin Is Associated with Increased Prostate Cancer Risk: A Nested Case-Referent Study J. Clin. Endocrinol. Metab., March 1, 2001; 86(3): 1341 - 1345. [Abstract] [Full Text]
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E. Riboli The European Prospective Investigation into Cancer and Nutrition (EPIC): Plans and Progress J. Nutr., January 1, 2001; 131(1): 170S - 175. [Full Text]
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E. A. Platz, E. B. Rimm, W. C. Willett, P. W. Kantoff, and E. Giovannucci Racial Variation in Prostate Cancer Incidence and in Hormonal System Markers Among Male Health Professionals J Natl Cancer Inst, December 20, 2000; 92(24): 2009 - 2017. [Abstract] [Full Text] [PDF]
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T. F. Shepard, E. A. Platz, P. W. Kantoff, W. G. Nelson, W. B. Isaacs, D. Freije, P. G. Febbo, M. J. Stampfer, and E. Giovannucci No Association between the I105V Polymorphism of the Glutathione S-Transferase P1 Gene (GSTP1) and Prostate Cancer Risk: A Prospective Study Cancer Epidemiol. Biomarkers Prev., November 1, 2000; 9(11): 1267 - 1268. [Full Text]
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G. Clarke and A. S. Whittemore Prostate Cancer Risk in Relation to Anthropometry and Physical Activity: The National Health and Nutrition Examination Survey I Epidemiological Follow-Up Study Cancer Epidemiol. Biomarkers Prev., September 1, 2000; 9(9): 875 - 881. [Abstract] [Full Text]
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 M. C. Bosland Chapter 2: The Role of Steroid Hormones in Prostate Carcinogenesis J Natl Cancer Inst Monographs, July 1, 2000; 2000(27): 39 - 66. [Abstract] [Full Text] [PDF]
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W. Demark-Wahnefried, J. M. Schildkraut, D. Thompson, S. M. Lesko, L. McIntyre, P. Schwingl, D. F. Paulson, C. N. Robertson, E. E. Anderson, and P. J. Walther Early Onset Baldness and Prostate Cancer Risk Cancer Epidemiol. Biomarkers Prev., March 1, 2000; 9(3): 325 - 328. [Abstract] [Full Text]
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 B. E. Henderson and H. S. Feigelson Hormonal carcinogenesis Carcinogenesis, March 1, 2000; 21(3): 427 - 433. [Abstract] [Full Text] [PDF]
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T. Shaneyfelt, R. Husein, G. Bubley, and C. S. Mantzoros Hormonal Predictors of Prostate Cancer: A Meta-Analysis J. Clin. Oncol., February 14, 2000; 18(4): 847 - 847. [Abstract] [Full Text] [PDF]
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S. Liu, I-M. Lee, P. Linson, U. Ajani, J. E Buring, and C. H Hennekens A prospective study of physical activity and risk of prostate cancer in US physicians Int. J. Epidemiol., February 1, 2000; 29(1): 29 - 35. [Abstract] [Full Text] [PDF]
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P. G. Febbo, P. W. Kantoff, E. A. Platz, D. Casey, S. Batter, E. Giovannucci, C. H. Hennekens, and M. J. Stampfer The V89L Polymorphism in the 5{{alpha}}-Reductase Type 2 Gene and Risk of Prostate Cancer Cancer Res., December 1, 1999; 59(23): 5878 - 581. [Abstract] [Full Text] [PDF]
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 T. J. Ahonen, P. L. Härkönen, J. Laine, H. Rui, P. M. Martikainen, and M. T. Nevalainen Prolactin Is a Survival Factor for Androgen-Deprived Rat Dorsal and Lateral Prostate Epithelium in Organ Culture Endocrinology, November 1, 1999; 140(11): 5412 - 5421. [Abstract] [Full Text]
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J. M. Chan, M. J. Stampfer, J. Ma, E. B. Rimm, W. C. Willett, and E. L. Giovannucci Supplemental Vitamin E Intake and Prostate Cancer Risk in a Large Cohort of Men in the United States Cancer Epidemiol. Biomarkers Prev., October 1, 1999; 8(10): 893 - 899. [Abstract] [Full Text]
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M. Marcelli and G. R. Cunningham Hormonal Signaling in Prostatic Hyperplasia and Neoplasia J. Clin. Endocrinol. Metab., October 1, 1999; 84(10): 3463 - 3468. [Full Text] [PDF]
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R. M. Lunn, D. A. Bell, J. L. Mohler, and J. A. Taylor Prostate cancer risk and polymorphism in 17 hydroxylase (CYP17) and steroid reductase (SRD5A2) Carcinogenesis, September 1, 1999; 20(9): 1727 - 1731. [Abstract] [Full Text] [PDF]
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R. T. Prehn On the Prevention and Therapy of Prostate Cancer by Androgen Administration Cancer Res., September 1, 1999; 59(17): 4161 - 4164. [Abstract] [Full Text] [PDF]
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 S. J. Winters Current Status of Testosterone Replacement Therapy in Men Arch Fam Med, May 1, 1999; 8(3): 257 - 263. [Abstract] [Full Text] [PDF]
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