BENIGN prostatic hyperplasia (BPH) is a common neoplasm

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1 X/97/$03.00/0 Vol. 82, No. 2 Journal of Clinical Endocrinology and Metabolism Printed in U.S.A. Copyright 1997 by The Endocrine Society Effects of Age and Sex Hormones on Transition and Peripheral Zone Volumes of Prostate and Benign Prostatic Hyperplasia in Twins* A. WAYNE MEIKLE, ROBERT A. STEPHENSON, CATHRYN M. LEWIS, AND RICHARD G. MIDDLETON Departments of Medicine (A.W.M.), Urology (R.A.S., R.G.M.), and Medical Informatics (C.M.L.), University of Utah School of Medicine, Salt Lake City, Utah ABSTRACT Benign prostatic hyperplasia has been shown to increase with age and be influenced by sex hormones. The relationship between aging and hormonal influences on growth of zones of the prostate is unresolved. We studied the relationship of age and sex hormones on volume of prostate zones in 214 male twins between 25 and 75 yr old. Volumes of the total prostate (TV), transition zone (TZ), and peripheral zones (PZ) were measured using transrectal ultrasound, and sex steroid concentrations were measured using RIA. Using transformed data corrected for age, TV (r 0.54, P ), TZ (r 0.58, P ), and PZ (r 0.39, P ) volumes increased with age. However, the PZ volume rose more rapidly than the TZ before age 50, and TZ showed a steeper increase after age 50 yr than the PZ volume. The TZ, PZ, and ratio TZ/PZ correlated significantly (r 0.87, 0.90, and 0.52, respectively; P ). After a TV exceeded 30 g, the rise BENIGN prostatic hyperplasia (BPH) is a common neoplasm of the prostate and causes considerable morbidity in aging men. BPH does not occur in androgen-deficient men who fail to virilize (1). High 5 -reductase activity of the prostate converts testosterone to dihydrotestosterone (DHT), which has higher affinity with the androgen receptor than testosterone and is, therefore, the main androgen-influencing prostate growth after puberty (1 5). Sex steroids secreted by the testes contribute to the development of BPH by yet unresolved mechanisms. The growth of the prostate rises from 1gatbirth to about 4 g before puberty and then to an average 20 g after virilization, after puberty, by age 20 yr (6 9). BPH arises from the periurethral glands [transition zone (TZ)], whereas prostate cancer arises most commonly in the peripheral zones (PZ). The TZ in young men comprises about 10% of the TV, and by age 60 yr, the TZ averages 30% of the TV (7, 10 13). Both the PZ and TZ contribute to prostate enlargement except that, in older men, the growth of the TZ exceeds that of the PZ. In a recent report, we observed that, after the TV exceeded 50 g, most of the growth was accounted for by the TZ. The cause of the differential growth rate between the TZ and PZ is Received June 28, Revision received September 10, Accepted October 10, Address all correspondence and requests for reprints to: A. Wayne Meikle, M.D., University of Utah School of Medicine, 50 North Medical Drive, Salt Lake City, Utah * This work was supported in part by NIH Grants DK-45760, DK , and RR of the PZ became attenuated, and the slope of the TZ became steeper. Age-adjusted sex hormone concentration was not evaluated in men with larger prostate volumes. Men with American Urological Association symptom scores above 10 had significantly (P 0.001) larger total prostate volume (TV) and TZ volume, but not PZ volumes, than men with scores below 10. Prostate volumes correlated inversely with age-adjusted serum testosterone (T), dihydrotestosterone, sex hormone binding globulin, and sex hormone binding globulin-bound T concentrations. These results demonstrate that before age 50 yr or beforea prostate weight exceeds 30 g, prostate growth may be mainly from enlargement of the PZ and after age 50, the TZ. In addition, elevated T and dihydrotestosterone concentrations do not predispose men to prostate enlargement or symptoms of benign prostatic hyperplasia. (J Clin Endocrinol Metab 82: , 1997) unknown, but sex steroids and growth factors are thought to contribute. During aging, several hormonal changes occur that have been associated with development of BPH and prostate cancer, including a rise in sex hormone binding globulin (SHBG) and estrogen relative to testosterone (14 19). Except for autopsy data, little is known about the relative rates of growth of the PZ and TZ after puberty and virilization. Accurate measurement of the TZ volume and TV of the prostate has been made possible by transrectal ultrasound (TRUS) and allows assessment of therapy and aging on relative changes of growth rates of zones of the prostate gland (10, 11, 20 25). We previously have observed that familial (genetic and environmental) factors substantially influence the variation in plasma sex steroid concentrations in normal male twins and in families at risk for prostate cancer (26 31). We now report on associations among ages, sex steroids, symptoms of urethral obstruction, and the size of the PZ and TZ in normal male twins ranging in age between 25 and 75 yr. Materials and Methods This study was done to assess the influence of age and hormonal factors on prostate size and BPH in male twin-pairs between 25 and 75 yr old. More than 1500 potential participants have been identified from data base registries, including a recent update of drivers license information. This was obtained by coupling genealogy information and birth and death records with drivers license data. We report data on 214 twins of 360 twins that have been studied where both twins of the pairs were evaluated and had no endocrine or health issues. 571

2 572 MEIKLE ET AL. JCE&M 1997 Vol 82 No 2 FIG. 1. Relationship between age (horizontal axis) and TV (A), TZ (B), PZ and TZ/PZ (D) ratio of volumes (vertical axis, respectively). The quadratic regression models with age are shown. The r was for TV and age, 0.58 for TZ, 0.43 for PZ, and 0.65 for TZ/PZ with P , respectively. One-hundred-twenty-six twins were monozygotic (age, yr, mean sd), range yr) and 88 dizygotic (age, yr, mean sd), range, yr). All men with prostate cancer or a history of treatment for BPH were excluded from analysis. Informed consent was obtained before entry into the study conducted on the Clinical Research Center of the University of Utah. None of the subjects was receiving medications known to affect sex steroid secretion. The American Urologic Association (AUA) questionnaire was administered to each twin, and the symptom score was calculated (32). Between 0800 and 1030 h, three blood samples for hormone concentrations were obtained in tubes by venipuncture at intervals of 15 to 20 min. An equal volume of each sample was pooled and stored at 20 C until assayed. The concentrations of testosterone, DHT, estradiol, estrone, SHBG, free testosterone, bioavailable testosterone, androstanediol glucuronide, LH, FSH, and prostate specific antigen were measured by assays reported previously (28, 29, 31). Intra- and interassay coefficients of variation were less than 12 % (33). Bioelectrical impedance was used to measure body fat, lean body mass, and body water (34, 35). The ratio of lean body mass to body fat was calculated. A digital rectal examination was done before TRUS imaging, using a Bruel and Kjaer 1 instrument fitting with a 7-mHz transducer (B&K Medical Systems, North Billerica, MA). The TV (assuming 1cc 1g)and the volume of the TZ were calculated by /6 width (maximal transverse dimension), length (maximal anterior and posterior dimension), and height (maximal sagittal proximal to distal dimension) (33). The TZ is significantly hypoechoic relative to PZ echodensities. This permits accurate visualization of zonal boundaries for the purposes of measurements used in volume calculations. The PZ volume (central zone is included in PZ calculation) was calculated by subtracting the TZ from the TV. The coefficient of variation is 5 % for TV and 11 % for TZ. Statistical analyses Data were obtained from a study of male twins. In the current analysis, correlations between twin pairs were accounted for by weighting twin pairs where both twins had data available. The effect of age on the growth of zones of the prostate was evaluated by filling linear models with quadratic (age, age**2) terms for age. The relationship between prostate zones and TV also was investigated. Linear models and ANOVA were used to determine whether sex hormone concentrations influenced the variation in prostate size. Models included quadratic terms for age and were fit for all age groups and for men more than 50 yr old. Results Age effects on TV Figure 1, A D shows an increase in TV, TZ and PZ volumes, and TZ/PZ with age. These figures show a quadratic

3 relationship with age for the TV, TZ and PZ volume, and the ratio of TZ/PZ, but the TZ shows a steeper increase compared with the TV and PZ volume. Age significantly correlated with the TV (r 0.56, P ), TZ (r 0.58, P ), PZ (r 0.43, P ), the ratio of the TZ/TV (r 0.65, P ), and TZ/PZ (r 0.57, P ). These results confirm our previous observations that age influences the TZ volume (26). These results suggest that, after age 50, both the PZ and TZ increase in volume, but the rise of the TZ is more rapid than the PZ volume. AGE, HORMONES, AND PROSTATE ZONES 573 Relationships of the volume of prostate zones Both the TZ and PZ volumes and the ratio of TZ/PZ (Fig. 2, A C) correlated highly (r 0.87, 0.90, and 0.52, respectively; P ; n 214) with the total volume. The TZ and PZ volumes also correlated significantly with each other (r 0.51, P , n 214). In contrast to the increase of TZ volume related to TV, the rise of PZ volume became attenuated as the TV exceeded 30 g. TV up to 30 g were predominated by the PZ volume relative to the TZ; TV above 30 g accounted for the further enlargement of the TZ. They also confirm the high correlation between the TV and the TZ (r 0.87, P ) and TV and PZ (r 0.90, P ), suggesting that both the PZ and TZ contribute to the prostate enlargement associated with aging. Prostate volumes and hormonal relationships Linear models were used to evaluate the relationship between sex hormones and TV and zones (TV, PZ, PZ). Any effect of age was accounted for through the inclusion of quadratic terms in the model. Table 1 gives statistical values for different effects of the sex hormone on prostate size. Study individuals were split into the upper and lower quartiles of the entire group and of those 50 yr old or less (Table 1). For TV and PZ volume, serum testosterone (T) was significantly lower (P 0.05 and 0.02, respectively) in men over 50 yr old with larger prostate volumes than those with smaller prostates, and for TZ volumes, DHT was significantly lower (P 0.002) in the older men with larger TZ volumes. For all three prostate volume measurements, SHBG-bound T (TV, P 0.03; PZ, P 0.03) was significantly lower in those with larger TV and PZ volume, and marginally significant for TZ volumes (P 0.07). These results might suggest that a relative androgen deficiency independent of aging contributes to growth of the gland because the data were corrected for aging influences. Any age effect on prostate volume was removed from the variable by quadratic transformation before statistical comparison. As shown in Table 2, the AUA symptom score was higher in the twins with larger TZ volumes (upper quartile) compared with those with smaller volumes. To evaluate this relationship further, those with a symptom score more than 10 (suggesting BPH) were compared with those with a score less than 10. The TV and TZ volume were significantly greater in men with higher scores compared with those with lower scores (P 0.001), but no significant relationship between the score and PZ volume was observed (Table 2). These results suggest that symptoms of BPH are produced, FIG. 2. Relationship of TV (horizontal axis) with volumes of TZ (A), PZ (B) and TZ/PZ ratio of volumes (vertical axis, respectively). The best fitting quadratic regression models are shown. The r for TZ and TV, 0.9 for PZ, 0.52 for TZ/PZ with P , respectively. in part, by enlargement of TZ and total prostate, but not enlargement of the PZ. Table 3 summarizes the relationships of volumes of the prostate and hormonal values adjusted for age. This confirms

4 574 MEIKLE ET AL. JCE&M 1997 Vol 82 No 2 TABLE 1. Comparison of prostate volumes in the upper and lower quartiles for all men and greater than 50 yr old TV 50 yr All Lower quart. mean SE Upper quart. mean SE P value Lower quart. mean SE Upper quart. mean SE P value T, nmol/l SHBG-T, nmol/l NS Lean/fat NS TZ SHBG-T, nmol/l NS DHT, nmol/l PZ T, nmol/l T/SHBG SHBG-T, nmol/l NS Lean/fat NS SHBG-T, bound to SHBG; NS, not significant. TABLE 2. Comparison of prostate volume in men with AUA symptom scores less than and greater than 10 Sx Score P value TV, g TZ, g PZ, g Sx score AUA, symptoms score. TABLE 3. Relationship between prostate volumes and hormone concentrations adjusted for age TV TZ PZ T 0.05 ( ) Free T DHT ( ) 0.18 DHEAS FSH ( ) LH ( ) 0.18 Estrone Estradiol SHBG 0.01 ( ) ( ) AG DHT/T ( ) 0.16 Estradiol/T T/SHBG ( ) SHBG-bound T ( ) DHEAS dehydroepiandrosterone; AG androstanediol glucuronide. P-values for TV with SHBG, TZ with DHT and LH, PZ with SHBG and SHBG-bound T required a quadratic model for an adequate fit. All other models include a linear term for the hormone level. For significant P-values (p 0.05), an indication of the relationship between the prostate volume and hormone level is given. ( ), prostate volume increases as hormone level increases. ( ), prostate volume decreases as the hormone level increases. the inverse relationship between T and SHBG and TV, DHT and DHT/T and TZ, and SHBG and SHBG-bound T and PZ. A positive relationship was observed for LH and TZ and FSH and T/SHBG and PZ. These findings do not suggest that higher serum sex steroid concentrations are associated with prostate enlargement. Discussion TRUS has made it possible to quantitate the volume of zones of the prostate and to evaluate the influences of age and therapy on them. This study shows that as men age, the relative size of zones of the prostate has variable influences on TV. Both the TZ and PZ volumes correlate with age and with TV of the gland, but they show a variable relationship with size of the gland at various ages. PZ enlargement and, to a lesser extent, the TZ contribute to moderate enlargement of the prostate between 25 and 50 yr old, and beyond age 50, the growth of the TZ predominates over the PZ. These results are consistent with the well-recognized clinical correlation that symptomatic BPH is variable among men after age 40 yr. The current results corroborate our previous report that TZ volume, as measured by TRUS, increases in men between 50 and 80 yr old. In contrast to previous findings where neither the PZ nor TV increased significantly with age in men between 45 and 80 yr, both PZ and TZ correlated significantly with age in men yr old. Thus, in the current study, the adult relationships between size of zones of the prostate and age can be assessed more completely because of the broader age range. The findings of the association concerning relationships between age and enlargement of the TZ and TV are consistent with published reports on autopsy and TRUS studies of prostate size (10, 11, 24, 25, 36). Although autopsy studies did not selectively compare the TZ volume with the total or PZ volume, they have established that total prostate size increases, but not in all men, particularly after age 50 yr (6 8, 25). In men with and without BPH, Greene et al. (11) performed TRUS and observed an increase in the size of the TZ with age, but they did not study the relationship among the zone volumes of the prostate. Partin et al. (14) reported that the volume of prostate tissue removed by transurethral resection for treatment of symptomatic BPH correlated significantly with age. In a cross-sectional study, Jakobsen et al. (12) found the TZ and PZ volumes measured by TRUS began increasing after age 25 yr, but the PZ growth rate was less than for the TZ. Those studies are consistent with the current study finding that PZ volume largely contributes to TV before age 50 yr and TZ after age 50. Long-term serial studies would be required to assess this possibility. The growth of the prostate up to 30 g is explained by the enlargement of both the PZ and TZ, with the PZ predominating over the TZ. As the gland increases above 30 g, the rate of growth of the TZ tends to exceed the PZ. Although age had a profound influence on prostate volume, the relationship of TV and age to TZ and PZ were even higher, indicating the strong influence of both zones of the prostate on TV. The ratio of TZ/PZ showed weaker relationships with TV than the

5 AGE, HORMONES, AND PROSTATE ZONES 575 volumes of the TZ and PZ, suggesting the differential rates of growth of these zones in contributing to TV. The relationship between prostate volume and symptomatic BPH are inconsistent. However, studies of prostate volume and symptoms of BPH have not been related to volumes of zones of the prostate. We found that men with higher AUA symptom scores (32), which are consistent with symptomatic BPH, have greater TZ volume and TV than men without symptomatic BPH. The PZ volumes did not show a relationship with the symptom score. These findings are consistent with the postulate that the growth of the TZ, as men age, results in urinary obstructive symptoms. Hormonal profiles of men with larger prostate volumes do not suggest that androgen excess causes BPH or prostate enlargement before or after age 50. We observed that men with larger prostates have lower serum T and DHT concentrations. A new finding in the current study is that men with lower T, DHT, and SHBG-bound T had larger prostate volumes. Rosner et al. (37) reported that camp formation in BPH tissue, in response to the SHBG-estradiol receptor, was inhibited by T and DHT. Our findings do not support the hypothesis that elevated T or DHT cause excessive prostate growth in aging men, but they may support the postulate that the activity of the SHBG-estradiol receptor increases in men with larger prostates because they have lower concentrations of T or DHT to inhibit the SHBG-estradiol receptor. Further, our observation and those reported elsewhere do not suggest that androgens are unimportant in prostate enlargement of aging men. References 1. Moore RA Benign hypertrophy and carcinoma of the prostate. Occurrence and experimental production in animals. Surgery. 16: Walsh PC Human benign prostatic hyperplasia: etiological considerations. Prog Clin Biol Res. 145: Walsh PC, Harrod MJ, Goldstein JL, et al Familial incomplete male pseudohermaphroditism, type 2, decreased dihydrotestosterone formation in pseudovaginal perineoscrotal hypospadias. N Engl J Med. 291: Ehrlichman RJ, Isaacs JT, Coffey DS Differences in the effects of estradiol on dihydrotestosterone induced prostatic growth of the castrate dog and rat. Invest Urol. 18: Imperato-Mcginley J, Peterson RE, Gantier T, et al Hormonal evaluation of a large kindred with complete androgen insensitivity: evidence of a secondary 5 -reductase deficiency. J Clin Endocrinol Metab. 54: McNeal JE Anatomy of the prostate and morphogenesis of BPH. Prog Clin Biol Res. 145: Berry SJ, Coffey DS, Walsh PC, Ewing LL Development of benign prostatic hyperplasia with age. J Urol. 132: Grover M Statistical study of the etiology of benign hypertrophy of the prostate gland. Johns Hopkins Hospital Report. 21: Isaacs JT Common characteristics of human and canine benign prostatic hyperplasia. In: Kimball FA, Buhl AE, Carter DB, eds. New approaches to the study of benign prostatic hyperplasia. New York: Alan R. Liss, Inc.; Jensen KM, Jorgensen JB, Morgensen P Some clinical aspects of uroflowmetry in elderly males. A population survey. Scand J Urol Nephrol. 20: Greene DR, Egawa S, Hellerstein DK, Scardino PT Sonographic measurements of transition zone of prostate in men with and without benign prostatic hyperplasia. Urology. 36: Jakobsen H, Torp-Pedersen S, Juul N Ultrasonic evaluation of agerelated human prostatic growth and development of benign prostatic hyperplasia. Scand J Urol Nephrol. (suppl) 107: Guess HA Benign prostatic hyperplasia: antecedents and natural history. Epidemiol Rev. 14: Partin AW, Oesterling JE, Epstein JI, et al Influence of age and endocrine factors on the volume of benign prostatic hyperplasia. Urology. 145: Deslypere JP, Vermeulen A Leydig cell function in normal men: effect of age, life-style, residence, diet, and activity. J Clin Endocrinol Metab. 59: Vermeulen A, Verdonck L, Van Der Straeten M, Orie N Capacity of the testosterone-binding globulin in human plasma and influence of specific binding of testosterone on its metabolic clearance rate. J Clin Endocrinol Metab. 29: Vermeulen A, Rubens R, Verdonck L Testosterone secretion and metabolism in male senescence. J Clin Endocrinol Metab. 34: Mirovics JC, Dunlop M, Rennie GC Changes in the pituitary-testicular system with age. Clin Endocrinol (Oxf). 5: Baker HW, Burger DM, de Kretser DM, et al Changes in the pituitarytesticular system with age. Clin Endocrinol (Oxf). 5: Rubin RT, Gouin PR, Lubin A, et al Nocturnal increase of plasma testosterone in men: relation to gonadotropins and prolactin. J Clin Endocrinol Metab. 40: Ohe H, Watanabe H Kinetic analysis of prostatic volume in treating prostatic cancer and its predictability for prognosis. Cancer. 62: Peters CA, Walsh PC The effect of nafarelin acetate, a luteinizinghormone-releasing hormone agent agonist, on benign prostatic hyperplasia. N Engl J Med. 317: Gabrilove JL, Levine AC, Kirschenbaum A, Droller M Effect of longacting gonadotropin-releasing hormone analog (leuprolide) therapy on prostatic size and symptoms in 15 men with benign prostatic hypertrophy. J Clin Endocrinol Metab. 69: Tempany CMC, Partin AW, Zerhouni SJ, et al The influence of finasteride on the volume of the peripheral and periurethral zones of the prostate in men with benign prostatic hyperplasia. Prostate. 22: Bostwick DG, Cooner WH, Denis L, et al The association of benign prostatic hyperplasia and cancer of the prostate. Cancer. [Suppl]70: Meikle AW, Stephenson RA, McWhorter WP, et al Effects of age, sex steroids, and family relationships on volumes of prostate zones in men with and without prostate cancer. Prostate. 26: Woolf CM An investigation of the familial aspects of carcinoma of the prostate. Cancer. 13: Meikle AW, Stanish WM Familial prostatic cancer risk and low testosterone. J Clin Endocrinol Metab. 54: Meikle AW, Stanish WM, Taylor N, et al Familial effects on plasma sex-steroid content in man: testosterone, estradiol and sex hormone-bindingglobulin. Metabolism. 31: Meikle AW, Smith JA, Stringham JD Production, clearance, and metabolism of testosterone in men with prostate cancer. Prostate. 10: Meikle AW, Bishop DT, Stringham JD, West DW Quantitating genetic and nongenetic factors that determine plasma sex-steroid variation in normal male twins. Metabolism. 35: Grayhack JT Benign prostatic hyperplasia: the scope of the problem. Cancer. 70: McWhorter WP, Hernandez AD, Meikle AW, et al A screening study of prostate cancer in high risk families. J Urol. 148: Lukaski HC, Johnson PE, Bolonchuk WW, et al Assessment of fat free mass using bio-electrical impedance measurements of the human body. Am J Clin Nutr. 41: Segal KR, Gutin B, Presta E, et al Estimation of human body composition by electrical impedance methods; a comparative study. J Appl Physiol. 58: Watanabe H Natural history of benign prostatic hypertrophy. Ultrasound Med Biol. 12: Nakhla AM, Ding VDH, Khan MS, et al [Alpha]-Androsta-3,17 -diol is a hormone: stimulation of camp accumulation in human and dog prostate. J Clin Endocrinol Metab. 80:

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