OSTEOPOROSIS IN MEN is a major public health problem
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1 X/04/$15.00/0 The Journal of Clinical Endocrinology & Metabolism 89(12): Printed in U.S.A. Copyright 2004 by The Endocrine Society doi: /jc Estrogens Are Essential for Male Pubertal Periosteal Bone Expansion ROGER BOUILLON, MARIE BEX, DIRK VANDERSCHUEREN,* AND STEVEN BOONEN* Divisions of Endocrinology (R.B., M.B., D.V.) and Geriatric Medicine (S.B.), Katholieke Universiteit Leuven, B-3000 Leuven, Belgium The skeletal response to estrogen therapy was studied in a 17-yr-old boy with congenital aromatase deficiency. As expected, estrogen therapy (1 mg estradiol valeriate/d from age 17 until 20 yr) normalized total and free testosterone and reduced the rate of bone remodeling. Dual-energy x-ray absorptiometry-assessed areal bone mineral density (BMD) of the lumbar spine and femoral neck increased significantly (by 23% and 14%, respectively), but peripheral quantitative computed tomography at the ultradistal radius revealed no gain of either trabecular or cortical volumetric BMD. The increase OSTEOPOROSIS IN MEN is a major public health problem that is associated with significant morbidity, mortality, and economic cost (1). As in women, susceptibility to osteoporosis and osteoporotic fracture in men is determined by skeletal accrual and subsequent bone loss. In both sexes, sex steroids are known to be critically involved in the developing human skeleton, with androgens traditionally assumed to drive the acquisition of bone mass in men. More recently, observations in men with estrogen insensitivity (due to a disruptive mutation in the estrogen receptor- gene or due to estrogen deficiency in the context of congenital aromatase deficiency) have provided evidence for a primary role of estrogens in male skeletal development (2 6). The affected men presented with open epiphyses and continuous growth resulting in tall stature, increased bone remodeling, and reduced bone mineral density (BMD). Administration of estrogen, started at ages yr, induced rapid epiphyseal closure and cessation of linear growth, reduced bone turnover, and increased (areal) bone density (3 6). In all these reports, BMD was assessed by dual-energy x-ray absorptiometry (DXA), providing a two-dimensional areal view of the three-dimensional mineralized mass of bone, but these studies were not designed to address the relative contribution of bone growth vs. changes in true bone density. Moreover, during puberty in men, the impact of estrogen on epiphyseal closure, linear growth, bone size, and/or bone mass may change over time (7). In this study of * D.V. and S.B. contributed equally to this work. Abbreviations: ABMD, Areal bone mineral density; BMAD, bone mineral apparent density; BMC, bone mineral content; BMD, bone mineral density; CSA, cross-sectional area; DXA, dual-energy x-ray absorptiometry; pqct, peripheral quantitative computed tomography; vbmd, volumetric bone mineral density. JCEM is published monthly by The Endocrine Society ( endo-society.org), the foremost professional society serving the endocrine community in areal BMD was thus driven by an increase in bone size. Indeed, longitudinal bone growth (height, 8.5%) and especially cross-sectional area of the radius ( 46%) and cortical thickness ( 12%), as measured by peripheral quantitative computed tomography, increased markedly during estrogen treatment. These findings demonstrate that androgens alone are insufficient, whereas estrogens are essential for the process of pubertal periosteal bone expansion typically associated with the male bone phenotype. (J Clin Endocrinol Metab 89: , 2004) a boy with congenital aromatase deficiency, we report the skeletal response to estrogen treatment at a significantly earlier stage of skeletal development. In addition to DXA measurements at the lumbar spine and femoral neck, bone size and true volumetric BMD (vbmd) were sequentially obtained at the radius, using peripheral quantitative computed tomography (pqct). Case reports Materials and Methods At the age of 16 yr and 4 months, genetic analysis confirmed the diagnosis of aromatase deficiency in our patient. The propositus was evaluated because this mutation had been suspected and subsequently confirmed in his older sister with pubertal failure. Physical examination revealed no gynecomastia or other abnormalities. He weighed 82 kg and was 172 cm tall at the time of diagnosis. Testicular volume and consistency and the degree of virilization were also normal for his age (Tanner stage V). The patient and his sister were of Moroccan descent, and their parents were first cousins. His history was unremarkable except for a congenital hearing loss of 85%, which was also present in his adult brother and a paternal cousin (also a product from a consanguineous marriage). The father of the propositus has less severe decreased hearing as well. The patient did not use any medication, alcohol, or drugs. He had a sedentary lifestyle, as his hearing impairment interfered with an active social life. Genetic analysis and biochemical measurements Genetic analysis of both siblings revealed homozygosity for a C-base deletion in exon 5 of the CYP19 gene, causing a frame-shift mutation that resulted in a truncated, inactive enzyme (8). Their parents and elder brother were heterozygous carriers. Serum concentrations of hormones and osteocalcin were measured by conventional RIAs. Free testosterone was computed as an estimate of biologically available testosterone from its total serum concentrations, SHBG, and albumin (9). Bone density measurements Areal BMD (abmd) of the lumbar spine, femoral neck, and radius (g/cm 2 ) was measured using the DXA QDR 4500a fan beam system (Hologic Inc., Waltham, MA) with a precision error of less than 1%. To
2 6026 J Clin Endocrinol Metab, December 2004, 89(12): Bouillon et al. Estrogens and Periosteal Bone Expansion account for changes in bone size, vbmd was also estimated by calculation of the bone mineral apparent density (BMAD; g/cm 3 ) as previously described (10). Spine BMAD was derived from the following equation: bone mineral content (BMC) Ap 3/2 ; and BMAD of the femoral neck and radius was determined using the following equation: BMC Ap 2 (BMC is the quantity of bone mineral within the scan area, and Ap is the projected area). pqct was performed at the ultradistal radius using Stratec XCT-960 equipment (Stratec GmbH, Pforzheim, Germany). Measurements of vbmd were taken at the 4% point (4% of ulna length proximal to the most proximal site of the radial articular surface). Image processing and the calculation of numerical values were performed using the manufacturer s software. The cross-sectional area (CSA) of the radius was determined after detecting the outer bone contour at a threshold of 280 mg/cm 3. Total vbmd was defined as the mean density of the total cross-section. Trabecular vbmd was determined as the mean density of the 45% central area of the bone s cross-section. The pqct system also yields a parameter called cortical subcortical vbmd, which is usually referred to as cortical vbmd. This represents the mean density in the 55% peripheral bone area. To include a measure of true cortical vbmd, an additional calculation was performed using a cortical threshold of 650 mg/cm 3. Cortical thickness was calculated using a formula assuming a circular ring model for the radius (11). Reproducibility was 1.28% for CSA, 1.72% for total vbmd, 1.02% for trabecular vbmd, and 1.14% for cortical vbmd. Results At the time of diagnosis, serum levels of testosterone (1305 ng/dl; reference range, ng/dl) (45 nmol/liter; range, nmol/liter) and free testosterone (42 ng/dl; reference range, 5 20 ng/dl) (1.46 nmol/liter; range, nmol/liter) were elevated. FSH (8 mu/ml; reference range, 2 10 mu/ml) and LH (8 mu/ml; reference range, 2 10 mu/ml) were in the upper normal range. Serum concentrations of estrone were below the lower normal limit (23 pg/ ml; reference range, pg/ml) (84 pmol/liter; range, pmol/liter), and serum estradiol was undetectable ( 5 pg/ml; reference range, 0 30 pg/ml) ( 18 pmol/liter; range, pmol/liter); serum osteocalcin (132 ng/dl; reference range, ng/dl) (244 pmol/liter; range, pmol/liter) provided evidence for an increased rate of bone remodeling. Despite full pubertal development and supraphysiological levels of total and free testosterone, x-rays of the left wrist and hand revealed open epiphyses and a bone age of only 12 yr (as assessed by roentgenographic standards for bone development by Gruelich and Pyle). At the age of 17 yr, treatment with estradiol valeriate at a daily oral dose of 1 mg was initiated, after obtaining informed consent. Administration of estrogen increased serum estradiol (16 pg/ml) (59 pmol/liter) and normalized total and free testosterone (468 ng/dl and 16 ng/dl, respectively) (16 nmol/liter and 0.55 nmol/liter, respectively), FSH (4.7 mu/ml), and LH (4.4 mu/ml). Serum osteocalcin (88 ng/ml) was significantly reduced as well (values were at 3 yr of estrogen therapy and representative of values obtained during active treatment). During treatment, body height increased by 8.5%, from 176 to 191 cm, and bone age matured from 12 yr and 5 months to 16 yr and 8 months, with near closure of the epiphyses only observed at 20 yr and 5 months of age (Figs. 1 and 2). Table 1 and Fig. 2 show the effect of estrogen therapy on abmd and vbmd. At baseline, lumbar spine and femoral neck BMD were remarkably low. From age 17 yr and 1 month FIG. 1. Growth curve and bone age before and during estrogen administration. to 20 yr and 5 months, during 41 months of estrogen treatment, abmd improved by 23% at the lumbar spine and by 14% at the femoral neck, as assessed by DXA. When these results were expressed as improvements in T scores (sds from the mean in normal young men), lumbar spine abmd increased from 2.31 to 0.55, and femoral neck abmd increased from 0.46 to An increase of BMAD was only observed at the spine (from to g/cm 3 at the spine vs to g/cm 3 at the femoral neck) At one third of the distance from the wrist to the elbow (one third radius site), abmd increased by 15%, and at the ultradistal radius, abmd increased by 18%. In contrast, BMAD at the radius (one third radius site) did not increase (0.255 vs g/cm 3 ). In line with the BMAD data, total vbmd, as assessed by pqct at the ultradistal radius, did not change either ( 4.3%; from 282 to 270 mg/cm 3 during treatment, below the least significant change of 4.8%; Table 1 and Fig. 2). Similarly, no significant changes were observed in trabecular or cortical vbmd (Table 1). Bone size (as determined by the CSA of the radius) increased dramatically by 46%, from 247 to 360 mm 2 ; cortical and trabecular area increased by 34 and 64%, respectively. The increase in cortical thickness was 12%. Discussion Androgens alone are not sufficient for normal skeletal pubertal maturation, as demonstrated by several case reports of men with estrogen insensitivity or deficiency (2 4, 6). In the patient affected by congenital aromatase deficiency presented in this article, we confirm improvements in (DXAassessed) axial and peripheral BMD during treatment with estrogen (3 6). Between the ages of 17 yr and 1 month and 20 yr and 5 months, daily administration of 1 mg of estradiol was associated with an increase in lumbar spine and femoral
3 Bouillon et al. Estrogens and Periosteal Bone Expansion J Clin Endocrinol Metab, December 2004, 89(12): FIG. 2. Changes from baseline in body height, bone size (cross-sectional area), cortical thickness, and total volumetric density (as assessed by pqct at the ultradistal radius) during estrogen administration. The change in total vbmd ( 4.3%) was below the least significant change (LSC). TABLE 1. Effect of estrogen therapy on areal and volumetric bone density Age 17 yr, 1 month 18 yr, 5 months 19 yr, 3 months 20 yr, 5 months Treatment duration (yr, month) 0 1 yr, 4 months 2 yr, 2 months 3 yr, 5 months Bone age (yr, month) 12 yr, 5 months 16 yr, 8 months Height (cm) Weight (kg) DXA Lumbar spine (L1 L4) abmd (g/cm 2 ) T score Area (cm 2 ) BMAD (g/cm 3 ) Femoral neck abmd (g/cm 2 ) T score Area (cm 2 ) BMAD (g/cm 3 ) One third radius abmd (g/cm 2 ) T score Area (cm 2 ) BMAD (g/cm 3 ) Ultradistal radius abmd (g/cm 2 ) T score Area (cm 2 ) pqct at ultradistal radius Cross-sectional area (mm 2 ) Total Cortical Trabecular Cortical thickness (mm) vbmd (g/cm 3 ) Total Cortical NA Cortical and subcortical Trabecular NA, Not applicable. neck BMD of 23 and 14%, respectively. This estrogen dose normalized testosterone, FSH, and LH values and thus represents a physiological replacement dose, which is equivalent to the mg of conjugated estrogens (4) or 50 g of transdermal estrogen (3, 12) used in previous case reports. In osteoporotic women, similar doses of oral and transdermal estrogen have comparable effects on bone density as well (13).
4 6028 J Clin Endocrinol Metab, December 2004, 89(12): Bouillon et al. Estrogens and Periosteal Bone Expansion In men with aromatase deficiency, estrogen treatment has been associated with rapid closure (within 3 6 months) of the initially unfused epiphyses (3, 4, 12), providing compelling evidence that estrogen fuses the epiphyses and terminates male linear growth. Our patient, however, continued linear growth during several years of estrogen therapy, with delayed closure of the epiphyses. This difference probably reflects the significantly younger bone age at which estrogen was initiated (12 yr and 5 months vs. 14 yr and 5 months to 16 yr and 5 months in previously reported cases). Earlier studies in patients with idiopathic delay of puberty already suggested a growth-promoting effect of low-dose estradiol (14), whereas administration of an aromatase inhibitor to patients with familial precocious puberty, a rare disorder associated with a mutation of the LH receptor resulting in adult levels of serum testosterone by the age of 2 yr, decreased growth rate (15). Overall, these findings support the concept that estrogens accelerate pubertal skeletal growth, followed by an estrogen-induced growth-limiting effect through epiphyseal maturation and closure. During treatment with estradiol, bone age increased from 12 yr and 5 months to 16 yr and 8 months after 41 months of estradiol treatment. Along with the maturation of the skeleton, axial and peripheral BMD increased substantially. However, abmd, as assessed by DXA, is a function of both the size of the bone and the true amount of bone within its periosteal envelope (vbmd). In the patient presented here, peripheral vbmd (whether estimated from DXA or directly measured by pqct) did not change significantly during treatment with estradiol. However, bone size (as determined by the CSA of the radius) increased dramatically by approximately 45%, with a concomitant increase in cortical thickness of 12%. The changes observed in our propositus are similar to those associated with normal pubertal growth and support the notion that, in growing bones, except for the spine, true density does not increase (7, 16). As the bone grows in length and diameter, the mass of bone inside the periosteum increases in proportion to the enlarging volume of the whole bone, including the marrow space. During normal growth, vbmd remains constant, but abmd increases due to an increase in external bone size. This increase is a particularly important contributor to bone strength because the resistance of bone to bending or torsional forces is related exponentially to its diameter (17). During normal male puberty, the enlargement of the bone diameter is associated with cortical thickening as a result of accelerated periosteal apposition (with less endocortical expansion). In this process, both the stimulatory effects of androgens and the lack of exposure to the inhibitory effects of estrogen on periosteal apposition are considered to be critical (7, 18, 19). During prepubertal growth, periosteal apposition increases bone width in both sexes. In pubertal males, periosteal diameter continues to expand; however, when females enter puberty, periosteal apposition is inhibited (20). These gender-specific patterns are considered to reflect differences in exposure to endogenous estrogens. However, in our patient, periosteal diameter did not cease to expand in response to estrogen therapy. In fact, CSA of the radius continued to increase during administration of estradiol. In other recent reports of affected men, increases in abmd were reported, but vbmd and bone size were not assessed. The periosteal expansion observed in our patient, without concomitant changes in vbmd, suggests that the estrogen-induced gain in abmd in the context of aromatase deficiency may be primarily driven by an increase in bone size. The enlargement of cortical bone in our patient cannot be explained by estrogen-stimulated endosteal apposition and demonstrates that, in growing men, estrogens stimulate rather than inhibit periosteal apposition. Although the stimulation of linear growth in our patient was generally modest (8.5% during the 41-month treatment period), his increase in bone size was substantial. At cortical sites, such as radius and femoral neck, DXA-assessed total area increased by 18 and 21%, respectively, without a significant change in BMAD. Direct measurements of vbmd using pqct at the radius confirmed that volumetric density was largely unaffected by estrogen treatment. Our observations challenge the traditional view that periosteal expansion of male pubertal bone results only from stimulation of the androgen receptor and lack of inhibitory signals from the estrogen receptor. The present data demonstrate the essential contribution of low-dose estrogen to periosteal pubertal growth, although we acknowledge that an individual case study, by design, does not allow us to elucidate the exact molecular or cellular mechanisms. Androgen action alone, without estrogen receptor activation, appears to be insufficient. Of course, it is possible and might even be likely that combined androgen receptor and estrogen receptor- activation are needed for male pubertal bone expansion. How can these findings be reconciled with the wellestablished gender differences in bone size? A unifying hypothesis could be that estrogens, rather than androgens, are driving periosteal bone apposition, with a biphasic, dosedependent effect of estrogen. Assuming a dose-response relationship between estradiol levels and bone expansion in both sexes, stimulation would occur at low levels, as is the case in males and in early pubertal girls, whereas increasing exposure to higher concentrations of estrogen (as found in late puberty and adulthood in females) would inhibit periosteal growth. This assumption is consistent with both the lifelong slow periosteal bone expansion in males and the resumption of bone expansion after menopause (21 22). Estrogen may induce periosteal bone formation in both sexes through estrogen receptor-, whereas inhibition of periosteal expansion may be primarily an estrogen receptor- effect. Observations of increased periosteal expansion in female estrogen receptor- knockout mice are consistent with this hypothesis (23, 24). Because of the biomechanical importance of the deposition of bone on the periosteal surface, identifying the molecular basis of estrogen actions on periosteal apposition and their potential interaction with local and systemic factors, such as androgens, GH, IGF-I, and PTH, could have major implications for bone physiology and therapy. Estrogens are critically involved in male linear growth, ultimately leading to growth plate closure. From our findings of low-dose estrogen treatment of an adolescent male with congenital aromatase deficiency, we conclude that exposure to estrogens is also essential for the process of pubertal periosteal bone expansion typically associated with the male
5 Bouillon et al. Estrogens and Periosteal Bone Expansion J Clin Endocrinol Metab, December 2004, 89(12): bone phenotype. Androgens alone are insufficient to drive periosteal bone formation. Acknowledgments Received March 30, Accepted September 9, Address all correspondence and requests for reprints to: Roger Bouillon, M.D., Ph.D., Laboratory for Experimental Medicine and Endocrinology, Onderwijs & Navorsing, Campus Gasthuisberg, Herestraat 49, B-3000 Leuven, Belgium. roger.bouillon@med.kuleuven.ac.be. References 1. Orwoll ES 1995 Osteoporosis in men. Endocr Rev 16: Smith EP, Boyd J, Frank GR, Takahashi H, Cohen RM, Specker B, Williams TC, Lubahn DB, Korach KS 1994 Estrogen resistance caused by a mutation in the estrogen-receptor gene in a man. N Engl J Med 331: Carani C, Qin K, Simoni M, Faustini-Fustini M, Serpente S, Boyd J, Korach KS, Simpson ER 1997 Effect of testosterone and estradiol in a man with aromatase deficiency. N Engl J Med 337: Bilezikian JP, Morishima A, Bell J, Grumbacj MM 1998 Increased bone mass as a result of estrogen therapy in a man with aromatase deficiency. N Engl J Med 339: Rochira V, Faustini-Fustini M, Balestrieri A, Carani C 2000 Estrogen replacement therapy in a man with congenital aromatase deficiency: effects of different doses of transdermal estradiol on bone mineral density and hormonal parameters. J Clin Endocrinol Metab 85: Maffei L, Murata Y, Rochira V, Tubert G, Aranda C, Vazquez M, Clyne CD, Davis S, Simpson ER, Carani C 2004 Dysmetabolic syndrome in a man with a novel mutation of the aromatase gene: effects of testosterone, alendronate, and estradiol treatment. J Clin Endocrinol Metab 89: Seeman E 2001 Sexual dimorphism in skeletal size, density, and strength. J Clin Endocrinol Metab 86: Deladoëy J, Flück C, Bex M, Yoshimura N, Harada N, Mullis PE 1999 Aromatase deficiency caused by a novel P450arom gene mutation: impact of absent estrogen production on serum gonadotropin concentration in a boy. J Clin Endocrinol Metab 84: Vermeulen A, Verdonck L, Kaufman JM 1999 A critical evaluation of simple methods for the estimation of free testosterone in serum. J Clin Endocrinol Metab 84: Katzman D, Bachrach L, Carter D, Marcus R 1991 Clinical and anthropometric correlates of bone mineral acquisition in healthy adolescent girls. J Clin Endocrinol Metab 73: Louis O, Boulpaep F, Willnecker J, Van den Winkel P, Osteaux M 1995 Cortical mineral content of the radius assessed by peripheral QCT predicts compressive strength on biomechanical testing. Bone 16: Herrmann BL, Saller B, Janssen OE, Gocke P, Bockisch A, Sperling H, Mann K, Broecker M 2002 Impact of estrogen replacement therapy in a male with congenital aromatase deficiency caused by a novel mutation in the CYP19 gene. J Clin Endocrinol Metab 87: Stevenson JC, Cust MP, Gangar KF, Hillard TC, Lees B, Whitehead MI 1990 Effects of transdermal versus oral hormone replacement therapy on bone density in spine and proximal femur in postmenopausal women. Lancet 336: Caruso-Nicoletti M, Cassorla FG, Skerda MC, Mineghisi T, Cutler GB 1985 Short-term low-dose estradiol accelerates ulnar growth in boys. J Clin Endocrinol Metab 61: Laue L, Kenigsberg D, Pescovitz O, Hench KD, Barnes KM, Loriaux DL, Cutler GB 1989 Treatment of familial precocious puberty with spironolactone and testolactone. N Engl J Med 320: Sundberg M, Gärdsell P, Johnell O, Ornstein E, Karlsson, Serbo I 2003 Pubertal growth in the femoral neck is predominantly characterized by increased bone size and not by increased bone density: a 4-year longitudinal study. Osteoporos Int 14: Turner CH, Burr DB 1993 Basic biomechanical measurements of bone. Bone 14: Orwoll ES 2003 Toward an expanded understanding of the role of the periosteum in skeletal health. J Bone Miner Res 18: Seeman E 2003 Pathogenesis of osteoporosis. J Appl Physiol 95: Garn S 1970 The earlier gain and later loss of cortical bone: nutritional perspectives. Charles C. Thomas, ed. Springfield, IL; Ahlborg HG, Johnell O, Turner CH, Rannevik G, Karlsson MK 2003 Bone loss and bone size after menopause. N Engl J Med 349: Seeman E 2003 Periosteal bone formation a neglected determinant of bone strength. N Engl J Med 349: Windahl SH, Vidal O, Andersson G, Gustafsson JA, Ohlsson C 1999 Increased cortical bone mineral content but unchanged trabecular bone mineral density in female ER (-/-) mice. J Clin Invest 104: Vanderschueren D, Vandenput L, Boonen S, Lindberg MK, Bouillon R, Ohlsson C 2004 Androgens and bone. Endocr Rev 25: JCEM is published monthly by The Endocrine Society ( the foremost professional society serving the endocrine community.
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