Association between sex steroid levels and bone microarchitecture in men: The STRAMBO study

Journal of Clinical Endocrinology and Metabolism

Volumn 99, Issue 4, 2014, Pages 1400-1410

  Argoud, Thomas ^a   Boutroy, Stéphanie ^a   Claustrat, Bruno ^a   Chapurlat, Roland ^a   Szulc, Pawel ^a  

^a UNIVERSITÉ DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGED; AGED, 80 AND OVER; AGING; BONE AND BONES; BONE DENSITY; COHORT STUDIES; CROSS-SECTIONAL STUDIES; ESTRADIOL; HUMANS; MALE; MIDDLE AGED; YOUNG ADULT;

EID: 84898411014     PISSN: 0021972X     EISSN: 19457197     Source Type: Journal    
DOI: 10.1210/jc.2013-3233     Document Type: Article

References (54)

1. Hippisley-Cox J, Coupland C. Predicting risk of osteoporotic fracture in men and women in England and Wales: prospective derivation and validation of QFractureScores. BMJ. 2009;339:b4229.
2. Szulc P, Munoz F, Duboeuf F, Marchand F, Delmas PD. Bone mineral density predicts osteoporotic fractures in elderly men: the MINOS study. Osteoporos Int. 2005;16(10):1184-1192.
3. Orwoll ES, Lambert LC, Marshall LM, et al. Testosterone and estradiol among older men. J Clin Endocrinol Metab. 2006;91(4): 1336-1344.
4. Ferrini RL, Barrett-Connor E. Sex hormones and age: a cross-sectional study of testosterone and estradiol and their bioavailable fractions in community-dwelling men. Am J Epidemiol. 1998;147(8): 750-754.
5. Drake MT, Murad MH, Mauck KF, et al. Clinical review. Risk factors for low bone mass-related fractures in men: a systematic review and meta-analysis. J Clin Endocrinol Metab. 2012;97(6): 1861-1870.
6. Barrett-Connor E, Mueller JE, von Muhlen DG, Laughlin GA, Schneider DL, Sartoris DJ. Low levels of estradiol are associated with vertebral fractures in older men, but not women: the Rancho Bernardo Study. J Clin Endocrinol Metab. 2000;85(1):219-223.
7. Amin S, Zhang Y, Felson DT, et al. Estradiol, testosterone, and the risk for hip fractures in elderly men from the Framingham Study. Am JMed. 2006;119(5):426-433.
8. Greendale GA, Edelstein S, Barrett-Connor E. Endogenous sex steroids and bone mineral density in older women and men: the Rancho Bernardo Study. J Bone Miner Res. 1997;12(11):1833-1843.
9. Center JR, Nguyen TV, Sambrook PN, Eisman JA. Hormonal and biochemical parameters in the determination of osteoporosis in elderly men. J Bone Miner Res. 2000;15(7):1405-1411.
10. Khosla S, Melton LJ, Atkinson EJ, O'Fallon WM, Klee GG, Riggs BL. Relationship of serum sex steroid levels and bone turnover markers with bone mineral density in men and women: a key role for bioavailable estrogen. J Clin Endocrinol Metab. 1998;83(7):2266-2274.
11. Szulc P, Munoz F, Claustrat B, et al. Bioavailable estradiol may be an important determinant of osteoporosis in men: the MINOS study. J Clin Endocrinol Metab. 2001;86(1):192-199.
12. Szulc P, Claustrat B, Marchand F, Delmas PD. Increased risk of falls and increased bone resorption in elderly men with partial androgen deficiency: the MINOS study. J Clin Endocrinol Metab. 2003; 88(11):5240-5247.
13. Khosla S, Atkinson EJ, Melton LJ, Riggs BL. Effects of age and estrogen status on serum parathyroid hormone levels and biochemical markers of bone turnover in women: a population-based study. JClin Endocrinol Metab. 1997;82(5):1522-1527.
14. Khosla S, Melton LJ, Atkinson EJ, O'Fallon WM. Relationship of serum sex steroid levels to longitudinal changes in bone density in young versus elderly men. J Clin Endocrinol Metab. 2001;86(8): 3555-3561.
15. Fink HA, Ewing SK, Ensrud KE, et al. Association of testosterone and estradiol deficiency with osteoporosis and rapid bone loss in older men. J Clin Endocrinol Metab 2006;91(10):3908-3915.
16. Ensrud KE, Lewis CE, Lambert LC, et al. Endogenous sex steroids, weight change and rates of hip bone loss in older men: the MrOS study. Osteoporos Int. 2006;17(9):1329-1336.
17. Gennari L, Merlotti D, Martini G, et al. Longitudinal association between sex hormone levels, bone loss, and bone turnover in elderly men. J Clin Endocrinol Metab. 2003;88(11):5327-5333.
18. Falahati-Nini A, Riggs BL, Atkinson EJ, O'Fallon WM, Eastell R, Khosla S. Relative contributions of testosterone and estrogen in regulating bone resorption and formation in normal elderly men. J Clin Invest. 2000;106(12):1553-1560.
19. Leder BZ, LeBlanc KM, Schoenfeld DA, Eastell R, Finkelstein JS. Differential effects of androgens and estrogens on bone turnover in normal men. J Clin Endocrinol Metab. 2003;88(1):204-210.
20. Benito M, Gomberg B, Wehrli FW, etal. Deterioration of trabecular architecture in hypogonadal men. J Clin Endocrinol Metab. 2003; 88:1497-1502.
21. Zhang XH, Liu XS, Vasilic B, et al. In vivo microMRI-based finite element and morphological analyses of tibial trabecular bone in eugonadal and hypogonadal men before and after T treatment. J Bone Miner Res. 2008;23:1426-1434.
22. Szulc P, Uusi-Rasi K, Claustrat B, Marchand B, Beck TJ, Delmas PD. Role of sex steroids in the regulation of bone morphology in men. The MINOS study. Osteoporos Int. 2004;15(11):909-917.
23. Lorentzon M, Swanson C, Andersson N, Mellstrom D, Ohlsson C. Free testosterone is a positive, whereas free estradiol is a negative, predictor of cortical bone size in young Swedish men: the GOOD study. J Bone Miner Res. 2005;20(8):1334-1341.
24. Khosla S, Melton LJ 3rd, Robb RA, et al. Relationship of volumetric BMD and structural parameters at different skeletal sites to sex steroid levels in men. J Bone Miner Res. 2005;20(5):730-740.
25. Khosla S, Melton LJ 3rd, Achenbach SJ, Oberg AL, Riggs BL. Hormonal and biochemical determinants of trabecular microstructure at the ultradistal radius in women and men. J Clin Endocrinol Metab. 2006;91(3):885-891.
26. Bredella MA, Lin E, Gerweck AV, et al. Determinants of bone microarchitecture and mechanical properties in obese men. JClin En-docrinol Metab. 2012;97(11):4115-4122.
27. Lanfranco F, Zirilli L, Baldi M, et al. A novel mutation in the human aromatase gene: insights on the relationship among serum estradiol, longitudinal growth and bone mineral density in an adult man under estrogen replacement treatment. Bone. 2008;43:628-635.
28. Maffei L, Murata Y, Rochira V, et al. Dysmetabolic syndrome in a man with a novel mutation of the aromatase gene: effects of testosterone, alendronate, and estradiol treatment. J Clin Endocrinol Metab. 2004;89:61-70.
29. Herrmann BL, Saller B, Janssen OE, et al. 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. 2002;87:5476-5484.
30. Rochira V, Faustini-Fustini M, Balestrieri A, Carani C. Estrogen replacement therapy in a man with congenital aromatase deficiency: effects of different doses of transdermal estradiol on bone mineral density and hormonal parameters. JClin Endocrinol Metab. 2000; 85:1841-1845.
31. CaraniC, Qin K, Simoni M, et al. Effect of testosterone and estradiol ina man witharomatasedeficiency. NEnglJMed. 1997;337:91-95.
32. Bilezikian JP, Morishima A, Bell J, Grumbach MM. Increased bone mass as a result of estrogen therapy in a man with aromatase deficiency. N Engl J Med. 1998;339:599-603.
33. Rochira V, Zirilli L, Madeo B, et al. Skeletal effects of long-term estrogen and testosterone replacement treatment in a man with congenital aromatase deficiency: evidences of a priming effect of estrogen for sex steroids action on bone. Bone. 2007;40:1662-1668.
34. Vanderschueren D, Venken K, Ophoff J, Bouillon R, Boonen S. Clinical review: sex steroids and the periosteum-reconsidering the roles of androgens and estrogens in periosteal expansion. J Clin Endocrinol Metab. 2006;91:378-382.
35. Bouillon R, Bex M, Vanderschueren D, Boonen S. Estrogens are essential for male pubertal periosteal bone expansion. JClin Endo-crinol Metab. 2004;89:6025-6029.
36. Bradney M, Karlsson MK, Duan Y, Stuckey S, Bass S, Seeman E. Heterogeneity in the growth of the axial and appendicular skeleton in boys: implications for the pathogenesis of bone fragility in men. JBone Miner Res. 2000;15:1871-1878.
37. Chaitou A, Boutroy S, Vilayphiou N, et al. Association between bone turnover rate and bone microarchitecture in men: the STRAMBO study. J Bone Miner Res. 2010;25(11):2313-2323.
38. Szulc P, Hawa G, Boutroy S, et al. Cortical bone status is associated with serum osteoprotegerin concentration in men: the STRAMBO study. J Clin Endocrinol Metab. 2011;96(7):2216-2226.
39. Szulc P, Claustrat B, Munoz F, Marchand F, Delmas PD. Assessment of the role of 17/3-oestradiol in bone metabolism in men: does the assay technique matter? The MINOS study. Clin Endocrinol (Oxf). 2004;61(4):447-457.
40. Boutroy S, Bouxsein ML, Munoz F, Delmas PD. In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. J Clin Endocrinol Metab. 2005;90(12):6508-6515.
41. Szulc P, Delmas PD. Bone width is correlated positively with the upper to the lower segment ratio in elderly men-the MINOS study. Bone. 2007;40:194-199.
42. Szulc P, Boutroy S, Vilayphiou N, Chaitou A, Delmas PD, Chapurlat R. Cross-sectional analysis of the association between fragility fractures and bone microarchitecture in older men: the STRAMBO study. J Bone Miner Res. 2011;26:1358-1367.
43. Mellstrom D, Vandenput L, Mallmin H, et al. Older men with low serum estradiol and high serum SHBG have an increased risk of fractures. J Bone Miner Res. 2008;23:1552-1560.
44. Ward KA, Pye SR, Adams JE, et al. Influence of age and sex steroids on bone density and geometry in middle-aged and elderly European men. Osteoporos Int. 2011;22(5):1513-1523.
45. Lapauw BM, Taes Y, Bogaert V, et al. Serum estradiol is associated with volumetric BMD and modulates the impact of physical activity on bone size at the age of peak bone mass: a study in healthy male siblings. J Bone Miner Res. 2009;24(6):1075-1085.
46. Neu CM, Rauch F, Manz F, Schoenau E. Modeling of cross-sectional bone size, mass and geometry at the proximal radius: a study of normal bone development using peripheral quantitative computed tomography. Osteoporos Int. 2001;12(7):538-547.
47. Nieves JW, Formica C, Ruffing J, et al. Males have larger skeletal size and bone mass than females, despite comparable body size. JBone Miner Res. 2005;20(3):529-535.
48. Cauley JA, Blackwell T, Zmuda JM, et al. Correlates of trabecular and cortical volumetric bone mineral density at the femoral neck and lumbar spine: the osteoporotic fractures in men study (MrOS). J Bone Miner Res. 2010;25(9):1958-1971.
49. LauretaniF, BandinelliS, RussoCR, etal. Correlates of bone quality in older persons. Bone. 2006;39(4):915-921.
50. SeemanE. Pathogenesis of bone fragility in women and men. Lancet. 2002;359:1841-1850.
51. Kawano H, Sato T, Yamada T, et al. Suppressive function of androgen receptor in bone resorption. Proc Natl Acad Sci USA. 2003; 100(16):9416-9421.
52. Colvard DS, Eriksen EF, Keeting PE, et al. Identification of androgen receptors in normal human osteoblast-like cells. Proc Natl Acad Sci USA. 1989;86(3):854-857.
53. Hamilton EJ, Ghasem-Zadeh A, Gianatti E, et al. Structural decay of bone microarchitecture in men with prostate cancer treated with androgen deprivation therapy. JClin Endocrinol Metab. 2010;95: E456-E463.
54. Riffle BW, Henderson WM, Laws SC. Measurement of steroids in rats after exposure to an endocrine disruptor: mass spectrometry and radioimmunoassay demonstrate similar results. J Pharmacol Toxicol Methods. 2013;68:314-322.