Home |
Current Issue |
Past Issues |
In the Clinic |
ACP Journal Club |
CME |
Collections |
Audio/Video |
Mobile |
Subscribe |
Tools |
Help |
ACP Online
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
19 December 2000 | Volume 133 Issue 12 | Pages 951-963
Background: Both hypogonadism and low estrogen levels adversely affect bone health in young men. In elderly men, who are at greatest risk for osteoporotic fracture, the influence of hypogonadism on bone mineral density remains unclear, as does the relative effect of estrogen status compared to hypogonadism.
Objective: To examine the relation of hypogonadism and estrogen status to bone mineral density in elderly men.
Design: Community-based, prospective cohort study.
Setting: Framingham, Massachusetts.
Patients: Male participants of the Framingham Study.
Measurements: Total testosterone, total estradiol, and luteinizing hormone were measured in participants at all four biennial examinations from 1981 to 1989. Values from at least three of four examinations were averaged. Hypogonadism was defined as a mean testosterone level less than 10.4 nmol/L (<3.0 ng/mL) or a mean luteinizing hormone level of 20 IU/L or greater. An alternate definition of hypogonadism based only on a mean testosterone level less than 10.4 nmol/L (<3.0 ng/mL) was also used. In 19881989, bone mineral density was measured at the proximal femur (femoral neck, Ward triangle, and trochanter) and lumbar spine by using dual-photon absorptiometry and at the radial shaft by using single-photon absorptiometry. The association of hypogonadism with bone mineral density was examined with adjustment for confounders, including estradiol levels. A similar model that adjusted for hypogonadism was used to examine the association of estradiol level (ranked as quartiles) with bone mineral density.
Results: Of 448 men with bone mineral density measurements, 405 had evaluable hormone levels (mean age, 75.7 years [range, 68 to 96 years]); 71 (17.5%) of the 405 men were hypogonadal. Bone mineral density at any site did not significantly differ in hypogonadal men compared with eugonadal men (for example, bone mineral density at the femoral neck was 0.89 g/cm2 vs. 0.87 g/cm2, respectively; P > 0.2), even when alternate definitions of hypogonadism were used. In contrast, compared with the lowest estradiol quartile, men with higher estradiol levels had greater mean bone mineral density at all sites (for example, bone mineral density at the femoral neck was 0.84 g/cm2, 0.88 g/cm2, 0.86 g/cm2, and 0.91 g/cm2 from the lowest to the highest estradiol quartile; P for trend = 0.002). The difference in mean bone mineral density between men in the lowest and those in the highest estradiol quartile levels was similar to the effect of 10 years of aging on bone mineral density.
Conclusions: In elderly men, hypogonadism related to aging has little influence on bone mineral density, but serum estradiol levels have a strong and positive association with bone mineral density.
Author and Article Information
From Boston University Multipurpose Arthritis and Musculoskeletal Diseases Center, Boston University School of Medicine, Hebrew Rehabilitation Center for Aged, Research and Training Institute, and Harvard Medical School Division on Aging, Boston, Massachusetts; Veterans Administration Headquarters, Washington, D.C.; and National Heart Lung and Blood Institute's Framingham Heart Study, Framingham, Massachusetts.
Acknowledgments: The authors thank the Framingham cohort and staff; Pamela Bacharach, who performed all sex hormone measurements; and Cherlyn Mercier and Mimi Brodsky, who performed bone mineral density measurements.
Grant Support: This work is from the National Heart, Lung, and Blood Institute's Framingham Heart Study, supported by National Institutes of Health/National Heart, Lung, and Blood Institute contract N01-HC-38038. This work was also supported in part by grants AR20613 and AR/AG41398 from the National Institutes of Health and by the Veterans Administration Research Institute, Boston Veterans Affairs Medical Center. Dr. Amin was supported by a research fellowship awarded by the Arthritis Foundation and, in part, by Merck Frosst Canada, Inc.
Requests for Single Reprints: Shreyasee Amin, MD, FRCP(C), MPH, Division of Rheumatology, Mayo Clinic, 200 First Street SW, Rochester, MN 55905.
Current Author Addresses: Dr. Amin: Division of Rheumatology, Mayo Clinic, 200 First Street SW, Rochester, MN 55905.
Drs. Zhang and Felson: Multipurpose Arthritis and Musculoskeletal Diseases Center, Boston University School of Medicine, 715 Albany Street, A203, Boston, MA 02118.
Dr. Sawin: Department of Veterans Affairs (Room 774y), Veterans Health Administration, Office Medical Inspector (1OMI), 810 Vermont Avenue NW, Washington, DC 20420.
Mr. Evans: Data Coordinating Center, Boston University School of Public Health, 715 Albany Street, T4E, Boston, MA 02118.
Drs. Hannan and Kiel: HRCA Research and Training Institute, Hebrew Rehabilitation Center for Aged, 1200 Centre Street, Boston, MA 02131-1097.
Dr. Wilson: Boston University School of Medicine, 715 Albany Street, A206, Boston, MA 02118.
Author Contributions: Conception and design: S. Amin, Y. Zhang, C.T. Sawin, M.T. Hannan, D.P. Kiel, D.T. Felson.
Analysis and interpretation of the data: S. Amin, Y. Zhang, C.T. Sawin, S.R. Evans, M.T. Hannan, D.P. Kiel, P.W.F. Wilson, D.T. Felson.
Drafting of the article: S. Amin, Y. Zhang, C.T. Sawin, D.T. Felson.
Critical revision of the article for important intellectual content: S. Amin, Y. Zhang, C.T. Sawin, S.R. Evans, M.T. Hannan, D.P. Kiel, P.W.F. Wilson, D.T. Felson.
Final approval of the article: S. Amin, Y. Zhang, C.T. Sawin, S.R. Evans, M.T. Hannan, D.P. Kiel, P.W.F. Wilson, D.T. Felson.
Provision of study materials or patients: C.T. Sawin, P.W.F. Wilson, D.T. Felson.
Statistical expertise: S. Amin, Y. Zhang, S.R. Evans, M.T. Hannan, D.T. Felson.
Obtaining of funding: P.W.F. Wilson, D.T. Felson.
Administrative, technical, or logistic support: C.T. Sawin, S.R. Evans, D.P. Kiel, P.W.F. Wilson.
Collection and assembly of data: S. Amin, C.T. Sawin, S.R. Evans, M.T. Hannan, D.T. Felson. ARTICLE
Association of Hypogonadism and Estradiol Levels with Bone Mineral Density in Elderly Men from the Framingham Study
![]()
Related articles in Annals:
This article has been cited by other articles:
![]() |
S. Khosla, S. Amin, and E. Orwoll Osteoporosis in Men Endocr. Rev., June 1, 2008; 29(4): 441 - 464. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. B. Araujo, T. G. Travison, B. Z. Leder, and J. B. McKinlay Correlations between Serum Testosterone, Estradiol, and Sex Hormone-Binding Globulin and Bone Mineral Density in a Diverse Sample of Men J. Clin. Endocrinol. Metab., June 1, 2008; 93(6): 2135 - 2141. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. Meier, T. V. Nguyen, D. J. Handelsman, C. Schindler, M. M. Kushnir, A. L. Rockwood, A. W. Meikle, J. R. Center, J. A. Eisman, and M. J. Seibel Endogenous Sex Hormones and Incident Fracture Risk in Older Men: The Dubbo Osteoporosis Epidemiology Study Arch Intern Med, January 14, 2008; 168(1): 47 - 54. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. M. Pino, J. M. Rodriguez, S. Rios, P. Astudillo, L. Leiva, G. Seitz, M. Fernandez, and J P. Rodriguez Aromatase activity of human mesenchymal stem cells is stimulated by early differentiation, vitamin D and leptin J. Endocrinol., December 1, 2006; 191(3): 715 - 725. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Wilcox, M. L Carnes, T. D Moon, R. Tobias, H. Baade, E. Stamos, and M. E Elliott Androgen Deprivation in Veterans with Prostate Cancer: Implications for Skeletal Health Ann. Pharmacother., December 1, 2006; 40(12): 2107 - 2114. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Arnlov, M. J. Pencina, S. Amin, B.-H. Nam, E. J. Benjamin, J. M. Murabito, T. J. Wang, P. E. Knapp, R. B. D'Agostino Sr., S. Bhasin, et al. Endogenous sex hormones and cardiovascular disease incidence in men. Ann Intern Med, August 1, 2006; 145(3): 176 - 184. [Abstract] [Full Text] [PDF] |
||||
![]() |
V. J. Wright Osteoporosis in Men J. Am. Acad. Ortho. Surg., June 1, 2006; 14(6): 347 - 353. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. P. Bilezikian What's Good for the Goose's Skeleton is Good for the Gander's Skeleton. J. Clin. Endocrinol. Metab., April 1, 2006; 91(4): 1223 - 1225. [Full Text] [PDF] |
||||
![]() |
V Rochira, A Balestrieri, B Madeo, L Zirilli, A R M Granata, and C Carani Osteoporosis and male age-related hypogonadism: role of sex steroids on bone (patho)physiology Eur. J. Endocrinol., February 1, 2006; 154(2): 175 - 185. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. L. Greenspan, P. Coates, S. M. Sereika, J. B. Nelson, D. L. Trump, and N. M. Resnick Bone Loss after Initiation of Androgen Deprivation Therapy in Patients with Prostate Cancer J. Clin. Endocrinol. Metab., December 1, 2005; 90(12): 6410 - 6417. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. M. Kaufman and A. Vermeulen The Decline of Androgen Levels in Elderly Men and Its Clinical and Therapeutic Implications Endocr. Rev., October 1, 2005; 26(6): 833 - 876. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Mueller, R. Dittrich, H. Binder, W. Kuehnel, T. Maltaris, I. Hoffmann, and M. W Beckmann High dose estrogen treatment increases bone mineral density in male-to-female transsexuals receiving gonadotropin-releasing hormone agonist in the absence of testosterone Eur. J. Endocrinol., July 1, 2005; 153(1): 107 - 113. [Abstract] [Full Text] [PDF] |
||||
![]() |
V.-V. Valimaki, H. Alfthan, K. K. Ivaska, E. Loyttyniemi, K. Pettersson, U.-H. Stenman, and M. J. Valimaki Serum Estradiol, Testosterone, and Sex Hormone-Binding Globulin as Regulators of Peak Bone Mass and Bone Turnover Rate in Young Finnish Men J. Clin. Endocrinol. Metab., August 1, 2004; 89(8): 3785 - 3789. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. W. Goderie-Plomp, M. van der Klift, W. de Ronde, A. Hofman, F. H. de Jong, and H. A. P. Pols Endogenous Sex Hormones, Sex Hormone-Binding Globulin, and the Risk of Incident Vertebral Fractures in Elderly Men and Women: The Rotterdam Study J. Clin. Endocrinol. Metab., July 1, 2004; 89(7): 3261 - 3269. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Hammond, L. H. Riley III, P. Gailloud, D. A. Nussbaum, M. Watkins, and K. J. Murphy Treatment Considerations for Vertebroplasty in Men AJNR Am. J. Neuroradiol., April 1, 2004; 25(4): 639 - 641. [Abstract] [Full Text] [PDF] |
||||
![]() |
Q. Wang, P. H. F. Nicholson, M. Suuriniemi, A. Lyytikainen, E. Helkala, M. Alen, H. Suominen, and S. Cheng Relationship of Sex Hormones to Bone Geometric Properties and Mineral Density in Early Pubertal Girls J. Clin. Endocrinol. Metab., April 1, 2004; 89(4): 1698 - 1703. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Khosla, B. L. Riggs, E. J. Atkinson, A. L. Oberg, C. Mavilia, F. Del Monte, L. J. Melton III, and M. L. Brandi Relationship of Estrogen Receptor Genotypes to Bone Mineral Density and to Rates of Bone Loss in Men J. Clin. Endocrinol. Metab., April 1, 2004; 89(4): 1808 - 1816. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. E. Nelson, S. K. Grebe, D. J. O'Kane, and R. J. Singh Liquid Chromatography-Tandem Mass Spectrometry Assay for Simultaneous Measurement of Estradiol and Estrone in Human Plasma Clin. Chem., February 1, 2004; 50(2): 373 - 384. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. Maffei, Y. Murata, V. Rochira, G. Tubert, C. Aranda, M. Vazquez, C. D. Clyne, S. Davis, E. R. Simpson, and C. Carani Dysmetabolic Syndrome in a Man with a Novel Mutation of the Aromatase Gene: Effects of Testosterone, Alendronate, and Estradiol Treatment J. Clin. Endocrinol. Metab., January 1, 2004; 89(1): 61 - 70. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. Szulc, B. Claustrat, F. Marchand, and P. D. Delmas Increased Risk of Falls and Increased Bone Resorption in Elderly Men with Partial Androgen Deficiency: The MINOS Study J. Clin. Endocrinol. Metab., November 1, 2003; 88(11): 5240 - 5247. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. Gennari, D. Merlotti, G. Martini, S. Gonnelli, B. Franci, S. Campagna, B. Lucani, N. Dal Canto, R. Valenti, C. Gennari, et al. Longitudinal Association between Sex Hormone Levels, Bone Loss, and Bone Turnover in Elderly Men J. Clin. Endocrinol. Metab., November 1, 2003; 88(11): 5327 - 5333. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. A. Anderson, A. M. Wallace, N. Sattar, N. Kumar, and K. Sundaram Evidence for Tissue Selectivity of the Synthetic Androgen 7{alpha}-Methyl-19-Nortestosterone in Hypogonadal Men J. Clin. Endocrinol. Metab., June 1, 2003; 88(6): 2784 - 2793. [Abstract] [Full Text] [PDF] |
||||
![]() |
F. M. Cicuttini, A. Wluka, M. Bailey, R. O'Sullivan, C. Poon, S. Yeung, and P. R. Ebeling Factors affecting knee cartilage volume in healthy men Rheumatology, February 1, 2003; 42(2): 258 - 262. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. Z. Leder, K. M. LeBlanc, D. A. Schoenfeld, R. Eastell, and J. S. Finkelstein Differential Effects of Androgens and Estrogens on Bone Turnover in Normal Men J. Clin. Endocrinol. Metab., January 1, 2003; 88(1): 204 - 210. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Compston Local Biosynthesis of Sex Steroids in Bone J. Clin. Endocrinol. Metab., December 1, 2002; 87(12): 5398 - 5400. [Full Text] [PDF] |
||||
![]() |
D. C. Bauer and E. Orwoll Quality Indicators for Management of Osteoporosis Ann Intern Med, October 1, 2002; 137(7): 621 - 622. [Full Text] [PDF] |
||||
![]() |
S P Tuck and R M Francis Osteoporosis Postgrad. Med. J., September 1, 2002; 78(923): 526 - 532. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. Luboshitzky, A. Aviv, A. Hefetz, P. Herer, Z. Shen-Orr, L. Lavie, and P. Lavie Decreased Pituitary-Gonadal Secretion in Men with Obstructive Sleep Apnea J. Clin. Endocrinol. Metab., July 1, 2002; 87(7): 3394 - 3398. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. L. Riggs, S. Khosla, and L. J. Melton III Sex Steroids and the Construction and Conservation of the Adult Skeleton Endocr. Rev., June 1, 2002; 23(3): 279 - 302. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Khosla, L. J. Melton III, and B. L. Riggs Estrogen and the Male Skeleton J. Clin. Endocrinol. Metab., April 1, 2002; 87(4): 1443 - 1450. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. J. Kahn and B. Halloran Dehydroepiandrosterone Supplementation and Bone Turnover in Middle-Aged to Elderly Men J. Clin. Endocrinol. Metab., April 1, 2002; 87(4): 1544 - 1549. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Khosla, E. J. Atkinson, C. R. Dunstan, and W. M. O'Fallon Effect of Estrogen versus Testosterone on Circulating Osteoprotegerin and Other Cytokine Levels in Normal Elderly Men J. Clin. Endocrinol. Metab., April 1, 2002; 87(4): 1550 - 1554. [Abstract] [Full Text] [PDF] |
||||
![]() |
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] |
||||
![]() |
L. Wartofsky Update in Endocrinology Ann Intern Med, October 16, 2001; 135(8_Part_1): 601 - 609. [Full Text] [PDF] |
||||
![]() |
S. Khosla, L. J. Melton III, E. J. Atkinson, and W. M. O'Fallon Relationship of Serum Sex Steroid Levels to Longitudinal Changes in Bone Density in Young Versus Elderly Men J. Clin. Endocrinol. Metab., August 1, 2001; 86(8): 3555 - 3561. [Abstract] [Full Text] [PDF] |
||||
![]() |
Aging, Hypogonadism, and Bone-Mineral Density in Men Journal Watch (General), January 19, 2001; 2001(119): 6 - 6. [Full Text] |
||||
![]() |
R. S. Swerdloff and C. Wang Androgens, Estrogens, and Bone in Men Ann Intern Med, December 19, 2000; 133(12): 1002 - 1004. [Full Text] [PDF] |
||||