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The Journal of Clinical Endocrinology & Metabolism Vol. 85, No. 9 3276-3282
Copyright © 2000 by The Endocrine Society

Original Studies

Measures of Bioavailable Serum Testosterone and Estradiol and Their Relationships with Muscle Strength, Bone Density, and Body Composition in Elderly Men1

Annewieke W. van den Beld, Frank H. de Jong, Diederick E. Grobbee, Huibert A. P. Pols and Steven W. J. Lamberts

Department of Internal Medicine III (A.W.v.d.B., F.H.d.J., H.A.P.P., S.W.J.L.), Erasmus University Rotterdam, 3015 GD Rotterdam; and Julius Center for Patient Oriented Research (A.W.v.d.B., D.E.G.), Utrecht University Hospital, Utrecht 3584 CX, The Netherlands

Address correspondence and requests for reprints to: Annewieke W. van den Beld, Department of Internal Medicine III, Room D433, University Hospital Dijkzigt, 40 Dr. Molenwaterplein, 3015 GD Rotterdam, The Netherlands. E-mail: vandenbeld{at}inw3.azr.nl

In the present cross-sectional study of 403 independently living elderly men, we tested the hypothesis that the decreases in bone mass, body composition, and muscle strength with age are related to the fall in circulating endogenous testosterone (T) and estrogen concentrations. We compared various measures of the level of bioactive androgen and estrogen to which tissues are exposed.

After exclusion of subjects with severe mobility problems and signs of dementia, 403 healthy men (age, 73–94 yr) were randomly selected from a population-based sample. Total T (TT), free T (FT), estrone (E1), estradiol (E2), and sex hormone-binding globulin (SHBG) were determined by RIA. Levels of non-SHBG-bound T (non-SHBG-T), FT (calc-FT), the TT/SHBG ratio, non-SHBG-bound E2, and free E2 were calculated. Physical characteristics of aging included muscle strength measured using dynamometry, total body bone mineral density (BMD), hip BMD, and body composition, including lean mass and fat mass, measured by dual-energy x-ray absorptiometry.

In this population of healthy elderly men, calc-FT, non-SHBG-T, E1, and E2 (total, free, and non-SHBG bound) decreased significantly with age. T (total and non-SHBG-T) was positively related with muscle strength and total body BMD (for non-SHBG-T, respectively, ß = 1.93 ± 0.52, P < 0.001 and ß = 0.011 ± 0.002, P < 0.001). An inverse association existed between T and fat mass (ß = -0.53 ± 0.15, P < 0.001). Non-SHBG-T and calc-FT were more strongly related to muscle strength, BMD, and fat mass than TT and were also significantly related to hip BMD. E1 and E2 were both positively, independently associated with BMD (for E2, ß = 0.21 ± 0.08, P < 0.01). Non-SHBG-bound E2 was slightly strongly related to BMD than total E2. The positive relation between T and BMD was independent of E2. E1 and E2 were not related with muscle strength or body composition.

In summary, bioavailable T, E1, total E2, and bioavailable E2 all decrease with age in healthy old men. In this cross-sectional study in healthy elderly men, non-SHBG-bound T seems to be the best parameter for serum levels of bioactive T, which seems to play a direct role in the various physiological changes that occur during aging. A positive relation with muscle strength and BMD and a negative relation with fat mass was found. In addition, both serum E1 and E2 seem to play a role in the age-related bone loss in elderly men, although the cross-sectional nature of the study precludes a definitive conclusion. Non-SHBG-bound E2 seems to be the best parameter of serum bioactive E2 in describing its positive relation with BMD.




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W. de Ronde, Y. T. van der Schouw, M. Muller, D. E. Grobbee, L. J. G. Gooren, H. A. P. Pols, and F. H. de Jong
Associations of Sex-Hormone-Binding Globulin (SHBG) with Non-SHBG-Bound Levels of Testosterone and Estradiol in Independently Living Men
J. Clin. Endocrinol. Metab., January 1, 2005; 90(1): 157 - 162.
[Abstract] [Full Text] [PDF]

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 Journals of Gerontology Series A: Biological Sciences and Medical SciencesHome page
H. Blain, A. Vuillemin, A. Blain, F. Guillemin, N. D. Talance, B. Doucet, and C. Jeandel
Age-Related Femoral Bone Loss in Men: Evidence for Hyperparathyroidism and Insulin-Like Growth Factor-1 Deficiency
J. Gerontol. A Biol. Sci. Med. Sci., December 1, 2004; 59(12): 1285 - 1289.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
I. Van Pottelbergh, S. Goemaere, H. Zmierczak, and J. M. Kaufman
Perturbed Sex Steroid Status in Men with Idiopathic Osteoporosis and Their Sons
J. Clin. Endocrinol. Metab., October 1, 2004; 89(10): 4949 - 4953.
[Abstract] [Full Text] [PDF]

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 Am. J. Clin. Nutr.Home page
P. Szulc, F. Duboeuf, F. Marchand, and P. D Delmas
Hormonal and lifestyle determinants of appendicular skeletal muscle mass in men: the MINOS study
Am. J. Clinical Nutrition, August 1, 2004; 80(2): 496 - 503.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
C. Wang, R. Swerdloff, M. Kipnes, A. M. Matsumoto, A. S. Dobs, G. Cunningham, L. Katznelson, T. J. Weber, T. C. Friedman, P. Snyder, et al.
New Testosterone Buccal System (Striant) Delivers Physiological Testosterone Levels: Pharmacokinetics Study in Hypogonadal Men
J. Clin. Endocrinol. Metab., August 1, 2004; 89(8): 3821 - 3829.
[Abstract] [Full Text] [PDF]

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 CirculationHome page
S. Stork, A. W. van den Beld, C. von Schacky, C. E. Angermann, S. W.J. Lamberts, D. E. Grobbee, and M. L. Bots
Carotid Artery Plaque Burden, Stiffness, and Mortality Risk in Elderly Men: A Prospective, Population-Based Cohort Study
Circulation, July 20, 2004; 110(3): 344 - 348.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
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]

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 J. Clin. Endocrinol. Metab.Home page
L. Gennari, L. Masi, D. Merlotti, L. Picariello, A. Falchetti, A. Tanini, C. Mavilia, F. Del Monte, S. Gonnelli, B. Lucani, et al.
A Polymorphic CYP19 TTTA Repeat Influences Aromatase Activity and Estrogen Levels in Elderly Men: Effects on Bone Metabolism
J. Clin. Endocrinol. Metab., June 1, 2004; 89(6): 2803 - 2810.
[Abstract] [Full Text] [PDF]

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 Journals of Gerontology Series A: Biological Sciences and Medical SciencesHome page
S. Asthana, S. Bhasin, R. N. Butler, H. Fillit, J. Finkelstein, S. M. Harman, L. Holstein, S. G. Korenman, A. M. Matsumoto, J. E. Morley, et al.
Masculine Vitality: Pros and Cons of Testosterone in Treating the Andropause
J. Gerontol. A Biol. Sci. Med. Sci., May 1, 2004; 59(5): M461 - M465.
[Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
B. Z. Leder, J. L. Rohrer, S. D. Rubin, J. Gallo, and C. Longcope
Effects of Aromatase Inhibition in Elderly Men with Low or Borderline-Low Serum Testosterone Levels
J. Clin. Endocrinol. Metab., March 1, 2004; 89(3): 1174 - 1180.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
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]

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 J. Clin. Endocrinol. Metab.Home page
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]

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 Journals of Gerontology Series A: Biological Sciences and Medical SciencesHome page
J. E. Morley
Editorial: Sarcopenia Revisited
J. Gerontol. A Biol. Sci. Med. Sci., October 1, 2003; 58(10): M909 - 910.
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 J. Clin. Endocrinol. Metab.Home page
S. Wickman, E. Kajantie, and L. Dunkel
Effects of Suppression of Estrogen Action by the P450 Aromatase Inhibitor Letrozole on Bone Mineral Density and Bone Turnover in Pubertal Boys
J. Clin. Endocrinol. Metab., August 1, 2003; 88(8): 3785 - 3793.
[Abstract] [Full Text] [PDF]

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 Journals of Gerontology Series A: Biological Sciences and Medical SciencesHome page
J. E. Morley
Editorial. Mobility Performance: A High-Tech Test for Geriatricians
J. Gerontol. A Biol. Sci. Med. Sci., August 1, 2003; 58(8): M712 - 714.
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 Journals of Gerontology Series A: Biological Sciences and Medical SciencesHome page
J. E. Morley
The Need for a Men's Health Initiative
J. Gerontol. A Biol. Sci. Med. Sci., July 1, 2003; 58(7): M614 - 617.
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 J. Clin. Endocrinol. Metab.Home page
J. F. Randolph Jr., M. Sowers, E. B. Gold, B. A. Mohr, J. Luborsky, N. Santoro, D. S. McConnell, J. S. Finkelstein, S. G. Korenman, K. A. Matthews, et al.
Reproductive Hormones in the Early Menopausal Transition: Relationship to Ethnicity, Body Size, and Menopausal Status
J. Clin. Endocrinol. Metab., April 1, 2003; 88(4): 1516 - 1522.
[Abstract] [Full Text] [PDF]

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 Journals of Gerontology Series A: Biological Sciences and Medical SciencesHome page
S. H. Tariq MD
KNOWLEDGE ABOUT LOW TESTOSTERONE IN OLDER MEN
J. Gerontol. A Biol. Sci. Med. Sci., April 1, 2003; 58(4): M382 - 383.
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 Arch NeurolHome page
T. den Heijer, M. I. Geerlings, A. Hofman, F. H. de Jong, L. J. Launer, H. A. P. Pols, and M. M. B. Breteler
Higher Estrogen Levels Are Not Associated With Larger Hippocampi and Better Memory Performance
Arch Neurol, February 1, 2003; 60(2): 213 - 220.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
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]

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 Hum ReprodHome page
P. T. Ellison, R. G. Bribiescas, G. R. Bentley, B. C. Campbell, S. F. Lipson, C. Panter-Brick, and K. Hill
Population variation in age-related decline in male salivary testosterone
Hum. Reprod., December 1, 2002; 17(12): 3251 - 3253.
[Abstract] [Full Text] [PDF]

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 Journals of Gerontology Series A: Biological Sciences and Medical SciencesHome page
M. Iannuzzi-Sucich, K. M. Prestwood, and A. M. Kenny
Prevalence of Sarcopenia and Predictors of Skeletal Muscle Mass in Healthy, Older Men and Women
J. Gerontol. A Biol. Sci. Med. Sci., December 1, 2002; 57(12): M772 - 777.
[Abstract] [Full Text] [PDF]

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 Journals of Gerontology Series A: Biological Sciences and Medical SciencesHome page
J. E. Morley, H. M. Perry III, and D. K. Miller
Editorial: Something About Frailty
J. Gerontol. A Biol. Sci. Med. Sci., November 1, 2002; 57(11): M698 - 704.
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 J. Clin. Endocrinol. Metab.Home page
A. E. Hak, J. C. M. Witteman, F. H. de Jong, M. I. Geerlings, A. Hofman, and H. A. P. Pols
Low Levels of Endogenous Androgens Increase the Risk of Atherosclerosis in Elderly Men: The Rotterdam Study
J. Clin. Endocrinol. Metab., August 1, 2002; 87(8): 3632 - 3639.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
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]

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 J AndrolHome page
M. Culty, L. Luo, Z.-X. Yao, H. Chen, V. Papadopoulos, and B. R. Zirkin
Cholesterol Transport, Peripheral Benzodiazepine Receptor, and Steroidogenesis in Aging Leydig Cells
J Androl, May 1, 2002; 23(3): 439 - 447.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
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]

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 Journals of Gerontology Series A: Biological Sciences and Medical SciencesHome page
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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 Clin. Chem.Home page
J. R. Opalka, F.-N. Gellerich, and S. Zierz
Age and Sex Dependency of Carnitine Concentration in Human Serum and Skeletal Muscle
Clin. Chem., December 1, 2001; 47(12): 2150 - 2153.
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 J. Clin. Endocrinol. Metab.Home page
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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