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Journal of Clinical Endocrinology & Metabolism Vol. 73, No. 5 1016-1025
doi:10.1210/jcem-73-5-1016
Copyright © 1991 by the Endocrine Society.
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*TESTOSTERONE

Age, Disease, and Changing Sex Hormone Levels in Middle-Aged Men: Results of the Massachusetts Male Aging Study*

ANNA GRAY, HENRY A. FELDMAN, JOHN B. MCKINLAY and CHRISTOPHER LONGCOPE

New England Research Institute Watertown, Massachusetts 02172
the Departments of Obstetrics and Gynecohgy and Medicine, University of Massachusetts Medical Center Worcester, Massachusetts 01655

Address all correspondence and requests for reprints to: Dr. John B. McKinlay, New England Research Institute, 9 Galen Street, Watertown, Massachusetts 02172.

To evaluate the hypothesis that endocrine profiles change with aging independently of specific disease states, we examined the age trends of 17 major sex hormones, metabolites, and related serum proteins in 2 large groups of adult males drawn from the Massachusetts Male Aging Study, a populationbased cross-sectional survey of men aged 39–70 yr conducted in 1986–89. Group 1 consisted of 415 men who were free of obesity, alcoholism, all prescription medication, prostate problems, and chronic illness (cancer, coronary heart disease, hypertension, diabetes, and ulcer). Group 2 consisted of 1294 men who reported 1 or more of the above conditions.

Each age trend was satisfactorily described by a constant percent change per yr between ages 39–70 yr. Free testosterone declined by 1.2%/yr, and albumin-bound testosterone by 1.0%/yr. Sex hormone-binding globulin (SHBG), the major serum carrier of testosterone, increased by 1.2%/yr, with the net effect that total serum testosterone declined more slowly (0.4%/yr) than the free or albumin-bound pools alone.

Among the major androgens and metabolites, androstane-3{alpha},17β-diol (androstanediol; 0.8%/yr) and androstanediol glucuronide (0.6%/yr) declined less rapidly than free testosterone, while 5{alpha}-dihydrotestosterone remained essentially constant between ages 39–70 yr. Androstenedione declined at 1.3%/yr, a rate comparable to that of free testosterone, while the adrenal androgen dehydroepiandrosterone (3.1%/yr) and its sulfate (2.2%/yr) declined 2–3 times more rapidly.

The levels of testosterone, SHBG, and several androgen metabolites followed a parallel course in groups 1 and 2, remaining consistently 10–15% lower in group 2 across the age range of the study. Subgroup analyses suggested that obese subjects might be responsible for much of the group difference in androgen level.

Serum concentrations of estrogens and cortisol did not change significantly with age or differ between groups. Of the pituitary gonadotropins, FSH increased at 1.9%/yr, LH increased at 1.3%/yr, and PRL declined at 0.4%/yr, with no significant difference between groups 1 and 2.

This study provides epidemiological evidence for some hormone age trends that were previously documented only in smaller, uncontrolled, or questionably representative samples. We found no significant difference between healthy men (group 1) and less healthy men (group 2) with respect to the percent rate of change of any of the serum hormone, metabolite, or protein concentrations measured. The 10–15% lower levels of testosterone, SHBG, and some androgen metabolites in the less healthy men, which were maintained between ages 39–70 yr, might be causes, effects, or mere correlates of disease.

* This work was supported by NIH/NIA Grant AG-04673.

Received January 28, 1991.




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Lifestyle Determinants of 5{{alpha}}-Reductase Metabolites in Older African-American, White, and Asian-American Men
Cancer Epidemiol. Biomarkers Prev., May 1, 2001; 10(5): 533 - 538.
[Abstract] [Full Text]


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J. Appl. Physiol.Home page
M. Izquierdo, K. Hakkinen, J. Ibanez, M. Garrues, A. Anton, A. Zuniga, J. L. Larrion, and E. M. Gorostiaga
Effects of strength training on muscle power and serum hormones in middle-aged and older men
J Appl Physiol, April 1, 2001; 90(4): 1497 - 1507.
[Abstract] [Full Text] [PDF]


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Am J EpidemiolHome page
H. A. Feldman, C. B. Johannes, A. B. Araujo, B. A. Mohr, C. Longcope, and J. B. McKinlay
Low Dehydroepiandrosterone and Ischemic Heart Disease in Middle-aged Men: Prospective Results from the Massachusetts Male Aging Study
Am. J. Epidemiol., January 1, 2001; 153(1): 79 - 89.
[Abstract] [Full Text] [PDF]


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JNCI J Natl Cancer InstHome page
E. A. Platz, E. B. Rimm, W. C. Willett, P. W. Kantoff, and E. Giovannucci
Racial Variation in Prostate Cancer Incidence and in Hormonal System Markers Among Male Health Professionals
J Natl Cancer Inst, December 20, 2000; 92(24): 2009 - 2017.
[Abstract] [Full Text] [PDF]


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ANN INTERN MEDHome page
S. Amin, Y. Zhang, C. T. Sawin, S. R. Evans, M. T. Hannan, D. P. Kiel, P. W.F. Wilson, and D. T. Felson
Association of Hypogonadism and Estradiol Levels with Bone Mineral Density in Elderly Men from the Framingham Study
Ann Intern Med, December 19, 2000; 133(12): 951 - 963.
[Abstract] [Full Text] [PDF]


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J. Clin. Endocrinol. Metab.Home page
G. A. Brown, M. D. Vukovich, E. R. Martini, M. L. Kohut, W. D. Franke, D. A. Jackson, and D. S. King
Endocrine Responses to Chronic Androstenedione Intake in 30- to 56-Year-Old Men
J. Clin. Endocrinol. Metab., November 1, 2000; 85(11): 4074 - 4080.
[Abstract] [Full Text]


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J. Clin. Endocrinol. Metab.Home page
G. A. Laughlin and E. Barrett-Connor
Sexual Dimorphism in the Influence of Advanced Aging on Adrenal Hormone Levels: The Rancho Bernardo Study
J. Clin. Endocrinol. Metab., October 1, 2000; 85(10): 3561 - 3568.
[Abstract] [Full Text]


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J. Clin. Endocrinol. Metab.Home page
F. J. Hayes
Testosterone--Fountain of Youth or Drug of Abuse?
J. Clin. Endocrinol. Metab., September 1, 2000; 85(9): 3020 - 3023.
[Full Text]


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J Geriatr Psychiatry NeurolHome page
H. C. Margolese
The Male Menopause and Mood: Testosterone Decline and Depression in the Aging Male--Is There a Link?
J Geriatr Psychiatry Neurol, July 1, 2000; 13(2): 93 - 101.
[Abstract] [PDF]


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Hum ReprodHome page
L. C. Morin-Papunen, I. Vauhkonen, R. M. Koivunen, A. Ruokonen, and J. S. Tapanainen
Insulin sensitivity, insulin secretion, and metabolic and hormonal parameters in healthy women and women with polycystic ovarian syndrome
Hum. Reprod., June 1, 2000; 15(6): 1266 - 1274.
[Abstract] [Full Text] [PDF]


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Cancer Epidemiol. Biomarkers Prev.Home page
A. J. Alberg, G. B. Gordon, S. C. Hoffman, G. W. Comstock, and K. J. Helzlsouer
Serum Dehydroepiandrosterone and Dehydroepiandrosterone Sulfate and the Subsequent Risk of Developing Colon Cancer
Cancer Epidemiol. Biomarkers Prev., May 1, 2000; 9(5): 517 - 521.
[Abstract] [Full Text]


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J. Clin. Endocrinol. Metab.Home page
C. Couillard, J. Gagnon, J. Bergeron, A. S. Leon, D. C. Rao, J. S. Skinner, J. H. Wilmore, J.-P. Després, and C. Bouchard
Contribution of Body Fatness and Adipose Tissue Distribution to the Age Variation in Plasma Steroid Hormone Concentrations in Men: The HERITAGE Family Study
J. Clin. Endocrinol. Metab., March 1, 2000; 85(3): 1026 - 1031.
[Abstract] [Full Text]


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J. Clin. Endocrinol. Metab.Home page
C. Longcope, H. A. Feldman, J. B. McKinlay, and A. B. Araujo
Diet and Sex Hormone-Binding Globulin
J. Clin. Endocrinol. Metab., January 1, 2000; 85(1): 293 - 296.
[Abstract] [Full Text]


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Alcohol AlcoholHome page
H. Iturriaga, X. Lioi, and L. Valladares
SEX HORMONE-BINDING GLOBULIN IN NON-CIRRHOTIC ALCOHOLIC PATIENTS DURING EARLY WITHDRAWAL AND AFTER LONGER ABSTINENCE
Alcohol Alcohol., November 1, 1999; 34(6): 903 - 909.
[Abstract] [Full Text] [PDF]


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CirculationHome page
C. M. Webb, J. G. McNeill, C. S. Hayward, D. de Zeigler, and P. Collins
Effects of Testosterone on Coronary Vasomotor Regulation in Men With Coronary Heart Disease
Circulation, October 19, 1999; 100(16): 1690 - 1696.
[Abstract] [Full Text] [PDF]


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J. Clin. Endocrinol. Metab.Home page
J. D. Veldhuis, Ali Iranmanesh, Thomas Mulligan, and Steven M. Pincus
Disruption of the Young-Adult Synchrony between Luteinizing Hormone Release and Oscillations in Follicle-Stimulating Hormone, Prolactin, and Nocturnal Penile Tumescence (NPT) in Healthy Older Men
J. Clin. Endocrinol. Metab., October 1, 1999; 84(10): 3498 - 3505.
[Abstract] [Full Text] [PDF]


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J. Clin. Endocrinol. Metab.Home page
B. Jin, L. Turner, Z. Zhou, E. L. Zhou, and D. J. Handelsman
Ethnicity and Migration as Determinants of Human Prostate Size
J. Clin. Endocrinol. Metab., October 1, 1999; 84(10): 3613 - 3619.
[Abstract] [Full Text] [PDF]


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J. Clin. Endocrinol. Metab.Home page
J. R. Center, T. V. Nguyen, P. N. Sambrook, and J. A. Eisman
Hormonal and Biochemical Parameters in the Determination of Osteoporosis in Elderly Men
J. Clin. Endocrinol. Metab., October 1, 1999; 84(10): 3626 - 3635.
[Abstract] [Full Text] [PDF]


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J. Appl. Physiol.Home page
W. J. Kraemer, K. Hakkinen, R. U. Newton, B. C. Nindl, J. S. Volek, M. McCormick, L. A. Gotshalk, S. E. Gordon, S. J. Fleck, W. W. Campbell, et al.
Effects of heavy-resistance training on hormonal response patterns in younger vs. older men
J Appl Physiol, September 1, 1999; 87(3): 982 - 992.
[Abstract] [Full Text] [PDF]


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Clin. Chem.Home page
H. M. Perry III
The Endocrinology of Aging
Clin. Chem., August 1, 1999; 45(8): 1369 - 1376.
[Abstract] [Full Text] [PDF]


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J. Clin. Endocrinol. Metab.Home page
W. Arlt, J. Haas, F. Callies, M. Reincke, D. Hübler, M. Oettel, M. Ernst, H. M. Schulte, and B. Allolio
Biotransformation of Oral Dehydroepiandrosterone in Elderly Men: Significant Increase in Circulating Estrogens
J. Clin. Endocrinol. Metab., June 1, 1999; 84(6): 2170 - 2176.
[Abstract] [Full Text]


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J. Clin. Endocrinol. Metab.Home page
E. Barrett-Connor, D. G. von Mühlen, and D. Kritz-Silverstein
Bioavailable Testosterone and Depressed Mood in Older Men: The Rancho Bernardo Study
J. Clin. Endocrinol. Metab., February 1, 1999; 84(2): 573 - 577.
[Abstract] [Full Text]


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J. Clin. Endocrinol. Metab.Home page
S. G. Korenman
VI. A Pragmatic Approach to Androgen Replacement in Older Men: Risks vs. Benefits
J. Clin. Endocrinol. Metab., October 1, 1998; 83(10): 3441 - 3443.
[Full Text]


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J. Clin. Endocrinol. Metab.Home page
S. R. Plymate
III. Which Testosterone Assay Should Be Used In Older Men?1
J. Clin. Endocrinol. Metab., October 1, 1998; 83(10): 3436a - 3438.
[Full Text]


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J. Clin. Endocrinol. Metab.Home page
W. Arlt, H.-G. Justl, F. Callies, M. Reincke, D. Hübler, M. Oettel, M. Ernst, H. M. Schulte, and B. Allolio
Oral Dehydroepiandrosterone for Adrenal Androgen Replacement: Pharmacokinetics and Peripheral Conversion to Androgens and Estrogens in Young Healthy Females after Dexamethasone Suppression
J. Clin. Endocrinol. Metab., June 1, 1998; 83(6): 1928 - 1934.
[Abstract] [Full Text]


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J. Clin. Endocrinol. Metab.Home page
H. M. Behre, S. Kliesch, E. Leifke, T. M. Link, and E. Nieschlag
Long-Term Effect of Testosterone Therapy on Bone Mineral Density in Hypogonadal Men
J. Clin. Endocrinol. Metab., August 1, 1997; 82(8): 2386 - 2390.
[Abstract] [Full Text] [PDF]


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J. Clin. Endocrinol. Metab.Home page
F. Labrie, A. Belanger, L. Cusan, J.-L. Gomez, and B. Candas
Marked Decline in Serum Concentrations of Adrenal C19 Sex Steroid Precursors and Conjugated Androgen Metabolites During Aging
J. Clin. Endocrinol. Metab., August 1, 1997; 82(8): 2396 - 2402.
[Abstract] [Full Text] [PDF]


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J. Clin. Endocrinol. Metab.Home page
O. T. Wolf, O. Neumann, D. H. HELLHAMMER, A. C. Geiben, C. J. Strasburger, R. A. Dressendorfer, K.-M. Pirke, and C. Kirschbaum
Effects of a Two-Week Physiological Dehydroepiandrosterone Substitution on Cognitive Performance and Well-Being in Healthy Elderly Women and Men
J. Clin. Endocrinol. Metab., July 1, 1997; 82(7): 2363 - 2367.
[Abstract] [Full Text] [PDF]


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J. Clin. Endocrinol. Metab.Home page
S. Bhasin and J. S. Tenover
Age-Associated Sarcopenia--Issues in the Use of Testosterone as an Anabolic Agent in Older Men
J. Clin. Endocrinol. Metab., June 1, 1997; 82(6): 1659 - 1660.
[Full Text] [PDF]


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NEJMHome page
C. J. Bagatell and W. J. Bremner
Androgens in Men -- Uses and Abuses
N. Engl. J. Med., March 14, 1996; 334(11): 707 - 715.
[Full Text] [PDF]


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Arterioscler. Thromb. Vasc. Bio.Home page
M. R. Adams, J. K. Williams, and J. R. Kaplan
Effects of Androgens on Coronary Artery Atherosclerosis and Atherosclerosis-Related Impairment of Vascular Responsiveness
Arterioscler Thromb Vasc Biol, May 1, 1995; 15(5): 562 - 570.
[Abstract] [Full Text]




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