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Andropause: Clinical Implications of the Decline in Serum Testosterone Levels With Aging in Men

Matsumoto, A. M.·2002·The Journals of Gerontology Series A: Biological Sciences and Medical Sciences

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Abstract

IT is now well accepted that serum testosterone (T) levels decline progressively with aging in men (1)(2)(3)(4)(5). This decline is associated with alterations in body composition; diminished energy, muscle strength, and physical function; reduced sexual function; depressed mood; and decreased cognitive function. Similar changes occur in young men with androgen deficiency and are improved with T replacement therapy. However, the physiological and clinical significance of the aging-associated decline in serum T levels in men is unclear, particularly because T levels may remain within the normal range for young men. From a practical clinical standpoint, it is most appropriate to define “andropause” as an age-related decline in serum T levels in older men to below the normal range in young men that is associated with a clinical syndrome (i.e., symptoms and signs) consistent with androgen deficiency. The decline in T levels is a consequence both of aging per se and age-associated comorbid illnesses and medications that are used to treat them (6)(7)(8)(9)(10)(11)(12)(13). However, regardless of the etiology, androgen deficiency may contribute, at least in part, to age-related decrements in physiological function and may be associated with a clinical syndrome. Andropause has also been referred to by some as “androgen deficiency in the aging male (ADAM),” “partial androgen deficiency in the aging male (PADAM),” or “aging-associated androgen deficiency (AAAD).” The term “male menopause” is inappropriate because there is no interruption or cessation of menses, and “viropause” is inaccurate because there is no loss of virilization. “Male climacteric” refers to the syndrome of endocrine, somatic, and psychic changes that occur in normal men with aging. This term emphasizes the multidimensional nature of age-related changes, including decreases in other hormones such as growth hormone (GH), insulin-like growth factor-1 (IGF-1), dehydroepiandrosterone (DHEA), and melatonin (1)(14)(15)(16)(17), but it does not relate aspects of the male aging syndrome specifically with androgen levels. The term “andropause” is not completely accurate because androgen secretion does not cease altogether. However, because it is the only term that relates the syndrome of age-related physiological changes with the gradual and progressive decline in T levels that occurs with aging, andropause will be used in this review. Andropause is a term also used commonly by experts in the field and by lay persons because it retains some analogy to menopause in women. In both cross-sectional (5)(6)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30)(31)(32)(33)(34)(35)(36)(37)(38) and longitudinal studies (39)(40)(41)(42), beginning in the third decade, aging is associated with a gradual and progressive decline in serum T levels at a rate of approximately 1% per year. As a result, ∼20% of men older than 60 and ∼50% of men older than 80 years of age have serum total T levels below the normal range for young men (39)(43)(44). Circulating T is approximately 98% bound to serum proteins, predominantly to sex hormone-binding globulin (SHBG), the major binding protein for T in blood, and albumin (45)(46)(47). Only 1% to 2% of T in circulation is completely unbound or free. Because T is bound with high affinity (i.e., tightly) to SHBG, SHBG-bound T is not available to most tissues for action. In contrast, T is bound with low affinity (weakly) to albumin, so both albumin-bound and free T are bioavailable to most tissues for action. Because the of with aging, T and bioavailable T albumin-bound decline than total T levels with aging a of older men have levels of of T below the normal range for young men and other alterations in have practical clinical in the of androgen deficiency. Because total T both free T and T bound to and albumin, alterations in albumin in changes in total T levels in the of bioavailable or free T are not by alterations in a of T in blood, in clinical such as aging in or in decreases Because levels with aging, older men with total T levels have free or bioavailable T levels that are below the normal range for young men. of bioavailable or free T or or of total T and are to androgen deficiency in older men. of free and bioavailable T are not in and are only available free T a free T this with by than an of in by or SHBG, and with alterations in levels free T may not clinical that of total T levels. to older men with androgen deficiency and androgen deficiency in men with low levels T levels a not be used in levels may be older The decline in serum T levels with aging is both to of T and secretion of hormone in of hormone secretion by the men a in the of the of the that in T and decreased in T secretion by the in to by of an hormone The of reduced T T levels is by the in of T that also occurs with aging The normal in serum T levels with in the is in older men to young men an in the function. Because of age-related of the normal in T serum T lev

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Kenny, A. M., Prestwood, K. M., Gruman, C. A., Marcello, K. M., & Raisz, L. G. (2001) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/56.5.m266 · Cited by 456
Sex steroids and bone mass in older men. Positive associations with serum estrogens and negative associations with androgens.
Slemenda, C. W., Longcope, C., Zhou, L., Hui, S. L., Peacock, M., & Johnston, C. C. (1997) · Journal of Clinical Investigation · doi:10.1172/jci119701 · Cited by 455 · cited 1×
“In recent studies, a stronger correlation is found between bioavailable E2 levels and BMD and fracture risk than between T and these outcomes, suggesting that the age-related reduction in bioavailable E2 levels may be a more important determinant of bone loss with aging in men than T levels (139,140,306,308,311, 318,3…”
Background
Testosterone replacement therapy improves mood in hypogonadal men--a clinical research center study
Wang, C., Alexander, G. M., Berman, N., Salehian, B., Davidson, T., McDonald, V., Steiner, B., Hull, L., Callegari, C. C., & Swerdloff, R. S. (1996) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.81.10.8855804 · Cited by 455
Influence of some biological indexes on sex hormone-binding globulin and androgen levels in aging or obese males
Vermeulen, A. (1996) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.81.5.1821 · Cited by 455
PROGRESSIVE OSTEOPOROSIS DURING ANDROGEN DEPRIVATION THERAPY FOR PROSTATE CANCER
Daniell, H., Dunn, S., FERGUSON, D. W., LOMAS, G., NIAZI, Z., & Stratte, P. (2000) · The Journal of Urology · doi:10.1016/s0022-5347(05)68000-7 · Cited by 452
Progressive loss of bone in the femoral neck in elderly people: longitudinal findings from the Dubbo osteoporosis epidemiology study
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Effects of Testosterone on Coronary Vasomotor Regulation in Men With Coronary Heart Disease
Webb, C. M., McNeill, J. G., Hayward, C. S., de Zeigler, D., & Collins, P. (1999) · Circulation · doi:10.1161/01.cir.100.16.1690 · Cited by 451
Testosterone supplementation improves spatial and verbal memory in healthy older men
Cherrier, M. M., Asthana, S., Plymate, S. R., Baker, L. D., Matsumoto, A. M., Peskind, E. R., Raskind, M. A., Brodkin, K. I., Bremner, W., Petrova, A., et al. (2001) · Neurology · doi:10.1212/wnl.57.1.80 · Cited by 450
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Polymorphic repeats in the androgen receptor gene: molecular markers of prostate cancer risk.
Stanford, J. L., Just, J. J., Gibbs, M., Wicklund, K. G., Neal, C. L., Blumenstein, B. A., & Ostrander, E. A. (1997) · PubMed · Cited by 447
Relationship of Serum Sex Steroid Levels and Bone Turnover Markers with Bone Mineral Density in Men and Women: A Key Role for Bioavailable Estrogen
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Effects of testosterone replacement on muscle mass and muscle protein synthesis in hypogonadal men--a clinical research center study.
Brodsky, I. G., Balagopal, P., & Nair, K. S. (1996) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.81.10.8855787 · Cited by 444
Risk Factors for Osteoporotic Fractures in Elderly Men
Ngugyen, T. V., Eisman, J. A., Kelly, P. J., & Sambroak, P. N. (1996) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a008920 · Cited by 441
Changes in serum concentrations of conjugated and unconjugated steroids in 40- to 80-year-old men
Bèlanger, A., Candas, B., Dupont, A., Cusan, L., Diamond, P., Gomez, J.-L., & Labrie, F. (1994) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.79.4.7962278 · Cited by 437
Skeletal muscle fiber quality in older men and women
Frontera, W. R., Suh, D., Krivickas, L. S., HUGHES, V. A., Goldstein, R., & Roubenoff, R. (2000) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.2000.279.3.c611 · Cited by 424
Testosterone influences spatial cognition in older men.
Janowsky, J. S., Oviatt, S. K., & ORWOLL, E. S. (1994) · Behavioral Neuroscience · doi:10.1037/0735-7044.108.2.325 · Cited by 424
Castrated Men Exhibit Bone Loss: Effect of Calcitonin Treatment on Biochemical Indices of Bone Remodeling*
Stepan, J. J., Lachman, M., ZVĚŘINA, J., Pacovský, V., & Baylink, D. J. (1989) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-69-3-523 · Cited by 423
The relation of smoking, age, relative weight, and dietary intake to serum adrenal steroids, sex hormones, and sex hormone-binding globulin in middle-aged men.
Field, A. E., Colditz, G. A., Willett, W. C., Longcope, C., & McKinlay, J. B. (1994) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.79.5.7962322 · Cited by 421
Testosterone Deficiency in Young Men: Marked Alterations in Whole Body Protein Kinetics, Strength, and Adiposity
Mauras, N., Hayes, V. Y., Welch, S., Rini, A., Helgeson, K., Dokler, M. L., Veldhuis, J. D., & Urban, R. J. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.6.4892 · Cited by 419
Regulation of Androgen Action
Roy, A. K., Lavrovsky, Y., Song, C., Chen, S., Jung, M. H., Velu, N., Bi, B., & Chatterjee, B. (1998) · Vitamins and hormones · doi:10.1016/s0083-6729(08)60938-3 · Cited by 418
The effect of six months treatment with a 100 mg daily dose of dehydroepiandrosterone (DHEA) on circulating sex steroids, body composition and muscle strength in age-advanced men and women.
Morales, A. J., Haubrich, R. H., Hwang, J. Y., Asakura, H., & Yen, S. S. C. (1998) · Clinical Endocrinology · doi:10.1046/j.1365-2265.1998.00507.x · Cited by 418
Long-term longitudinal measurements of plasma dehydroepiandrosterone sulfate in normal men
Orentreich, N., Brind, J. L., Vogelman, J. H., Andres, R., & Baldwin, H. (1992) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.75.4.1400863 · Cited by 417
Estrogen: Consequences and Implications of Human Mutations in Synthesis and Action
Grumbach, M. M., & Auchus, R. J. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.12.6290 · Cited by 412
Osteoporosis in Men with Idiopathic Hypogonadotropic Hypogonadism
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The association of hypotestosteronemia with coronary artery disease in men.
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Androgens in the Aging Male
Vermeulen, A. (1991) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-73-2-221 · Cited by 384
Pharmacokinetics, Efficacy, and Safety of a Permeation-Enhanced Testosterone Transdermal System in Comparison with Bi-Weekly Injections of Testosterone Enanthate for the Treatment of Hypogonadal Men
Dobs, A. S. (1999) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.84.10.3469 · Cited by 381
Hormonal Changes and Sexual Function in Aging Men*
Davidson, J. M., Chen, J. J., CRAPO, L., Gray, G. D., GREENLEAF, W. J., & Catania, J. A. (1983) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-57-1-71 · Cited by 377
Reproductive hormones in aging men. I. Measurement of sex steroids, basal luteinizing hormone, and Leydig cell response to human chorionic gonadotropin
HARMAN, S. M., & TSITOURAS, P. D. (1980) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-51-1-35 · Cited by 370
Endogenous sex hormones and cardiovascular disease in men. A prospective population-based study.
Barrett-Connor, E. L., & Khaw, K. (1988) · Circulation · doi:10.1161/01.cir.78.3.539 · Cited by 367
Acute Anti-Ischemic Effect of Testosterone in Men With Coronary Artery Disease
Rosano, G. M. C., Leonardo, F., Pagnotta, P., Pelliccia, F., Panina, G., Cerquetani, E., della Monica, P. L., Bonfigli, B., Volpe, M., & Chierchia, S. L. (1999) · Circulation · doi:10.1161/01.cir.99.13.1666 · Cited by 367
Sex Steroids Modify Working Memory
Janowsky, J. S., Chavez, B., & ORWOLL, E. S. (2000) · Journal of Cognitive Neuroscience · doi:10.1162/089892900562228 · Cited by 364
Untitled work
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Longitudinal Relation between Endogenous Testosterone and Cardiovascular Disease Risk Factors in Middle-aged Men: A 13-Year Follow-up of Former Multiple Risk Factor Intervention Trial Participants
Zmuda, J. M., Cauley, J. A., Kriska, A. M., Glynn, N. W., Gutai, J. P., & Kuller, L. H. (1997) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a009326 · Cited by 362
Effects of Androgen on Sexual Behavior in Hypogonadal Men
Davidson, J. M., CAMARGO, C. A., & Smith, E. R. (1979) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-48-6-955 · Cited by 361
Transdermal Testosterone Gel Improves Sexual Function, Mood, Muscle Strength, and Body Composition Parameters in Hypogonadal Men
Wang, C. (2000) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.85.8.2839 · Cited by 359
Aging, Total Body Potassium, Fat-free Mass, and Cell Mass in Males and Females Between Ages 18 and 85 Years
Novâk, L. P. (1972) · Journal of Gerontology · doi:10.1093/geronj/27.4.438 · Cited by 358
Increases in Bone Density During Treatment of Men with Idiopathic Hypogonadotropic Hypogonadism*
Finkelstein, J. S., Klibanski, A., Neer, R. M., Doppelt, S. H., Rosenthal, D. I., Segre, G. V., & Crowley, W. F. (1989) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-69-4-776 · Cited by 354
Men with coronary artery disease have lower levels of androgens than men with normal coronary angiograms
English, K. (2000) · European Heart Journal · doi:10.1053/euhj.1999.1873 · Cited by 350
Attenuated luteinizing hormone (LH) pulse amplitude but normal LH pulse frequency, and its relation to plasma androgens in hypogonadism of obese men
Vermeulen, A. (1993) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.76.5.1140 · Cited by 346
Androgen Treatment of Abdominally Obese Men
Mårin, P., Holmtäng, S., Gustafsson, C., Jönsson, ‡., Kvist, ‡., Elander, A., Eldh, J., Sjöström, L., Holm, G., & Björntorp, P. (1993) · Obesity Research · doi:10.1002/j.1550-8528.1993.tb00618.x · Cited by 345
Osteoporosis in Men
ORWOLL, E. S., & KLEIN, R. F. (1995) · Endocrine Reviews · doi:10.1210/edrv-16-1-87 · Cited by 344
Long-Term Pharmacokinetics of Transdermal Testosterone Gel in Hypogonadal Men 1
Swerdloff, R. S., Wang, C., Cunningham, G. R., Dobs, A. S., Iranmanesh, A., Matsumoto, A. M., Snyder, P. J., Weber, T. J., Longstreth, J. A., & Berman, N. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.12.7045 · Cited by 343
Self-citation
Endogenous Sex Hormones and Cognitive Function in Older Men
Barrett-Connor, E. L., Goodman‐Gruen, D., & Patay, B. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.10.6086 · Cited by 343
Leydig Cell Function in Normal Men: Effect of Age, Life-Style, Residence, Diet, and Activity*
DESLYPERE, J. P., & VERMEULENf, A. (1984) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-59-5-955 · Cited by 343
The nature of androgen action on male sexuality: a combined laboratory-self-report study on hypogonadal men
KWAN, M., GREENLEAF, W. J., MANN, J., CRAPO, L., & DAVIDSON, J. M. (1983) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-57-3-557 · Cited by 339
Transient hypogonadotropic hypogonadism caused by critical illness
WOOLF, P. D., HAMILL, R. W., McDONALD, J. V., LEE, L. A., & KELLY, M. (1985) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-60-3-444 · Cited by 338
Older males secrete luteinizing hormone and testosterone more irregularly, and jointly more asynchronously, than younger males
Pincus, S. M., Mulligan, T., Iranmanesh, A., Gheorghiu, S., Godschalk, M., & Veldhuis, P. P. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.24.14100 · Cited by 337
Prostate volume in testosterone‐treated and untreated hypogonadal men in comparison to age‐matched normal controls
Behre, H. M., Bohmeyer, J., & Nieschlag, E. (1994) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1994.tb03929.x · Cited by 335
Assimilation and mobilization of triglycerides in subcutaneous abdominal and femoral adipose tissue in vivo in men: effects of androgens.
Mårin, P., Odén, B., & Björntorp, P. (1995) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.80.1.7829619 · Cited by 332 · cited 1×
“T treatment inhibited triglyceride uptake and lipoprotein lipase activity in abdominal but not femoral subcutaneous adipose tissue depots (407).”
Background
Outcomes of Long-Term Testosterone Replacement in Older Hypogonadal Males: A Retrospective Analysis
Hajjar, R. R., Kaiser, F. E., & Morley, J. E. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.82.11.4387 · Cited by 324
Sleep Disorders and Aging
Desforges, J. F., Prinz, P. N., Vitiello, M. V., Raskind, M. A., & Thorpy, M. J. (1990) · New England Journal of Medicine · doi:10.1056/nejm199008233230805 · Cited by 323
Low Levels of Sex Hormone-binding Globulin and Testosterone Predict the Development of Non-Insulin-dependent Diabetes Mellitus in Men
Haffner, S. M., Shaten, J., Stem, M. P., Smith, G. D., Kuller, L., & MRFIT Research Group (1996) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a008832 · Cited by 320
IS LOW SERUM FREE TESTOSTERONE A MARKER FOR HIGH GRADE PROSTATE CANCER?
Hoffman, M. A., DeWolf, W. C., & Morgentaler, A. (2000) · The Journal of Urology · doi:10.1016/s0022-5347(05)67812-3 · Cited by 318
Secondary Hypogonadism in Older Men: Its Relation to Impotence*
Korenman, S. G., Morley, J. E., Mooradian, A. D., Davis, S. S., Kaiser, F. E., Silver, A. J., Viosca, S. P., & Garza, D. E. (1990) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-71-4-963 · Cited by 317
An examination of research design effects on the association of testosterone and male aging: Results of a meta-analysis
Gray, A., Berlin, J. A., McKinlay, J. B., & Longcope, C. (1991) · Journal of Clinical Epidemiology · doi:10.1016/0895-4356(91)90028-8 · Cited by 315
Reproductive Functions in Young Fathers and Grandfathers
Nieschlag, E., LAMMERS, U., Freischem, C. W., Langer, K., & Wickings, E. J. (1982) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-55-4-676 · Cited by 312
CHANGES IN THE PITUITARY‐TESTICULAR SYSTEM WITH AGE
Baker, H. W. G., Burger, H., KRETSER, D. M. D., Hudson, B., O'connor, S., Wang, C.-L., MIROVICS, A., Court, J. M., Dunlop, M., & RENNIE, G. C. (1976) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1976.tb01964.x · Cited by 305
Neuroendocrine Dysfunction in Sleep Apnea: Reversal by Continuous Positive Airways Pressure Therapy*
GRUNSTEIN, R. R., HANDELSMAN, D. J., LAWRENCE, S. J., BLACKWELL, C., CATERSON, I. D., & SULLIVAN, C. E. (1989) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-68-2-352 · Cited by 302
Treatment of Male Hypogonadism with Testosterone Enanthate*
Snyder, P. J., & Lawrence, D. A. (1980) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-51-6-1335 · Cited by 299
Risk Factors for Proximal Humerus, Forearm, and Wrist Fractures in Elderly Men and Women The Dubbo Osteoporosis Epidemiology Study
Nguyen, T. V., Sambrook, P. N., & Eisman, J. A. (2001) · American Journal of Epidemiology · doi:10.1093/aje/153.6.587 · Cited by 298
Association of Hypogonadism and Estradiol Levels with Bone Mineral Density in Elderly Men from the Framingham Study
Amin, S., Zhang, Y., Sawin, C. T., Evans, S. R., Hannan, M. T., Kiel, D. P., Wilson, P. W. F., & Felson, D. T. (2000) · Annals of Internal Medicine · doi:10.7326/0003-4819-133-12-200012190-00010 · Cited by 291
Potentially predictive and manipulable blood serum correlates of aging in the healthy human male: Progressive decreases in bioavailable testosterone, dehydroepiandrosterone sulfate, and the ratio of insulin-like growth factor 1 to growth hormone
Morley, J. E., Kaiser, F. E., Raum, W. J., Perry, H. M., Flood, J. F., Jensen, J., Silver, A. J., & Roberts, E. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.14.7537 · Cited by 289
Changes in erectile responsiveness during androgen replacement therapy
Bancroft, J., & Wu, F. C. W. (1983) · Archives of Sexual Behavior · doi:10.1007/bf01542116 · Cited by 288
Lower Endogenous Androgen Levels and Dyslipidemia in Men with Non-Insulin-Dependent Diabetes Mellitus
Barrett-Connor, E. (1992) · Annals of Internal Medicine · doi:10.7326/0003-4819-117-10-807 · Cited by 281
Testosterone, body composition and aging.
Vermeulen, A. T., Goemaere, S., & Kaufman, J. (1999) · PubMed · Cited by 280
Occult Prostate Cancer in Men With Low Serum Testosterone Levels
Morgentaler, A. (1996) · JAMA · doi:10.1001/jama.1996.03540230054035 · Cited by 272
Further Studies on Leydig Cell Function in Old Age
Rubens, R. D., Dhont, M. A., & Vermeulen, A. (1974) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-39-1-40 · Cited by 271
Testosterone concentrations in women and men with NIDDM
Andersson, B., Märin, P., Lissner, L., Vermeulen, A., & Björntorp, P. (1994) · Diabetes Care · doi:10.2337/diacare.17.5.405 · Cited by 268
Bioavailability of Albumin-Bound Testosterone†
Manni, A., Pardridge, W. M., Cefalu, W. T., NISULA, B. C., Bardin, C. W., Santner, S. J., & Santen, R. J. (1985) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-61-4-705 · Cited by 267
Declining testicular function with age
Stearns, E. L., MacDonnell, J. A., Kaufman, B. J., Padua, R., Lucman, T. S., Winter, J. S. D., & Faiman, C. (1974) · The American Journal of Medicine · doi:10.1016/0002-9343(74)90850-x · Cited by 266
Ageing of the Hypothalamo-Pituitary- Testicular Axis in Men
Vermeulen, A., & Kaufman, J. M. (2008) · Hormone Research · doi:10.1159/000184233 · Cited by 265
Effect of the androgen receptor CAG repeat polymorphism on transcriptional activity: specificity in prostate and non-prostate cell lines
Beilin, J., Ball, E., Favaloro, J., & Zajac, J. D. (2000) · Journal of Molecular Endocrinology · doi:10.1677/jme.0.0250085 · Cited by 265
Skin Thickness Changes in Normal Aging Skin
Branchet, M., Boisnic, S., Francès, C., & Robert, A. M. (2009) · Gerontology · doi:10.1159/000213172 · Cited by 263
Does Hypogonadism Contribute to the Occurrence of a Minimal Trauma Hip Fracture in Elderly Men?
Stanley, H. L., Schmitt, B. P., Poses, R. M., & Deiss, W. P. (1991) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.1991.tb02698.x · Cited by 263
Age‐related changes of serum sex hormones, insulin‐like growth factor‐1 and sex‐hormone binding globulin levels in men: cross‐sectional data from a healthy male cohort
Leifke, E., Gorenoi, V., Wichers, C., Von Zur Mühlen, A., Von Büren, E., & Brabant, G. (2000) · Clinical Endocrinology · doi:10.1046/j.1365-2265.2000.01159.x · Cited by 262
Long-Term Pharmacokinetics of Transdermal Testosterone Gel in Hypogonadal Men
Swerdloff, R. S. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.85.12.4500 · Cited by 262
A long-term, prospective study of the physiologic and behavioral effects of hormone replacement in untreated hypogonadal men
BURRIS, A. S., BANKS, S. M., CARTER, C. S., DAVIDSON, J. M., & SHERINS, R. J. (1992) · Journal of Andrology · doi:10.1002/j.1939-4640.1992.tb00319.x · Cited by 259
Body Composition and Aging
Steen, B. C. (2009) · Nutrition Reviews · doi:10.1111/j.1753-4887.1988.tb05386.x · Cited by 259
Sublingual testosterone replacement improves muscle mass and strength, decreases bone resorption, and increases bone formation markers in hypogonadal men--a clinical research center study
Wang, C., Eyre, D. R., Clark, R. V., Kleinberg, D. L., Newman, C. B., Iranmanesh, A., Veldhuis, J. D., Dudley, R. E., Berman, N., Davidson, T., et al. (1996) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.81.10.3654 · Cited by 259
The Response of Metastatic Adenocarcinoma of the Prostate to Exogenous Testosterone
Fowler, J. E., & Whitmore, W. F. (1981) · The Journal of Urology · doi:10.1016/s0022-5347(17)54531-0 · Cited by 259
Sex Hormones and Cognitive Functioning in Men
Christiansen, K., & Knußmann, R. (2008) · Neuropsychobiology · doi:10.1159/000118389 · Cited by 258
Quantification of the Human Sertoli Cell Population: Its Distribution, Relation to Germ Cell Numbers, and Age-Related Decline 1
Johnson, L. W., Zane, R. S., Petty, C. S., & Neaves, W. B. (1984) · Biology of Reproduction · doi:10.1095/biolreprod31.4.785 · Cited by 258
The Effects of Aging in Normal Men on Bioavailable Testosterone and Luteinizing Hormone Secretion: Response to Clomiphene Citrate*
Tenover, J. L., Matsumoto, A. M., Plymate, S. R., & Bremner, W. J. (1987) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-65-6-1118 · Cited by 256
Self-citation
Androgen receptor CAG repeat lengths in prostate cancer: correlation with age of onset
Hardy, D. O., Scher, H. I., Bogenreider, T., Sabbatini, P. J., Zhang, Z., Nanus, D. M., & Catterall, J. F. (1996) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.81.12.8954049 · Cited by 248
Lower endogenous androgens predict central adiposity in men
Khaw, K., & Barrett-Connor, E. L. (1992) · Annals of Epidemiology · doi:10.1016/1047-2797(92)90012-f · Cited by 247
TESTOSTERONE REPLACEMENT IN HYPOGONADAL MEN: EFFECTS ON OBSTRUCTIVE SLEEP APNOEA, RESPIRATORY DRIVES, AND SLEEP
Matsumoto, A. M., Sandblom, R. E., Schoene, R. B., Lee, K. A., Giblin, E. C., Pierson, D. J., & Bremner, W. J. (1985) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1985.tb00161.x · Cited by 246
Self-citation
Metabolic and behavioral effects of high-dose, exogenous testosterone in healthy men
Bagatell, C. J., Heiman, J. R., Matsumoto, A. M., Rivier, J., & Bremner, W. J. (1994) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.79.2.8045977 · Cited by 244
Self-citation
Epidemiology of Geriatric Affective Disorders
Koenig, H. G., & Blazer, D. G. (1992) · Clinics in Geriatric Medicine · doi:10.1016/s0749-0690(18)30476-2 · Cited by 244
Effect of acute testosterone on myocardial ischemia in men with coronary artery disease
Webb, C. M., Adamson, D. L., de Zeigler, D., & Collins, P. D. (1999) · The American Journal of Cardiology · doi:10.1016/s0002-9149(98)00880-7 · Cited by 242
Circadian variation in testosterone, sex hormone-binding globulin, and calculated non-sex hormone-binding globulin bound testosterone in healthy young and elderly men
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Authors: Matsumoto, A. M.
Affiliations: University of Washington (US)
Corresponding author: Matsumoto, A. M.
ORCID: Matsumoto, A. M.
Venue: The Journals of Gerontology Series A: Biological Sciences and Medical Sciences
Publisher: Oxford University Press (OUP)
Published: 2002-02-01
Volume: 57
Issue: 2
Pages: M76-M99
ISSN: 1079-5006 (ISSN-L)
1758-535X
DOI: 10.1093/gerona/57.2.m76
OpenAlex: W2148058581
Cited by: 490
References: 499
Citations by year: 2026: 9 · 2025: 16 · 2024: 14 · 2023: 8 · 2022: 22 · 2021: 15 · 2020: 15 · 2019: 12 · 2018: 19 · 2017: 9 · 2016: 14 · 2015: 17 · 2014: 26 · 2013: 21 · 2012: 29
FWCI: 6.94
Type: journal article
Language: en
Open access: closed
Locations: The Journals of Gerontology Series A (publishedVersion)
PubMed (publishedVersion)
Funders: Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD-12629)
Topics: Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Hormonal and reproductive studies
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Menopause: Health Impacts and Treatments
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adrenal Hormones and Disorders
Keywords: aging, andropause, testosterone replacement therapy, age-related comorbidities, sexual function, body composition, male climacteric, cognitive function, mood, physical function, growth hormone, insulin-like growth factor I, dehydroepiandrosterone, melatonin
MeSH terms: Age Factors, Aged, Climacteric, Clinical Trials as Topic, Humans, Male, Testosterone, Hormone Replacement Therapy

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Andropause: Clinical Implications of the Decline in Serum Testosterone Levels With Aging in Men

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