{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,4]],"date-time":"2026-06-04T11:10:23Z","timestamp":1780571423504,"version":"3.54.1"},"reference-count":62,"publisher":"The Endocrine Society","issue":"10","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[1999,10,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>The extent to which changes in several hormonal and biochemical parameters are involved in the pathogenesis of osteoporosis in men remains controversial. This study examined the roles of free testosterone (T), estradiol (E2), sex hormone-binding globulin (SHBG), 25-hydroxyvitamin D, PTH, and insulin-like growth factor I in the determination of bone mineral density (BMD) in 437 community-dwelling elderly men. Age, height, weight, quadriceps strength, and femoral neck (FN) and lumbar spine (LS) BMD were also obtained. In multiple regression analysis, after adjusting for age and weight, low E2 (P = 0.01), and high SHBG (P = 0.0002) levels were common determinants of FN and LS BMD. In addition, high PTH (P = 0.03) was an independent predictor of FN BMD, and low free T (P = 0.02) was an independent predictor of LS BMD. Low free T was associated with FN BMD in univariate analysis only. The hormonal measurements collectively accounted for 5% and 7% of the age- and weight-adjusted variance of FN and LS BMD, respectively. The sex steroids, SHBG and insulin-like growth-I were found to be interrelated using a technique of path analysis that examines the intercorrelation between these variables. A subject with any one abnormal serum parameter had a 4-fold increase in the risk of osteoporosis, whereas three abnormal parameters were associated with an 11-fold increased risk, although the latter group only applied to 1% of the study population. Although the precise causal effects these biochemical parameters may have on the development of osteoporosis remains to be determined, the present findings support an important interrelated role for these hormonal and biochemical parameters on changes in bone density in elderly men.<\/jats:p>","DOI":"10.1210\/jcem.84.10.6051","type":"journal-article","created":{"date-parts":[[2014,1,8]],"date-time":"2014-01-08T17:03:58Z","timestamp":1389200638000},"page":"3626-3635","source":"Crossref","is-referenced-by-count":4,"title":["Hormonal and Biochemical Parameters in the Determination of Osteoporosis in Elderly Men*"],"prefix":"10.1210","volume":"84","author":[{"given":"Jacqueline R.","family":"Center","sequence":"first","affiliation":[{"name":"Bone and Mineral Research Program, Garvan Institute of Medical Research (J.R.C., T.V.N., J.A.E.), Sydney, New South Wales 2010"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tuan V.","family":"Nguyen","sequence":"additional","affiliation":[{"name":"Bone and Mineral Research Program, Garvan Institute of Medical Research (J.R.C., T.V.N., J.A.E.), Sydney, New South Wales 2010"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Philip N.","family":"Sambrook","sequence":"additional","affiliation":[{"name":"University of Sydney, Royal North Shore Hospital (P.N.S.), St. Leonards, Sydney 2065, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"John A.","family":"Eisman","sequence":"additional","affiliation":[{"name":"Bone and Mineral Research Program, Garvan Institute of Medical Research (J.R.C., T.V.N., J.A.E.), Sydney, New South Wales 2010"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"80","reference":[{"key":"2020071613390269600_R1","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1007\/BF01623352","article-title":"Symptomatic fracture incidence in elderly men and women: the Dubbo Osteoporosis Epidemiology Study (DOES).","volume":"4","author":"Jones","year":"1994","journal-title":"Osteoporosis Int"},{"key":"2020071613390269600_R2","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1007\/BF02555245","article-title":"Secular trends in the incidence of hip fractures.","volume":"41","author":"Melton","year":"1987","journal-title":"Calcif Tissue Int"},{"key":"2020071613390269600_R3"},{"key":"2020071613390269600_R4","doi-asserted-by":"crossref","first-page":"878","DOI":"10.1016\/S0140-6736(98)09075-8","article-title":"Mortality after all major types of osteoporotic fracture: an observational study.","volume":"353","author":"Center","year":"1999","journal-title":"Lancet"},{"key":"2020071613390269600_R5","doi-asserted-by":"crossref","first-page":"1016","DOI":"10.1210\/jcem-73-5-1016","article-title":"Age, disease, and changing sex hormone levels in middle-aged men: results of the Massachusetts male aging study.","volume":"73","author":"Gray","year":"1991","journal-title":"J Clin Endocrinol Metab"},{"key":"2020071613390269600_R6","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1111\/j.1365-2265.1995.tb02669.x","article-title":"Age related changes in the pituitary-testicular axis in normal men; lower serum testosterone results from decreased bioactive LH drive.","volume":"42","author":"Mitchell","year":"1995","journal-title":"Clin Endocrinol (Oxf)"},{"key":"2020071613390269600_R7","doi-asserted-by":"crossref","first-page":"354","DOI":"10.7326\/0003-4819-106-3-","article-title":"Osteoporosis in men with idiopathic hypogonadotrophic hypogonadism.","volume":"106","author":"Finkelstein","year":"1987","journal-title":"Ann Intern Med"},{"key":"2020071613390269600_R8","doi-asserted-by":"crossref","first-page":"526","DOI":"10.7326\/0003-4819-110-7-526","article-title":"Importance of gonadal steroids to bone mass in men with hyperprolactinemic hyopogonadism.","volume":"110","author":"Greenspan","year":"1989","journal-title":"Ann Intern Med"},{"key":"2020071613390269600_R9","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1093\/ageing\/21.2.139","article-title":"Pathogenesis of vertebral crush fractures in men.","volume":"21","author":"Baillie","year":"1992","journal-title":"Age Ageing"},{"key":"2020071613390269600_R10","doi-asserted-by":"crossref","first-page":"766","DOI":"10.1111\/j.1532-5415.1991.tb02698.x","article-title":"Does hypogonadism contribute to the occurrence of a minimal trauma hip fracture in elderly men?","volume":"39","author":"Stanley","year":"1991","journal-title":"J Am Geriatr Soc"},{"key":"2020071613390269600_R11","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1097\/00000441-199207000-00003","article-title":"Testosterone deficiency as a risk factor for hip fractures in men: a case-control study.","volume":"304","author":"Jackson","year":"1992","journal-title":"Am J Med Sci"},{"key":"2020071613390269600_R12","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1016\/S0169-6009(08)80022-0","article-title":"Sex hormones and bone mineral density in elderly men.","volume":"20","author":"Murphy","year":"1993","journal-title":"Bone Miner"},{"key":"2020071613390269600_R13","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1111\/j.1365-2265.1994.tb03018.x","article-title":"Relations of endogenous anabolic hormones and physical activity to bone mineral density and lean body mass in elderly men.","volume":"40","author":"Rudman","year":"1994","journal-title":"Clin Endocrinol (Oxf)"},{"key":"2020071613390269600_R14","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1007\/BF00675629","article-title":"Lack of association between free testosterone and bone density separate from age in elderly males.","volume":"52","author":"Drinka","year":"1993","journal-title":"Calcif Tissue Int"},{"key":"2020071613390269600_R15","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1111\/j.1532-5415.1987.tb02308.x","article-title":"Marked decline in trabecular bone mineral content in healthy men with age: lack of association with sex steroid levels.","volume":"35","author":"Meier","year":"1987","journal-title":"J Am Geriatr Soc"},{"key":"2020071613390269600_R16","doi-asserted-by":"crossref","first-page":"1056","DOI":"10.1056\/NEJM199410203311604","article-title":"Estrogen resistance caused by a mutation in the estrogen-receptor gene in a man.","volume":"331","author":"Smith","year":"1994","journal-title":"N Engl J Med"},{"key":"2020071613390269600_R17","doi-asserted-by":"crossref","first-page":"1833","DOI":"10.1359\/jbmr.1997.12.11.1833","article-title":"Endogenous sex steroids and bone mineral density in older women and men: the Rancho Bernardo Study.","volume":"12","author":"Greendale","year":"1997","journal-title":"J Bone Miner Res"},{"key":"2020071613390269600_R18","first-page":"2266","article-title":"Relationship of serum sex steriod levels and bone turnover markers with bone mineral density in men and women: a key role for bioavailable estrogen.","volume":"83","author":"Khosla","year":"1998","journal-title":"J Clin Endocrinol Metab"},{"key":"2020071613390269600_R19","doi-asserted-by":"crossref","first-page":"1755","DOI":"10.1172\/JCI119701","article-title":"Sex steroids and bone mass in older men.","volume":"100","author":"Slemenda","year":"1997","journal-title":"J Clin Invest"},{"key":"2020071613390269600_R20"},{"key":"2020071613390269600_R21","doi-asserted-by":"crossref","first-page":"1167","DOI":"10.1359\/jbmr.1998.13.7.1167","article-title":"Hormonal predictors of bone loss in elderly women: a prospective study.","volume":"13","author":"Stone","year":"1998","journal-title":"J Bone Miner Res"},{"key":"2020071613390269600_R22","first-page":"2239","article-title":"Associations between low levels of serum estradiol, bone density, and fractures among elderly women: the Study of Osteoporotic Fractures.","volume":"83","author":"Ettinger","year":"1998","journal-title":"J Clin Endocrinol Metab"},{"key":"2020071613390269600_R23","doi-asserted-by":"crossref","first-page":"733","DOI":"10.1056\/NEJM199809103391104","article-title":"Endogenous hormones and the risk of hip and vertebral fractures among older women.","volume":"339","author":"Cummings","year":"1998","journal-title":"N Engl J Med"},{"key":"2020071613390269600_R24","doi-asserted-by":"crossref","first-page":"915","DOI":"10.1002\/jbmr.5650090617","article-title":"Growth hormone-dependent insulin-like growth factor binding protein is a major determinant of bone mineral density in healthy men.","volume":"9","author":"Johansson","year":"1994","journal-title":"J Bone Miner Res"},{"key":"2020071613390269600_R25","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1111\/j.1365-2796.1993.tb00740.x","article-title":"Decreased serum levels of insulin-like growth factors and IGF binding protein 3 in osteoporosis.","volume":"234","author":"Wu\u0308ster","year":"1993","journal-title":"J Intern Med"},{"key":"2020071613390269600_R26","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1159\/000213811","article-title":"Deficiency of the growth hormone-insulin-like growth factor-1 axis potentially involved in age-related alterations in body composition.","volume":"42","author":"Boonen","year":"1996","journal-title":"Gerontology"},{"key":"2020071613390269600_R27","first-page":"1011","article-title":"Age-related decreases in insulin-like growth factor-1 and transforming growth factor-\u03b2 in femoral cortical bone from both men and women: implications for bone loss with aging.","volume":"78","author":"Nicholas","year":"1994","journal-title":"J Clin Endocrinol Metab"},{"key":"2020071613390269600_R28","doi-asserted-by":"crossref","first-page":"150","DOI":"10.1530\/eje.0.1310150","article-title":"No evidence for reduced spontaneous or growth-hormone-stimulated serum levels of insulin-like growth factor IGF-1, IGF-11 or IGF binding protein 3 in women with spinal osteoporosis.","volume":"131","author":"Kassem","year":"1994","journal-title":"Eur J Endocrinol"},{"key":"2020071613390269600_R29","doi-asserted-by":"crossref","first-page":"1343","DOI":"10.1359\/jbmr.1998.13.8.1343","article-title":"Gender differences in Insulin-like Growth Factor and bone mineral density association in old age: the Rancho Bernardo Study.","volume":"13","author":"Barrett-Connor","year":"1998","journal-title":"J Bone Miner Res"},{"key":"2020071613390269600_R30","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1210\/jcem-64-1-51","article-title":"Effects of sex and age on the 24-hour profile of growth hormone secretion in man: importance of endogenous estradiol concentrations.","volume":"64","author":"Ho","year":"1987","journal-title":"J Clin Endocrinol Metab"},{"key":"2020071613390269600_R31","first-page":"776","article-title":"Testosterone administration increases insulin-like growth factor-1 levels in normal men.","volume":"77","author":"Hobbs","year":"1993","journal-title":"J Clin Endocrinol Metab"},{"key":"2020071613390269600_R32","first-page":"2","article-title":"The dilemma of osteoporosis in men.","volume":"98","year":"1995","journal-title":"Am J Med"},{"key":"2020071613390269600_R33","doi-asserted-by":"crossref","first-page":"755","DOI":"10.1093\/ajcn\/45.4.755","article-title":"Vitamin status in the elderly: seasonal substrate deficiency causes 1,25-dihydroxycholecalciferol deficiency.","volume":"45","author":"Bouillon","year":"1987","journal-title":"Am J Clin Nutr"},{"key":"2020071613390269600_R34","first-page":"494","article-title":"Influence of vitamin D on parathyroid function in the elderly.","volume":"75","author":"Quesada","year":"1992","journal-title":"J Clin Endocrinol Metab"},{"key":"2020071613390269600_R35","first-page":"101","volume":"11","year":"1997"},{"key":"2020071613390269600_R36","first-page":"3487","article-title":"Longitudinal changes in bone mineral density and bone turnover in postmenopausal women with primary hyperparathyroidism.","volume":"81","author":"Guo","year":"1996","journal-title":"J Clin Endocrinol Metab"},{"key":"2020071613390269600_R37","doi-asserted-by":"crossref","first-page":"1177","DOI":"10.1002\/jbmr.5650100806","article-title":"Vitamin D status and sex hormone binding globulin: determinants of bone turnover and bone mineral density in elderly women.","volume":"10","author":"Ooms","year":"1995","journal-title":"J Bone Miner Res"},{"key":"2020071613390269600_R38","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1002\/jbmr.5650110307","article-title":"Increased bone turnover in late postmenopausal women is a major determinant of osteoporosis.","volume":"11","author":"Garnero","year":"1996","journal-title":"J Bone Miner Res"},{"key":"2020071613390269600_R39","doi-asserted-by":"crossref","first-page":"1014","DOI":"10.1093\/ajcn\/36.5.1014","article-title":"Vitamin D and bone health in the elderly.","volume":"36","author":"Parfitt","year":"1982","journal-title":"Am J Clin Nutr"},{"key":"2020071613390269600_R40","first-page":"1522","article-title":"Effects of age and estrogen status on serum parathyroid hormone levels and biochemical markers of bone turnover in women: a population-based study.","volume":"82","author":"Khosla","year":"1997","journal-title":"J Clin Endocrinol Metab"},{"key":"2020071613390269600_R41","doi-asserted-by":"crossref","first-page":"777","DOI":"10.1056\/NEJM199803193381201","article-title":"Hypovitaminosis D in medical inpatients.","volume":"338","author":"Thomas","year":"1998","journal-title":"N Engl J Med"},{"key":"2020071613390269600_R42","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1007\/s001980050030","article-title":"Prevalence of vitamin D insufficiency in an adult normal population.","volume":"7","author":"Chapuy","year":"1997","journal-title":"Osteoporosis Int"},{"key":"2020071613390269600_R43","doi-asserted-by":"crossref","first-page":"783","DOI":"10.1111\/j.1445-5994.1990.tb00423.x","article-title":"The Dubbo study: an Australian prospective community study of the health of the elderly.","volume":"20","author":"Simons","year":"1990","journal-title":"Aust NZ J Med"},{"key":"2020071613390269600_R44","doi-asserted-by":"crossref","first-page":"1339","DOI":"10.1002\/jbmr.5650090904","article-title":"Lifestyle factors and bone density in the elderly: implications for osteoporosis prevention.","volume":"9","author":"Nguyen","year":"1994","journal-title":"J Bone Miner Res"},{"key":"2020071613390269600_R45","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1359\/jbmr.1997.12.1.124","article-title":"Sources of variability in bone mineral density measurements: Implications for study design and analysis of bone loss.","volume":"12","author":"Nguyen","year":"1997","journal-title":"J Bone Miner Res"},{"key":"2020071613390269600_R46","author":"Asher","year":"1988"},{"key":"2020071613390269600_R47","year":"1990"},{"key":"2020071613390269600_R48","doi-asserted-by":"crossref","first-page":"499","DOI":"10.1111\/j.1365-2265.1989.tb01274.x","article-title":"Sex hormone binding globulin in postmenopausal women: a predictor of osteoporosis superior to endogenous oestregens.","volume":"31","author":"Hemert","year":"1989","journal-title":"Clin Endocrinol (Oxf)"},{"key":"2020071613390269600_R49","first-page":"281","article-title":"The impact of gonadal steroid action on growth hormone secretion during childhood and adolescence.","volume":"13","author":"Kerrigan","year":"1992","journal-title":"Endocr Rev"},{"key":"2020071613390269600_R50","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1210\/jcem-58-1-87","article-title":"Effect of testosterone on somatomedin-C levels in prepubertal boys.","volume":"58","author":"Parker","year":"1984","journal-title":"J Clin Endocrinol Metab"},{"key":"2020071613390269600_R51","first-page":"513","article-title":"Estrogen receptor blockade with tamoxifen diminishes growth hormone secretion in boys: evidence for a stimulatory role of endogenous estrogens during male adolescence.","volume":"79","author":"Metzger","year":"1994","journal-title":"J Clin Endocrinol Metab"},{"key":"2020071613390269600_R52","first-page":"1407","article-title":"Activation of the somatotropic axis by testosterone in adult males: evidence for the role of aromatization.","volume":"76","author":"Weissberger","year":"1993","journal-title":"J Clin Endocrinol Metab"},{"key":"2020071613390269600_R53","doi-asserted-by":"crossref","first-page":"733","DOI":"10.1210\/endo-123-2-733","article-title":"Insulin-like growth factor 1 and insulin potentiate luteinizing hormone-induced androgen synthesis by rat ovarian thecal-interstitial cells.","volume":"123","author":"Cara","year":"1988","journal-title":"Endocrinology"},{"key":"2020071613390269600_R54","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1530\/acta.0.1250227","article-title":"Effect of insulin-like growth factor I on gonadotrophin release from hypothalamus-pituitary axis in vitro.","volume":"125","author":"Kanamatsu","year":"1991","journal-title":"Acta Endocrinol (Copenh)"},{"key":"2020071613390269600_R55","first-page":"2534","article-title":"Relationship between circulating insulin-like growth factor components and sex hormones in a population-based sample of 50- to 80-year-old men and women.","volume":"81","author":"Pfeilschifter","year":"1996","journal-title":"J Clin Endocrinol Metab"},{"key":"2020071613390269600_R56","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1016\/0022-4731(89)90272-0","article-title":"On the regulation of sex-hormone-binding globulin\u2013a challenge of an old dogma and outlines of an alternative mechanism.","volume":"32","author":"Schoultz","year":"1989","journal-title":"J Steroid Biochem"},{"key":"2020071613390269600_R57","doi-asserted-by":"crossref","first-page":"1107","DOI":"10.1210\/jcem-65-6-1107","article-title":"High serum sex hormone-binding globulin (SHBG) and non-SHBG-bound testosterone in boys with idiopathic hypopituitarism: effect of recombinant human growth hormone treatment.","volume":"65","author":"Belgorosky","year":"1987","journal-title":"J Clin Endocrinol Metab"},{"key":"2020071613390269600_R58","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1111\/j.1365-2796.1992.tb00550.x","article-title":"Low plasma levels in insulin-like growth factor 1 (IGF-1) in male patients with ideopathic osteoporosis.","volume":"232","author":"Ljunghall","year":"1992","journal-title":"J Intern Med"},{"key":"2020071613390269600_R59","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1007\/BF01623311","article-title":"Calciotropic hormones in elderly people with and without hip fracture.","volume":"5","author":"Benhamou","year":"1995","journal-title":"Osteoporosis Int"},{"key":"2020071613390269600_R60","doi-asserted-by":"crossref","first-page":"164","DOI":"10.1007\/s002239900208","article-title":"Factors associated with cortical and trabecular loss as quantified by peripheral computed tomography (pQCT) at the ultradistal radius in aging women.","volume":"60","author":"Boonen","year":"1997","journal-title":"Calcif Tissue Int"},{"key":"2020071613390269600_R61","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1016\/S0140-6736(95)91266-5","article-title":"Serum vitamin D concentrations among elderly people in Europe.","volume":"346","author":"Wielen","year":"1995","journal-title":"Lancet"},{"key":"2020071613390269600_R62","doi-asserted-by":"crossref","first-page":"1005","DOI":"10.1093\/ajcn\/46.6.1005","article-title":"Determinants of vitamin D status in patients with hip fracture and in elderly control subjects.","volume":"46","author":"Lips","year":"1987","journal-title":"Am J Clin Nutr"}],"container-title":["The Journal of Clinical Endocrinology &amp; Metabolism"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/jcem\/article-pdf\/84\/10\/3626\/9061377\/jcem3626.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/jcem\/article-pdf\/84\/10\/3626\/9061377\/jcem3626.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,7,17]],"date-time":"2020-07-17T00:18:58Z","timestamp":1594945138000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jcem\/article\/84\/10\/3626\/2660627"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[1999,10,1]]},"references-count":62,"journal-issue":{"issue":"10","published-print":{"date-parts":[[1999,10,1]]}},"URL":"https:\/\/doi.org\/10.1210\/jcem.84.10.6051","relation":{},"ISSN":["0021-972X","1945-7197"],"issn-type":[{"value":"0021-972X","type":"print"},{"value":"1945-7197","type":"electronic"}],"subject":[],"published":{"date-parts":[[1999,10,1]]}}}