Abstract
Male osteoporosis represents an important, although long underestimated, public health problem. Both in men and in women aging is accompanied by continuous bone loss and by an exponential increase in the incidence of osteoporotic fracture, with a female to male incidence ratio of about 2 to 3 to 1 in the elderly for hip and vertebral fractures. Morbidity after osteoporotic fractures appears to be more serious and mortality more common in men than in women. To date, no single treatment has been proved to be effective and safe in published prospective studies. The present report, based on a systematic search of the literature on male osteoporosis, summarises the state of the art on the clinical consequences of male osteoporosis and its risk factors, in relation to the present state of knowledge about female osteoporosis. This constitutes the background for the design of rational clinical development strategies for therapeutic interventions in male osteoporosis. From this review of the literature it is apparent that notwithstanding the existing sex differences in pathophysiology of osteoporosis and the difference in age-specific incidence of osteoporotic fractures, there are also important similarities between osteoporosis in women and men. The higher incidence of fracture in women than in men results from quantitative differences in risk factors rather than from different risk factors. Even though there are sex differences in bone geometry, incidence of fracture seems to be similar in men and women for a same absolute areal bone mineral density. However, the lack of data on the changes in fracture rates in men resulting from pharmacological intervention, leading to changes in bone mineral density or bone turnover, remains the main limitation for extrapolation of established treatment outcomes from women to men.
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- Adachi J. D., Bensen W. G., Brown J., Hanley D., Hodsman A., Josse R., Kendler D. L., Lentle B., Olszynski W., Ste-Marie L. G. Intermittent etidronate therapy to prevent corticosteroid-induced osteoporosis. N Engl J Med. 1997 Aug 7;337(6):382–387. doi: 10.1056/NEJM199708073370603. [DOI] [PubMed] [Google Scholar]
- Baron Y. M., Brincat M., Galea R., Baron A. M. The epidemiology of osteoporotic fractures in a Mediterranean country. Calcif Tissue Int. 1994 May;54(5):365–369. doi: 10.1007/BF00305520. [DOI] [PubMed] [Google Scholar]
- Beck T. J., Ruff C. B., Scott W. W., Jr, Plato C. C., Tobin J. D., Quan C. A. Sex differences in geometry of the femoral neck with aging: a structural analysis of bone mineral data. Calcif Tissue Int. 1992 Jan;50(1):24–29. doi: 10.1007/BF00297293. [DOI] [PubMed] [Google Scholar]
- Behre H. M., Kliesch S., Leifke E., Link T. M., Nieschlag E. Long-term effect of testosterone therapy on bone mineral density in hypogonadal men. J Clin Endocrinol Metab. 1997 Aug;82(8):2386–2390. doi: 10.1210/jcem.82.8.4163. [DOI] [PubMed] [Google Scholar]
- Bengnér U., Johnell O., Redlund-Johnell I. Changes in incidence and prevalence of vertebral fractures during 30 years. Calcif Tissue Int. 1988 May;42(5):293–296. doi: 10.1007/BF02556362. [DOI] [PubMed] [Google Scholar]
- Bilezikian J. P., Morishima A., Bell J., Grumbach M. M. Increased bone mass as a result of estrogen therapy in a man with aromatase deficiency. N Engl J Med. 1998 Aug 27;339(9):599–603. doi: 10.1056/NEJM199808273390905. [DOI] [PubMed] [Google Scholar]
- Black D. M., Cummings S. R., Karpf D. B., Cauley J. A., Thompson D. E., Nevitt M. C., Bauer D. C., Genant H. K., Haskell W. L., Marcus R. Randomised trial of effect of alendronate on risk of fracture in women with existing vertebral fractures. Fracture Intervention Trial Research Group. Lancet. 1996 Dec 7;348(9041):1535–1541. doi: 10.1016/s0140-6736(96)07088-2. [DOI] [PubMed] [Google Scholar]
- Boereboom F. T., Raymakers J. A., de Groot R. R., Duursma S. A. Epidemiology of hip fractures in The Netherlands: women compared with men. Osteoporos Int. 1992 Nov;2(6):279–284. doi: 10.1007/BF01623183. [DOI] [PubMed] [Google Scholar]
- Boonen S., Vanderschueren D., Cheng X. G., Verbeke G., Dequeker J., Geusens P., Broos P., Bouillon R. Age-related (type II) femoral neck osteoporosis in men: biochemical evidence for both hypovitaminosis D- and androgen deficiency-induced bone resorption. J Bone Miner Res. 1997 Dec;12(12):2119–2126. doi: 10.1359/jbmr.1997.12.12.2119. [DOI] [PubMed] [Google Scholar]
- Burger H., Van Daele P. L., Grashuis K., Hofman A., Grobbee D. E., Schütte H. E., Birkenhäger J. C., Pols H. A. Vertebral deformities and functional impairment in men and women. J Bone Miner Res. 1997 Jan;12(1):152–157. doi: 10.1359/jbmr.1997.12.1.152. [DOI] [PubMed] [Google Scholar]
- Burger H., de Laet C. E., van Daele P. L., Weel A. E., Witteman J. C., Hofman A., Pols H. A. Risk factors for increased bone loss in an elderly population: the Rotterdam Study. Am J Epidemiol. 1998 May 1;147(9):871–879. doi: 10.1093/oxfordjournals.aje.a009541. [DOI] [PubMed] [Google Scholar]
- Center J. R., Nguyen T. V., Schneider D., Sambrook P. N., Eisman J. A. Mortality after all major types of osteoporotic fracture in men and women: an observational study. Lancet. 1999 Mar 13;353(9156):878–882. doi: 10.1016/S0140-6736(98)09075-8. [DOI] [PubMed] [Google Scholar]
- Chevalley T., Rizzoli R., Nydegger V., Slosman D., Tkatch L., Rapin C. H., Vasey H., Bonjour J. P. Preferential low bone mineral density of the femoral neck in patients with a recent fracture of the proximal femur. Osteoporos Int. 1991 Jun;1(3):147–154. doi: 10.1007/BF01625444. [DOI] [PubMed] [Google Scholar]
- Clarke B. L., Ebeling P. R., Jones J. D., Wahner H. W., O'Fallon W. M., Riggs B. L., Fitzpatrick L. A. Changes in quantitative bone histomorphometry in aging healthy men. J Clin Endocrinol Metab. 1996 Jun;81(6):2264–2270. doi: 10.1210/jcem.81.6.8964862. [DOI] [PubMed] [Google Scholar]
- Cooper C., Atkinson E. J., Jacobsen S. J., O'Fallon W. M., Melton L. J., 3rd Population-based study of survival after osteoporotic fractures. Am J Epidemiol. 1993 May 1;137(9):1001–1005. doi: 10.1093/oxfordjournals.aje.a116756. [DOI] [PubMed] [Google Scholar]
- Cooper C., Atkinson E. J., O'Fallon W. M., Melton L. J., 3rd Incidence of clinically diagnosed vertebral fractures: a population-based study in Rochester, Minnesota, 1985-1989. J Bone Miner Res. 1992 Feb;7(2):221–227. doi: 10.1002/jbmr.5650070214. [DOI] [PubMed] [Google Scholar]
- Cooper C., Campion G., Melton L. J., 3rd Hip fractures in the elderly: a world-wide projection. Osteoporos Int. 1992 Nov;2(6):285–289. doi: 10.1007/BF01623184. [DOI] [PubMed] [Google Scholar]
- Cummings S. R., Black D. M., Thompson D. E., Applegate W. B., Barrett-Connor E., Musliner T. A., Palermo L., Prineas R., Rubin S. M., Scott J. C. Effect of alendronate on risk of fracture in women with low bone density but without vertebral fractures: results from the Fracture Intervention Trial. JAMA. 1998 Dec 23;280(24):2077–2082. doi: 10.1001/jama.280.24.2077. [DOI] [PubMed] [Google Scholar]
- Davis J. W., Ross P. D., Vogel J. M., Wasnich R. D. Age-related changes in bone mass among Japanese-American men. Bone Miner. 1991 Dec;15(3):227–236. doi: 10.1016/0169-6009(91)90128-m. [DOI] [PubMed] [Google Scholar]
- De Laet C. E., Van Hout B. A., Burger H., Weel A. E., Hofman A., Pols H. A. Hip fracture prediction in elderly men and women: validation in the Rotterdam study. J Bone Miner Res. 1998 Oct;13(10):1587–1593. doi: 10.1359/jbmr.1998.13.10.1587. [DOI] [PubMed] [Google Scholar]
- De Laet C. E., van Hout B. A., Burger H., Hofman A., Pols H. A. Bone density and risk of hip fracture in men and women: cross sectional analysis. BMJ. 1997 Jul 26;315(7102):221–225. doi: 10.1136/bmj.315.7102.221. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Diez A., Puig J., Martinez M. T., Diez J. L., Aubia J., Vivancos J. Epidemiology of fractures of the proximal femur associated with osteoporosis in Barcelona, Spain. Calcif Tissue Int. 1989 Jun;44(6):382–386. doi: 10.1007/BF02555965. [DOI] [PubMed] [Google Scholar]
- Eastell R., Boyle I. T., Compston J., Cooper C., Fogelman I., Francis R. M., Hosking D. J., Purdie D. W., Ralston S., Reeve J. Management of male osteoporosis: report of the UK Consensus Group. QJM. 1998 Feb;91(2):71–92. doi: 10.1093/qjmed/91.2.71. [DOI] [PubMed] [Google Scholar]
- Ebbesen E. N., Thomsen J. S., Beck-Nielsen H., Nepper-Rasmussen H. J., Mosekilde L. Vertebral bone density evaluated by dual-energy X-ray absorptiometry and quantitative computed tomography in vitro. Bone. 1998 Sep;23(3):283–290. doi: 10.1016/s8756-3282(98)00091-x. [DOI] [PubMed] [Google Scholar]
- Ettinger B., Black D. M., Mitlak B. H., Knickerbocker R. K., Nickelsen T., Genant H. K., Christiansen C., Delmas P. D., Zanchetta J. R., Stakkestad J. Reduction of vertebral fracture risk in postmenopausal women with osteoporosis treated with raloxifene: results from a 3-year randomized clinical trial. Multiple Outcomes of Raloxifene Evaluation (MORE) Investigators. JAMA. 1999 Aug 18;282(7):637–645. doi: 10.1001/jama.282.7.637. [DOI] [PubMed] [Google Scholar]
- Ettinger B., Pressman A., Sklarin P., Bauer D. C., Cauley J. A., Cummings S. R. Associations between low levels of serum estradiol, bone density, and fractures among elderly women: the study of osteoporotic fractures. J Clin Endocrinol Metab. 1998 Jul;83(7):2239–2243. doi: 10.1210/jcem.83.7.4708. [DOI] [PubMed] [Google Scholar]
- Falch J. A., Kaastad T. S., Bøhler G., Espeland J., Sundsvold O. J. Secular increase and geographical differences in hip fracture incidence in Norway. Bone. 1993 Jul-Aug;14(4):643–645. doi: 10.1016/8756-3282(93)90086-p. [DOI] [PubMed] [Google Scholar]
- Ferrini R. L., Barrett-Connor E. Sex hormones and age: a cross-sectional study of testosterone and estradiol and their bioavailable fractions in community-dwelling men. Am J Epidemiol. 1998 Apr 15;147(8):750–754. doi: 10.1093/oxfordjournals.aje.a009519. [DOI] [PubMed] [Google Scholar]
- Fujiwara S., Kasagi F., Yamada M., Kodama K. Risk factors for hip fracture in a Japanese cohort. J Bone Miner Res. 1997 Jul;12(7):998–1004. doi: 10.1359/jbmr.1997.12.7.998. [DOI] [PubMed] [Google Scholar]
- Gallagher J. C., Kinyamu H. K., Fowler S. E., Dawson-Hughes B., Dalsky G. P., Sherman S. S. Calciotropic hormones and bone markers in the elderly. J Bone Miner Res. 1998 Mar;13(3):475–482. doi: 10.1359/jbmr.1998.13.3.475. [DOI] [PubMed] [Google Scholar]
- Gillberg P., Johansson A. G., Ljunghall S. Decreased estradiol levels and free androgen index and elevated sex hormone-binding globulin levels in male idiopathic osteoporosis. Calcif Tissue Int. 1999 Mar;64(3):209–213. doi: 10.1007/s002239900604. [DOI] [PubMed] [Google Scholar]
- Gilsanz V., Boechat M. I., Gilsanz R., Loro M. L., Roe T. F., Goodman W. G. Gender differences in vertebral sizes in adults: biomechanical implications. Radiology. 1994 Mar;190(3):678–682. doi: 10.1148/radiology.190.3.8115610. [DOI] [PubMed] [Google Scholar]
- Goldray D., Weisman Y., Jaccard N., Merdler C., Chen J., Matzkin H. Decreased bone density in elderly men treated with the gonadotropin-releasing hormone agonist decapeptyl (D-Trp6-GnRH). J Clin Endocrinol Metab. 1993 Feb;76(2):288–290. doi: 10.1210/jcem.76.2.7679397. [DOI] [PubMed] [Google Scholar]
- Greendale G. A., Edelstein S., Barrett-Connor E. Endogenous sex steroids and bone mineral density in older women and men: the Rancho Bernardo Study. J Bone Miner Res. 1997 Nov;12(11):1833–1843. doi: 10.1359/jbmr.1997.12.11.1833. [DOI] [PubMed] [Google Scholar]
- Grisso J. A., Kelsey J. L., O'Brien L. A., Miles C. G., Sidney S., Maislin G., LaPann K., Moritz D., Peters B. Risk factors for hip fracture in men. Hip Fracture Study Group. Am J Epidemiol. 1997 May 1;145(9):786–793. doi: 10.1093/oxfordjournals.aje.a009171. [DOI] [PubMed] [Google Scholar]
- Gullberg B., Johnell O., Kanis J. A. World-wide projections for hip fracture. Osteoporos Int. 1997;7(5):407–413. doi: 10.1007/pl00004148. [DOI] [PubMed] [Google Scholar]
- Gärdsell P., Johnell O., Nilsson B. E. The predictive value of forearm bone mineral content measurements in men. Bone. 1990;11(4):229–232. doi: 10.1016/8756-3282(90)90074-9. [DOI] [PubMed] [Google Scholar]
- Hannan M. T., Felson D. T., Anderson J. J. Bone mineral density in elderly men and women: results from the Framingham osteoporosis study. J Bone Miner Res. 1992 May;7(5):547–553. doi: 10.1002/jbmr.5650070511. [DOI] [PubMed] [Google Scholar]
- Harris S. T., Watts N. B., Genant H. K., McKeever C. D., Hangartner T., Keller M., Chesnut C. H., 3rd, Brown J., Eriksen E. F., Hoseyni M. S. Effects of risedronate treatment on vertebral and nonvertebral fractures in women with postmenopausal osteoporosis: a randomized controlled trial. Vertebral Efficacy With Risedronate Therapy (VERT) Study Group. JAMA. 1999 Oct 13;282(14):1344–1352. doi: 10.1001/jama.282.14.1344. [DOI] [PubMed] [Google Scholar]
- Heilbrun L. K., Ross P. D., Wasnich R. D., Yano K., Vogel J. M. Characteristics of respondents and nonrespondents in a prospective study of osteoporosis. J Clin Epidemiol. 1991;44(3):233–239. doi: 10.1016/0895-4356(91)90034-7. [DOI] [PubMed] [Google Scholar]
- Hofman A., Grobbee D. E., de Jong P. T., van den Ouweland F. A. Determinants of disease and disability in the elderly: the Rotterdam Elderly Study. Eur J Epidemiol. 1991 Jul;7(4):403–422. doi: 10.1007/BF00145007. [DOI] [PubMed] [Google Scholar]
- Høidrup S., Grønbaek M., Gottschau A., Lauritzen J. B., Schroll M. Alcohol intake, beverage preference, and risk of hip fracture in men and women. Copenhagen Centre for Prospective Population Studies. Am J Epidemiol. 1999 Jun 1;149(11):993–1001. doi: 10.1093/oxfordjournals.aje.a009760. [DOI] [PubMed] [Google Scholar]
- Jackson J. A., Kleerekoper M. Osteoporosis in men: diagnosis, pathophysiology, and prevention. Medicine (Baltimore) 1990 May;69(3):137–152. doi: 10.1097/00005792-199005000-00002. [DOI] [PubMed] [Google Scholar]
- Jackson J. A., Riggs M. W., Spiekerman A. M. Testosterone deficiency as a risk factor for hip fractures in men: a case-control study. Am J Med Sci. 1992 Jul;304(1):4–8. doi: 10.1097/00000441-199207000-00003. [DOI] [PubMed] [Google Scholar]
- Johansson C., Black D., Johnell O., Odén A., Mellström D. Bone mineral density is a predictor of survival. Calcif Tissue Int. 1998 Sep;63(3):190–196. doi: 10.1007/s002239900513. [DOI] [PubMed] [Google Scholar]
- Johnell O., Gullberg B., Kanis J. A., Allander E., Elffors L., Dequeker J., Dilsen G., Gennari C., Lopes Vaz A., Lyritis G. Risk factors for hip fracture in European women: the MEDOS Study. Mediterranean Osteoporosis Study. J Bone Miner Res. 1995 Nov;10(11):1802–1815. doi: 10.1002/jbmr.5650101125. [DOI] [PubMed] [Google Scholar]
- Johnell O., Nilsson B., Obrant K., Sernbo I. Age and sex patterns of hip fracture--changes in 30 years. Acta Orthop Scand. 1984 Jun;55(3):290–292. doi: 10.3109/17453678408992358. [DOI] [PubMed] [Google Scholar]
- Jones G., Nguyen T., Sambrook P. N., Kelly P. J., Gilbert C., Eisman J. A. Symptomatic fracture incidence in elderly men and women: the Dubbo Osteoporosis Epidemiology Study (DOES). Osteoporos Int. 1994 Sep;4(5):277–282. doi: 10.1007/BF01623352. [DOI] [PubMed] [Google Scholar]
- Jones G., Nguyen T., Sambrook P., Kelly P. J., Eisman J. A. Progressive loss of bone in the femoral neck in elderly people: longitudinal findings from the Dubbo osteoporosis epidemiology study. BMJ. 1994 Sep 17;309(6956):691–695. [PMC free article] [PubMed] [Google Scholar]
- Jónsson B., Bengnér U., Redlund-Johnell I., Johnell O. Forearm fractures in Malmö, Sweden. Changes in the incidence occurring during the 1950s, 1980s and 1990s. Acta Orthop Scand. 1999 Apr;70(2):129–132. doi: 10.3109/17453679909011249. [DOI] [PubMed] [Google Scholar]
- Kanis J., Johnell O., Gullberg B., Allander E., Elffors L., Ranstam J., Dequeker J., Dilsen G., Gennari C., Vaz A. L. Risk factors for hip fracture in men from southern Europe: the MEDOS study. Mediterranean Osteoporosis Study. Osteoporos Int. 1999;9(1):45–54. doi: 10.1007/s001980050115. [DOI] [PubMed] [Google Scholar]
- Kannus P., Niemi S., Parkkari J., Palvanen M., Vuori I., Järvinen M. Hip fractures in Finland between 1970 and 1997 and predictions for the future. Lancet. 1999 Mar 6;353(9155):802–805. doi: 10.1016/S0140-6736(98)04235-4. [DOI] [PubMed] [Google Scholar]
- Karlsson M. K., Johnell O., Nilsson B. E., Sernbo I., Obrant K. J. Bone mineral mass in hip fracture patients. Bone. 1993 Mar-Apr;14(2):161–165. doi: 10.1016/8756-3282(93)90243-4. [DOI] [PubMed] [Google Scholar]
- Katznelson L., Finkelstein J. S., Schoenfeld D. A., Rosenthal D. I., Anderson E. J., Klibanski A. Increase in bone density and lean body mass during testosterone administration in men with acquired hypogonadism. J Clin Endocrinol Metab. 1996 Dec;81(12):4358–4365. doi: 10.1210/jcem.81.12.8954042. [DOI] [PubMed] [Google Scholar]
- Kaufman J. M., Vermeulen A. Declining gonadal function in elderly men. Baillieres Clin Endocrinol Metab. 1997 Jul;11(2):289–309. doi: 10.1016/s0950-351x(97)80302-3. [DOI] [PubMed] [Google Scholar]
- Khosla S., Melton L. J., 3rd, Atkinson E. J., O'Fallon W. M., Klee G. G., Riggs B. L. Relationship of serum sex steroid levels and bone turnover markers with bone mineral density in men and women: a key role for bioavailable estrogen. J Clin Endocrinol Metab. 1998 Jul;83(7):2266–2274. doi: 10.1210/jcem.83.7.4924. [DOI] [PubMed] [Google Scholar]
- Langdahl B. L., Ralston S. H., Grant S. F., Eriksen E. F. An Sp1 binding site polymorphism in the COLIA1 gene predicts osteoporotic fractures in both men and women. J Bone Miner Res. 1998 Sep;13(9):1384–1389. doi: 10.1359/jbmr.1998.13.9.1384. [DOI] [PubMed] [Google Scholar]
- Legrand E., Chappard D., Pascaretti C., Duquenne M., Krebs S., Rohmer V., Basle M. F., Audran M. Trabecular bone microarchitecture, bone mineral density, and vertebral fractures in male osteoporosis. J Bone Miner Res. 2000 Jan;15(1):13–19. doi: 10.1359/jbmr.2000.15.1.13. [DOI] [PubMed] [Google Scholar]
- Legrand E., Chappard D., Pascaretti C., Duquenne M., Rondeau C., Simon Y., Rohmer V., Basle M. F., Audran M. Bone mineral density and vertebral fractures in men. Osteoporos Int. 1999;10(4):265–270. doi: 10.1007/s001980050225. [DOI] [PubMed] [Google Scholar]
- Lips P., Cooper C., Agnusdei D., Caulin F., Egger P., Johnell O., Kanis J. A., Kellingray S., Leplege A., Liberman U. A. Quality of life in patients with vertebral fractures: validation of the Quality of Life Questionnaire of the European Foundation for Osteoporosis (QUALEFFO). Working Party for Quality of Life of the European Foundation for Osteoporosis. Osteoporos Int. 1999;10(2):150–160. doi: 10.1007/s001980050210. [DOI] [PubMed] [Google Scholar]
- Lips P., Cooper C., Agnusdei D., Caulin F., Egger P., Johnell O., Kanis J. A., Liberman U., Minne H., Reeve J. Quality of life as outcome in the treatment of osteoporosis: the development of a questionnaire for quality of life by the European Foundation for Osteoporosis. Osteoporos Int. 1997;7(1):36–38. doi: 10.1007/BF01623457. [DOI] [PubMed] [Google Scholar]
- Looker A. C., Orwoll E. S., Johnston C. C., Jr, Lindsay R. L., Wahner H. W., Dunn W. L., Calvo M. S., Harris T. B., Heyse S. P. Prevalence of low femoral bone density in older U.S. adults from NHANES III. J Bone Miner Res. 1997 Nov;12(11):1761–1768. doi: 10.1359/jbmr.1997.12.11.1761. [DOI] [PubMed] [Google Scholar]
- Maggi S., Kelsey J. L., Litvak J., Heyse S. P. Incidence of hip fractures in the elderly: a cross-national analysis. Osteoporos Int. 1991 Sep;1(4):232–241. doi: 10.1007/BF03187467. [DOI] [PubMed] [Google Scholar]
- Mann T., Oviatt S. K., Wilson D., Nelson D., Orwoll E. S. Vertebral deformity in men. J Bone Miner Res. 1992 Nov;7(11):1259–1265. doi: 10.1002/jbmr.5650071120. [DOI] [PubMed] [Google Scholar]
- Mazess R. B., Barden H. S., Drinka P. J., Bauwens S. F., Orwoll E. S., Bell N. H. Influence of age and body weight on spine and femur bone mineral density in U.S. white men. J Bone Miner Res. 1990 Jun;5(6):645–652. doi: 10.1002/jbmr.5650050614. [DOI] [PubMed] [Google Scholar]
- Melton L. J., 3rd, Atkinson E. J., O'Connor M. K., O'Fallon W. M., Riggs B. L. Bone density and fracture risk in men. J Bone Miner Res. 1998 Dec;13(12):1915–1923. doi: 10.1359/jbmr.1998.13.12.1915. [DOI] [PubMed] [Google Scholar]
- Melton L. J., 3rd, Kan S. H., Wahner H. W., Riggs B. L. Lifetime fracture risk: an approach to hip fracture risk assessment based on bone mineral density and age. J Clin Epidemiol. 1988;41(10):985–994. doi: 10.1016/0895-4356(88)90036-4. [DOI] [PubMed] [Google Scholar]
- Mosekilde L., Mosekilde L. Sex differences in age-related changes in vertebral body size, density and biomechanical competence in normal individuals. Bone. 1990;11(2):67–73. doi: 10.1016/8756-3282(90)90052-z. [DOI] [PubMed] [Google Scholar]
- Murphy S., Khaw K. T., Cassidy A., Compston J. E. Sex hormones and bone mineral density in elderly men. Bone Miner. 1993 Feb;20(2):133–140. doi: 10.1016/s0169-6009(08)80022-0. [DOI] [PubMed] [Google Scholar]
- Mussolino M. E., Looker A. C., Madans J. H., Langlois J. A., Orwoll E. S. Risk factors for hip fracture in white men: the NHANES I Epidemiologic Follow-up Study. J Bone Miner Res. 1998 Jun;13(6):918–924. doi: 10.1359/jbmr.1998.13.6.918. [DOI] [PubMed] [Google Scholar]
- Nguyen T. V., Eisman J. A., Kelly P. J., Sambrook P. N. Risk factors for osteoporotic fractures in elderly men. Am J Epidemiol. 1996 Aug 1;144(3):255–263. doi: 10.1093/oxfordjournals.aje.a008920. [DOI] [PubMed] [Google Scholar]
- Nyquist F., Gärdsell P., Sernbo I., Jeppsson J. O., Johnell O. Assessment of sex hormones and bone mineral density in relation to occurrence of fracture in men: a prospective population-based study. Bone. 1998 Feb;22(2):147–151. doi: 10.1016/s8756-3282(97)00250-0. [DOI] [PubMed] [Google Scholar]
- O'Neill T. W., Felsenberg D., Varlow J., Cooper C., Kanis J. A., Silman A. J. The prevalence of vertebral deformity in european men and women: the European Vertebral Osteoporosis Study. J Bone Miner Res. 1996 Jul;11(7):1010–1018. doi: 10.1002/jbmr.5650110719. [DOI] [PubMed] [Google Scholar]
- Oden A., Dawson A., Dere W., Johnell O., Jonsson B., Kanis J. A. Lifetime risk of hip fractures is underestimated. Osteoporos Int. 1998;8(6):599–603. doi: 10.1007/s001980050105. [DOI] [PubMed] [Google Scholar]
- Orwoll E. S., Klein R. F. Osteoporosis in men. Endocr Rev. 1995 Feb;16(1):87–116. doi: 10.1210/edrv-16-1-87. [DOI] [PubMed] [Google Scholar]
- Orwoll E. S., Meier D. E. Alterations in calcium, vitamin D, and parathyroid hormone physiology in normal men with aging: relationship to the development of senile osteopenia. J Clin Endocrinol Metab. 1986 Dec;63(6):1262–1269. doi: 10.1210/jcem-63-6-1262. [DOI] [PubMed] [Google Scholar]
- Orwoll E. S., Oviatt S. K., McClung M. R., Deftos L. J., Sexton G. The rate of bone mineral loss in normal men and the effects of calcium and cholecalciferol supplementation. Ann Intern Med. 1990 Jan 1;112(1):29–34. doi: 10.7326/0003-4819-112-1-29. [DOI] [PubMed] [Google Scholar]
- Poór G., Atkinson E. J., O'Fallon W. M., Melton L. J., 3rd Predictors of hip fractures in elderly men. J Bone Miner Res. 1995 Dec;10(12):1900–1907. doi: 10.1002/jbmr.5650101209. [DOI] [PubMed] [Google Scholar]
- Reginster J. Y., Gillet P., Ben Sedrine W., Brands G., Ethgen O., de Froidmont C., Gosset C. Direct costs of hip fractures in patients over 60 years of age in Belgium. Pharmacoeconomics. 1999 May;15(5):507–514. doi: 10.2165/00019053-199915050-00008. [DOI] [PubMed] [Google Scholar]
- Riggs B. L., Khosla S., Melton L. J., 3rd A unitary model for involutional osteoporosis: estrogen deficiency causes both type I and type II osteoporosis in postmenopausal women and contributes to bone loss in aging men. J Bone Miner Res. 1998 May;13(5):763–773. doi: 10.1359/jbmr.1998.13.5.763. [DOI] [PubMed] [Google Scholar]
- Riggs B. L., Melton L. J., 3rd Involutional osteoporosis. N Engl J Med. 1986 Jun 26;314(26):1676–1686. doi: 10.1056/NEJM198606263142605. [DOI] [PubMed] [Google Scholar]
- Riggs B. L., Wahner H. W., Dunn W. L., Mazess R. B., Offord K. P., Melton L. J., 3rd Differential changes in bone mineral density of the appendicular and axial skeleton with aging: relationship to spinal osteoporosis. J Clin Invest. 1981 Feb;67(2):328–335. doi: 10.1172/JCI110039. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Riggs B. L., Wahner H. W., Seeman E., Offord K. P., Dunn W. L., Mazess R. B., Johnson K. A., Melton L. J., 3rd Changes in bone mineral density of the proximal femur and spine with aging. Differences between the postmenopausal and senile osteoporosis syndromes. J Clin Invest. 1982 Oct;70(4):716–723. doi: 10.1172/JCI110667. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ringe J. D., Dorst A., Kipshoven C., Rovati L. C., Setnikar I. Avoidance of vertebral fractures in men with idiopathic osteoporosis by a three year therapy with calcium and low-dose intermittent monofluorophosphate. Osteoporos Int. 1998;8(1):47–52. doi: 10.1007/s001980050047. [DOI] [PubMed] [Google Scholar]
- Rogmark C., Sernbo I., Johnell O., Nilsson J. A. Incidence of hip fractures in Malmö, Sweden, 1992-1995. A trend-break. Acta Orthop Scand. 1999 Feb;70(1):19–22. doi: 10.3109/17453679909000950. [DOI] [PubMed] [Google Scholar]
- Saag K. G., Emkey R., Schnitzer T. J., Brown J. P., Hawkins F., Goemaere S., Thamsborg G., Liberman U. A., Delmas P. D., Malice M. P. Alendronate for the prevention and treatment of glucocorticoid-induced osteoporosis. Glucocorticoid-Induced Osteoporosis Intervention Study Group. N Engl J Med. 1998 Jul 30;339(5):292–299. doi: 10.1056/NEJM199807303390502. [DOI] [PubMed] [Google Scholar]
- Scane A. C., Sutcliffe A. M., Francis R. M. Osteoporosis in men. Baillieres Clin Rheumatol. 1993 Oct;7(3):589–601. doi: 10.1016/s0950-3579(05)80081-0. [DOI] [PubMed] [Google Scholar]
- Seeman E. Osteoporosis in men. Baillieres Clin Rheumatol. 1997 Aug;11(3):613–629. doi: 10.1016/s0950-3579(97)80023-4. [DOI] [PubMed] [Google Scholar]
- Sernbo I., Johnell O. Consequences of a hip fracture: a prospective study over 1 year. Osteoporos Int. 1993 May;3(3):148–153. doi: 10.1007/BF01623276. [DOI] [PubMed] [Google Scholar]
- Slemenda C. W., Christian J. C., Reed T., Reister T. K., Williams C. J., Johnston C. C., Jr Long-term bone loss in men: effects of genetic and environmental factors. Ann Intern Med. 1992 Aug 15;117(4):286–291. doi: 10.7326/0003-4819-117-4-286. [DOI] [PubMed] [Google Scholar]
- Slemenda C. W., Longcope C., Zhou L., Hui S. L., Peacock M., Johnston C. C. Sex steroids and bone mass in older men. Positive associations with serum estrogens and negative associations with androgens. J Clin Invest. 1997 Oct 1;100(7):1755–1759. doi: 10.1172/JCI119701. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Smith E. P., Boyd J., Frank G. R., Takahashi H., Cohen R. M., Specker B., Williams T. C., Lubahn D. B., Korach K. S. Estrogen resistance caused by a mutation in the estrogen-receptor gene in a man. N Engl J Med. 1994 Oct 20;331(16):1056–1061. doi: 10.1056/NEJM199410203311604. [DOI] [PubMed] [Google Scholar]
- Snyder P. J., Peachey H., Hannoush P., Berlin J. A., Loh L., Holmes J. H., Dlewati A., Staley J., Santanna J., Kapoor S. C. Effect of testosterone treatment on bone mineral density in men over 65 years of age. J Clin Endocrinol Metab. 1999 Jun;84(6):1966–1972. doi: 10.1210/jcem.84.6.5741. [DOI] [PubMed] [Google Scholar]
- Stanley H. L., Schmitt B. P., Poses R. M., Deiss W. P. Does hypogonadism contribute to the occurrence of a minimal trauma hip fracture in elderly men? J Am Geriatr Soc. 1991 Aug;39(8):766–771. doi: 10.1111/j.1532-5415.1991.tb02698.x. [DOI] [PubMed] [Google Scholar]
- Stepán J. J., Lachman M., Zverina J., Pacovský V., Baylink D. J. Castrated men exhibit bone loss: effect of calcitonin treatment on biochemical indices of bone remodeling. J Clin Endocrinol Metab. 1989 Sep;69(3):523–527. doi: 10.1210/jcem-69-3-523. [DOI] [PubMed] [Google Scholar]
- Vermeulen A. Clinical review 24: Androgens in the aging male. J Clin Endocrinol Metab. 1991 Aug;73(2):221–224. doi: 10.1210/jcem-73-2-221. [DOI] [PubMed] [Google Scholar]