The pathogenesis of osteoporosis in older women and men: A review

Journal of Steroid Biochemistry and Molecular Biology

Volumn 82, Issue 1, 2002, Pages 1-6

  Enriori, Pablo J ^a   Enriori, Carlos L ^a  

^a Lab de Analisis Clinicos   (Argentina)

Author keywords

Bone mineral density; Estradiol; Osteoporosis

Indexed keywords

ESTROGEN; GROWTH HORMONE; INSULIN; SEX HORMONE BINDING GLOBULIN; SOMATOMEDIN; SOMATOMEDIN BINDING PROTEIN;

BONE DENSITY; BONE MASS; BONE MINERAL; DISEASE PREDISPOSITION; ESTROGEN THERAPY; FEMALE; FRACTURE; HUMAN; MALE; MENOPAUSE; PATHOGENESIS; POSTMENOPAUSE; REVIEW; RISK FACTOR; SENILE OSTEOPOROSIS; SEX DIFFERENCE;

AGED; FEMALE; HUMANS; MALE; OSTEOPOROSIS; OSTEOPOROSIS, POSTMENOPAUSAL;

EID: 0036757260     PISSN: 09600760     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0960-0760(02)00144-9     Document Type: Review

References (118)

1. Albright F., Smith P.H., Richardson A.M. Postmenopausal osteoporosis, its clinical features. JAMA. 116:1941;2465-2473.
2. US Bureau of the Census, Statistical Abstract of the United States, vol. 148, 118th ed., Washington, DC, 1998.
3. Fox K.M., Magaziner J., Sherwin R.et al. Reproductive correlates of bone mass in elderly women. J. Bone Miner. Res. 8:1993;901-908.
4. Drinkwater B.L., Nilson K., Chestnut C.H.et al. Bone mineral content of eumenorrheic athletes. N. Engl. J. Med. 311:1984;277-281.
5. Klibanski A., Neer R.M., Beitins I.Z., Ridgway E.C., Zervas N.T., McArthur J.W. Decreased bone density in amenorrheic hyperprolactinemic women. N. Engl. J. Med. 303:1980;1511-1514.
6. Prior J.C., Vigna I.M., Schechter M.T., Burgess A.E. Spinal bone loss and ovulatory disturbances. N. Engl. J. Med. 323:1990;1221-1227.
7. Riggs B.L., Jowsey J., Kelly P.J., Jones J.D., Maher F.T. Effect of sex hormones on bone in primary osteoporosis. J. Clin. Invest. 48:1969;1065-1072.
8. Prior J.C. Progesterone as a bone-trophic hormone. Endocr. Rev. 11:1990;386-398.
9. Tremollieres F.A., Strong D.D., Baylink D., Mohan S. Progesterone and promegestone stimulate human bone cell proliferation and insulin like growth factor 2 production. Acta Endocrinol. 126:1992;329-337.
10. Prior J.C., Vigna Y.M., Barr S.Y.et al. Cyclic medroxiprogesterone treatment increases bone density: a controlled trial in active women with menstrual cycle disturbances. Am. J. Med. 96:1994;521-530.
11. Eriksen E.F., Colvard D.S., Berg N.J.et al. Evidence of estrogen-receptors in normal human osteoblast-like cells. Science. 241:1988;84-86.
12. Walter P., Green S., Green G.et al. Cloning of the human estrogen receptor gene. Proc. Natl. Acad. Sci. U.S.A. 82:1985;7889-7893.
13. Fuqua S.A.W., Wolf D.M. Molecular aspects of estrogen-receptor variants in breast cancer. Breast Cancer Res. Treat. 35:1995;233-241.
14. Warner M., Nilsson S., Gustafsson J.A. The estrogen receptor family. Curr. Opin. Obstet. Gynecol. 11:1999;249-254.
15. Anandappa S.Y., Sibson R., Platt-Higgins A.et al. Variant estrogen receptor α mRNAs in human breast cancer specimens. Int. J. Cancer. 88:2000;209-216.
16. Prestwood K.M., Kenny A.M., Unson C., Kulldorf M. The effect of low dose micronized 17β-estradiol on bone turnover, double blind, placebo-controlled study. J. Clin. Endocrinol. Metab. 85:2000;4462-4469.
17. Enriori C.L. Biochemistry, bioregulation and clinical significance of sex hormone-binding globulin (SHBG). Acta Bioquim. Clin. Latinoamer. 22:1988;77-129.
18. Peiris A.N., Sothmann M.S., Aiman E.J., Kissebah A.H. The relation of insulin to sex hormone-binding globulin: role of adiposity. Fertil. Steril. 52:1989;69-72.
19. Plymate S.R., Matej L.A., Jones R.E., Frienl K.E. Inhibition of sex-hormone binding globulin in the human hepatoma (HepG2) cell line by insulin and prolactin. J. Clin. Endocrinol. Metab. 67:1988;460-464.
20. Nestler J., Powers I., Matt D.et al. A direct effect of hyperinsulinemia on serum sex hormone binding globulin levels in obese women with the polycystic ovary syndrome. J. Clin. Endocrinol. Metab. 72:1991;83-89.
21. Baxter R.C. Insulin growth factor binding proteins in the human circulation, a review. Hormone Res. 42:1994;140-144.
22. Crave J.C., Lejeune H., Brébant C., Baret C., Pugeat M. Differential effects of insulin-like growth factor I on the production of plasma steroid-binding globulin by human hepatoblastomaderived (HepG2) cells. J. Clin. Endocrinol. Metab. 80:1995;1283-1289.
23. Barrett-Connor E., Kritz-Silverstein D. Does hyperinsulinemia preserve bone? Diabetes Care. 19:1996;1388-1392.
24. L.C. Giudice, Role of insulin-growth factors (IGFs) and IGF binding proteins in PCOs, in: R.N.J. Azziz, D. Dewailly (Eds.), Androgen Excess Disorder in Women. Lippincott-Raven, Philadelphia, 1997, pp. 507-519.
25. Scaglia H. Insulin resistance. Biochemical and molecular aspects. Rev. Argent Endocrinol. Metab. 37:2000;200-220.
26. Reid I.R., Ames R., Evans M.C.et al. Determinant of total body and regional bone mineral density in normal postmenopausal - a key role for fat mass. J. Clin. Endocrinol. Metab. 75:1992;451-454.
27. Suzuki M., Yano T., Nakazawa N.et al. A possible role of estrone produced in adipose tissues in modulating postmenopausal bone density. Maturitas. 22:1995;9-12.
28. Zborowsky J.V., Cauley J.A., Talbot E.O.et al. Bone mineral density, androgens and the polycystic ovary: the complex and controversial issue of androgenic influency in female bone. J. Clin. Endocrinol. Metab. 85:2000;3496-3506.
29. P. Cohen, R.G. Rosenfeld, The IGF Axis, Human Growth Hormone, Basic and Scientific Aspect, CRC Press, Boca Raton, FL, 1995.
30. Ferry R.J., Liu B., Cohen P. New roles for IGF binding proteins. Endocrinologist. 9:1999;438-450.
31. Rosenfeld R.G., Pham H., Cohen P.et al. Insulin-like growth factor binding proteins and their regulation. Acta Paediatr. 339:1994;154-158.
32. Underwood L.E., Thissen J.P., Lemozy S., Ketelsleger J.M., Clemmons D.R. Hormonal and nutritional regulation of IGF-I and its binding proteins. Hormone Res. 42:1994;145-151.
33. Reaven G.M. Role of insulin resistance in human disease. Banting Lecture. Diabetes. 37:1988;1595-1607.
34. Stoll B.A. Breast cancer: further metabolic-endocrine risk markers? Br. J. Cancer. 76:1997;1652-1654.
35. Stracke H., Schulz A., Rossol R., Moeller D., Schatz H. Effect of growth hormone on osteoblasts and demonstration of somatomedin-C/IGF-I in bone organ culture. Acta Endocrinol. 107:1984;16-24.
36. Canalis E., McCarthy T., Centrella M. Growth factors and the regulation of bone remodeling. J. Clin. Invest. 81:1988;277-281.
37. Ljunghall S., Johansson A.G., Burmann P.et al. Low plasma levels of insulin-like growth factor-1 (IGF-I) in male patients with idiopathic osteoporosis. J. Intern. Med. 232:1992;59-64.
38. Wüster C., Blum W.F., Schlemilch S., Ranke M., Ziegler R. Decreased serum levels of insulin-like growth factors and IGF binding protein 3 in osteoporosis. J. Intern. Med. 234:1993;249-255.
39. Langlois J.A., Rosen C.J., Visser M.et al. Association between insulin-like growth factor-I and bone mineral density in older women and men: the framingham heart study. J. Clin. Endocrinol. Metab. 83:1998;4257-4262.
40. Kassem M., Blum W., Risteli J.et al. Growth hormone stimulates proliferation and differentiation of normal human osteoblast-like cells in vitro. Calcif. Tissue Int. 52:1993;222-226.
41. Kassem M., Brixen K., Blum W.et al. No evidence for reduced spontaneous or growth-hormone-stimulated serum levels of insulin-like growth factor IGF-I, IGF-II or IGFBP-3 in women with spinal osteoporosis. Eur. J. Endocrinol. 131:1994;150-155.
42. Biller B.M.K. Efficacy of growth hormone-replacement therapy. Endocrinologist. 8:1998;15S-21S.
43. Baxter R.C., Binoux M.A., Clemmons D.R.et al. Recommendations for nomenclature of the insulin-like growth factor binding protein superfamily. Endocrinology. 139:1998;4036.
44. Ferry J.R., Liu B., Cohen P. New roles for IGF binding proteins. Endocrinologist. 9:1999;438-450.
45. Hwa V., Oh Y., Rosenfeld R.G. The insulin-like growth factor-binding protein (IGFBP) superfamily. Endocr. Rev. 20:1999;761-787.
46. Khan S.N., Mathias P.G., Bostrom M.P.G., Lane J.M. Bone growth factors. Orthop. Clin. North Am. 31:2000;375-387.
47. Canalis E. Skeletal growth factors and aging. J. Clin. Endocrinol. Metab. 78:1994;1009-1010.
48. Nicolas V., Prewett A., Bettica P.et al. Age-related decreases of insulin-like growth factor-1 and transforming growth factor-β in femoral cortical bone from both men and women: implications for bone loss with aging. J. Clin. Endocrinol. Metab. 78:1994;1011-1016.
49. Plotkin L., Sarly M., Sgarlata C.et al. Insulin-like growth factor I (IGF-I) and insulin-like-binding protein-3 (IGFBP-3) in osteoporotic patients. Rev. Argent Endocrinol. Metab. 35:1998;67-75.
50. Jones J.I., Clemmons D.R. Insulin-like growth factors and their binding proteins: biological actions. Endocr. Rev. 16:1995;3-34.
51. Humbel R.E. Insulin-like growth factors I and II. Eur. J. Biochem. 190:1990;445-462.
52. Mohan S., Baylink D.J. Bone growth factors. Clin. Orthop. 263:1991;30-48.
53. Bayling D.J., Finkelman R.D., Mohan S. Growth factors to stimulate bone formation. J. Bone Miner. Res. 85:1993;565-572.
54. Donahue L.R., Hunter S.J., Sherblom A.P., Rosen C. Age-related changes in serum insulin-like growth factor-binding proteins in women. J. Clin. Endocrinol. Metab. 71:1990;575-579.
55. Kelijman M. Age-related alterations of the growth hormone/insulin-like growth factor I axis. J. Am. Geriatr. Soc. 39:1991;295-307.
56. Helle S.I., Omsjo I.H., Hughes S.C.C.et al. Effects of oral and transdermal oestrogen replacement therapy on plasma levels of insulin-like growth factors and IGF binding proteins 1 and 3: a cross over study. Clin. Endocrinol. (Oxf). 45:1996;727-732.
57. Gower B.A., Nyman L. Association among oral estrogen use, free testosterone concentration, and lean body mass among postmenopausal women. J. Clin. Endocrinol. Metab. 85:2000;4476-4480.
58. Burger H.G., Dudley E.C., Cui J., Dennerstein L., Hopper J.L. A prospective longitudinal study of serum testosterone, dehydroepiandrosterone sulfate, and sex hormone-binding globulin levels through the menopausal transition. J. Clin. Endocrinol. Metab. 85:2000;2832-2838.
59. Sodergard R., Backstrom T., Shanbhag V., Carstensen H.et al. Calculation of free and bound fractions of testosterone and estradiol-17β to human plasma proteins at body temperature. J. Steroid Biochem. 16:1982;801-810.
60. Tanaka S., Haji M., Nishi Y.et al. Aromatase activity in human osteoblast-like osteosarcoma cell. Calcif. Tissue Int. 52:1993;107-109.
61. Bilezikian J.P., Morishima A., Bell J., Grumbach M.M. Increased bone mass as a result of estrogen therapy in man with aromatase deficiency. N. Engl. J. Med. 339:1998;599-603.
62. Buchanan J.R., Myers C., Lloyd T.et al. Determinants of peak trabecular bone density in women: the role of androgens, estrogens and exercise. J. Bone Miner. Res. 3:1988;673-680.
63. Dixon J.E., Rodin A., Murby B.et al. Bone mass in hirsute women with androgen excess. Clin. Endocrinol. (Oxf). 30:1989;271-277.
64. Raisz L.G., Wiita B., Artis A.et al. Comparison of the effects of estrogen alone and estrogen plus androgen on biochemical markers of bone formation and resorption in postmenopausal women. J. Clin. Endocrinol. Metab. 81:1996;37-43.
65. Cummings S.R., Nevitt M.C., Browner W.S.et al. Risk factors for hip fracture in white women. Study of osteoporotic fractures research group. N. Engl. J. Med. 332:1995;767-773.
66. Keen R.W., Hart D.J., Arden N.K., Doyle D.V., Spector T.D. Family history of appendicular fracture and risk of osteoporosis: a population-based study. Osteoporosis Int. 10:1999;161-166.
67. Stewart T.L., Ralston S.H. Role of genetic factors in the pathogenesis of osteoporosis. J. Endocrinol. 166:2000;235-245.
68. Melton L.J. Epidemiology of spinal osteoporosis. Spine. 22:1997;25-115.
69. Nawata H., Tanaka S., Tanaka Y.et al. Aromatase in bone cell: association with osteoporosis in postmenopausal women. J. Steroid Biochem. Mol. Biol. 53:1995;165-174.
70. Morishima A., Grumbach M.M., Simpson E.R.et al. Aromatase deficiency in male and female siblings caused by a novel mutation and the physiological role of estrogens. J. Clin. Endocrinol. Metab. 80:1995;3689-3698.
71. Kasperk C.H., Wakley G.K., Hierl T.et al. Gonadal and adrenal androgens are potent regulators of human bone cell metabolism in vitro. J. Bone Miner. Res. 12:1997;464-471.
72. Arisaka O., Hoshi M., Kanazawa S.et al. Effects of adrenal and estrogen on bone maturation and bone mineral density. Metabolism. 50:2001;377-379.
73. Pasqualini J.R., Schatz B., Varin C.et al. Recent data on estrogen sulfatases and sulfotransferases activities in human breast cancer. J. Steroid Biochem. Mol. Biol. 41:1992;323-329.
74. Cauley J.A., Lucas F.L., Kuller L.H.et al. Bone mineral density and risk of breast cancer in older women. The study of osteoporotic fractures. JAMA. 276:1996;1404-1408.
75. Zhang Y., Kiel D.P., Kreger B.E.et al. Bone mass and the risk of breast cancer among postmenopausal women. N. Engl. J. Med. 336:1997;611-617.
76. He Yu. Comment on association between insulin-like growth factor-I (IGF-I) and bone mineral density: further evidence linking IGF-I to breast cancer risk. J. Clin. Endocrinol. Metab. 84:1999;1760-1761.
77. Cummings S.R., Kelsey J., Newitt M., O'Dowd K. Epidemiology of osteoporosis and osteoporotic fractures. Epidemiol. Rev. 7:1985;178-208.
78. Chrischilles E., Butler C., Davis C.et al. A model of life-time osteoporosis impact. Arch. Intern. Med. 151:1991;2026-2032.
79. Melton L. Hip fractures: a worldwide problem today and tomorrow. Bone. 14:1993;51-58.
80. Keene G., Parker M., Pryor G. Mortality and morbidity after hip fractures. Br. Med. J. 307:1993;1248-1250.
81. Orwoll P.R., Klein R.F. Osteoporosis in men. Endocr. Rev. 16:1995;87-116.
82. Poor G., Atkinson E.J., Lewallen D.G.et al. Age-related hip fractures in men: clinical spectrum and short-term outcome. Osteop. Int. 5:1995;419-426.
83. Burger H., Van Daele P.L.A., Grasluis K.et al. Vertebral deformities and functional impairment in men and women. J. Bone Miner. Res. 12:1997;152-157.
84. Ebeling P.R. Osteoporosis in men. New insights into aetiology, pathogenesis, prevention and management. Drugs Aging. 13:1998;421-434.
85. Hayden J.M., Mohan S., Baylink D.J. The insulin-like growth factor system and the coupling of formation to resorption. Bone. 17:1994;93S-98S.
86. Bilezikian J.P. Osteoporosis in men. J. Clin. Endocrinol. Metab. 84:1999;3431-3434.
87. Szulc P., Munoz F., Claustrat B.et al. Bioavailable estradiol may be an important determinant of osteoporosis in men. The MINOS study. J. Clin. Endocrinol. Metab. 86:2001;192-199.
88. Lukert B., Raisz L. Glucocorticoid-induced osteoporosis: pathogenesis and management. Ann. Intern. Med. 112:1990;352-364.
89. Canalis E. Mechanisms of glucocortcoid action in bone: implications to glucocorticoid-induced osteoporosis. J. Clin. Endocrinol. Metab. 81:1996;3441-3447.
90. Van Staa T.P., Leufkens H.G.M., Abenhaim L., Zhang B., Cooper C. Use of oral corticosteroids and riks of fractures. J. Bone Miner. Res. 15:2000;993-1000.
91. Manelli F., Giustina A. Glucocorticoid-induced osteoporosis. Trends Endocrinol. Metab. 11:2000;79-85.
92. Canalis E., Giustina A. Glucocorticoid-induced osteoporosis: summary of a workshop. J. Clin. Endocrinol. Metab. 86:2001;5681-5685.
93. Slemenda C.W., Longscope C., Zhou L.et al. Sex steroids and bone mass in older men. J. Clin. Invest. 100:1997;1755-1759.
94. Khosla S., Melton L.J., Atkinson E.J.et al. Relationship of 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. 83:1998;2266-2274.
95. Enriori C.L., Reforzo-Membrives J. Peripheral aromatization as a risk factor for breast and endometrial cancer in postmenopausal women: a review. Gynecol. Oncol. 17:1984;1-21.
96. Enriori C.L., Orsini W., Cremona M., Del C.et al. Decrease of circulating SHBG in postmenopausal obese women as a risk factor in breast cancer reversible effect of weigth loss. Gynecol. Oncol. 23:1986;77-86.
97. Sharpe R.M. The rol of estrogens in the male. Trends Endocrinol. Metab. 9:1998;371-378.
98. Vanderschueren D., Boullion R. Estrogen deficiency in men is a challenge for both the hypothalamus and pituitary. J. Clin. Endocrinol. Metab. 85:2000;3024-3026.
99. Simpson E., Rubin G., Clyne C.et al. The role of local estrogen biosynthesis in males and females. Trends Endocrinol. Metab. 11:2000;184-188.
100. Sasano H., Uziki M., Sawai T.et al. Aromatase in human bone tissue. J. Bone Miner. Res. 12:1997;1416-1423.
101. 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. 339:1998;599-603.
102. Cauley J.A., Zmuda J.M., Ensrud K.E., Bauer D.C., Ettinger B. For the study of osteoporotic fractures research group. Timing of estrogen replacement therapy for optimal osteoporosis prevention. J. Clin. Endocrinol. Metab. 86:2001;5700-5705.
103. Behre H.M., Kliesch S., Leifke E., Link T.M., Nieschla E. Long-term effect of testosterone therapy on bone mineral density in hypogonadal men. J. Clin. Endocrinol. Metab. 82:1997;2386-2390.
104. Kurlan E.S., Cosman F., McMahon D.J.et al. Parathyroid hormone as a therapy for idiopathic osteoporosis in men: effects on bone mineral density and bone markers. J. Clin. Endocrinol. Metab. 85:2000;3069-3076.
105. A. Gray, H.A. Feldman, McKinglay, et al., Age, disease and changing levels in middle-aged men: Results of the Massachusetts male aging study, J. Clin. Endocrinol. Metab. 73 (1991) 1016-1025.
106. Mitchell R., Hollis S., Rothwell C., Robertson W.R. Age-related changes in the pituitary-testicular axis in normal men lower testosterone results from decreased bioactive LH drive. Clin. Endocrinol. (Oxf). 42:1995;501-507.
107. Center J.R., Nguyen T.V., Sambrook P.N., Eisman J.A. Hormonal and biochemical parameters in the determination of osteoporosis in elderly men. J. Clin. Endocrinol. Metab. 84:1999;3626-3635.
108. Bembassat C.A., Maki K.C., Unterman T.G. Circulating levels of insulin-like growth factor (IGF) binding protein-1 and -3 in aging men: relationships to insulin, glucose, IGF and dehydro-epiandrosterone sulfate levels and anthropometric measures. J. Clin. Endocrinol. Metab. 82:1997;1484-1491.
109. Lee P.D.K., Conover C.A., Power D.R. Regulation and function of insulin-like growth factor-binding protein-1. Proc. Soc. Exp. Biol. Med. 204:1993;4-29.
110. Lamsom G., Cohen P., Giudice L.C.et al. Proteolysis of IGFBP-3 may be a common regulatory mechanism of IGF action in vivo. Growth Regul. 3:1993;91-95.
111. Yki-Järvinen H., Mäkimattila S., Utriainen T., Rutanen E.-T. Portal insulin concentrations rather than insulin sensitivity regulate serum sex hormone-binding globulin and insulin-like growth factor binding protein 1 in vivo. J. Clin. Endocrinol. Metab. 80:1995;3227-3232.
112. Rudman D., Drinka P.J., Wilson C.R.et al. Relations of endogenous anabolic hormones and physical activity to bone mineral density and lean body mass in elderly men. Clin. Endocrinol. (Oxf). 40:1994;653-661.
113. Seeman E. Osteoporosis in men. Am. J. Med. 95:1994;22-28.
114. Seeman E. The dilemma of osteoporosis in men. Am. J. Med. 98(Suppl. 2A):1995;S76-S88.
115. Kurland E.S., Chan F.K.W., Rosen C.J., Bilezikian J.P. Normal growth hormone secretory reserve in men with idiopathic osteoporosis and reduced circulating levels of insulin-like growth factor-I. J. Clin. Endocrinol. Metab. 83:1998;1-4.
116. Blanton C.A., Horwitz B., McDonald R.B. Neurochemical anterations during age-related anorexia. Proc. Soc. Exp. Biol. Med. 221:1999;153-155.
117. Longcope C., Feldman H.A., McInlay J.B., Araujo A.B. Diet and sex hormone-binding globulin. J. Clin. Endocrinol. Metab. 85:2000;293-296.
118. van den Beld A.W., de Jong F.H., Grobbee D.E., Pols H.A.P., Lamberts S.W.J. Measures of bioavailable serum testosterone and estradiol and their relationships with muscle strength, bone density and body composition in elderly men. J. Clin. Endocrinol. Metab. 85:2000;3276-3282.