Rates of bone loss in the appendicular and axial skeletons of women:​ evidence of substantial vertebral bone loss before menopause

Riggs, B. Lawrence; Wahner, Heinz W.; Melton, III, L. Joseph; Richelson, Linda S.; Judd, Howard L.; Offord, Kenneth P.

Affiliations

¹Endocrine Research Unit, Division of Endocrinology, Metabolism, and Internal Medicine; Section of Diagnostic Nuclear Medicine, and Department of Medical Statistics and Epidemiology, Mayo Clinic and Mayo Foundation, Rochester, Minnesota 55905

²University of California at Los Angeles, School of Medicine, Center for the Health Services, Los Angeles, California 90024

Abstract

We made longitudinal measurements of bone mineral density (BMD) in 139 normal women (ages 20-88 yr) at midradius (99% cortical bone) and lumbar spine (approximately 70% trabecular bone) by single- and dual-photon absorptiometry. BMD was measured 2-6 (median, 3) times over an interval of 0.8-3.4 yr (median, 2.1 yr). For midradius, BMD did not change (+0.48%/yr, NS) before menopause but decreased (-1.01%/yr, P<0.001) after menopause. For lumbar spine, there was significant bone loss both before (-1.32%/yr, P<0.001) and after (-0.97%/yr, P = 0.006) menopause; these rates did not differ significantly from each other. Our data show that before menopause little, if any, bone is lost from the appendicular skeleton but substantial amounts are lost from the axial skeleton. Thus, factors in addition to estrogen deficiency must contribute to pathogenesis of involutional osteoporosis in women because about half of overall vertebral bone loss occurs premenopausally.

Links

DOI: 10.1172/JCI112462.

PubMed: 3700651

WoS: A1986C111100012

History

Received: 1985-08-09

Revised: 1986-01-28

Cited Works (12)

Year	Entry
1983	Riggs BL, Melton LJ III. Evidence for two distinct syndromes of involutional osteoporosis. Am J Med. December 1983;75(6):899-901.
1982	Riggs BL, Wahner HW, Seeman E, Offord KP, Dunn WL, Mazess RB, Johnson KA, Melton LJ III. Changes in bone mineral density of the proximal femur and spine with aging: differences between the postmenopausal and senile osteoporosis syndromes. J Clin Invest. October 1982;70(4):716-723.
1981	Riggs BL, Wahner HW, Dunn WL, Mazess RB, Offord KP, Melton LJ III. Differential changes in bone mineral density of the appendicular and axial skeleton with aging: relationship to spinal osteoporosis. J Clin Invest. February 1981;67(2):328-335.
1985	Cann CE, Genant HK, Kolb FO, Ettinger B. Quantitative computed tomography for prediction of vertebral fracture risk. Bone. 1985;6(1):1-7.
1973	Meunier P, Courpron P, Edouard C, Bernard J, Bringuier J, Vignon G. Physiological senile involution and pathological rarefaction of bone: quantitative and comparative histological data. Clin Endocrinol Metab. July 1973;2(2):239-256.
1970	Merz WA, Schenk RK. A quantitative histological study on bone formation in human cancellous bone. Acta Anat. 1970;76(1):1-15.
1980	Lindsay R, Hart DM, Forrest C, Baird C. Prevention of spinal osteoporosis in oophorectomised women. Lancet. November 29, 1980;2(8205):1151-1154.
1977	Recker RR, Saville PD, Heaney RP. Effect of estrogens and calcium carbonate on bone loss in postmenopausal women. Ann Intern Med. December 1977;87(6):649-655.
1966	Weaver JK, Chalmers J. Cancellous bone: its strength and changes with aging and an evaluation of some methods for measuring its mineral content, I: age changes in cancellous bone. J Bone Joint Surg. March 1966;48A(2):289-298.
1982	Genant HK, Cann CE, Ettinger B, Gordan GS. Quantitative computed tomography of vertebral spongiosa: a sensitive method for detecting early bone loss after oophorectomy. Ann Intern Med. 1982;97(5):699-705.
1982	Krølner B, Pors Nielsen S. Bone mineral content of the lumbar spine in normal and osteoporotic women: cross-sectional and longitudinal studies. Clin Sci (London). March 1982;62(3):329-336.
1982	Mazess RB. On aging bone loss. Clin Orthop Relat Res. May 1982;165:239-252.

Cited By (33)

Year	Entry
1988	Parfitt AM. Bone remodeling: relationship to the amount and structure of bone, and the pathogenesis and prevention of fractures. In: Riggs BL, Melton LJ III, eds. Osteoporosis: Etiology, Diagnosis, and Management. New York, NY: Raven Press; 1988:45-93.
1988	Mazess RB, Wahner HW. Nuclear medicine and densitometry. In: Riggs BL, Melton LJ III, eds. Osteoporosis: Etiology, Diagnosis, and Management. New York, NY: Raven Press; 1988:251-295.
1988	Riggs BL. Practical management of the patient with osteoporosis. In: Riggs BL, Melton LJ III, eds. Osteoporosis: Etiology, Diagnosis, and Management. New York, NY: Raven Press; 1988:481-490.
1988	Dalsky GP, Stocke KS, Ehsani AA, Slatopolsky E, Lee WC, Birge SJ Jr. Weight-bearing exercise training and lumbar bone mineral content in postmenopausal women. Ann Intern Med. June 1988;108(6):824-828.
1990	Melton LJ III, Eddy DM, Johnston C Jr. Screening for osteoporosis. Ann Intern Med. April 1, 1990;112(7):516-528.
1992	Lufkin EG, Wahner HW, O'Fallon WM, Hodgson SF, Kotowicz MA, Lane AW, Judd HL, Caplan RH, Riggs BL. Treatment of postmenopausal osteoporosis with transdermal estrogen. Ann Intern Med. July 1, 1992;117(1):1-9.
1995	Newman E, Turner AS, Wark JD. The potential of sheep for the study of osteopenia: current status and comparison with other animal models. Bone. April 1, 1995;16(4)(suppl):S277-S284.
2013	Willie BM, Birkhold AI, Razi H, Thiele T, Aido M, Kruck B, Schill A, Checa S, Main RP, Duda GN. Diminished response to in vivo mechanical loading in trabecular and not cortical bone in adulthood of female C57Bl/6 mice coincides with a reduction in deformation to load. Bone. August 2013;55(2):335-346.
1993	Forwood MR, Burr DB. Physical activity and bone mass: exercises in futility? Bone Miner. May 1993;21(2):89-112.
1994	Bouxsein ML, Myburgh KH, van der Meulen MCH, Lindenberger E, Marcus R. Age-related differences in cross-sectional geometry of the forearm bones in healthy women. Calcif Tiss Int. February 1994;54(2):113-118.
2002	Riggs BL, Khosla S, Melton LJ III. Sex steroids and the construction and conservation of the adult skeleton. Endocr Rev. June 2002;23(3):279-302.
1990	Eriksen EF, Hodgson SF, Eastell R, Cedel SL, O'Fallon WM, Riggs BL. Cancellous bone remodeling in type I (postmenopausal) osteoporosis: quantitative assessment of rates of formation, resorption, and bone loss at tissue and cellular levels. J Bone Miner Res. April 1990;5(4):311-319.
1992	Steiger P, Cummings SR, Black DM, Spencer NE, Genant HK. Age‐related decrements in bone mineral density in women over 65. J Bone Miner Res. June 1992;7(6):625-632.
1994	Greenspan SL, Maitland LA, Myers ER, Krasnow MB, Kido TH. Femoral bone loss progresses with age: a longitudinal study in women over age 65. J Bone Miner Res. December 1994;9(12):1959-1965.
1995	Ensrud KE, Palermo L, Black DM, Cauley J, Jergas M, Orwoll ES, Nevitt MC, Fox KM, Cummings SR. Hip and calcaneal bone loss increase with advancing age: longitudinal results from the study of osteoporotic fractures. J Bone Miner Res. November 1995;10(11):1778-1787.
1996	Aspray TJ, Prentice A, Cole TJ, Sawo Y, Reeve J, Francis RM. Low bone mineral content is common but osteoporotic fractures are rare in elderly rural Gambian women. J Bone Miner Res. July 1996;11(7):1019-1025.
1997	Arlot ME, Sornay-Rendu E, Garnero P, Vey-Marty B, Delmas PD. Apparent pre- and postmenopausal bone loss evaluated by DXA at different skeletal sites in women: the OFELY cohort. J Bone Miner Res. April 1997;12(4):683-690.
2004	Riggs BL, Melton LJ III, Robb RA, Camp JJ, Atkinson EJ, Peterson JM, Rouleau PA, McCollough CH, Bouxsein ML, Khosla S. Population-based study of age and sex differences in bone volumetricdensity, size, geometry, and structure at different skeletal sites. J Bone Miner Res. December 2004;19(12):1945-1954.
2005	Bouxsein ML, Myers KS, Shultz KL, Donahue LR, Rosen CJ, Beamer WG. Ovariectomy‐induced bone loss varies among inbred strains of mice. J Bone Miner Res. July 2005;20(7):1085-1092.
2008	Riggs BL, Melton LJ, Robb RA, Camp JJ, Atkinson EJ, McDaniel L, Amin S, Rouleau PA, Khosla S. A population‐based assessment of rates of bone loss at multiple skeletal sites: evidence for substantial trabecular bone loss in young adult women and men. J Bone Miner Res. February 2008;23(2):205-214.
2020	Chapurlat R, Bui M, Sornay‐Rendu E, Zebaze R, Delmas PD, Liew D, Lespessailles E, Seeman E. Deterioration of cortical and trabecular microstructure identifies women with osteopenia or normal bone mineral density at imminent and long‐term risk for fragility fracture: a prospective study. J Bone Miner Res. May 2020;35(5):833-844.
1988	Ruff CB, Hayes WC. Sex differences in age‐related remodeling of the femur and tibia. J Orthop Res. November 1988;6(6):886-896.
2002	Seeman E. Pathogenesis of bone fragility in women and men. Lancet. May 25, 2002;359(9320):1841-1850.
1986	Riggs BL, Melton LJ III. Involutional osteoporosis. NEJM. June 26, 1986;314(26):1676-1686.
2003	Ahlborg HG, Johnell O, Turner CH, Rannevik G, Karlsson MK. Bone loss and bone size after menopause. NEJM. July 24, 2003;349(4):327-334.
2003	Seeman E. Reduced bone formation and increased bone resorption: rational targets for the treatment of osteoporosis. Osteoporos Int. March 2003;14(suppl 3):S2-S8.
2003	Bredbenner TL. Damage Modeling of Vertebral Trabecular Bone [PhD thesis]. Cleveland, OH: Case Western Reserve University; January 2003.
2007	Schneider P. Ultrastructural Phenotyping of Murine Bone Using Synchrotron Micro- and Nano-Computed Tomography [PhD thesis]. Swiss Federal Institute of Technology Zürich; 2007.
1992	Bouxsein ML. Physical Activity and Bone Density [PhD thesis]. Stanford University; August 1992.
1998	Giddings VL. Computer Simulations of Calcaneal Loading and Bone Adaptation [PhD thesis]. Stanford University; June 1998.
1998	Ciarelli TE. Architectural and Material Contributions to Fracture of the Spine and Proximal Femur [PhD thesis]. University of Michigan; 1998.
2006	Winzenberg T. Osteoporosis Prevention in Premenopausal Women and Children [PhD thesis]. University of Tasmania; March 2006.
2021	Tibert N. Non-Pharmacological Management of Osteoporotic Vertebral Fractures: A Qualitative Analysis of Patient and Health-Care Professional Perspectives and Experiences [Master's thesis]. University of Waterloo; 2021.