Skip to main content
Top
Published in: Osteoporosis International 6/2003

01-06-2003 | Original Article

Changes in bone mineral density in the hip and spine before, during, and after the menopause in elite runners

Authors: Alexandra Tomkinson, Jane H. Gibson, Mark Lunt, Mark Harries, Jonathan Reeve

Published in: Osteoporosis International | Issue 6/2003

Login to get access

Abstract

This study was undertaken to determine the degree of interaction between hormonal and athletic effects on changes in bone mineral density (BMD, g/cm2) with time in women around the menopause. Thirty-five elite female runners aged over 40 participated in a longitudinal cohort study of hip and spine bone density changes and had two measurements a mean of 4.1 years apart. Eighteen remained estrogenized throughout the study (E+ to +), ten remained postmenopausal throughout (E− to −), while seven showed a change in status (E− to +) or (E+ to −). At study exit, both postmenopausal E+ and E− subjects had significantly higher than expected broadband ultrasound attenuation (BUA) and velocity of sound (VOS) values at the calcaneus. However, Z-score 95% confidence intervals for BMD of the hip and spine embraced zero except at the femoral trochanter in E+ women. The E+ to + group did not lose bone at any site. The E− to − group lost bone significantly, but only at the femoral neck and spine at rates close to 1% annually. Multiple analysis of variance repeated measures analysis showed a significant interaction in the effects of estrogen exposure with DXA measurement site, with the femoral trochanter being less affected by E− status than the spine and femoral neck. Body mass index (BMI: weight/height2, kg/m2) had a significantly positive effect on total hip and femoral neck BMD independently of estrogen status. In conclusion, in this pilot study, postmenopausal elite runners not on hormone replacement therapy lost BMD from the femoral neck and spine at the expected rates but in the femoral trochanter bone loss appeared reduced and in the calcaneus BUA and VOS were maintained close to young normal values.
Appendix
Available only for authorised users
Literature
1.
go back to reference Frost H (1988) Vital biomechanics: proposed general concepts for skeletal adaptions to mechanical usage. Calcif Tissue Int 42:145–156. Frost H (1988) Vital biomechanics: proposed general concepts for skeletal adaptions to mechanical usage. Calcif Tissue Int 42:145–156.
2.
go back to reference Lanyon L (1996) Using functional loading to influence bone mass and architecture: objectives, mechanisms, and relationship with oestrogen of the mechanically adaptive process in bone. Bone 18:S37–S43. Lanyon L (1996) Using functional loading to influence bone mass and architecture: objectives, mechanisms, and relationship with oestrogen of the mechanically adaptive process in bone. Bone 18:S37–S43.
3.
go back to reference Turner CH, Robling AG, Duncan RL, Burr DB (2002) Do bone cells behave like a neuronal network? Calcif Tissue Int 70:435–442. Turner CH, Robling AG, Duncan RL, Burr DB (2002) Do bone cells behave like a neuronal network? Calcif Tissue Int 70:435–442.
4.
go back to reference Heinonen A, Oja P, Kannus P, Sievanen H, Haapasalo H, Manttari A, Vuori I (1995) Bone mineral density in female athletes representing sports with different loading characteristics of the skeleton. Bone 17:197–203. Heinonen A, Oja P, Kannus P, Sievanen H, Haapasalo H, Manttari A, Vuori I (1995) Bone mineral density in female athletes representing sports with different loading characteristics of the skeleton. Bone 17:197–203.
5.
go back to reference Fehling P, Alekel L, Clasey J, Rector A (1995) A comparison of bone mineral densities among female athletes in impact loading and active loading sports. Bone 17:205–210. Fehling P, Alekel L, Clasey J, Rector A (1995) A comparison of bone mineral densities among female athletes in impact loading and active loading sports. Bone 17:205–210.
6.
go back to reference Kerr D, Morton A, Dick I, Prina R (1996) Exercise effects on bone mass in postmenopausal women are site specific and load dependent. J Bone Miner Res 11:218–225. Kerr D, Morton A, Dick I, Prina R (1996) Exercise effects on bone mass in postmenopausal women are site specific and load dependent. J Bone Miner Res 11:218–225.
7.
go back to reference Rubin C, Lanyon L (1984) Regulation of bone formation by applied dynamic loads. J Bone Joint Surg Am 66:397–402. Rubin C, Lanyon L (1984) Regulation of bone formation by applied dynamic loads. J Bone Joint Surg Am 66:397–402.
8.
go back to reference Bennell K, Malcolm S, Khan K (1997) Bone mass and bone turnover in power athletes, endurance athletes and controls: a 12 month longitudinal study. Bone 20:477–484. Bennell K, Malcolm S, Khan K (1997) Bone mass and bone turnover in power athletes, endurance athletes and controls: a 12 month longitudinal study. Bone 20:477–484.
9.
go back to reference Snow C (1996) Exercise and bone mass in young and premenopausal women. Bone 18:51S–55S. Snow C (1996) Exercise and bone mass in young and premenopausal women. Bone 18:51S–55S.
10.
go back to reference Snow C, Shaw J, Mathin C (1996) Physical activity and risk for osteoporosis. In: Marcus R, Feldman D, Kelsey J (eds) Osteoporosis, 1st edn. Academic Press, California, pp 511–528. Snow C, Shaw J, Mathin C (1996) Physical activity and risk for osteoporosis. In: Marcus R, Feldman D, Kelsey J (eds) Osteoporosis, 1st edn. Academic Press, California, pp 511–528.
11.
go back to reference Rubin C, Turner AS, Muller R, et al. (2002) Quantity and quality of trabecular bone in the femur are enhanced by a strongly anabolic, noninvasive mechanical intervention. J Bone Miner Res 17:349–357. Rubin C, Turner AS, Muller R, et al. (2002) Quantity and quality of trabecular bone in the femur are enhanced by a strongly anabolic, noninvasive mechanical intervention. J Bone Miner Res 17:349–357.
12.
go back to reference Brahm H, Strom H, Piehl-Aukin K, Mallmin H, Ljunghall S (1997) Bone metabolism in endurance trained athletes: a comparison to population based controls based on DXA, SXA, quantitative ultrasound and biochemical markers. Calcif Tissue Int 61:448–454. Brahm H, Strom H, Piehl-Aukin K, Mallmin H, Ljunghall S (1997) Bone metabolism in endurance trained athletes: a comparison to population based controls based on DXA, SXA, quantitative ultrasound and biochemical markers. Calcif Tissue Int 61:448–454.
13.
go back to reference Marcus R, Cann N, Madvig P, Minkoff J, Gaddard M (1985) Menstrual function and bone mass in elite women distant runners. Ann Intern Med 102:158–163. Marcus R, Cann N, Madvig P, Minkoff J, Gaddard M (1985) Menstrual function and bone mass in elite women distant runners. Ann Intern Med 102:158–163.
14.
go back to reference Capozzo A (1983) Force actions in the human trunk during running. J Sports Med 23:14–22. Capozzo A (1983) Force actions in the human trunk during running. J Sports Med 23:14–22.
15.
go back to reference Gibson JH, Harries M, Mitchell A, Godfrey R, Lunt M, Reeve J (2000) Determinants of bone density and prevalence of osteopenia among female runners in their second to seventh decades of age. Bone 26:591–598. Gibson JH, Harries M, Mitchell A, Godfrey R, Lunt M, Reeve J (2000) Determinants of bone density and prevalence of osteopenia among female runners in their second to seventh decades of age. Bone 26:591–598.
16.
go back to reference Winters K, Adams W, Meredith C, Loan M, Lasley B (1996) Bone density and cyclic ovarian function in trained runners and active controls. Med Sci Sports Exerc 28:776–785. Winters K, Adams W, Meredith C, Loan M, Lasley B (1996) Bone density and cyclic ovarian function in trained runners and active controls. Med Sci Sports Exerc 28:776–785.
17.
go back to reference Hetland M, Haarbo J, Christiansen C, Larsen T (1993) Running induces menstrual disturbances but bone mass is unaffected, except in amenorrheic women. Am J Med 95:53–60. Hetland M, Haarbo J, Christiansen C, Larsen T (1993) Running induces menstrual disturbances but bone mass is unaffected, except in amenorrheic women. Am J Med 95:53–60.
18.
go back to reference Clement D, Ammann W, Taunton J, Lloyd-Smith R, Jesperson D, McKay H, Goldring J (1993) Exercise-induced stress injuries to the femur. Int J Sports Med 14:347–352. Clement D, Ammann W, Taunton J, Lloyd-Smith R, Jesperson D, McKay H, Goldring J (1993) Exercise-induced stress injuries to the femur. Int J Sports Med 14:347–352.
19.
go back to reference Rutherford O (1993) Spine and total body bone mineral density in amenorrheic endurance athletes. J Appl Physiol 74:2904–2908. Rutherford O (1993) Spine and total body bone mineral density in amenorrheic endurance athletes. J Appl Physiol 74:2904–2908.
20.
go back to reference Goto S, Shigeta H, Hyakutake S, Yamagata M (1996) Comparison between menopause related changes in bone mineral density of the lumbar spine and the proximal femur in Japanese female athletes: a long term longitudinal study using dual energy X-ray absorptiometry. Calcif Tissue Int 59:461–465. Goto S, Shigeta H, Hyakutake S, Yamagata M (1996) Comparison between menopause related changes in bone mineral density of the lumbar spine and the proximal femur in Japanese female athletes: a long term longitudinal study using dual energy X-ray absorptiometry. Calcif Tissue Int 59:461–465.
21.
go back to reference Kirk S, Sharp C, Elbaum N, Endres D, Simons S (1989) Effect of long-distance running on bone mass in women. J Bone Miner Res 4:515–522. Kirk S, Sharp C, Elbaum N, Endres D, Simons S (1989) Effect of long-distance running on bone mass in women. J Bone Miner Res 4:515–522.
22.
go back to reference Lane N, Bloch D, Hubert H, Jones H (1990) Running, osteoarthritis, and bone density: initial 2-year longitudinal study. Am J Med 88:452–459. Lane N, Bloch D, Hubert H, Jones H (1990) Running, osteoarthritis, and bone density: initial 2-year longitudinal study. Am J Med 88:452–459.
23.
go back to reference Nelson M, Meredith C, Dawson-Hughes B, Evans W (1988) Hormone and bone mineral status in endurance-trained and sedentary postmenopausal women. J Clin Endocrinol Metab 66:927–933. Nelson M, Meredith C, Dawson-Hughes B, Evans W (1988) Hormone and bone mineral status in endurance-trained and sedentary postmenopausal women. J Clin Endocrinol Metab 66:927–933.
24.
go back to reference Suominen H (1993) Bone mineral density and long term exercise. An overview of cross sectional athlete studies. Sports Med 16:316–330. Suominen H (1993) Bone mineral density and long term exercise. An overview of cross sectional athlete studies. Sports Med 16:316–330.
25.
go back to reference Raab D, Smith E, Crenshaw T, Thomas D (1990) Bone mechanical properties after exercise training in young and old rats. J Appl Physiol 68:130–134. Raab D, Smith E, Crenshaw T, Thomas D (1990) Bone mechanical properties after exercise training in young and old rats. J Appl Physiol 68:130–134.
26.
go back to reference Reeve J, Walton J, Russell LJ, Lunt M, Wolman R, Abraham R et al.(1999) Determinants of the first decade of bone loss after menopause at spine, hip and radius: the Harrow post-menopausal bone loss study. Q J Med 92:261–273. Reeve J, Walton J, Russell LJ, Lunt M, Wolman R, Abraham R et al.(1999) Determinants of the first decade of bone loss after menopause at spine, hip and radius: the Harrow post-menopausal bone loss study. Q J Med 92:261–273.
27.
go back to reference Pearson J (1995) Dual X-ray absorptiometry of the proximal femur: normal European values standardised with the European spine phantom. J Bone Miner Res 10:315–324. Pearson J (1995) Dual X-ray absorptiometry of the proximal femur: normal European values standardised with the European spine phantom. J Bone Miner Res 10:315–324.
28.
go back to reference Dequeker J (1995) Dual x-ray absorptiometry—cross calibration and normative reference ranges for the spine. Results of a European Community concerted action. Bone 17:247–254. Dequeker J (1995) Dual x-ray absorptiometry—cross calibration and normative reference ranges for the spine. Results of a European Community concerted action. Bone 17:247–254.
29.
go back to reference Lunt M, Felsenberg D, Adams J, Benevolenskaya L, Cannata J, Dequeker J et al. (1997) Population-based geographic variations in DXA bone density in Europe: the EVOS study. Osteoporos Int 7:175–189. Lunt M, Felsenberg D, Adams J, Benevolenskaya L, Cannata J, Dequeker J et al. (1997) Population-based geographic variations in DXA bone density in Europe: the EVOS study. Osteoporos Int 7:175–189.
30.
go back to reference Reid I, Legge M, Stapleton J, Evans M, Grey A (1995) Regular exercise dissociates fat mass and bone mineral density in premenopausal women. J Clin Endocrinol Metab 80:1764–1768. Reid I, Legge M, Stapleton J, Evans M, Grey A (1995) Regular exercise dissociates fat mass and bone mineral density in premenopausal women. J Clin Endocrinol Metab 80:1764–1768.
31.
go back to reference Kröger H, Tuppurainen M, Honkanen R, Alhara E, Saarikoski S (1994) Bone mineral density and risk factors for osteoporosis — a population based study of 1600 perimenopausal women. Calcif Tissue Int 55:1–7. Kröger H, Tuppurainen M, Honkanen R, Alhara E, Saarikoski S (1994) Bone mineral density and risk factors for osteoporosis — a population based study of 1600 perimenopausal women. Calcif Tissue Int 55:1–7.
32.
go back to reference Alekel L, Clasey J, Fehling P, Weigel R, Boileau R, Erdman J, Stillamn R (1995) Contributions of exercise, body composition and age to bone mineral density in premenopausal women. Med Sci Sports Exerc 27:1477–1485. Alekel L, Clasey J, Fehling P, Weigel R, Boileau R, Erdman J, Stillamn R (1995) Contributions of exercise, body composition and age to bone mineral density in premenopausal women. Med Sci Sports Exerc 27:1477–1485.
33.
go back to reference Alfredson H, Nordstrom P, Lorentzon R (1997) Aerobic workout and bone mass in females. Scand J Med Sci Sports 7:336–341. Alfredson H, Nordstrom P, Lorentzon R (1997) Aerobic workout and bone mass in females. Scand J Med Sci Sports 7:336–341.
34.
go back to reference Uusi–Rasi K, Sievanen H, Vuori I, Pasanen M, Heinonen A, Oja P (1998) Associations of physical activity and calcium intake with bone mass and size in healthy women at different ages. J Bone Miner Res 13:133–142. Uusi–Rasi K, Sievanen H, Vuori I, Pasanen M, Heinonen A, Oja P (1998) Associations of physical activity and calcium intake with bone mass and size in healthy women at different ages. J Bone Miner Res 13:133–142.
35.
go back to reference Heinonen A, Kannus P, Sievisan H, Oja P, Pasanen M, Rinne M, Uusi-Rasi K, Vuori I (1996) Randomised controlled trial of the effect of high impact exercise on selected risk factors for osteoporotic fractures. Lancet 348:1343–1347. Heinonen A, Kannus P, Sievisan H, Oja P, Pasanen M, Rinne M, Uusi-Rasi K, Vuori I (1996) Randomised controlled trial of the effect of high impact exercise on selected risk factors for osteoporotic fractures. Lancet 348:1343–1347.
36.
go back to reference Lohman T, Going S, Pamenter R, Hall M, Boyden T, Houtkooper L (1995) Effects of resistance training on regional and total bone mineral density in premenopausal women: a randomized prospective study. J Bone Miner Res 10:1015–1024. Lohman T, Going S, Pamenter R, Hall M, Boyden T, Houtkooper L (1995) Effects of resistance training on regional and total bone mineral density in premenopausal women: a randomized prospective study. J Bone Miner Res 10:1015–1024.
37.
go back to reference Friedlander A, Genant H, Sadowsky S, Byl N, Gluer C (1995) A two year program of aerobics and weight training enhances bone mineral density of young women. J Bone Miner Res 10:574–585. Friedlander A, Genant H, Sadowsky S, Byl N, Gluer C (1995) A two year program of aerobics and weight training enhances bone mineral density of young women. J Bone Miner Res 10:574–585.
38.
go back to reference Greendale GA, Edelstein S, Barrett-Connor E (1997) Endogenous sex steroids and bone mineral density in older women and men: the Rancho Bernardo study. J Bone Miner Res 12:1833–1843. Greendale GA, Edelstein S, Barrett-Connor E (1997) Endogenous sex steroids and bone mineral density in older women and men: the Rancho Bernardo study. J Bone Miner Res 12:1833–1843.
39.
go back to reference Heikkinen J, Kyllonen E, Kurttila-Matero E, Wilen Rosenquist G, Lankinen K, Rita H, Vaananen H (1997) HRT and exercise: effects on bone density, muscle strength and lipid metabolism in healthy postmenopausal women. Maturitas 26:139–149. Heikkinen J, Kyllonen E, Kurttila-Matero E, Wilen Rosenquist G, Lankinen K, Rita H, Vaananen H (1997) HRT and exercise: effects on bone density, muscle strength and lipid metabolism in healthy postmenopausal women. Maturitas 26:139–149.
40.
go back to reference Martin D, Notelovitz M (1993) Effects of aerobic training on bone mineral density of postmenopausal women. J Bone Miner Res 8:931–936. Martin D, Notelovitz M (1993) Effects of aerobic training on bone mineral density of postmenopausal women. J Bone Miner Res 8:931–936.
41.
go back to reference Bassey EJ, Rothwell MC, Littlewood JJ, Pye DW (1998) Pre- and post-menopausal women have different bone mineral density responses to the same high impact exercise. J Bone Miner Res 13:1805–1813. Bassey EJ, Rothwell MC, Littlewood JJ, Pye DW (1998) Pre- and post-menopausal women have different bone mineral density responses to the same high impact exercise. J Bone Miner Res 13:1805–1813.
42.
go back to reference Kohrt W, Ehsani A, Birge S (1998) HRT preserves increases in bone mineral density and reductions in body fat after a supervised exercise program. J Appl Physiol 84:1506–1512. Kohrt W, Ehsani A, Birge S (1998) HRT preserves increases in bone mineral density and reductions in body fat after a supervised exercise program. J Appl Physiol 84:1506–1512.
43.
go back to reference Kohrt W, Snead D, Slatopolsky E, Birge S (1995) Additive effects of weight bearing exercise and estrogen on bone mineral density in older women. J Bone Miner Res 10:1303–1311. Kohrt W, Snead D, Slatopolsky E, Birge S (1995) Additive effects of weight bearing exercise and estrogen on bone mineral density in older women. J Bone Miner Res 10:1303–1311.
44.
go back to reference Dook J, James C, Henderson N, Price R (1997) Exercise and bone mineral density in mature female athletes. Med Sci Sports Exerc 29:291–296. Dook J, James C, Henderson N, Price R (1997) Exercise and bone mineral density in mature female athletes. Med Sci Sports Exerc 29:291–296.
45.
go back to reference Shimegi S, Yanagita M, Okano H, Yamada M, Fukui H, Fukumura Y, Ibuki Y (1994) Physical exercise increases bone mineral density in postmenopausal women. Endocr J 41:49–56. Shimegi S, Yanagita M, Okano H, Yamada M, Fukui H, Fukumura Y, Ibuki Y (1994) Physical exercise increases bone mineral density in postmenopausal women. Endocr J 41:49–56.
46.
go back to reference Cummings SR, Browner WS, Bauer D, Stone K, Ensrud K, Jamal S, Ettinger B (1998) Endogenous hormones and the risk of hip and vertebral fractures among older women. N Engl J Med 339:733–738. Cummings SR, Browner WS, Bauer D, Stone K, Ensrud K, Jamal S, Ettinger B (1998) Endogenous hormones and the risk of hip and vertebral fractures among older women. N Engl J Med 339:733–738.
47.
go back to reference Thomas T, Burguera B (2002) Is leptin the link between fat and bone mass? J Bone Miner Res 17:1563–1569. Thomas T, Burguera B (2002) Is leptin the link between fat and bone mass? J Bone Miner Res 17:1563–1569.
48.
go back to reference Beck TJ, Looker AC, Ruff CB, Sievanen H, Wahner HW (2000) Structural trends in the ageing femoral neck and proximal shaft: analysis of the third national health and nutrition examination survey dual-energy X-ray absorptiometry data. J Bone Miner Res 15:2297–2308. Beck TJ, Looker AC, Ruff CB, Sievanen H, Wahner HW (2000) Structural trends in the ageing femoral neck and proximal shaft: analysis of the third national health and nutrition examination survey dual-energy X-ray absorptiometry data. J Bone Miner Res 15:2297–2308.
49.
go back to reference Crabtree N, Lunt M, Holt G, et al. (2000) Hip geometry, bone mineral distribution and bone strength in European men and women: the EPOS study. Bone 27:151–160. Crabtree N, Lunt M, Holt G, et al. (2000) Hip geometry, bone mineral distribution and bone strength in European men and women: the EPOS study. Bone 27:151–160.
Metadata
Title
Changes in bone mineral density in the hip and spine before, during, and after the menopause in elite runners
Authors
Alexandra Tomkinson
Jane H. Gibson
Mark Lunt
Mark Harries
Jonathan Reeve
Publication date
01-06-2003
Publisher
Springer-Verlag
Published in
Osteoporosis International / Issue 6/2003
Print ISSN: 0937-941X
Electronic ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-003-1376-5

Other articles of this Issue 6/2003

Osteoporosis International 6/2003 Go to the issue