Skip to main content
Top
Published in: Calcified Tissue International 6/2011

01-06-2011 | Original Research

Influence of Insulin-Like Growth Factor Binding Protein (IGFBP)-1 and IGFBP-3 on Bone Health: Results from the European Male Ageing Study

Authors: Stephen R. Pye, Bader Almusalam, Steven Boonen, Dirk Vanderschueren, Herman Borghs, Evelien Gielen, Judith E. Adams, Kate A. Ward, Gyorgy Bartfai, Felipe F. Casanueva, Joseph D. Finn, Gianni Forti, Aleksander Giwercman, Thang S. Han, Ilpo T. Huhtaniemi, Krzysztof Kula, Fernand Labrie, Michael E. J. Lean, Neil Pendleton, Margus Punab, Alan J. Silman, Frederick C. W. Wu, Terence W. O’Neill, The EMAS Study Group

Published in: Calcified Tissue International | Issue 6/2011

Login to get access

Abstract

The aim of this study was to determine the influence of insulin-like growth factor binding protein (IGFBP)-1, IGFBP-3, and IGF-I on calcaneal ultrasound parameters in middle-aged and elderly European men. Men aged 40–79 years were recruited from population registers for participation in the European Male Ageing Study (EMAS). Subjects were invited by letter to complete a postal questionnaire and to attend for an interviewer-assisted questionnaire, quantitative ultrasound (QUS) of the calcaneus, and a fasting blood sample from which serum levels of IGFBP-1, IGFBP-3, IGF-I, estradiol (E2), and SHBG were assayed. The questionnaires included the Physical Activity Scale for the Elderly (PASE) and questions about smoking and alcohol consumption. Estimated bone mineral density (eBMD) was derived as a function of the QUS parameters speed of sound and broadband ultrasound attenuation. Height and weight were measured in all subjects. 3057 men, mean age 59.7 years (standard deviation 11.0) were included in the analysis. After adjusting for age, center, and BMI, higher levels of IGFBP-1 were associated with lower eBMD. Higher levels of both IGFBP-3 and IGF-I were associated with higher eBMD. After further adjustment for PASE score, current smoking, alcohol consumption, free E2, and SHBG, IGFBP-3 and IGF-I, though not IGFBP-1, remained significantly associated with eBMD. IGFBP-1 was associated with bone health, though the effect could be explained by other factors. IGFBP-3 and IGF-I were independent determinants of bone health in middle-aged and elderly European men.
Appendix
Available only for authorised users
Literature
1.
go back to reference Giustina A, Mazziotti G, Canalis E (2008) Growth hormone, insulin-like growth factors, and the skeleton. Endocr Rev 29:535–559PubMedCrossRef Giustina A, Mazziotti G, Canalis E (2008) Growth hormone, insulin-like growth factors, and the skeleton. Endocr Rev 29:535–559PubMedCrossRef
2.
go back to reference Fall C, Hindmarsh P, Dennison E et al (1998) Programming of growth hormone secretion and bone mineral density in elderly men: a hypothesis. J Clin Endocrinol Metab 83:135–139PubMedCrossRef Fall C, Hindmarsh P, Dennison E et al (1998) Programming of growth hormone secretion and bone mineral density in elderly men: a hypothesis. J Clin Endocrinol Metab 83:135–139PubMedCrossRef
3.
go back to reference Gillberg P, Olofsson H, Mallmin H et al (2002) Bone mineral density in femoral neck is positively correlated to circulating insulin-like growth factor (IGF)-I and IGF-binding protein (IGFBP)-3 in Swedish men. Calcif Tissue Int 70:22–29PubMedCrossRef Gillberg P, Olofsson H, Mallmin H et al (2002) Bone mineral density in femoral neck is positively correlated to circulating insulin-like growth factor (IGF)-I and IGF-binding protein (IGFBP)-3 in Swedish men. Calcif Tissue Int 70:22–29PubMedCrossRef
4.
go back to reference Janssen JA, Burger H, Stolk RP et al (1998) Gender-specific relationship between serum free and total IGF-I and bone mineral density in elderly men and women. Eur J Endocrinol 138:627–632PubMedCrossRef Janssen JA, Burger H, Stolk RP et al (1998) Gender-specific relationship between serum free and total IGF-I and bone mineral density in elderly men and women. Eur J Endocrinol 138:627–632PubMedCrossRef
5.
go back to reference Krassas GE, Papadopoulou P, Koliakos G et al (2003) Growth hormone, insulin growth factor-1, and IGF binding protein-3 axis relationship with bone mineral density among healthy men. Arch Androl 49:191–199PubMedCrossRef Krassas GE, Papadopoulou P, Koliakos G et al (2003) Growth hormone, insulin growth factor-1, and IGF binding protein-3 axis relationship with bone mineral density among healthy men. Arch Androl 49:191–199PubMedCrossRef
6.
go back to reference Patel MB, Arden NK, Masterson LM et al (2005) Investigating the role of the growth hormone–insulin-like growth factor (GH–IGF) axis as a determinant of male bone mineral density (BMD). Bone 37:833–841PubMedCrossRef Patel MB, Arden NK, Masterson LM et al (2005) Investigating the role of the growth hormone–insulin-like growth factor (GH–IGF) axis as a determinant of male bone mineral density (BMD). Bone 37:833–841PubMedCrossRef
7.
go back to reference Sugimoto T, Nishiyama K, Kuribayashi F et al (1997) Serum levels of insulin-like growth factor (IGF) I, IGF-binding protein (IGFBP)-2, and IGFBP-3 in osteoporotic patients with and without spinal fractures. J Bone Miner Res 12:1272–1279PubMedCrossRef Sugimoto T, Nishiyama K, Kuribayashi F et al (1997) Serum levels of insulin-like growth factor (IGF) I, IGF-binding protein (IGFBP)-2, and IGFBP-3 in osteoporotic patients with and without spinal fractures. J Bone Miner Res 12:1272–1279PubMedCrossRef
8.
go back to reference Rucker D, Ezzat S, Diamandi A et al (2004) IGF-I and testosterone levels as predictors of bone mineral density in healthy, community-dwelling men. Clin Endocrinol 60:491–499CrossRef Rucker D, Ezzat S, Diamandi A et al (2004) IGF-I and testosterone levels as predictors of bone mineral density in healthy, community-dwelling men. Clin Endocrinol 60:491–499CrossRef
9.
go back to reference Barrett-Connor E, Goodman-Gruen D (1998) Gender differences in insulin-like growth factor and bone mineral density association in old age: the Rancho Bernardo Study. J Bone Miner Res 13:1343–1349PubMedCrossRef Barrett-Connor E, Goodman-Gruen D (1998) Gender differences in insulin-like growth factor and bone mineral density association in old age: the Rancho Bernardo Study. J Bone Miner Res 13:1343–1349PubMedCrossRef
10.
go back to reference Jehle PM, Jehle DR, Mohan S et al (1998) Serum levels of insulin-like growth factor system components and relationship to bone metabolism in type 1 and type 2 diabetes mellitus patients. J Endocrinol 159:297–306PubMedCrossRef Jehle PM, Jehle DR, Mohan S et al (1998) Serum levels of insulin-like growth factor system components and relationship to bone metabolism in type 1 and type 2 diabetes mellitus patients. J Endocrinol 159:297–306PubMedCrossRef
11.
go back to reference Rosen CJ (1999) Serum insulin-like growth factors and insulin-like growth factor-binding proteins: clinical implications. Clin Chem 45:1384–1390PubMed Rosen CJ (1999) Serum insulin-like growth factors and insulin-like growth factor-binding proteins: clinical implications. Clin Chem 45:1384–1390PubMed
12.
go back to reference Conover CA, Bale LK, Clarkson JT et al (1993) Potentiation of insulin-like growth factor action by insulin-like growth factor binding protein-3: studies of underlying mechanism. Growth Regul 3:87–88PubMed Conover CA, Bale LK, Clarkson JT et al (1993) Potentiation of insulin-like growth factor action by insulin-like growth factor binding protein-3: studies of underlying mechanism. Growth Regul 3:87–88PubMed
13.
go back to reference Szulc P, Joly-Pharaboz MO, Marchand F et al (2004) Insulin-like growth factor I is a determinant of hip bone mineral density in men less than 60 years of age: MINOS study. Calcif Tissue Int 74:322–329PubMedCrossRef Szulc P, Joly-Pharaboz MO, Marchand F et al (2004) Insulin-like growth factor I is a determinant of hip bone mineral density in men less than 60 years of age: MINOS study. Calcif Tissue Int 74:322–329PubMedCrossRef
14.
go back to reference Johansson AG, Eriksen EF, Lindh E et al (1997) Reduced serum levels of the growth hormone-dependent insulin-like growth factor binding protein and a negative bone balance at the level of individual remodeling units in idiopathic osteoporosis in men. J Clin Endocrinol Metab 82:2795–2798PubMedCrossRef Johansson AG, Eriksen EF, Lindh E et al (1997) Reduced serum levels of the growth hormone-dependent insulin-like growth factor binding protein and a negative bone balance at the level of individual remodeling units in idiopathic osteoporosis in men. J Clin Endocrinol Metab 82:2795–2798PubMedCrossRef
15.
go back to reference Conover CA, Lee PD, Riggs BL et al (1996) Insulin-like growth factor-binding protein-1 expression in cultured human bone cells: regulation by insulin and glucocorticoid. Endocrinology 137:3295–3301PubMedCrossRef Conover CA, Lee PD, Riggs BL et al (1996) Insulin-like growth factor-binding protein-1 expression in cultured human bone cells: regulation by insulin and glucocorticoid. Endocrinology 137:3295–3301PubMedCrossRef
16.
go back to reference Jassal SK, von Muhlen D, Barrett-Connor E et al (2005) Serum insulin-like growth factor binding protein-1 levels and bone mineral density in older adults: the Rancho Bernardo Study. Osteoporos Int 16:1948–1954PubMedCrossRef Jassal SK, von Muhlen D, Barrett-Connor E et al (2005) Serum insulin-like growth factor binding protein-1 levels and bone mineral density in older adults: the Rancho Bernardo Study. Osteoporos Int 16:1948–1954PubMedCrossRef
17.
go back to reference Lee DM, O’Neill TW, Pye SR et al (2009) The European Male Ageing Study (EMAS): design, methods and recruitment. Int J Androl 32:11–24PubMedCrossRef Lee DM, O’Neill TW, Pye SR et al (2009) The European Male Ageing Study (EMAS): design, methods and recruitment. Int J Androl 32:11–24PubMedCrossRef
18.
go back to reference Washburn RA, Smith KW, Jette AM et al (1993) The Physical Activity Scale for the Elderly (PASE): development and evaluation. J Clin Epidemiol 46:153–162PubMedCrossRef Washburn RA, Smith KW, Jette AM et al (1993) The Physical Activity Scale for the Elderly (PASE): development and evaluation. J Clin Epidemiol 46:153–162PubMedCrossRef
19.
go back to reference Wu FC, Tajar A, Pye SR et al (2008) Hypothalamic–pituitary–testicular axis disruptions in older men are differentially linked to age and modifiable risk factors: the European Male Aging Study. J Clin Endocrinol Metab 93:2737–2745PubMedCrossRef Wu FC, Tajar A, Pye SR et al (2008) Hypothalamic–pituitary–testicular axis disruptions in older men are differentially linked to age and modifiable risk factors: the European Male Aging Study. J Clin Endocrinol Metab 93:2737–2745PubMedCrossRef
20.
go back to reference Labrie F, Belanger A, Belanger P et al (2007) Metabolism of DHEA in postmenopausal women following percutaneous administration. J Steroid Biochem Mol Biol 103:178–188PubMedCrossRef Labrie F, Belanger A, Belanger P et al (2007) Metabolism of DHEA in postmenopausal women following percutaneous administration. J Steroid Biochem Mol Biol 103:178–188PubMedCrossRef
21.
go back to reference Labrie F, Belanger A, Belanger P et al (2006) Androgen glucuronides, instead of testosterone, as the new markers of androgenic activity in women. J Steroid Biochem Mol Biol 99:182–188PubMedCrossRef Labrie F, Belanger A, Belanger P et al (2006) Androgen glucuronides, instead of testosterone, as the new markers of androgenic activity in women. J Steroid Biochem Mol Biol 99:182–188PubMedCrossRef
22.
go back to reference Van Pottelbergh I, Goemaere S, Kaufman JM (2003) Bioavailable estradiol and an aromatase gene polymorphism are determinants of bone mineral density changes in men over 70 years of age. J Clin Endocrinol Metab 88:3075–3081PubMedCrossRef Van Pottelbergh I, Goemaere S, Kaufman JM (2003) Bioavailable estradiol and an aromatase gene polymorphism are determinants of bone mineral density changes in men over 70 years of age. J Clin Endocrinol Metab 88:3075–3081PubMedCrossRef
23.
go back to reference Vermeulen A, Verdonck L, Kaufman JM (1999) A critical evaluation of simple methods for the estimation of free testosterone in serum. J Clin Endocrinol Metab 84:3666–3672PubMedCrossRef Vermeulen A, Verdonck L, Kaufman JM (1999) A critical evaluation of simple methods for the estimation of free testosterone in serum. J Clin Endocrinol Metab 84:3666–3672PubMedCrossRef
24.
go back to reference Pye SR, Devakumar V, Boonen S et al (2010) Influence of lifestyle factors on quantitative heel ultrasound measurements in middle-aged and elderly men. Calcif Tissue Int 86:211–219PubMedCrossRef Pye SR, Devakumar V, Boonen S et al (2010) Influence of lifestyle factors on quantitative heel ultrasound measurements in middle-aged and elderly men. Calcif Tissue Int 86:211–219PubMedCrossRef
25.
go back to reference Kurland ES, Rosen CJ, Cosman F et al (1997) Insulin-like growth factor-I in men with idiopathic osteoporosis. J Clin Endocrinol Metab 82:2799–2805PubMedCrossRef Kurland ES, Rosen CJ, Cosman F et al (1997) Insulin-like growth factor-I in men with idiopathic osteoporosis. J Clin Endocrinol Metab 82:2799–2805PubMedCrossRef
26.
27.
go back to reference Rosen CJ, Donahue LR, Hunter SJ (1994) Insulin-like growth factors and bone: the osteoporosis connection. Proc Soc Exp Biol Med 206:83–102PubMed Rosen CJ, Donahue LR, Hunter SJ (1994) Insulin-like growth factors and bone: the osteoporosis connection. Proc Soc Exp Biol Med 206:83–102PubMed
28.
go back to reference Ebeling PR, Jones JD, O’Fallon WM et al (1993) Short-term effects of recombinant human insulin-like growth factor I on bone turnover in normal women. J Clin Endocrinol Metab 77:1384–1387PubMedCrossRef Ebeling PR, Jones JD, O’Fallon WM et al (1993) Short-term effects of recombinant human insulin-like growth factor I on bone turnover in normal women. J Clin Endocrinol Metab 77:1384–1387PubMedCrossRef
29.
go back to reference Grinspoon S, Baum H, Lee K et al (1996) Effects of short-term recombinant human insulin-like growth factor I administration on bone turnover in osteopenic women with anorexia nervosa. J Clin Endocrinol Metab 81:3864–3870PubMedCrossRef Grinspoon S, Baum H, Lee K et al (1996) Effects of short-term recombinant human insulin-like growth factor I administration on bone turnover in osteopenic women with anorexia nervosa. J Clin Endocrinol Metab 81:3864–3870PubMedCrossRef
30.
go back to reference Langlois JA, Rosen CJ, Visser M et al (1998) Association between insulin-like growth factor I and bone mineral density in older women and men: the Framingham Heart Study. J Clin Endocrinol Metab 83:4257–4262PubMedCrossRef Langlois JA, Rosen CJ, Visser M et al (1998) Association between insulin-like growth factor I and bone mineral density in older women and men: the Framingham Heart Study. J Clin Endocrinol Metab 83:4257–4262PubMedCrossRef
31.
go back to reference Bauer DC, Rosen C, Cauley J et al (1998) Low serum IGF-I but not IGFBP-3 predicts hip and spine fracture: the study of osteoporotic fracture. Bone 23(5 Suppl 1):S561 Bauer DC, Rosen C, Cauley J et al (1998) Low serum IGF-I but not IGFBP-3 predicts hip and spine fracture: the study of osteoporotic fracture. Bone 23(5 Suppl 1):S561
32.
go back to reference O’Neill TW, Marsden D, Matthis C et al (1995) Survey response rates: national and regional differences in a European multicentre study of vertebral osteoporosis. J Epidemiol Community Health 49:87–93PubMedCrossRef O’Neill TW, Marsden D, Matthis C et al (1995) Survey response rates: national and regional differences in a European multicentre study of vertebral osteoporosis. J Epidemiol Community Health 49:87–93PubMedCrossRef
33.
go back to reference Feldman HA, Goldstein I, Hatzichristou DG et al (1994) Impotence and its medical and psychosocial correlates: results of the Massachusetts Male Aging Study. J Urol 151:54–61PubMed Feldman HA, Goldstein I, Hatzichristou DG et al (1994) Impotence and its medical and psychosocial correlates: results of the Massachusetts Male Aging Study. J Urol 151:54–61PubMed
Metadata
Title
Influence of Insulin-Like Growth Factor Binding Protein (IGFBP)-1 and IGFBP-3 on Bone Health: Results from the European Male Ageing Study
Authors
Stephen R. Pye
Bader Almusalam
Steven Boonen
Dirk Vanderschueren
Herman Borghs
Evelien Gielen
Judith E. Adams
Kate A. Ward
Gyorgy Bartfai
Felipe F. Casanueva
Joseph D. Finn
Gianni Forti
Aleksander Giwercman
Thang S. Han
Ilpo T. Huhtaniemi
Krzysztof Kula
Fernand Labrie
Michael E. J. Lean
Neil Pendleton
Margus Punab
Alan J. Silman
Frederick C. W. Wu
Terence W. O’Neill
The EMAS Study Group
Publication date
01-06-2011
Publisher
Springer-Verlag
Published in
Calcified Tissue International / Issue 6/2011
Print ISSN: 0171-967X
Electronic ISSN: 1432-0827
DOI
https://doi.org/10.1007/s00223-011-9484-2

Other articles of this Issue 6/2011

Calcified Tissue International 6/2011 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.