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Published in: Calcified Tissue International 6/2009

01-06-2009

Bone Histomorphometry in Male Idiopathic Osteoporosis

Authors: Ylva Pernow, Ellen M. Hauge, Kristina Linder, Eilif Dahl, Maria Sääf

Published in: Calcified Tissue International | Issue 6/2009

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Abstract

The pathogenesis of male osteoporosis at the cellular level is still elusive. We performed histomorphometric analysis of bone biopsy samples from 51 eugonadal men with idiopathic osteoporosis. Their median age was 54 (range 29–73) years. Eighty-two percent of the patients had a fracture history, and 57% had vertebral fractures. Bone volume, trabecular thickness, wall thickness, and osteoid thickness were significantly reduced in osteoporotic men compared with healthy men. Erosion depth was similar, as were the bone remodeling parameters such as bone formation rate, mineral apposition rate, and activation frequency. In the osteoporotic men, osteoid thickness was correlated to bone mineral density at the lumbar spine (R 2 = 0.19, P < 0.01); together with wall thickness, the two parameters could explain 27% of the variation in lumbar spine bone mineral density. The osteoid thickness was correlated to anthropometric variables such as body weight (R 2 = 0.24, P < 0.001) and body mass index (R 2 = 0.14, P < 0.01), as well as to serum estradiol levels (R 2 = 0.14, P < 0.01) and to the ratio insulin-like growth factor-1 (IGF-1) to IGF-binding protein-1 (IGFBP-1) (R 2 = 0.12, P < 0.01). Regression analysis showed that 36% of the variation in osteoid thickness could be predicted by body weight and estradiol levels. In conclusion, bone histomorphometry in male idiopathic osteoporosis was characterized by thin bone structural units, which might suggest osteoblast dysfunction. Bone histomorphometry parameters were associated with low body weight, low estradiol levels, and increased levels of IGFBP-1, supporting the notion that estrogens and IGFs play regulatory roles in male bone turnover.
Literature
1.
go back to reference Gennari L, Bilezikian JP (2007) Osteoporosis in men: pathophysiology and treatment. Curr Rheumatol Rep 9:71–77PubMedCrossRef Gennari L, Bilezikian JP (2007) Osteoporosis in men: pathophysiology and treatment. Curr Rheumatol Rep 9:71–77PubMedCrossRef
2.
go back to reference Gillberg P, Johansson AG, Ljunghall S (1999) Decreased estradiol levels and free androgen index and elevated sex hormone–binding globulin levels in male idiopathic osteoporosis. Calcif Tissue Int 64:209–213PubMedCrossRef Gillberg P, Johansson AG, Ljunghall S (1999) Decreased estradiol levels and free androgen index and elevated sex hormone–binding globulin levels in male idiopathic osteoporosis. Calcif Tissue Int 64:209–213PubMedCrossRef
3.
go back to reference Kurland ES, Rosen CJ, Cosman F, McMahon D, Chan F, Shane E, Lindsay R, Dempster D, Bilezikian JP (1997) Insulin-like growth factor-1 in men with idiopathic osteoporosis. J Clin Endocrinol Metab 82:2799–2805PubMedCrossRef Kurland ES, Rosen CJ, Cosman F, McMahon D, Chan F, Shane E, Lindsay R, Dempster D, Bilezikian JP (1997) Insulin-like growth factor-1 in men with idiopathic osteoporosis. J Clin Endocrinol Metab 82:2799–2805PubMedCrossRef
4.
go back to reference Johansson AG, Eriksen EF, Lindh E, Langdahl B, Blum WF, Lindahl A, Ljunggren Ö, Ljunghall S (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 8:2795–2798CrossRef Johansson AG, Eriksen EF, Lindh E, Langdahl B, Blum WF, Lindahl A, Ljunggren Ö, Ljunghall S (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 8:2795–2798CrossRef
5.
go back to reference Carlsen CG, Soerensen TH, Eriksen EF (2000) Prevalence of low serum estradiol levels in male osteoporosis. Osteoporosis Int 11:697–701CrossRef Carlsen CG, Soerensen TH, Eriksen EF (2000) Prevalence of low serum estradiol levels in male osteoporosis. Osteoporosis Int 11:697–701CrossRef
6.
go back to reference Pernow Y, Granberg B, Sääf M, Weidenhielm L (2006) Osteoblast dysfunction in male idiopathic osteoporosis. Calcif Tissue Int 78:90–97PubMedCrossRef Pernow Y, Granberg B, Sääf M, Weidenhielm L (2006) Osteoblast dysfunction in male idiopathic osteoporosis. Calcif Tissue Int 78:90–97PubMedCrossRef
7.
go back to reference Francis RM, Peacock M, Marshall DH, Horsman A, Aaron JE (1989) Spinal osteoporosis in men. Bone Miner 5:347–357PubMedCrossRef Francis RM, Peacock M, Marshall DH, Horsman A, Aaron JE (1989) Spinal osteoporosis in men. Bone Miner 5:347–357PubMedCrossRef
8.
go back to reference Marie PJ, de Vernejoul MC, Connes D, Hott M (1991) Decreased DNA synthesis by cultured osteoblastic cells in eugonadal osteoporostic men with defective bone formation. J Clin Invest 88:1167–1172PubMedCrossRef Marie PJ, de Vernejoul MC, Connes D, Hott M (1991) Decreased DNA synthesis by cultured osteoblastic cells in eugonadal osteoporostic men with defective bone formation. J Clin Invest 88:1167–1172PubMedCrossRef
9.
go back to reference Zerwekh JE, Sakhaee K, Breslau NA, Gottschalk F, Pak CYC (1992) Impaired bone formation in male idiopathic osteoporosis: further reduction in the presence of concomitant hypercalcuria. Osteoporosis Int 2:128–134CrossRef Zerwekh JE, Sakhaee K, Breslau NA, Gottschalk F, Pak CYC (1992) Impaired bone formation in male idiopathic osteoporosis: further reduction in the presence of concomitant hypercalcuria. Osteoporosis Int 2:128–134CrossRef
10.
go back to reference Reed BY, Zerwekh JE, Sakhaee K, Breslau N, Gottschalk F, Pak CYC (1995) Serum IGF-1 is low and correlated with osteoblastic surface in idiopathic osteoporosis. J Bone Miner Res 10:1218–1224PubMed Reed BY, Zerwekh JE, Sakhaee K, Breslau N, Gottschalk F, Pak CYC (1995) Serum IGF-1 is low and correlated with osteoblastic surface in idiopathic osteoporosis. J Bone Miner Res 10:1218–1224PubMed
11.
go back to reference Kelepouris N, Harper KD, Gannon F, Kaplan FS, Haddad JG (1995) Severe osteoporosis in men. Ann Intern Med 56:359–363 Kelepouris N, Harper KD, Gannon F, Kaplan FS, Haddad JG (1995) Severe osteoporosis in men. Ann Intern Med 56:359–363
12.
go back to reference Delichatsios HK, Lane JM, Rivlin RS (1995) Bone histomorphometry in men with osteoporosis. Calcif Tissue Int 56:359–363PubMedCrossRef Delichatsios HK, Lane JM, Rivlin RS (1995) Bone histomorphometry in men with osteoporosis. Calcif Tissue Int 56:359–363PubMedCrossRef
13.
go back to reference Ciria-Recasens M, Perez-Edo L, Blanch-Rubio J, Marinoso ML, Benito-Ruiz P, Serrano S, Carbonell-Abello J (2005) Bone histomorphometry in 22 male patients with normocalcuric idiopathic osteoporosis. Bone 36:926–930PubMedCrossRef Ciria-Recasens M, Perez-Edo L, Blanch-Rubio J, Marinoso ML, Benito-Ruiz P, Serrano S, Carbonell-Abello J (2005) Bone histomorphometry in 22 male patients with normocalcuric idiopathic osteoporosis. Bone 36:926–930PubMedCrossRef
14.
go back to reference Legrand E, Chappard D, Pascaretti C, Duquenne M, Krebs S, Rohmer V, Baslé MF, Audran M (2000) Trabecular bone microarchitecture, bone mineral density, and vertebral fractures in male osteoporosis. J Bone Miner Res 15:13–19PubMedCrossRef Legrand E, Chappard D, Pascaretti C, Duquenne M, Krebs S, Rohmer V, Baslé MF, Audran M (2000) Trabecular bone microarchitecture, bone mineral density, and vertebral fractures in male osteoporosis. J Bone Miner Res 15:13–19PubMedCrossRef
15.
go back to reference Legrand E, Audran M, Guggenbuhl P, Levasseur R, Chalès G, Baslé MF, Chappard D (2007) Trabecular bone microarchitecture is related to the number of risk factors and etiology in osteoporotic men. Microsc Res Tech 70:952–959PubMedCrossRef Legrand E, Audran M, Guggenbuhl P, Levasseur R, Chalès G, Baslé MF, Chappard D (2007) Trabecular bone microarchitecture is related to the number of risk factors and etiology in osteoporotic men. Microsc Res Tech 70:952–959PubMedCrossRef
16.
go back to reference Chavassieux P, Meunier PJ (2001) Histomorphometric approach of bone loss in men. Calcif Tissue Int 69:209–213PubMedCrossRef Chavassieux P, Meunier PJ (2001) Histomorphometric approach of bone loss in men. Calcif Tissue Int 69:209–213PubMedCrossRef
17.
go back to reference Genant HK, Grampp S, Gluer CC, Faulkner KG, Jergas M, Engelke K, Hagiwara S, van Kuijk C (1994) Universal standardization for dual x-ray absorptiometry: patient and phantom cross-calibration results. J Bone Miner Res 9:1503–1514PubMed Genant HK, Grampp S, Gluer CC, Faulkner KG, Jergas M, Engelke K, Hagiwara S, van Kuijk C (1994) Universal standardization for dual x-ray absorptiometry: patient and phantom cross-calibration results. J Bone Miner Res 9:1503–1514PubMed
18.
go back to reference Dahl E, Nordahl KP, Halse J, Attramadal A (1988) Histomorphometric analysis of normal bone from the iliac crest of Norwegian subjects. Bone Miner 3:369–377PubMed Dahl E, Nordahl KP, Halse J, Attramadal A (1988) Histomorphometric analysis of normal bone from the iliac crest of Norwegian subjects. Bone Miner 3:369–377PubMed
19.
go back to reference Eriksen EF, Melsen F, Mosekilde L (1984) Reconstruction of the resorptive site in iliac trabecular bone: a kinetic model for bone resorption in 20 normal individuals. Metab Bone Dis Relat Res 5:235–242PubMedCrossRef Eriksen EF, Melsen F, Mosekilde L (1984) Reconstruction of the resorptive site in iliac trabecular bone: a kinetic model for bone resorption in 20 normal individuals. Metab Bone Dis Relat Res 5:235–242PubMedCrossRef
20.
go back to reference Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR (1987) Bone histomorphometry: standardization of nomenclature, symbols, and units Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 2:595–610PubMedCrossRef Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR (1987) Bone histomorphometry: standardization of nomenclature, symbols, and units Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 2:595–610PubMedCrossRef
21.
go back to reference Hauge EM, Mosekilde L, Melsen F, Frydenberg M (2001) How many patients are needed? Variation and design considerations in bone histomorphometry. Bone 28:556–562PubMedCrossRef Hauge EM, Mosekilde L, Melsen F, Frydenberg M (2001) How many patients are needed? Variation and design considerations in bone histomorphometry. Bone 28:556–562PubMedCrossRef
22.
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
23.
go back to reference Bang P, Eriksson U, Sara V, Wivall IL, Hall K (1991) Comparison of acid ethanol extraction and acid gel filtration prior to IGF-1 and IGF-2 radioimmunoassays: improvement of determination in acid ethanol extracts by the use of truncated IGF-I as radioligand. Acta Endocrinol (Copenh) 124:620–629 Bang P, Eriksson U, Sara V, Wivall IL, Hall K (1991) Comparison of acid ethanol extraction and acid gel filtration prior to IGF-1 and IGF-2 radioimmunoassays: improvement of determination in acid ethanol extracts by the use of truncated IGF-I as radioligand. Acta Endocrinol (Copenh) 124:620–629
24.
go back to reference Hilding A, Hall K, Wivall-Helleryd IL, Sääf M, Melin AL, Thoren M (1999) Serum levels of insulin-like growth factor-I in 152 patients with growth hormone deficiency, aged 19–82 years, in relation to those in healthy subjects. J Clin Endocrinol Metab 84:2013–2019PubMedCrossRef Hilding A, Hall K, Wivall-Helleryd IL, Sääf M, Melin AL, Thoren M (1999) Serum levels of insulin-like growth factor-I in 152 patients with growth hormone deficiency, aged 19–82 years, in relation to those in healthy subjects. J Clin Endocrinol Metab 84:2013–2019PubMedCrossRef
25.
go back to reference Povoa G, Roovete A, Hall K (1984) Crossreaction of somatomedin-binding protein a radioimmunoassay developed for somatomedin binding protein isolated from human amniotic fluid. Acta Endocrinol (Copenh) 107:563–570 Povoa G, Roovete A, Hall K (1984) Crossreaction of somatomedin-binding protein a radioimmunoassay developed for somatomedin binding protein isolated from human amniotic fluid. Acta Endocrinol (Copenh) 107:563–570
26.
go back to reference Siersbaek-Nielsen K, Hansen JM, Kampmann J, Kistensen M (1971) Rapid evaluation of creatinine clearance. Lancet 1:1133–1134PubMedCrossRef Siersbaek-Nielsen K, Hansen JM, Kampmann J, Kistensen M (1971) Rapid evaluation of creatinine clearance. Lancet 1:1133–1134PubMedCrossRef
27.
go back to reference Hauge E, Mosekilde L, Melsen F (1999) Missing observations in bone histomorphometry on osteoporosis: implications and suggestions for an approach. Bone 25:389–395PubMedCrossRef Hauge E, Mosekilde L, Melsen F (1999) Missing observations in bone histomorphometry on osteoporosis: implications and suggestions for an approach. Bone 25:389–395PubMedCrossRef
28.
go back to reference Khosla S, Melton JLIII, Atkinson AT, O′Fallon WM, Klee GG, Riggs LB (1988) Relationship between 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 83:2266–2274CrossRef Khosla S, Melton JLIII, Atkinson AT, O′Fallon WM, Klee GG, Riggs LB (1988) Relationship between 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 83:2266–2274CrossRef
29.
go back to reference Resch H, Pietschmann P, Woloszczuk W, Krexner E, Bernecker P, Willvonseder R (1992) Bone mass and biochemical parameters of bone metabolism in men with spinal osteoporosis. Eur J Clin Invest 22:542–545PubMedCrossRef Resch H, Pietschmann P, Woloszczuk W, Krexner E, Bernecker P, Willvonseder R (1992) Bone mass and biochemical parameters of bone metabolism in men with spinal osteoporosis. Eur J Clin Invest 22:542–545PubMedCrossRef
30.
go back to reference Pietschmann P, Kudlacek S, Grisar J, Spitzauer S, Woloszczuk W, Willvonseder R, Peterlik M (2001) Bone turnover markers and sex hormones in men with idiopathic osteoporosis. Eur J Clin Invest 31:444–451PubMedCrossRef Pietschmann P, Kudlacek S, Grisar J, Spitzauer S, Woloszczuk W, Willvonseder R, Peterlik M (2001) Bone turnover markers and sex hormones in men with idiopathic osteoporosis. Eur J Clin Invest 31:444–451PubMedCrossRef
31.
go back to reference Szulc P, Munoz F, Claustrat B, Garnero P, Marchand F, Duboeuf F, Delmas PD (2001) Bioavailable estradiol may be an important determinant of osteoporosis in men: the MINOS Study. J Clin Endocrinol Metab 86:192–199PubMedCrossRef Szulc P, Munoz F, Claustrat B, Garnero P, Marchand F, Duboeuf F, Delmas PD (2001) Bioavailable estradiol may be an important determinant of osteoporosis in men: the MINOS Study. J Clin Endocrinol Metab 86:192–199PubMedCrossRef
32.
go back to reference Jehle PM, Schulten K, Schulz W, Jehle DR, Stracke S, Manfras B, Boehm BO, Baylink DJ, Mohan S (2003) Serum levels of insulin-like growth factor (IGF)-I and IGF binding protein (IGFBP) 1–6 and their relationship to bone metabolism in osteoporosis patients. Eur J Intern Med 14:32–38PubMedCrossRef Jehle PM, Schulten K, Schulz W, Jehle DR, Stracke S, Manfras B, Boehm BO, Baylink DJ, Mohan S (2003) Serum levels of insulin-like growth factor (IGF)-I and IGF binding protein (IGFBP) 1–6 and their relationship to bone metabolism in osteoporosis patients. Eur J Intern Med 14:32–38PubMedCrossRef
33.
go back to reference Wolk K, Larsson SC, Vessby B, Wolk A, Brismar K (2004) Metabolic, anthropometric and nutritional factors as predictors of circulating insulin-like growth factor binding protein-1 levels in middle-aged and elderly men. J Clin Endocrinol Metab 89:1879–1884PubMedCrossRef Wolk K, Larsson SC, Vessby B, Wolk A, Brismar K (2004) Metabolic, anthropometric and nutritional factors as predictors of circulating insulin-like growth factor binding protein-1 levels in middle-aged and elderly men. J Clin Endocrinol Metab 89:1879–1884PubMedCrossRef
34.
go back to reference Underwood LE, Thissen JP, Lemozy S, Ketelsleger JM, Clemmons DR (1994) Hormonal and nutritional regulation og IGF-1 and its binding proteins. Horm Res 42:145–151PubMedCrossRef Underwood LE, Thissen JP, Lemozy S, Ketelsleger JM, Clemmons DR (1994) Hormonal and nutritional regulation og IGF-1 and its binding proteins. Horm Res 42:145–151PubMedCrossRef
35.
go back to reference Jassal SK, Muhlen D, Barrett-Connor E, Rosen CJ (2005) Serum insulin-like growth factor binding protein-1 levels and bone mineral density in older adults: the Rancho Bernado Study. Osteoporosis Int 16:1948–1954CrossRef Jassal SK, Muhlen D, Barrett-Connor E, Rosen CJ (2005) Serum insulin-like growth factor binding protein-1 levels and bone mineral density in older adults: the Rancho Bernado Study. Osteoporosis Int 16:1948–1954CrossRef
36.
go back to reference De Laet C, Kanis JA, Oden A, Johanson H, Johnell O, Delmas P, Eisman JA, Kroger H, Fujiwara S, Garnero P, McCloskey EV, Mellstrom D, Melton LJ III, Meunier PJ, Pols HAP, Reeve J, Silman A, Tenenhouse A (2005) Body mass index as a predictor of fracture risk: a meta analysis. Osteoporosis Int 16:1330–1338CrossRef De Laet C, Kanis JA, Oden A, Johanson H, Johnell O, Delmas P, Eisman JA, Kroger H, Fujiwara S, Garnero P, McCloskey EV, Mellstrom D, Melton LJ III, Meunier PJ, Pols HAP, Reeve J, Silman A, Tenenhouse A (2005) Body mass index as a predictor of fracture risk: a meta analysis. Osteoporosis Int 16:1330–1338CrossRef
37.
go back to reference Kanis J, Johnell O, Gullberg B, Allander E, Elffors L, Ranstam I, Dequeker J, Dilsen G, Gennari C, Vaz AL, Lyritis G, Mazzuoli G, Miravet L, Passeri M, Perez Cano R, Rapado A, Ribot C (1999) Risk factors for hip fracture in men from southern Europe: the MEDOS Study, Mediterranean Osteoporosis Study. Osteoporos Int 9:45–54PubMedCrossRef Kanis J, Johnell O, Gullberg B, Allander E, Elffors L, Ranstam I, Dequeker J, Dilsen G, Gennari C, Vaz AL, Lyritis G, Mazzuoli G, Miravet L, Passeri M, Perez Cano R, Rapado A, Ribot C (1999) Risk factors for hip fracture in men from southern Europe: the MEDOS Study, Mediterranean Osteoporosis Study. Osteoporos Int 9:45–54PubMedCrossRef
Metadata
Title
Bone Histomorphometry in Male Idiopathic Osteoporosis
Authors
Ylva Pernow
Ellen M. Hauge
Kristina Linder
Eilif Dahl
Maria Sääf
Publication date
01-06-2009
Publisher
Springer-Verlag
Published in
Calcified Tissue International / Issue 6/2009
Print ISSN: 0171-967X
Electronic ISSN: 1432-0827
DOI
https://doi.org/10.1007/s00223-009-9239-5

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