Skip to main content
Top

Open Access 01-12-2013 | Original Article

Early changes in biochemical markers of bone formation during teriparatide therapy correlate with improvements in vertebral strength in men with glucocorticoid-induced osteoporosis

Authors: P. Farahmand, F. Marin, F. Hawkins, R. Möricke, J. D. Ringe, C.-C. Glüer, N. Papaioannou, S. Minisola, G. Martínez, J. M. Nolla, C. Niedhart, N. Guañabens, R. Nuti, E. Martín-Mola, F. Thomasius, J. Peña, C. Graeff, G. Kapetanos, H. Petto, A. Gentzel, A. Reisinger, P. K. Zysset

Published in: Osteoporosis International | Issue 12/2013

Login to get access

Abstract

Summary

Changes of the bone formation marker PINP correlated positively with improvements in vertebral strength in men with glucocorticoid-induced osteoporosis (GIO) who received 18-month treatment with teriparatide, but not with risedronate. These results support the use of PINP as a surrogate marker of bone strength in GIO patients treated with teriparatide.

Introduction

To investigate the correlations between biochemical markers of bone turnover and vertebral strength estimated by finite element analysis (FEA) in men with GIO.

Methods

A total of 92 men with GIO were included in an 18-month, randomized, open-label trial of teriparatide (20 μg/day, n = 45) and risedronate (35 mg/week, n = 47). High-resolution quantitative computed tomography images of the 12th thoracic vertebra obtained at baseline, 6 and 18 months were converted into digital nonlinear FE models and subjected to anterior bending, axial compression and torsion. Stiffness and strength were computed for each model and loading mode. Serum biochemical markers of bone formation (amino-terminal-propeptide of type I collagen [PINP]) and bone resorption (type I collagen cross-linked C-telopeptide degradation fragments [CTx]) were measured at baseline, 3 months, 6 months and 18 months. A mixed-model of repeated measures analysed changes from baseline and between-group differences. Spearman correlations assessed the relationship between changes from baseline of bone markers with FEA variables.

Results

PINP and CTx levels increased in the teriparatide group and decreased in the risedronate group. FEA-derived parameters increased in both groups, but were significantly higher at 18 months in the teriparatide group. Significant positive correlations were found between changes from baseline of PINP at 3, 6 and 18 months with changes in FE strength in the teriparatide-treated group, but not in the risedronate group.

Conclusions

Positive correlations between changes in a biochemical marker of bone formation and improvement of biomechanical properties support the use of PINP as a surrogate marker of bone strength in teriparatide-treated GIO patients.
Literature
1.
go back to reference Vasikaran S, Eastell R, Bruyère O, Foldes AJ, Garnero P, Griesmacher A, McClung M, Morris HA, Silverman S, Trenti T, Wahl DA, Cooper C, Kanis JA, IOF–IFCC Bone Marker Standards Working Group (2011) Markers of bone turnover for the prediction of fracture risk and monitoring of osteoporosis treatment: a need for international reference standards. Osteoporos Int 22:391–420PubMedCrossRef Vasikaran S, Eastell R, Bruyère O, Foldes AJ, Garnero P, Griesmacher A, McClung M, Morris HA, Silverman S, Trenti T, Wahl DA, Cooper C, Kanis JA, IOF–IFCC Bone Marker Standards Working Group (2011) Markers of bone turnover for the prediction of fracture risk and monitoring of osteoporosis treatment: a need for international reference standards. Osteoporos Int 22:391–420PubMedCrossRef
2.
go back to reference Szulc P (2012) The role of bone turnover markers in monitoring treatment in postmenopausal osteoporosis. Clin Biochem 45:907–919PubMedCrossRef Szulc P (2012) The role of bone turnover markers in monitoring treatment in postmenopausal osteoporosis. Clin Biochem 45:907–919PubMedCrossRef
3.
go back to reference Ravn P, Clemmesen B, Christiansen C (1999) Biochemical markers can predict the response in bone mass during alendronate treatment in early postmenopausal women. Alendronate Osteoporosis Prevention Study Group. Bone 24:237–244PubMedCrossRef Ravn P, Clemmesen B, Christiansen C (1999) Biochemical markers can predict the response in bone mass during alendronate treatment in early postmenopausal women. Alendronate Osteoporosis Prevention Study Group. Bone 24:237–244PubMedCrossRef
4.
go back to reference Lane NE, Sanchez S, Genant HK, Jenkins DK, Arnaud CD (2000) Short-term increases in bone turnover markers predict parathyroid hormone-induced spinal bone mineral density gains in postmenopausal women with glucocorticoid-induced osteoporosis. Osteoporos Int 11:434–442PubMedCrossRef Lane NE, Sanchez S, Genant HK, Jenkins DK, Arnaud CD (2000) Short-term increases in bone turnover markers predict parathyroid hormone-induced spinal bone mineral density gains in postmenopausal women with glucocorticoid-induced osteoporosis. Osteoporos Int 11:434–442PubMedCrossRef
5.
go back to reference Bjarnason NH, Sarkar S, Duong T, Mitlak B, Delmas PD, Christiansen C (2001) Six and twelve month changes in bone turnover are related to reduction in vertebral fracture risk during 3 years of raloxifene treatment in postmenopausal osteoporosis. Osteoporos Int 12:922–930PubMedCrossRef Bjarnason NH, Sarkar S, Duong T, Mitlak B, Delmas PD, Christiansen C (2001) Six and twelve month changes in bone turnover are related to reduction in vertebral fracture risk during 3 years of raloxifene treatment in postmenopausal osteoporosis. Osteoporos Int 12:922–930PubMedCrossRef
6.
go back to reference Reginster JY, Sarkar S, Zegels B, Henrotin Y, Bruyere O, Agnusdei D, Collette J (2004) Reduction in PINP, a marker of bone metabolism, with raloxifene treatment and its relationship with vertebral fracture risk. Bone 34:344–351PubMedCrossRef Reginster JY, Sarkar S, Zegels B, Henrotin Y, Bruyere O, Agnusdei D, Collette J (2004) Reduction in PINP, a marker of bone metabolism, with raloxifene treatment and its relationship with vertebral fracture risk. Bone 34:344–351PubMedCrossRef
7.
go back to reference Bauer DC, Black DM, Garnero P, Hochberg M, Ott S, Orloff J, Thompson DE, Ewing SK, Delmas PD; Fracture Intervention Trial Study Group (2004) Change in bone turnover and hip, non-spine, and vertebral fracture in alendronate-treated women: the Fracture Intervention Trial. J Bone Miner Res 19:1250–1258CrossRef Bauer DC, Black DM, Garnero P, Hochberg M, Ott S, Orloff J, Thompson DE, Ewing SK, Delmas PD; Fracture Intervention Trial Study Group (2004) Change in bone turnover and hip, non-spine, and vertebral fracture in alendronate-treated women: the Fracture Intervention Trial. J Bone Miner Res 19:1250–1258CrossRef
8.
go back to reference Sarkar S, Reginster JY, Crans GG, Diez-Perez A, Pinette KV, Delmas PD (2004) Relationship between changes in biochemical markers of bone turnover and BMD to predict vertebral fracture risk. J Bone Miner Res 19:394–401PubMedCrossRef Sarkar S, Reginster JY, Crans GG, Diez-Perez A, Pinette KV, Delmas PD (2004) Relationship between changes in biochemical markers of bone turnover and BMD to predict vertebral fracture risk. J Bone Miner Res 19:394–401PubMedCrossRef
9.
go back to reference Chen P, Satterwhite JH, Licata AA, Lewiecki EM, Sipos AA, Misurski DM, Wagman RB (2005) Early changes in biochemical markers of bone formation predict BMD response to teriparatide in postmenopausal women with osteoporosis. J Bone Miner Res 20:962–970PubMedCrossRef Chen P, Satterwhite JH, Licata AA, Lewiecki EM, Sipos AA, Misurski DM, Wagman RB (2005) Early changes in biochemical markers of bone formation predict BMD response to teriparatide in postmenopausal women with osteoporosis. J Bone Miner Res 20:962–970PubMedCrossRef
10.
go back to reference Dobnig H, Sipos A, Jiang Y, Fahrleitner-Pammer A, Ste-Marie LG, Gallagher JC, Pavo I, Wang J, Eriksen EF (2005) Early changes in biochemical markers of bone formation correlate with improvements in bone structure during teriparatide therapy. J Clin Endocrinol Metab 90:3970–3977PubMedCrossRef Dobnig H, Sipos A, Jiang Y, Fahrleitner-Pammer A, Ste-Marie LG, Gallagher JC, Pavo I, Wang J, Eriksen EF (2005) Early changes in biochemical markers of bone formation correlate with improvements in bone structure during teriparatide therapy. J Clin Endocrinol Metab 90:3970–3977PubMedCrossRef
11.
go back to reference Greenspan SL, Resnick NM, Parker RA (2005) Early changes in biochemical markers of bone turnover are associated with long-term changes in bone mineral density in elderly women on alendronate, hormone replacement therapy, or combination therapy: a three-year, double-blind, placebo-controlled, randomized clinical trial. J Clin Endocrinol Metab 90:2762–2767PubMedCrossRef Greenspan SL, Resnick NM, Parker RA (2005) Early changes in biochemical markers of bone turnover are associated with long-term changes in bone mineral density in elderly women on alendronate, hormone replacement therapy, or combination therapy: a three-year, double-blind, placebo-controlled, randomized clinical trial. J Clin Endocrinol Metab 90:2762–2767PubMedCrossRef
12.
go back to reference Bauer DC, Garnero P, Bilezikian JP, Greenspan SL, Ensrud KE, Rosen CJ, Palermo L, Black DM (2006) Short-term changes in bone turnover markers and bone mineral density response to parathyroid hormone in postmenopausal women with osteoporosis. J Clin Endocrinol Metab 91:1370–1375PubMedCrossRef Bauer DC, Garnero P, Bilezikian JP, Greenspan SL, Ensrud KE, Rosen CJ, Palermo L, Black DM (2006) Short-term changes in bone turnover markers and bone mineral density response to parathyroid hormone in postmenopausal women with osteoporosis. J Clin Endocrinol Metab 91:1370–1375PubMedCrossRef
13.
go back to reference Finkelstein JS, Leder BZ, Burnett SM, Wyland JJ, Lee H, de la Paz AV, Gibson K, Neer RM (2006) Effects of teriparatide, alendronate, or both on bone turnover in osteoporotic men. J Clin Endocrinol Metab 91:2882–2887PubMedCrossRef Finkelstein JS, Leder BZ, Burnett SM, Wyland JJ, Lee H, de la Paz AV, Gibson K, Neer RM (2006) Effects of teriparatide, alendronate, or both on bone turnover in osteoporotic men. J Clin Endocrinol Metab 91:2882–2887PubMedCrossRef
14.
go back to reference Jacobs JW, de Nijs RN, Lems WF, Geusens PM, Laan RF, Huisman AM, Algra A, Buskens E, Hofbauer LC, Oostveen AC, Bruyn GA, Dijkmans BA, Bijlsma JW (2007) Prevention of glucocorticoid induced osteoporosis with alendronate or alfacalcidol: relations of change in bone mineral density, bone markers, and calcium homeostasis. J Rheumatol 34:1051–1057PubMed Jacobs JW, de Nijs RN, Lems WF, Geusens PM, Laan RF, Huisman AM, Algra A, Buskens E, Hofbauer LC, Oostveen AC, Bruyn GA, Dijkmans BA, Bijlsma JW (2007) Prevention of glucocorticoid induced osteoporosis with alendronate or alfacalcidol: relations of change in bone mineral density, bone markers, and calcium homeostasis. J Rheumatol 34:1051–1057PubMed
15.
go back to reference Delmas PD, Munoz F, Black DM, Cosman F, Boonen S, Watts NB, Kendler D, Eriksen EF, Mesenbrink PG, Eastell R; HORIZON-PFT Research Group (2009) Effects of yearly zoledronic acid 5 mg on bone turnover markers and relation of PINP with fracture reduction in postmenopausal women with osteoporosis. J Bone Miner Res 24:1544–1551CrossRef Delmas PD, Munoz F, Black DM, Cosman F, Boonen S, Watts NB, Kendler D, Eriksen EF, Mesenbrink PG, Eastell R; HORIZON-PFT Research Group (2009) Effects of yearly zoledronic acid 5 mg on bone turnover markers and relation of PINP with fracture reduction in postmenopausal women with osteoporosis. J Bone Miner Res 24:1544–1551CrossRef
16.
go back to reference Burshell AL, Möricke R, Correa-Rotter R, Chen P, Warner MR, Dalsky GP, Taylor KA, Krege JH (2010) Correlations between biochemical markers of bone turnover and bone density responses in patients with glucocorticoid-induced osteoporosis treated with teriparatide or alendronate. Bone 46:935–939PubMedCrossRef Burshell AL, Möricke R, Correa-Rotter R, Chen P, Warner MR, Dalsky GP, Taylor KA, Krege JH (2010) Correlations between biochemical markers of bone turnover and bone density responses in patients with glucocorticoid-induced osteoporosis treated with teriparatide or alendronate. Bone 46:935–939PubMedCrossRef
17.
go back to reference Hochberg MC, Silverman SL, Barr CE, Miller PD (2010) The utility of changes in serum levels of C-terminal telopeptide of type I collagen in predicting patient response to oral monthly ibandronate therapy. J Clin Densitom 13:181–189PubMedCrossRef Hochberg MC, Silverman SL, Barr CE, Miller PD (2010) The utility of changes in serum levels of C-terminal telopeptide of type I collagen in predicting patient response to oral monthly ibandronate therapy. J Clin Densitom 13:181–189PubMedCrossRef
18.
go back to reference Blumsohn A, Marin F, Nickelsen T, Brixen K, Sigurdsson G, González de la Vera J, Boonen S, Liu-Léage S, Barker C, Eastell R; EUROFORS Study Group (2011) Early changes in biochemical markers of bone turnover and their relationship with bone mineral density changes after 24 months of treatment with teriparatide. Osteoporos Int 22:1935–1946CrossRef Blumsohn A, Marin F, Nickelsen T, Brixen K, Sigurdsson G, González de la Vera J, Boonen S, Liu-Léage S, Barker C, Eastell R; EUROFORS Study Group (2011) Early changes in biochemical markers of bone turnover and their relationship with bone mineral density changes after 24 months of treatment with teriparatide. Osteoporos Int 22:1935–1946CrossRef
19.
go back to reference Eastell R, Vrijens B, Cahall DL, Ringe JD, Garnero P, Watts NB (2011) Bone turnover markers and bone mineral density response with risedronate therapy: relationship with fracture risk and patient adherence. J Bone Miner Res 26:1662–1669PubMedCrossRef Eastell R, Vrijens B, Cahall DL, Ringe JD, Garnero P, Watts NB (2011) Bone turnover markers and bone mineral density response with risedronate therapy: relationship with fracture risk and patient adherence. J Bone Miner Res 26:1662–1669PubMedCrossRef
20.
go back to reference Eastell R, Christiansen C, Grauer A, Kutilek S, Libanati C, McClung MR, Reid IR, Resch H, Siris E, Uebelhart D, Wang A, Weryha G, Cummings SR (2011) Effects of denosumab on bone turnover markers in postmenopausal osteoporosis. J Bone Miner Res 26:530–537PubMedCrossRef Eastell R, Christiansen C, Grauer A, Kutilek S, Libanati C, McClung MR, Reid IR, Resch H, Siris E, Uebelhart D, Wang A, Weryha G, Cummings SR (2011) Effects of denosumab on bone turnover markers in postmenopausal osteoporosis. J Bone Miner Res 26:530–537PubMedCrossRef
21.
go back to reference Tsujimoto M, Chen P, Miyauchi A, Sowa H, Krege JH (2011) PINP as an aid for monitoring patients treated with teriparatide. Bone 48:793–803CrossRef Tsujimoto M, Chen P, Miyauchi A, Sowa H, Krege JH (2011) PINP as an aid for monitoring patients treated with teriparatide. Bone 48:793–803CrossRef
22.
go back to reference Faulkner KG, Cann CE, Hasegawa BH (1991) Effect of bone distribution on vertebral strength: assessment with patient-specific nonlinear finite element analysis. Radiology 179:669–674PubMed Faulkner KG, Cann CE, Hasegawa BH (1991) Effect of bone distribution on vertebral strength: assessment with patient-specific nonlinear finite element analysis. Radiology 179:669–674PubMed
23.
go back to reference Crawford RP, Cann CE, Keaveny TM (2003) Finite element models predict in vitro vertebral body compressive strength better than quantitative computed tomography. Bone 33:744–750PubMedCrossRef Crawford RP, Cann CE, Keaveny TM (2003) Finite element models predict in vitro vertebral body compressive strength better than quantitative computed tomography. Bone 33:744–750PubMedCrossRef
24.
25.
go back to reference Dall’Ara E, Pahr D, Varga P, Kainberger F, Zysset P (2012) QCT-based finite element models predict human vertebral strength in vitro significantly better than simulated DEXA. Osteoporos Int 23:563–572PubMedCrossRef Dall’Ara E, Pahr D, Varga P, Kainberger F, Zysset P (2012) QCT-based finite element models predict human vertebral strength in vitro significantly better than simulated DEXA. Osteoporos Int 23:563–572PubMedCrossRef
26.
go back to reference Keaveny TM, Donley DW, Hoffmann PF, Mitlak BH, Glass EV, San Martin JA (2007) Effects of teriparatide and alendronate on vertebral strength as assessed by finite element modeling of QCT scans in women with osteoporosis. J Bone Miner Res 22:149–157PubMedCrossRef Keaveny TM, Donley DW, Hoffmann PF, Mitlak BH, Glass EV, San Martin JA (2007) Effects of teriparatide and alendronate on vertebral strength as assessed by finite element modeling of QCT scans in women with osteoporosis. J Bone Miner Res 22:149–157PubMedCrossRef
27.
go back to reference Graeff C, Chevalier Y, Charlebois M, Varga P, Pahr D, Nickelsen TN, Morlock MM, Glüer CC, Zysset PK (2009) Improvements in vertebral body strength under teriparatide treatment assessed in vivo by finite element analysis: results from the EUROFORS study. J Bone Miner Res 24:1672–1680PubMedCrossRef Graeff C, Chevalier Y, Charlebois M, Varga P, Pahr D, Nickelsen TN, Morlock MM, Glüer CC, Zysset PK (2009) Improvements in vertebral body strength under teriparatide treatment assessed in vivo by finite element analysis: results from the EUROFORS study. J Bone Miner Res 24:1672–1680PubMedCrossRef
28.
go back to reference Chevalier Y, Quek E, Borah B, Gross G, Stewart J, Lang T, Zysset P (2010) Biomechanical effects of teriparatide in women with osteoporosis treated previously with alendronate and risedronate: results from quantitative computed tomography-based finite element analysis of the vertebral body. Bone 46:41–48PubMedCrossRef Chevalier Y, Quek E, Borah B, Gross G, Stewart J, Lang T, Zysset P (2010) Biomechanical effects of teriparatide in women with osteoporosis treated previously with alendronate and risedronate: results from quantitative computed tomography-based finite element analysis of the vertebral body. Bone 46:41–48PubMedCrossRef
29.
go back to reference Keaveny TM, McClung MR, Wan X, Kopperdahl DL, Mitlak BH, Krohn K (2012) Femoral strength in osteoporotic women treated with teriparatide or alendronate. Bone 50:165–170PubMedCrossRef Keaveny TM, McClung MR, Wan X, Kopperdahl DL, Mitlak BH, Krohn K (2012) Femoral strength in osteoporotic women treated with teriparatide or alendronate. Bone 50:165–170PubMedCrossRef
30.
go back to reference Gluer CC, Marin F, Ringe JD, Hawkins F, Moricke R, Papaioannu N, Farahmand P, Minisola S, Martinez G, Nolla J, Niedhart C, Guanabens N, Nuti R, Martin-Mola E, Thomasius F, Kapetanos G, Pena J, Graeff C, Petto H, Sanz B, Reisinger A, Zysset P (2013) Comparative effects of teriparatide and risedronate in glucocorticoid-induced osteoporosis in men: 18-month results of the randomized EuroGIOPs trial. J Bone Miner Res. doi:10.1002/jbmr.1870 Gluer CC, Marin F, Ringe JD, Hawkins F, Moricke R, Papaioannu N, Farahmand P, Minisola S, Martinez G, Nolla J, Niedhart C, Guanabens N, Nuti R, Martin-Mola E, Thomasius F, Kapetanos G, Pena J, Graeff C, Petto H, Sanz B, Reisinger A, Zysset P (2013) Comparative effects of teriparatide and risedronate in glucocorticoid-induced osteoporosis in men: 18-month results of the randomized EuroGIOPs trial. J Bone Miner Res. doi:10.​1002/​jbmr.​1870
31.
go back to reference Canalis E, Mazziotti G, Giustina A, Bilezikian JP (2007) Glucocorticoid-induced osteoporosis: pathophysiology and therapy. Osteoporos Int 18:1319–1328PubMedCrossRef Canalis E, Mazziotti G, Giustina A, Bilezikian JP (2007) Glucocorticoid-induced osteoporosis: pathophysiology and therapy. Osteoporos Int 18:1319–1328PubMedCrossRef
32.
go back to reference Hofbauer LC, Rauner M (2009) Minireview: live and let die: molecular effects of glucocorticoids on bone cells. Mol Endocrinol 23:1525–1531PubMedCrossRef Hofbauer LC, Rauner M (2009) Minireview: live and let die: molecular effects of glucocorticoids on bone cells. Mol Endocrinol 23:1525–1531PubMedCrossRef
33.
go back to reference Weinstein RS (2010) Glucocorticoids, osteocytes, and skeletal fragility: the role of bone vascularity. Bone 46:564–570PubMedCrossRef Weinstein RS (2010) Glucocorticoids, osteocytes, and skeletal fragility: the role of bone vascularity. Bone 46:564–570PubMedCrossRef
34.
go back to reference Ton FN, Gunawardene SC, Lee H, Neer RM (2005) Effects of low-dose prednisone on bone metabolism. J Bone Miner Res 20:464–470PubMedCrossRef Ton FN, Gunawardene SC, Lee H, Neer RM (2005) Effects of low-dose prednisone on bone metabolism. J Bone Miner Res 20:464–470PubMedCrossRef
35.
go back to reference Minisola S, Del Fiacco R, Piemonte S, Iorio M, Mascia ML, Fidanza F, Cipriani C, Raso I, Porfiri ML, Francucci CM, D'Erasmo E, Romagnoli E (2008) Biochemical markers in glucocorticoid-induced osteoporosis. J Endocrinol Invest 31(7 Suppl):28–32PubMed Minisola S, Del Fiacco R, Piemonte S, Iorio M, Mascia ML, Fidanza F, Cipriani C, Raso I, Porfiri ML, Francucci CM, D'Erasmo E, Romagnoli E (2008) Biochemical markers in glucocorticoid-induced osteoporosis. J Endocrinol Invest 31(7 Suppl):28–32PubMed
36.
go back to reference Eastell R, Chen P, Saag KG, Burshell AL, Wong M, Warner MR, Krege JH (2010) Bone formation markers in patients with glucocorticoid-induced osteoporosis treated with teriparatide or alendronate. Bone 46:929–934PubMedCrossRef Eastell R, Chen P, Saag KG, Burshell AL, Wong M, Warner MR, Krege JH (2010) Bone formation markers in patients with glucocorticoid-induced osteoporosis treated with teriparatide or alendronate. Bone 46:929–934PubMedCrossRef
37.
go back to reference Graeff C, Marin F, Petto H, Kayser O, Reisinger A, Pena J, Zysset P, Gluer CC (2013) High resolution quantitative computed tomography-based assessment of trabecular microstructure and strength estimates by finite-element analysis of the spine, but not DXA, reflects vertebral fracture status in men with glucocorticoid-induced osteoporosis. Bone 52:568–577PubMedCrossRef Graeff C, Marin F, Petto H, Kayser O, Reisinger A, Pena J, Zysset P, Gluer CC (2013) High resolution quantitative computed tomography-based assessment of trabecular microstructure and strength estimates by finite-element analysis of the spine, but not DXA, reflects vertebral fracture status in men with glucocorticoid-induced osteoporosis. Bone 52:568–577PubMedCrossRef
38.
go back to reference Graeff C, Timm W, Nickelsen TN, Farrerons J, Marín F, Barker C, Glüer CC; EUROFORS High Resolution Computed Tomography Substudy Group (2007) Monitoring teriparatide-associated changes in vertebral microstructure by high-resolution CT in vivo: results from the EUROFORS study. J Bone Miner Res 22:1426–1433CrossRef Graeff C, Timm W, Nickelsen TN, Farrerons J, Marín F, Barker C, Glüer CC; EUROFORS High Resolution Computed Tomography Substudy Group (2007) Monitoring teriparatide-associated changes in vertebral microstructure by high-resolution CT in vivo: results from the EUROFORS study. J Bone Miner Res 22:1426–1433CrossRef
39.
go back to reference Chevalier Y, Charlebois M, Pahra D, Varga P, Heini P, Schneider E, Zysset P (2008) A patient-specific finite element methodology to predict damage accumulation in vertebral bodies under axial compression, sagittal flexion and combined loads. Comput Methods Biomech Biomed Engin 11:477–487PubMedCrossRef Chevalier Y, Charlebois M, Pahra D, Varga P, Heini P, Schneider E, Zysset P (2008) A patient-specific finite element methodology to predict damage accumulation in vertebral bodies under axial compression, sagittal flexion and combined loads. Comput Methods Biomech Biomed Engin 11:477–487PubMedCrossRef
40.
go back to reference Keaveny TM (2010) Biomechanical computed tomography—non-invasive bone strength analysis using clinical computed tomography scans. Ann N Y Acad Sci 1192:57–65PubMedCrossRef Keaveny TM (2010) Biomechanical computed tomography—non-invasive bone strength analysis using clinical computed tomography scans. Ann N Y Acad Sci 1192:57–65PubMedCrossRef
41.
go back to reference Cosman F, Nieves JW, Zion M, Barbuto N, Lindsay R (2008) Effect of prior and ongoing raloxifene therapy on response to PTH and maintenance of BMD after PTH therapy. Osteoporos Int 19:529–535PubMedCrossRef Cosman F, Nieves JW, Zion M, Barbuto N, Lindsay R (2008) Effect of prior and ongoing raloxifene therapy on response to PTH and maintenance of BMD after PTH therapy. Osteoporos Int 19:529–535PubMedCrossRef
42.
go back to reference Recker RR, Marin F, Ish-Shalom S, Möricke R, Hawkins F, Kapetanos G, de la Peña MP, Kekow J, Farrerons J, Sanz B, Oertel H, Stepan J (2009) Comparative effects of teriparatide and strontium ranelate on bone biopsies and biochemical markers of bone turnover in postmenopausal women with osteoporosis. J Bone Miner Res 24:1358–1368PubMedCrossRef Recker RR, Marin F, Ish-Shalom S, Möricke R, Hawkins F, Kapetanos G, de la Peña MP, Kekow J, Farrerons J, Sanz B, Oertel H, Stepan J (2009) Comparative effects of teriparatide and strontium ranelate on bone biopsies and biochemical markers of bone turnover in postmenopausal women with osteoporosis. J Bone Miner Res 24:1358–1368PubMedCrossRef
43.
go back to reference Stepan JJ, Burr DB, Li J, Ma YL, Petto H, Sipos A, Dobnig H, Fahrleitner-Pammer A, Michalska D, Pavo I (2010) Histomorphometric changes by teriparatide in alendronate-pretreated women with osteoporosis. Osteoporos Int 21:2027–2036PubMedCrossRef Stepan JJ, Burr DB, Li J, Ma YL, Petto H, Sipos A, Dobnig H, Fahrleitner-Pammer A, Michalska D, Pavo I (2010) Histomorphometric changes by teriparatide in alendronate-pretreated women with osteoporosis. Osteoporos Int 21:2027–2036PubMedCrossRef
44.
go back to reference Cosman F, Keaveny TM, Kopperdahl D, Wermers RA, Wan X, Krohn KD, Krege JH (2012) Hip and spine strength effects of adding versus switching to teriparatide in postmenopausal women with osteoporosis treated with prior alendronate or raloxifene. J Bone Miner Res. doi:10.1002/jbmr.1853 Cosman F, Keaveny TM, Kopperdahl D, Wermers RA, Wan X, Krohn KD, Krege JH (2012) Hip and spine strength effects of adding versus switching to teriparatide in postmenopausal women with osteoporosis treated with prior alendronate or raloxifene. J Bone Miner Res. doi:10.​1002/​jbmr.​1853
45.
go back to reference Eastell R, Barton I, Hannon RA, Chines A, Garnero P, Delmas PD (2003) Relationship of early changes in bone resorption to the reduction in fracture risk with risedronate. J Bone Miner Res 18:1051–1056PubMedCrossRef Eastell R, Barton I, Hannon RA, Chines A, Garnero P, Delmas PD (2003) Relationship of early changes in bone resorption to the reduction in fracture risk with risedronate. J Bone Miner Res 18:1051–1056PubMedCrossRef
46.
go back to reference Bruyère O, Collette J, Rizzoli R, Decock C, Ortolani S, Cormier C, Detilleux J, Reginster JY (2010) Relationship between 3-month changes in biochemical markers of bone remodelling and changes in bone mineral density and fracture incidence in patients treated with strontium ranelate for 3 years. Osteoporos Int 21:1031–1036PubMedCrossRef Bruyère O, Collette J, Rizzoli R, Decock C, Ortolani S, Cormier C, Detilleux J, Reginster JY (2010) Relationship between 3-month changes in biochemical markers of bone remodelling and changes in bone mineral density and fracture incidence in patients treated with strontium ranelate for 3 years. Osteoporos Int 21:1031–1036PubMedCrossRef
47.
go back to reference Melton LJ 3rd, Riggs BL, Keaveny TM, Achenbach SJ, Hoffmann PF, Camp JJ, Rouleau PA, Bouxsein ML, Amin S, Atkinson EJ, Robb RA, Khosla S (2007) Structural determinants of vertebral fracture risk. J Bone Miner Res 22:1885–1892PubMedCrossRef Melton LJ 3rd, Riggs BL, Keaveny TM, Achenbach SJ, Hoffmann PF, Camp JJ, Rouleau PA, Bouxsein ML, Amin S, Atkinson EJ, Robb RA, Khosla S (2007) Structural determinants of vertebral fracture risk. J Bone Miner Res 22:1885–1892PubMedCrossRef
48.
go back to reference Amin S, Kopperdhal DL, Melton LJ, Achenbach SJ, Therneua TM, Riggs BL, Keaveny TM (2011) Khosla S (2011) Association of hip strength estimates by finite-element analysis with fractures in women and men. J Bone Miner Res 26:1593–1600PubMedCrossRef Amin S, Kopperdhal DL, Melton LJ, Achenbach SJ, Therneua TM, Riggs BL, Keaveny TM (2011) Khosla S (2011) Association of hip strength estimates by finite-element analysis with fractures in women and men. J Bone Miner Res 26:1593–1600PubMedCrossRef
49.
go back to reference Keyak JH, Sigurdsson S, Karlsdottir G, Oskarsdottir D, Sigmarsdottir A, Zhao S, Kornak J, Harris TB, Sigurdsson G, Jonsson BY, Siggeirsdottir K, Eiriksdottir G, Gudnason V, Lang TF (2011) Male–female differences in the association between incident hip fracture and proximal femoral strength: a finite element analysis study. Bone 48:1239–1245PubMedCrossRef Keyak JH, Sigurdsson S, Karlsdottir G, Oskarsdottir D, Sigmarsdottir A, Zhao S, Kornak J, Harris TB, Sigurdsson G, Jonsson BY, Siggeirsdottir K, Eiriksdottir G, Gudnason V, Lang TF (2011) Male–female differences in the association between incident hip fracture and proximal femoral strength: a finite element analysis study. Bone 48:1239–1245PubMedCrossRef
50.
go back to reference Sheu Y, Zmuda JM, Boudreau RM, Petit MA, Ensrud KE, Bauer DC, Gordon CL, Orwoll ES, Cauley JA; Osteoporotic Fractures in Men MrOS Research Group (2011) Bone strength measured by peripheral quantitative computed tomography and the risk of nonvertebral fractures: the osteoporotic fractures in men (MrOS) study. J Bone Miner Res 26:63–71CrossRef Sheu Y, Zmuda JM, Boudreau RM, Petit MA, Ensrud KE, Bauer DC, Gordon CL, Orwoll ES, Cauley JA; Osteoporotic Fractures in Men MrOS Research Group (2011) Bone strength measured by peripheral quantitative computed tomography and the risk of nonvertebral fractures: the osteoporotic fractures in men (MrOS) study. J Bone Miner Res 26:63–71CrossRef
51.
go back to reference Wang X, Sanyal A, Cawthon PM, Palermo L, Jekir M, Christensen J, Ensrud KE, Cummings SR, Orwoll E, Black DM; Osteoporotic Fractures in Men (MrOS) Research Group, Keaveny TM (2012) Prediction of new clinical vertebral fractures in elderly men using finite element analysis of CT scans. J Bone Miner Res 27:808–816CrossRef Wang X, Sanyal A, Cawthon PM, Palermo L, Jekir M, Christensen J, Ensrud KE, Cummings SR, Orwoll E, Black DM; Osteoporotic Fractures in Men (MrOS) Research Group, Keaveny TM (2012) Prediction of new clinical vertebral fractures in elderly men using finite element analysis of CT scans. J Bone Miner Res 27:808–816CrossRef
52.
go back to reference Vilayphiou N, Boutroy S, Szulc P, van Rietbergen B, Munoz F, Delmas PD, Chapurlat R (2011) Finite element analysis performed on radius and tibia HR-pQCT images and fragility fractures at all sites in men. J Bone Miner Res 26:965–973PubMedCrossRef Vilayphiou N, Boutroy S, Szulc P, van Rietbergen B, Munoz F, Delmas PD, Chapurlat R (2011) Finite element analysis performed on radius and tibia HR-pQCT images and fragility fractures at all sites in men. J Bone Miner Res 26:965–973PubMedCrossRef
53.
go back to reference Kurland ES, Cosman F, McMahon DJ, Rosen CJ, Lindsay R, Bilezikian JP (2000) Parathyroid hormone as a therapy for idiopathic osteoporosis in men: effects on bone mineral density and bone markers. J Clin Endocrinol Metab 85:3069–3076PubMedCrossRef Kurland ES, Cosman F, McMahon DJ, Rosen CJ, Lindsay R, Bilezikian JP (2000) Parathyroid hormone as a therapy for idiopathic osteoporosis in men: effects on bone mineral density and bone markers. J Clin Endocrinol Metab 85:3069–3076PubMedCrossRef
54.
go back to reference Orwoll ES, Scheele WH, Pual S, Adami S, Syversen U, Diez-Perez A, Kaufman J-M, Clancy AD, Gaich GA (2003) The effect of teriparatide [human parathyroid hormone (1–34)] therapy on bone density in men with osteoporosis. J Bone Miner Res 18:9–17PubMedCrossRef Orwoll ES, Scheele WH, Pual S, Adami S, Syversen U, Diez-Perez A, Kaufman J-M, Clancy AD, Gaich GA (2003) The effect of teriparatide [human parathyroid hormone (1–34)] therapy on bone density in men with osteoporosis. J Bone Miner Res 18:9–17PubMedCrossRef
55.
go back to reference Eastell R, Krege JH, Chen P, Glass EV, Reginster JY (2006) Development of an algorithm for using PINP to monitor treatment of patients with teriparatide. Curr Med Res Opin 22:61–66PubMedCrossRef Eastell R, Krege JH, Chen P, Glass EV, Reginster JY (2006) Development of an algorithm for using PINP to monitor treatment of patients with teriparatide. Curr Med Res Opin 22:61–66PubMedCrossRef
56.
go back to reference Saag KG, Shane E, Boonen S, Marin F, Donley DW, Taylor KA, Dalsky GP, Marcus R (2007) Teriparatide or alendronate in glucocorticoid-induced osteoporosis. N Engl J Med 357:2028–2039PubMedCrossRef Saag KG, Shane E, Boonen S, Marin F, Donley DW, Taylor KA, Dalsky GP, Marcus R (2007) Teriparatide or alendronate in glucocorticoid-induced osteoporosis. N Engl J Med 357:2028–2039PubMedCrossRef
57.
go back to reference Glover SJ, Eastell R, McCloskey EV, Rogers A, Garnero P, Lowery J, Belleli R, Wright TM, John MR (2009) Rapid and robust response of biochemical markers of bone formation to teriparatide therapy. Bone 45:1053–1058PubMedCrossRef Glover SJ, Eastell R, McCloskey EV, Rogers A, Garnero P, Lowery J, Belleli R, Wright TM, John MR (2009) Rapid and robust response of biochemical markers of bone formation to teriparatide therapy. Bone 45:1053–1058PubMedCrossRef
Metadata
Title
Early changes in biochemical markers of bone formation during teriparatide therapy correlate with improvements in vertebral strength in men with glucocorticoid-induced osteoporosis
Authors
P. Farahmand
F. Marin
F. Hawkins
R. Möricke
J. D. Ringe
C.-C. Glüer
N. Papaioannou
S. Minisola
G. Martínez
J. M. Nolla
C. Niedhart
N. Guañabens
R. Nuti
E. Martín-Mola
F. Thomasius
J. Peña
C. Graeff
G. Kapetanos
H. Petto
A. Gentzel
A. Reisinger
P. K. Zysset
Publication date
01-12-2013
Publisher
Springer London
Published in
Osteoporosis International / Issue 12/2013
Print ISSN: 0937-941X
Electronic ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-013-2379-5