Skip to main content
Top
Published in: Osteoporosis International 6/2018

01-06-2018 | Original Article

The trabecular bone score is associated with bone mineral density, markers of bone turnover and prevalent fracture in patients with end stage kidney disease

Authors: J. Aleksova, S. Kurniawan, G. J. Elder

Published in: Osteoporosis International | Issue 6/2018

Login to get access

Abstract

Summary

Fracture risk increases in end-stage kidney disease (ESKD), but bone mineral density (BMD) measurement is less predictive of risk than in the general population. In this study of patients with ESKD, a lower trabecular bone score (TBS), indicative of microarchitectural deterioration, was associated with higher bone turnover markers and prevalent non-vertebral fracture.

Introduction

Declining renal function carries increased fracture risks, but BMD is less predictive of fracture for dialysis patients than the general population. The TBS, obtained from lumbar spine dual-energy X-ray absorptiometry (DXA) images, provides information on microarchitectural integrity not captured by BMD. The aim of this study was to assess associations of the TBS to clinical, DXA, radiological, and laboratory measures in patients with ESKD undergoing kidney and simultaneous pancreas kidney (SPK) transplantation.

Methods

A total of 147 patients with ESKD underwent pre-transplant laboratory testing, DXA, lateral spine X-ray, and structured history within 4 weeks of transplantation. Associations of the TBS to demographic data, prevalent fracture, BMD, and laboratory variables were assessed.

Results

Of 147 patients (60% male, mean age 48 ± 13 years), 36% had diabetes mellitus (DM) and 54 patients had fractures: 21 prevalent vertebral fractures only, 22 non-vertebral fractures only, and 11 had both. The mean TBS (1.345 ± 0.125) was lower in patients undergoing SPK than kidney-only transplants (1.292 vs. 1.364, p = 0.001). The TBS correlated to spine and total hip BMD, body mass index and inversely to parathyroid hormone, alkaline phosphatase and procollagen 1 N-propeptide. By multivariable logistic regression, lower TBS was significantly associated to prior non-vertebral fracture (p = 0.026).

Conclusions

A lower TBS, suggestive of increased microarchitectural damage, was associated with type 1 DM, markers of higher bone turnover, and prevalent fracture. These data support the need for prospective studies to evaluate whether TBS inclusion improves fracture prediction in patients with ESKD.
Literature
1.
go back to reference Ball AM, Gillen DL, Sherrard D, Weiss NS, Emerson SS, Seliger SL, Kestenbaum BR, Stehman-Breen C (2002) Risk of hip fracture among dialysis and renal transplant recipients. JAMA 288(23):3014–3018CrossRefPubMed Ball AM, Gillen DL, Sherrard D, Weiss NS, Emerson SS, Seliger SL, Kestenbaum BR, Stehman-Breen C (2002) Risk of hip fracture among dialysis and renal transplant recipients. JAMA 288(23):3014–3018CrossRefPubMed
2.
go back to reference Alem AM, Sherrard DJ, Gillen DL, Weiss NS, Beresford SA, Heckbert SR, Wong C, Stehman-Breen C (2000) Increased risk of hip fracture among patients with end-stage renal disease. Kidney Int 58(1):396–399CrossRefPubMed Alem AM, Sherrard DJ, Gillen DL, Weiss NS, Beresford SA, Heckbert SR, Wong C, Stehman-Breen C (2000) Increased risk of hip fracture among patients with end-stage renal disease. Kidney Int 58(1):396–399CrossRefPubMed
3.
go back to reference Group KDIGOKC-MW (2009) KDIGO clinical practice guideline for the diagnosis, evaluation, prevention, and treatment of chronic kidney disease-mineral and bone disorder (CKD-MBD). Kidney Int Suppl 113:S1–S130 Group KDIGOKC-MW (2009) KDIGO clinical practice guideline for the diagnosis, evaluation, prevention, and treatment of chronic kidney disease-mineral and bone disorder (CKD-MBD). Kidney Int Suppl 113:S1–S130
4.
go back to reference Nickolas TL, Stein EM, Dworakowski E, Nishiyama KK, Komandah-Kosseh M, Zhang CA, McMahon DJ, Liu XS, Boutroy S, Cremers S, Shane E (2013) Rapid cortical bone loss in patients with chronic kidney disease. J Bone Miner Res 28(8):1811–1820CrossRefPubMedPubMedCentral Nickolas TL, Stein EM, Dworakowski E, Nishiyama KK, Komandah-Kosseh M, Zhang CA, McMahon DJ, Liu XS, Boutroy S, Cremers S, Shane E (2013) Rapid cortical bone loss in patients with chronic kidney disease. J Bone Miner Res 28(8):1811–1820CrossRefPubMedPubMedCentral
5.
go back to reference Moe S, Drüeke T, Cunningham J, Goodman W, Martin K, Olgaard K, Ott S, Sprague S, Lameire N, Eknoyan G, Kidney Disease: Improving Global Outcomes (KDIGO) (2006) Definition, evaluation, and classification of renal osteodystrophy: a position statement from kidney disease: improving global outcomes (KDIGO). Kidney Int 69(11):1945–1953CrossRefPubMed Moe S, Drüeke T, Cunningham J, Goodman W, Martin K, Olgaard K, Ott S, Sprague S, Lameire N, Eknoyan G, Kidney Disease: Improving Global Outcomes (KDIGO) (2006) Definition, evaluation, and classification of renal osteodystrophy: a position statement from kidney disease: improving global outcomes (KDIGO). Kidney Int 69(11):1945–1953CrossRefPubMed
6.
go back to reference Nickolas TL, McMahon DJ, Shane E (2006) Relationship between moderate to severe kidney disease and hip fracture in the United States. J Am Soc Nephrol 17(11):3223–3232CrossRefPubMed Nickolas TL, McMahon DJ, Shane E (2006) Relationship between moderate to severe kidney disease and hip fracture in the United States. J Am Soc Nephrol 17(11):3223–3232CrossRefPubMed
7.
go back to reference Ensrud KE, Lui LY, Taylor BC, Ishani A, Shlipak MG, Stone KL, Cauley JA, Jamal SA, Antoniucci DM, Cummings SR, Osteoporotic Fractures Research Group (2007) Renal function and risk of hip and vertebral fractures in older women. Arch Intern Med 167(2):133–139CrossRefPubMed Ensrud KE, Lui LY, Taylor BC, Ishani A, Shlipak MG, Stone KL, Cauley JA, Jamal SA, Antoniucci DM, Cummings SR, Osteoporotic Fractures Research Group (2007) Renal function and risk of hip and vertebral fractures in older women. Arch Intern Med 167(2):133–139CrossRefPubMed
8.
go back to reference Johnell O, Kanis JA, Oden A, Johansson H, De Laet C, Delmas P et al (2005) Predictive value of BMD for hip and other fractures. J Bone Miner Res 20(7):1185–1194CrossRefPubMed Johnell O, Kanis JA, Oden A, Johansson H, De Laet C, Delmas P et al (2005) Predictive value of BMD for hip and other fractures. J Bone Miner Res 20(7):1185–1194CrossRefPubMed
9.
go back to reference Iimori S, Mori Y, Akita W, Kuyama T, Takada S, Asai T, Kuwahara M, Sasaki S, Tsukamoto Y (2012) Diagnostic usefulness of bone mineral density and biochemical markers of bone turnover in predicting fracture in CKD stage 5D patients--a single-center cohort study. Nephrol Dial Transplant 27(1):345–351CrossRefPubMed Iimori S, Mori Y, Akita W, Kuyama T, Takada S, Asai T, Kuwahara M, Sasaki S, Tsukamoto Y (2012) Diagnostic usefulness of bone mineral density and biochemical markers of bone turnover in predicting fracture in CKD stage 5D patients--a single-center cohort study. Nephrol Dial Transplant 27(1):345–351CrossRefPubMed
10.
go back to reference West SL, Lok CE, Langsetmo L, Cheung AM, Szabo E, Pearce D, Fusaro M, Wald R, Weinstein J, Jamal SA (2015) Bone mineral density predicts fractures in chronic kidney disease. J Bone Miner Res 30(5):913–919CrossRefPubMed West SL, Lok CE, Langsetmo L, Cheung AM, Szabo E, Pearce D, Fusaro M, Wald R, Weinstein J, Jamal SA (2015) Bone mineral density predicts fractures in chronic kidney disease. J Bone Miner Res 30(5):913–919CrossRefPubMed
11.
go back to reference Seeman E, Delmas PD (2006) Bone quality--the material and structural basis of bone strength and fragility. N Engl J Med 354(21):2250–2261CrossRefPubMed Seeman E, Delmas PD (2006) Bone quality--the material and structural basis of bone strength and fragility. N Engl J Med 354(21):2250–2261CrossRefPubMed
12.
go back to reference Nickolas TL, Stein E, Cohen A, Thomas V, Staron RB, McMahon DJ et al (2010) Bone mass and microarchitecture in CKD patients with fracture. J Am Soc Nephrol 21(8):1371–1380CrossRefPubMedPubMedCentral Nickolas TL, Stein E, Cohen A, Thomas V, Staron RB, McMahon DJ et al (2010) Bone mass and microarchitecture in CKD patients with fracture. J Am Soc Nephrol 21(8):1371–1380CrossRefPubMedPubMedCentral
13.
go back to reference Silva BC, Leslie WD, Resch H, Lamy O, Lesnyak O, Binkley N, McCloskey EV, Kanis JA, Bilezikian JP (2014) Trabecular bone score: a noninvasive analytical method based upon the DXA image. J Bone Miner Res 29(3):518–530CrossRefPubMed Silva BC, Leslie WD, Resch H, Lamy O, Lesnyak O, Binkley N, McCloskey EV, Kanis JA, Bilezikian JP (2014) Trabecular bone score: a noninvasive analytical method based upon the DXA image. J Bone Miner Res 29(3):518–530CrossRefPubMed
14.
go back to reference Winzenrieth R, Michelet F, Hans D (2013) Three-dimensional (3D) microarchitecture correlations with 2D projection image gray-level variations assessed by trabecular bone score using high-resolution computed tomographic acquisitions: effects of resolution and noise. J Clin Densitom 16(3):287–296CrossRefPubMed Winzenrieth R, Michelet F, Hans D (2013) Three-dimensional (3D) microarchitecture correlations with 2D projection image gray-level variations assessed by trabecular bone score using high-resolution computed tomographic acquisitions: effects of resolution and noise. J Clin Densitom 16(3):287–296CrossRefPubMed
15.
go back to reference Roux JP, Wegrzyn J, Boutroy S, Bouxsein ML, Hans D, Chapurlat R (2013) The predictive value of trabecular bone score (TBS) on whole lumbar vertebrae mechanics: an ex vivo study. Osteoporos Int 24(9):2455–2460CrossRefPubMed Roux JP, Wegrzyn J, Boutroy S, Bouxsein ML, Hans D, Chapurlat R (2013) The predictive value of trabecular bone score (TBS) on whole lumbar vertebrae mechanics: an ex vivo study. Osteoporos Int 24(9):2455–2460CrossRefPubMed
16.
go back to reference Hans D, Barthe N, Boutroy S, Pothuaud L, Winzenrieth R, Krieg MA (2011) Correlations between trabecular bone score, measured using anteroposterior dual-energy X-ray absorptiometry acquisition, and 3-dimensional parameters of bone microarchitecture: an experimental study on human cadaver vertebrae. J Clin Densitom 14(3):302–312CrossRefPubMed Hans D, Barthe N, Boutroy S, Pothuaud L, Winzenrieth R, Krieg MA (2011) Correlations between trabecular bone score, measured using anteroposterior dual-energy X-ray absorptiometry acquisition, and 3-dimensional parameters of bone microarchitecture: an experimental study on human cadaver vertebrae. J Clin Densitom 14(3):302–312CrossRefPubMed
17.
go back to reference Hans D, Goertzen AL, Krieg MA, Leslie WD (2011) Bone microarchitecture assessed by TBS predicts osteoporotic fractures independent of bone density: the Manitoba study. J Bone Miner Res 26(11):2762–2769CrossRefPubMed Hans D, Goertzen AL, Krieg MA, Leslie WD (2011) Bone microarchitecture assessed by TBS predicts osteoporotic fractures independent of bone density: the Manitoba study. J Bone Miner Res 26(11):2762–2769CrossRefPubMed
18.
go back to reference Harvey NC, Glüer CC, Binkley N, McCloskey EV, Brandi ML, Cooper C et al (2015) Trabecular bone score (TBS) as a new complementary approach for osteoporosis evaluation in clinical practice. Bone 78:216–224CrossRefPubMedPubMedCentral Harvey NC, Glüer CC, Binkley N, McCloskey EV, Brandi ML, Cooper C et al (2015) Trabecular bone score (TBS) as a new complementary approach for osteoporosis evaluation in clinical practice. Bone 78:216–224CrossRefPubMedPubMedCentral
19.
go back to reference Koumakis E, Avouac J, Winzenrieth R, Toth E, Payet J, Kahan A, Allanore Y, Cormier C (2015) Trabecular bone score in female patients with systemic sclerosis: comparison with rheumatoid arthritis and influence of glucocorticoid exposure. J Rheumatol 42(2):228–235CrossRefPubMed Koumakis E, Avouac J, Winzenrieth R, Toth E, Payet J, Kahan A, Allanore Y, Cormier C (2015) Trabecular bone score in female patients with systemic sclerosis: comparison with rheumatoid arthritis and influence of glucocorticoid exposure. J Rheumatol 42(2):228–235CrossRefPubMed
20.
go back to reference Leslie WD, Aubry-Rozier B, Lamy O, Hans D, Program MBD (2013) TBS (trabecular bone score) and diabetes-related fracture risk. J Clin Endocrinol Metab 98(2):602–609CrossRefPubMed Leslie WD, Aubry-Rozier B, Lamy O, Hans D, Program MBD (2013) TBS (trabecular bone score) and diabetes-related fracture risk. J Clin Endocrinol Metab 98(2):602–609CrossRefPubMed
21.
go back to reference Yavropoulou MP, Vaios V, Pikilidou M, Chryssogonidis I, Sachinidou M, Tournis S, Makris K, Kotsa K, Daniilidis M, Haritanti A, Liakopoulos V (2016) Bone quality assessment as measured by trabecular bone score in patients with end-stage renal disease on Dialysis. J Clin Densitom 20(4):490–497CrossRefPubMed Yavropoulou MP, Vaios V, Pikilidou M, Chryssogonidis I, Sachinidou M, Tournis S, Makris K, Kotsa K, Daniilidis M, Haritanti A, Liakopoulos V (2016) Bone quality assessment as measured by trabecular bone score in patients with end-stage renal disease on Dialysis. J Clin Densitom 20(4):490–497CrossRefPubMed
22.
go back to reference Brunerová L, Ronová P, Verešová J, Beranová P, Potoèková J, Kasalický P, Rychlík I (2016) Osteoporosis and impaired trabecular bone score in hemodialysis patients. Kidney Blood Press Res 41(3):345–354CrossRefPubMed Brunerová L, Ronová P, Verešová J, Beranová P, Potoèková J, Kasalický P, Rychlík I (2016) Osteoporosis and impaired trabecular bone score in hemodialysis patients. Kidney Blood Press Res 41(3):345–354CrossRefPubMed
23.
go back to reference Luckman M, Hans D, Cortez N, Nishiyama KK, Agarawal S, Zhang C, Nikkel L, Iyer S, Fusaro M, Guo EX, McMahon DJ, Shane E, Nickolas TL (2017) Spine trabecular bone score as an Indicator of bone microarchitecture at the peripheral skeleton in kidney transplant recipients. Clin J Am Soc Nephrol 12(4):644–652CrossRefPubMedPubMedCentral Luckman M, Hans D, Cortez N, Nishiyama KK, Agarawal S, Zhang C, Nikkel L, Iyer S, Fusaro M, Guo EX, McMahon DJ, Shane E, Nickolas TL (2017) Spine trabecular bone score as an Indicator of bone microarchitecture at the peripheral skeleton in kidney transplant recipients. Clin J Am Soc Nephrol 12(4):644–652CrossRefPubMedPubMedCentral
24.
go back to reference Levey AS, Stevens LA, Schmid CH, Zhang YL, Castro AF, Feldman HI et al (2009) A new equation to estimate glomerular filtration rate. Ann Intern Med 150(9):604–612CrossRefPubMedPubMedCentral Levey AS, Stevens LA, Schmid CH, Zhang YL, Castro AF, Feldman HI et al (2009) A new equation to estimate glomerular filtration rate. Ann Intern Med 150(9):604–612CrossRefPubMedPubMedCentral
25.
go back to reference Henry MJ, Pasco JA, Korn S, Gibson JE, Kotowicz MA, Nicholson GC (2010) Bone mineral density reference ranges for Australian men: Geelong osteoporosis study. Osteoporos Int 21(6):909–917CrossRefPubMed Henry MJ, Pasco JA, Korn S, Gibson JE, Kotowicz MA, Nicholson GC (2010) Bone mineral density reference ranges for Australian men: Geelong osteoporosis study. Osteoporos Int 21(6):909–917CrossRefPubMed
26.
go back to reference Henry MJ, Pasco JA, Pocock NA, Nicholson GC, Kotowicz MA (2004) Reference ranges for bone densitometers adopted Australia-wide: Geelong osteoporosis study. Australas Radiol 48(4):473–475CrossRefPubMed Henry MJ, Pasco JA, Pocock NA, Nicholson GC, Kotowicz MA (2004) Reference ranges for bone densitometers adopted Australia-wide: Geelong osteoporosis study. Australas Radiol 48(4):473–475CrossRefPubMed
27.
go back to reference Genant HK, Wu CY, van Kuijk C, Nevitt MC (1993) Vertebral fracture assessment using a semiquantitative technique. J Bone Miner Res 8(9):1137–1148CrossRefPubMed Genant HK, Wu CY, van Kuijk C, Nevitt MC (1993) Vertebral fracture assessment using a semiquantitative technique. J Bone Miner Res 8(9):1137–1148CrossRefPubMed
28.
go back to reference McCloskey EV, Oden A, Harvey NC, Leslie WD, Hans D, Johansson H et al (2016) A meta-analysis of trabecular bone score in fracture risk prediction and its relationship to FRAX. J Bone Miner Res 31(5):940–948CrossRefPubMed McCloskey EV, Oden A, Harvey NC, Leslie WD, Hans D, Johansson H et al (2016) A meta-analysis of trabecular bone score in fracture risk prediction and its relationship to FRAX. J Bone Miner Res 31(5):940–948CrossRefPubMed
29.
go back to reference Eller-Vainicher C, Filopanti M, Palmieri S, Ulivieri FM, Morelli V, Zhukouskaya VV, Cairoli E, Pino R, Naccarato A, Verga U, Scillitani A, Beck-Peccoz P, Chiodini I (2013) Bone quality, as measured by trabecular bone score, in patients with primary hyperparathyroidism. Eur J Endocrinol 169(2):155–162CrossRefPubMed Eller-Vainicher C, Filopanti M, Palmieri S, Ulivieri FM, Morelli V, Zhukouskaya VV, Cairoli E, Pino R, Naccarato A, Verga U, Scillitani A, Beck-Peccoz P, Chiodini I (2013) Bone quality, as measured by trabecular bone score, in patients with primary hyperparathyroidism. Eur J Endocrinol 169(2):155–162CrossRefPubMed
30.
go back to reference Stein EM, Silva BC, Boutroy S, Zhou B, Wang J, Udesky J, Zhang C, McMahon DJ, Romano M, Dworakowski E, Costa AG, Cusano N, Irani D, Cremers S, Shane E, Guo XE, Bilezikian JP (2013) Primary hyperparathyroidism is associated with abnormal cortical and trabecular microstructure and reduced bone stiffness in postmenopausal women. J Bone Miner Res 28(5):1029–1040CrossRefPubMedPubMedCentral Stein EM, Silva BC, Boutroy S, Zhou B, Wang J, Udesky J, Zhang C, McMahon DJ, Romano M, Dworakowski E, Costa AG, Cusano N, Irani D, Cremers S, Shane E, Guo XE, Bilezikian JP (2013) Primary hyperparathyroidism is associated with abnormal cortical and trabecular microstructure and reduced bone stiffness in postmenopausal women. J Bone Miner Res 28(5):1029–1040CrossRefPubMedPubMedCentral
31.
32.
go back to reference Nicodemus KK, Folsom AR (2001) Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care 24(7):1192–1197CrossRefPubMed Nicodemus KK, Folsom AR (2001) Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care 24(7):1192–1197CrossRefPubMed
33.
go back to reference Starup-Linde J, Lykkeboe S, Gregersen S, Hauge EM, Langdahl BL, Handberg A, Vestergaard P (2016) Bone structure and predictors of fracture in type 1 and type 2 diabetes. J Clin Endocrinol Metab 101(3):928–936CrossRefPubMed Starup-Linde J, Lykkeboe S, Gregersen S, Hauge EM, Langdahl BL, Handberg A, Vestergaard P (2016) Bone structure and predictors of fracture in type 1 and type 2 diabetes. J Clin Endocrinol Metab 101(3):928–936CrossRefPubMed
34.
go back to reference Vestergaard P (2007) Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes--a meta-analysis. Osteoporos Int 18(4):427–444CrossRefPubMed Vestergaard P (2007) Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes--a meta-analysis. Osteoporos Int 18(4):427–444CrossRefPubMed
35.
go back to reference Dhaliwal R, Cibula D, Ghosh C, Weinstock RS, Moses AM (2014) Bone quality assessment in type 2 diabetes mellitus. Osteoporos Int 25(7):1969–1973CrossRefPubMed Dhaliwal R, Cibula D, Ghosh C, Weinstock RS, Moses AM (2014) Bone quality assessment in type 2 diabetes mellitus. Osteoporos Int 25(7):1969–1973CrossRefPubMed
36.
go back to reference Neumann T, Lodes S, Kastner B, Lehmann T, Hans D, Lamy O et al (2016) Trabecular bone score in type 1 diabetes--a cross-sectional study. Osteoporos Int 27(1):127–133CrossRefPubMed Neumann T, Lodes S, Kastner B, Lehmann T, Hans D, Lamy O et al (2016) Trabecular bone score in type 1 diabetes--a cross-sectional study. Osteoporos Int 27(1):127–133CrossRefPubMed
37.
go back to reference Del Rio LM, Winzenrieth R, Cormier C, Di Gregorio S (2013) Is bone microarchitecture status of the lumbar spine assessed by TBS related to femoral neck fracture? A Spanish case-control study. Osteoporos Int 24(3):991–998CrossRefPubMed Del Rio LM, Winzenrieth R, Cormier C, Di Gregorio S (2013) Is bone microarchitecture status of the lumbar spine assessed by TBS related to femoral neck fracture? A Spanish case-control study. Osteoporos Int 24(3):991–998CrossRefPubMed
38.
go back to reference Rabier B, Heraud A, Grand-Lenoir C, Winzenrieth R, Hans D (2010) A multicentre, retrospective case-control study assessing the role of trabecular bone score (TBS) in menopausal Caucasian women with low areal bone mineral density (BMDa): Analysing the odds of vertebral fracture. Bone 46(1):176–181CrossRefPubMed Rabier B, Heraud A, Grand-Lenoir C, Winzenrieth R, Hans D (2010) A multicentre, retrospective case-control study assessing the role of trabecular bone score (TBS) in menopausal Caucasian women with low areal bone mineral density (BMDa): Analysing the odds of vertebral fracture. Bone 46(1):176–181CrossRefPubMed
39.
go back to reference Leib E, Winzenrieth R, Aubry-Rozier B, Hans D (2014) Vertebral microarchitecture and fragility fracture in men: a TBS study. Bone 62:51–55CrossRefPubMed Leib E, Winzenrieth R, Aubry-Rozier B, Hans D (2014) Vertebral microarchitecture and fragility fracture in men: a TBS study. Bone 62:51–55CrossRefPubMed
40.
go back to reference Breban S, Briot K, Kolta S, Paternotte S, Ghazi M, Fechtenbaum J et al (2012) Identification of rheumatoid arthritis patients with vertebral fractures using bone mineral density and trabecular bone score. J Clin Densitom 15(3):260–266CrossRefPubMed Breban S, Briot K, Kolta S, Paternotte S, Ghazi M, Fechtenbaum J et al (2012) Identification of rheumatoid arthritis patients with vertebral fractures using bone mineral density and trabecular bone score. J Clin Densitom 15(3):260–266CrossRefPubMed
41.
go back to reference Naylor KL, Lix LM, Hans D, Garg AX, Rush DN, Hodsman AB, Leslie WD (2016) Trabecular bone score in kidney transplant recipients. Osteoporos Int 27(3):1115–1121CrossRefPubMed Naylor KL, Lix LM, Hans D, Garg AX, Rush DN, Hodsman AB, Leslie WD (2016) Trabecular bone score in kidney transplant recipients. Osteoporos Int 27(3):1115–1121CrossRefPubMed
42.
go back to reference Naylor KL, Prior J, Garg AX, Berger C, Langsetmo L, Adachi JD, Goltzman D, Kovacs CS, Josse RG, Leslie WD (2016) Trabecular bone score and incident fragility fracture risk in adults with reduced kidney function. Clin J Am Soc Nephrol 11(11):2032–2040CrossRefPubMedPubMedCentral Naylor KL, Prior J, Garg AX, Berger C, Langsetmo L, Adachi JD, Goltzman D, Kovacs CS, Josse RG, Leslie WD (2016) Trabecular bone score and incident fragility fracture risk in adults with reduced kidney function. Clin J Am Soc Nephrol 11(11):2032–2040CrossRefPubMedPubMedCentral
43.
go back to reference Perez-Saez MJ, Herrera S, Prieto-Alhambra D, Nogues X, Vera M, Redondo-Pachon D et al (2016) Bone density, microarchitecture and tissue quality long-term after kidney transplant. Transplantation 101(6):1290–1294CrossRef Perez-Saez MJ, Herrera S, Prieto-Alhambra D, Nogues X, Vera M, Redondo-Pachon D et al (2016) Bone density, microarchitecture and tissue quality long-term after kidney transplant. Transplantation 101(6):1290–1294CrossRef
44.
go back to reference Leslie WD, Krieg MA, Hans D (2013) Clinical factors associated with trabecular bone score. J Clin Densitom 16(3):374–379CrossRefPubMed Leslie WD, Krieg MA, Hans D (2013) Clinical factors associated with trabecular bone score. J Clin Densitom 16(3):374–379CrossRefPubMed
45.
go back to reference Yenchek RH, Ix JH, Shlipak MG, Bauer DC, Rianon NJ, Kritchevsky SB, Harris TB, Newman AB, Cauley JA, Fried LF, for the Health, Aging, and Body Composition Study (2012) Bone mineral density and fracture risk in older individuals with CKD. Clin J Am Soc Nephrol 7(7):1130–1136CrossRefPubMedPubMedCentral Yenchek RH, Ix JH, Shlipak MG, Bauer DC, Rianon NJ, Kritchevsky SB, Harris TB, Newman AB, Cauley JA, Fried LF, for the Health, Aging, and Body Composition Study (2012) Bone mineral density and fracture risk in older individuals with CKD. Clin J Am Soc Nephrol 7(7):1130–1136CrossRefPubMedPubMedCentral
46.
go back to reference Ketteler M, Elder GJ, Evenepoel P, Ix JH, Jamal SA, Lafage-Proust MH, Shroff R, Thadhani RI, Tonelli MA, Kasiske BL, Wheeler DC, Leonard MB (2015) Revisiting KDIGO clinical practice guideline on chronic kidney disease-mineral and bone disorder: a commentary from a kidney disease: improving global outcomes controversies conference. Kidney Int 87(3):502–528CrossRefPubMed Ketteler M, Elder GJ, Evenepoel P, Ix JH, Jamal SA, Lafage-Proust MH, Shroff R, Thadhani RI, Tonelli MA, Kasiske BL, Wheeler DC, Leonard MB (2015) Revisiting KDIGO clinical practice guideline on chronic kidney disease-mineral and bone disorder: a commentary from a kidney disease: improving global outcomes controversies conference. Kidney Int 87(3):502–528CrossRefPubMed
47.
go back to reference Jamal SA, Hayden JA, Beyene J (2007) Low bone mineral density and fractures in long-term hemodialysis patients: a meta-analysis. Am J Kidney Dis 49(5):674–681CrossRefPubMed Jamal SA, Hayden JA, Beyene J (2007) Low bone mineral density and fractures in long-term hemodialysis patients: a meta-analysis. Am J Kidney Dis 49(5):674–681CrossRefPubMed
Metadata
Title
The trabecular bone score is associated with bone mineral density, markers of bone turnover and prevalent fracture in patients with end stage kidney disease
Authors
J. Aleksova
S. Kurniawan
G. J. Elder
Publication date
01-06-2018
Publisher
Springer London
Published in
Osteoporosis International / Issue 6/2018
Print ISSN: 0937-941X
Electronic ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-018-4468-y

Other articles of this Issue 6/2018

Osteoporosis International 6/2018 Go to the issue