Skip to main content
Top
Published in: Journal of Bone and Mineral Metabolism 3/2016

01-05-2016 | Original Article

Dual-energy X-ray absorptiometry, peripheral quantitative computed tomography, and micro-computed tomography techniques are discordant for bone density and geometry measurements in the guinea pig

Authors: Ivy L. Mak, Jason R. DeGuire, Paula Lavery, Sherry Agellon, Hope A. Weiler

Published in: Journal of Bone and Mineral Metabolism | Issue 3/2016

Login to get access

Abstract

This study aims to examine agreement among bone mineral content (BMC) and density (BMD) estimates obtained using dual-energy X-ray absorptiometry (DXA), peripheral quantitative computed tomography (pQCT), and micro-computed tomography (μCT) against high-resolution μCT and bone ash of the guinea pig femur. Middle-aged (n = 40, 86 weeks) male guinea pigs underwent in vivo followed by ex vivo DXA (Hologic QDR 4500A) scanning for intact and excised femur BMC and areal density. To assess bone architecture and strength, excised femurs were scanned on pQCT (Stratec XCT 2000L) as well as on two μCT scanners (LaTheta LCT-200; Skyscan 1174), followed by three-point bending test. Reproducibility was determined using triplicate scans; and agreement assessed using Bland–Altman plots with reference methods being high-resolution μCT (Skyscan) for BMD and bone ashing for BMC. All techniques showed satisfactory ex vivo precision (CV 0.05–4.3 %). However, bias compared to the reference method was highest (207.5 %) in trabecular bone volume fraction (BV/TV) measured by LaTheta, and unacceptable in most total femur and cortical bone measurements. Volumetric BMD (vBMD) and BV/TV derived by LaTheta and pQCT at the distal metaphysis were biased from the Skyscan by an average of 49.3 and 207.5 %, respectively. Variability of vBMD, BV/TV and cross-sectional area at the diaphysis ranged from −5.5 to 30.8 %. LaTheta best quantified total femur BMC with an upper bias of 3.3 %. The observed differences among imaging techniques can be attributable to inherent dissimilarity in construction design, calibration, segmentation and scanning resolution used. These bone imaging tools are precise but are not comparable, at least when assessing guinea pig bones.
Appendix
Available only for authorised users
Literature
1.
go back to reference Binkley N, Dahl D, Engelke J, Kawahara-Baccus T, Krueger D, Colman R (2003) Bone loss detection in rats using a mouse densitometer. J Bone Miner Res 18:370–375CrossRefPubMed Binkley N, Dahl D, Engelke J, Kawahara-Baccus T, Krueger D, Colman R (2003) Bone loss detection in rats using a mouse densitometer. J Bone Miner Res 18:370–375CrossRefPubMed
2.
go back to reference Brochmann EJ, Duarte ME, Zaidi HA, Murray SS (2003) Effects of dietary restriction on total body, femoral, and vertebral bone in SENCAR, C57BL/6, and DBA/2 mice. Metabolism 52:1265–1273CrossRefPubMed Brochmann EJ, Duarte ME, Zaidi HA, Murray SS (2003) Effects of dietary restriction on total body, femoral, and vertebral bone in SENCAR, C57BL/6, and DBA/2 mice. Metabolism 52:1265–1273CrossRefPubMed
3.
go back to reference Iida-Klein A, Lu SS, Cosman F, Lindsay R, Dempster DW (2007) Effects of cyclic vs. daily treatment with human parathyroid hormone (1–34) on murine bone structure and cellular activity. Bone 40:391–398CrossRefPubMed Iida-Klein A, Lu SS, Cosman F, Lindsay R, Dempster DW (2007) Effects of cyclic vs. daily treatment with human parathyroid hormone (1–34) on murine bone structure and cellular activity. Bone 40:391–398CrossRefPubMed
4.
go back to reference Klein RF, Shea M, Gunness ME, Pelz GB, Belknap JK, Orwoll ES (2001) Phenotypic characterization of mice bred for high and low peak bone mass. J Bone Miner Res 16:63–71CrossRefPubMed Klein RF, Shea M, Gunness ME, Pelz GB, Belknap JK, Orwoll ES (2001) Phenotypic characterization of mice bred for high and low peak bone mass. J Bone Miner Res 16:63–71CrossRefPubMed
5.
go back to reference Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, Müller R (2010) Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res 25:1468–1486CrossRefPubMed Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, Müller R (2010) Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res 25:1468–1486CrossRefPubMed
6.
go back to reference Muraoka T, Hagino H, Okano T, Enokida M, Teshima R (2007) Role of subchondral bone in osteoarthritis development: a comparative study of two strains of guinea pigs with and without spontaneously occurring osteoarthritis. Arthritis Rheum 56:3366–3374CrossRefPubMed Muraoka T, Hagino H, Okano T, Enokida M, Teshima R (2007) Role of subchondral bone in osteoarthritis development: a comparative study of two strains of guinea pigs with and without spontaneously occurring osteoarthritis. Arthritis Rheum 56:3366–3374CrossRefPubMed
7.
go back to reference Lochmüller E, Jung V, Weusten A, Wehr U, Wolf E, Eckstein F (2001) Precision of high-resolution dual energy X-ray absorptiometry measurements of bone mineral status and body composition in small animal models. Eur Cells Mater 1:43–51 Lochmüller E, Jung V, Weusten A, Wehr U, Wolf E, Eckstein F (2001) Precision of high-resolution dual energy X-ray absorptiometry measurements of bone mineral status and body composition in small animal models. Eur Cells Mater 1:43–51
8.
go back to reference Iida-Klein A, Lu SS, Yokoyama K, Dempster DW, Nieves JW, Lindsay R (2003) Precision, accuracy, and reproducibility of dual X-ray absorptiometry measurements in mice in vivo. J Clin Densitom 6:25–33CrossRefPubMed Iida-Klein A, Lu SS, Yokoyama K, Dempster DW, Nieves JW, Lindsay R (2003) Precision, accuracy, and reproducibility of dual X-ray absorptiometry measurements in mice in vivo. J Clin Densitom 6:25–33CrossRefPubMed
9.
go back to reference Schmidt C, Priemel M, Kohler T, Weusten A, Müller R, Amling M, Eckstein F (2003) Precision and accuracy of peripheral quantitative computed tomography (pQCT) in the mouse skeleton compared with histology and microcomputed tomography (μCT). J Bone Miner Res 18:1486–1496CrossRefPubMed Schmidt C, Priemel M, Kohler T, Weusten A, Müller R, Amling M, Eckstein F (2003) Precision and accuracy of peripheral quantitative computed tomography (pQCT) in the mouse skeleton compared with histology and microcomputed tomography (μCT). J Bone Miner Res 18:1486–1496CrossRefPubMed
10.
go back to reference Müller R, Hildebrand T, Häuselmann H, Rüegsegger P (1996) In vivo reproducibility of three-dimensional structural properties of noninvasive bone biopsies using 3D-pQCT. J Bone Miner Res 11:1745–1750CrossRefPubMed Müller R, Hildebrand T, Häuselmann H, Rüegsegger P (1996) In vivo reproducibility of three-dimensional structural properties of noninvasive bone biopsies using 3D-pQCT. J Bone Miner Res 11:1745–1750CrossRefPubMed
11.
go back to reference Kohler T, Beyeler M, Webster D, Müller R (2005) Compartmental bone morphometry in the mouse femur: reproducibility and resolution dependence of microtomographic measurements. Calcif Tissue Int 77:281–290CrossRefPubMed Kohler T, Beyeler M, Webster D, Müller R (2005) Compartmental bone morphometry in the mouse femur: reproducibility and resolution dependence of microtomographic measurements. Calcif Tissue Int 77:281–290CrossRefPubMed
12.
go back to reference Barou O, Valentin D, Vico L, Tirode C, Barbier A, Alexandre C, Lafage-Proust MH (2002) High-resolution three-dimensional micro-computed tomography detects bone loss and changes in trabecular architecture early: comparison with DEXA and bone histomorphometry in a rat model of disuse osteoporosis. Investig Radiol 37:40–46CrossRef Barou O, Valentin D, Vico L, Tirode C, Barbier A, Alexandre C, Lafage-Proust MH (2002) High-resolution three-dimensional micro-computed tomography detects bone loss and changes in trabecular architecture early: comparison with DEXA and bone histomorphometry in a rat model of disuse osteoporosis. Investig Radiol 37:40–46CrossRef
13.
go back to reference Libouban H, Moreau M-F, Legrand E, Baslé MF, Audran M, Chappard D (2001) Comparison insight dual X-ray absorptiometry (DXA), histomorphometry, ash weight, and morphometric indices for bone evaluation in an animal model (the orchidectomized rat) of male osteoporosis. Calcif Tissue Int 68:31–37CrossRefPubMed Libouban H, Moreau M-F, Legrand E, Baslé MF, Audran M, Chappard D (2001) Comparison insight dual X-ray absorptiometry (DXA), histomorphometry, ash weight, and morphometric indices for bone evaluation in an animal model (the orchidectomized rat) of male osteoporosis. Calcif Tissue Int 68:31–37CrossRefPubMed
14.
go back to reference Fink C, Cooper H, Huebner J, Guilak F, Kraus V (2002) Precision and accuracy of a transportable dual-energy X-ray absorptiometry unit for bone mineral measurements in guinea pigs. Calcif Tissue Int 70:164–169CrossRefPubMed Fink C, Cooper H, Huebner J, Guilak F, Kraus V (2002) Precision and accuracy of a transportable dual-energy X-ray absorptiometry unit for bone mineral measurements in guinea pigs. Calcif Tissue Int 70:164–169CrossRefPubMed
15.
go back to reference DeGuire JR, Mak IL, Lavery P, Agellon S, Wykes LJ, Weiler HA (2014) Orchidectomy-induced alterations in volumetric bone density, cortical porosity and strength of femur are attenuated by dietary conjugated linoleic acid in aged guinea pigs. Bone 73:42–50CrossRefPubMed DeGuire JR, Mak IL, Lavery P, Agellon S, Wykes LJ, Weiler HA (2014) Orchidectomy-induced alterations in volumetric bone density, cortical porosity and strength of femur are attenuated by dietary conjugated linoleic acid in aged guinea pigs. Bone 73:42–50CrossRefPubMed
16.
go back to reference Subcommittee on Laboratory Animal Nutrition. Committee on Animal Nutrition, Board on Agricultural, and National Research Council (1995) Nutrient requirements of laboratory animals, 4th revised edn. National Academy Press, Washington, DC Subcommittee on Laboratory Animal Nutrition. Committee on Animal Nutrition, Board on Agricultural, and National Research Council (1995) Nutrient requirements of laboratory animals, 4th revised edn. National Academy Press, Washington, DC
17.
go back to reference Canadian Council on Animal Care (1996) Guide to the care and use of experimental animals, 2nd edn. The Canadian Council on Animal Care, Ottawa Canadian Council on Animal Care (1996) Guide to the care and use of experimental animals, 2nd edn. The Canadian Council on Animal Care, Ottawa
18.
go back to reference Meganck JA, Kozloff KM, Thornton MM, Broski SM, Goldstein SA (2009) Beam hardening artifacts in micro-computed tomography scanning can be reduced by X-ray beam filtration and the resulting images can be used to accurately measure BMD. Bone 45:1104–1116CrossRefPubMedPubMedCentral Meganck JA, Kozloff KM, Thornton MM, Broski SM, Goldstein SA (2009) Beam hardening artifacts in micro-computed tomography scanning can be reduced by X-ray beam filtration and the resulting images can be used to accurately measure BMD. Bone 45:1104–1116CrossRefPubMedPubMedCentral
19.
go back to reference Sijbers J, Postnov A (2004) Reduction of ring artefacts in high resolution micro-CT reconstructions. Phys Med Biol 49:N247–N253CrossRefPubMed Sijbers J, Postnov A (2004) Reduction of ring artefacts in high resolution micro-CT reconstructions. Phys Med Biol 49:N247–N253CrossRefPubMed
20.
21.
go back to reference Bland JM, Altman DG (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 327:307–310CrossRef Bland JM, Altman DG (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 327:307–310CrossRef
22.
go back to reference Bland JM, Altman DG (1995) Comparing methods of measurement: why plotting difference against standard method is misleading. Lancet 346:1085–1087CrossRefPubMed Bland JM, Altman DG (1995) Comparing methods of measurement: why plotting difference against standard method is misleading. Lancet 346:1085–1087CrossRefPubMed
23.
go back to reference Critchley LA (2011) Validation of the MostCare pulse contour cardiac output monitor: beyond the Bland and Altman plot. Anesth Analg 113:1292–1294CrossRefPubMed Critchley LA (2011) Validation of the MostCare pulse contour cardiac output monitor: beyond the Bland and Altman plot. Anesth Analg 113:1292–1294CrossRefPubMed
24.
go back to reference Petersen PH, Stöckl D, Blaabjerg O, Pedersen B, Birkemose E, Thienpont L, Lassen JF, Kjeldsen J (1997) Graphical interpretation of analytical data from comparison of a field method with a reference method by use of difference plots. Clin Chem 43:2039–2046PubMed Petersen PH, Stöckl D, Blaabjerg O, Pedersen B, Birkemose E, Thienpont L, Lassen JF, Kjeldsen J (1997) Graphical interpretation of analytical data from comparison of a field method with a reference method by use of difference plots. Clin Chem 43:2039–2046PubMed
25.
go back to reference Holdsworth DW, Thornton MM (2002) Micro-CT in small animal and specimen imaging. Trends Biotechnol 20:S34–S39CrossRef Holdsworth DW, Thornton MM (2002) Micro-CT in small animal and specimen imaging. Trends Biotechnol 20:S34–S39CrossRef
26.
go back to reference Laperre K, Depypere M, van Gastel N, Torrekens S, Moermans K, Bogaerts R, Maes F, Carmeliet G (2011) Development of micro-CT protocols for in vivo follow-up of mouse bone architecture without major radiation side effects. Bone 49:613–622CrossRefPubMed Laperre K, Depypere M, van Gastel N, Torrekens S, Moermans K, Bogaerts R, Maes F, Carmeliet G (2011) Development of micro-CT protocols for in vivo follow-up of mouse bone architecture without major radiation side effects. Bone 49:613–622CrossRefPubMed
27.
go back to reference Brodt M, Pelz G, Taniguchi J, Silva M (2003) Accuracy of peripheral quantitative computed tomography (pQCT) for assessing area and density of mouse cortical bone. Calcif Tissue Int 73:411–418CrossRefPubMed Brodt M, Pelz G, Taniguchi J, Silva M (2003) Accuracy of peripheral quantitative computed tomography (pQCT) for assessing area and density of mouse cortical bone. Calcif Tissue Int 73:411–418CrossRefPubMed
28.
go back to reference Hara T, Tanck E, Homminga J, Huiskes R (2002) The influence of microcomputed tomography threshold variations on the assessment of structural and mechanical trabecular bone properties. Bone 31:107–109CrossRefPubMed Hara T, Tanck E, Homminga J, Huiskes R (2002) The influence of microcomputed tomography threshold variations on the assessment of structural and mechanical trabecular bone properties. Bone 31:107–109CrossRefPubMed
29.
go back to reference Burghardt AJ, Kazakia GJ, Majumdar S (2007) A local adaptive threshold strategy for high resolution peripheral quantitative computed tomography of trabecular bone. Ann Biomed Eng 35:1678–1686CrossRefPubMed Burghardt AJ, Kazakia GJ, Majumdar S (2007) A local adaptive threshold strategy for high resolution peripheral quantitative computed tomography of trabecular bone. Ann Biomed Eng 35:1678–1686CrossRefPubMed
30.
go back to reference Cordey J, Schneider M, Belendez C, Ziegler WJ, Rahn BA, Perren SM (1992) Effect of bone size, not density, on the stiffness of the proximal part of normal and osteoporotic human femora. J Bone Miner Res 7:S437–S444CrossRefPubMed Cordey J, Schneider M, Belendez C, Ziegler WJ, Rahn BA, Perren SM (1992) Effect of bone size, not density, on the stiffness of the proximal part of normal and osteoporotic human femora. J Bone Miner Res 7:S437–S444CrossRefPubMed
31.
go back to reference Ferretti JL, Capozza RF, Mondelo N, Zanchetta JR (1993) Interrelationships between densitometric, geometric, and mechanical properties of rat femora: inferences concerning mechanical regulation of bone modeling. J Bone Miner Res 8:1389–1396CrossRefPubMed Ferretti JL, Capozza RF, Mondelo N, Zanchetta JR (1993) Interrelationships between densitometric, geometric, and mechanical properties of rat femora: inferences concerning mechanical regulation of bone modeling. J Bone Miner Res 8:1389–1396CrossRefPubMed
32.
go back to reference Beck TJ, Ruff CB, Warden KE, Scott WW Jr, Rao GU (1990) Predicting femoral neck strength from bone mineral data: a structural approach. Investig Radiol 25:6–18CrossRef Beck TJ, Ruff CB, Warden KE, Scott WW Jr, Rao GU (1990) Predicting femoral neck strength from bone mineral data: a structural approach. Investig Radiol 25:6–18CrossRef
33.
go back to reference Yeni Y, Brown C, Wang Z, Norman T (1997) The influence of bone morphology on fracture toughness of the human femur and tibia. Bone 21:453–459CrossRefPubMed Yeni Y, Brown C, Wang Z, Norman T (1997) The influence of bone morphology on fracture toughness of the human femur and tibia. Bone 21:453–459CrossRefPubMed
34.
go back to reference Wang X, Masilamani N, Mabrey J, Alder M, Agrawal C (1998) Changes in the fracture toughness of bone may not be reflected in its mineral density, porosity, and tensile properties. Bone 23:67–72CrossRefPubMed Wang X, Masilamani N, Mabrey J, Alder M, Agrawal C (1998) Changes in the fracture toughness of bone may not be reflected in its mineral density, porosity, and tensile properties. Bone 23:67–72CrossRefPubMed
35.
go back to reference Martin R, Ishida J (1989) The relative effects of collagen fiber orientation, porosity, density, and mineralization on bone strength. J Biomech 22:419–426CrossRefPubMed Martin R, Ishida J (1989) The relative effects of collagen fiber orientation, porosity, density, and mineralization on bone strength. J Biomech 22:419–426CrossRefPubMed
36.
go back to reference Ferretti J (1995) Perspectives of pQCT technology associated to biomechanical studies in skeletal research employing rat models. Bone 17:S353–S364CrossRef Ferretti J (1995) Perspectives of pQCT technology associated to biomechanical studies in skeletal research employing rat models. Bone 17:S353–S364CrossRef
37.
go back to reference Currey J (1969) The mechanical consequences of variation in the mineral content of bone. J Biomech 2:1–11CrossRefPubMed Currey J (1969) The mechanical consequences of variation in the mineral content of bone. J Biomech 2:1–11CrossRefPubMed
38.
go back to reference Currey J (1975) The effects of strain rate, reconstruction and mineral content on some mechanical properties of bovine bone. J Biomech 8:81–86CrossRefPubMed Currey J (1975) The effects of strain rate, reconstruction and mineral content on some mechanical properties of bovine bone. J Biomech 8:81–86CrossRefPubMed
39.
go back to reference Currey JD (1988) The effect of porosity and mineral content on the Young’s modulus of elasticity of compact bone. J Biomech 21:131–139CrossRefPubMed Currey JD (1988) The effect of porosity and mineral content on the Young’s modulus of elasticity of compact bone. J Biomech 21:131–139CrossRefPubMed
40.
go back to reference Sottile V, Seuwen K, Kneissel M (2004) Enhanced marrow adipogenesis and bone resorption in estrogen-deprived rats treated with the PPARγ agonist BRL49653 (rosiglitazone). Calcif Tissue Int 75:329–337CrossRefPubMed Sottile V, Seuwen K, Kneissel M (2004) Enhanced marrow adipogenesis and bone resorption in estrogen-deprived rats treated with the PPARγ agonist BRL49653 (rosiglitazone). Calcif Tissue Int 75:329–337CrossRefPubMed
41.
go back to reference Müller R, Van Campenhout H, Van Damme B, Van der Perre G, Dequeker J, Hildebrand T, Rüegsegger P (1998) Morphometric analysis of human bone biopsies: a quantitative structural comparison of histological sections and micro-computed tomography. Bone 23:59–66CrossRefPubMed Müller R, Van Campenhout H, Van Damme B, Van der Perre G, Dequeker J, Hildebrand T, Rüegsegger P (1998) Morphometric analysis of human bone biopsies: a quantitative structural comparison of histological sections and micro-computed tomography. Bone 23:59–66CrossRefPubMed
Metadata
Title
Dual-energy X-ray absorptiometry, peripheral quantitative computed tomography, and micro-computed tomography techniques are discordant for bone density and geometry measurements in the guinea pig
Authors
Ivy L. Mak
Jason R. DeGuire
Paula Lavery
Sherry Agellon
Hope A. Weiler
Publication date
01-05-2016
Publisher
Springer Japan
Published in
Journal of Bone and Mineral Metabolism / Issue 3/2016
Print ISSN: 0914-8779
Electronic ISSN: 1435-5604
DOI
https://doi.org/10.1007/s00774-015-0675-1

Other articles of this Issue 3/2016

Journal of Bone and Mineral Metabolism 3/2016 Go to the issue