Skip to main content
Top
Published in: BMC Musculoskeletal Disorders 1/2017

Open Access 01-12-2017 | Research article

Quantitative evaluation of subchondral bone microarchitecture in knee osteoarthritis using 3T MRI

Authors: Chenglei Liu, Chang Liu, Xvhua Ren, Liping Si, Hao Shen, Qian Wang, Weiwu Yao

Published in: BMC Musculoskeletal Disorders | Issue 1/2017

Login to get access

Abstract

Background

Osteoarthritis (OA) is now increasingly recognized as being related to the whole joint instead of the cartilage alone. In particular, the importance of subchondral bone in OA pathogenesis has drawn a lot of interest. The aim of this study is to investigate subchondral bone microstructural features in two femoral condyles of human knee osteoarthritis.

Methods

Eighty subjects were enrolled in our study and divided into three groups: without OA (group 0), mild OA (group 1), and severe OA (group 2). Sagittal 3D Balanced Fast Field Echo (3D–FFE) images were obtained by 3T MRI to quantify trabecular bone structure, and sagittal FatSat 3D Fast Field Echo (3D–FFE) images were acquired to assess cartilage thickness. Trabecular bone parameters, including bone volume fraction (BVF), erosion index (EI) and the trabecular plate-to-rod ratio (SCR), and trabecular thickness were evaluated using digital topological analysis. Subchondral bone and cartilage parameters between different groups and different locations were compared, and their correlations were analyzed.

Results

Within two femoral condyles, subchondral bone structure was deteriorated in mild OA, showing a lower BVF (−0.011 to −0.014 P < 0.001), a higher EI (0.346 to 0.310 P < 0.001), a lower SCR (−0.581 to −0.542 P < 0.001)) and lower trabecular thickness (−6.588 to −4.759 P < 0.05). In severe OA, BVF was further decreased, but EI, SCR and trabecular thickness showed no significant difference than mild OA(P > 0.05). Moreover, there was a lower BVF, SCR and higher EI in the medial femoral condyle in each group. Interestingly, cartilage attrition mainly occurred in the medial femoral condyle. Medial cartilage thickness was not only positively correlated with the ipsilateral femoral BVF (r = 0.321 P = 0.004) but also with the opposite femoral BVF (r = 0.270 P = 0.015).

Conclusions

Our results indicated that deterioration in the trabecular bone structure in both femoral condyles could more sensitively reveal early OA, and BVF could be a better biomarker to evaluate OA severity.
Literature
1.
go back to reference Hunter DJ. Pharmacologic therapy for osteoarthritis--the era of disease modification. Nature reviews. Rheumatology. 2011;7(1):13–22.PubMed Hunter DJ. Pharmacologic therapy for osteoarthritis--the era of disease modification. Nature reviews. Rheumatology. 2011;7(1):13–22.PubMed
2.
go back to reference Funck-Brentano T, Cohen-Solal M. Subchondral bone and osteoarthritis. Curr Opin Rheumatol. 2015;27(4):420–6.CrossRefPubMed Funck-Brentano T, Cohen-Solal M. Subchondral bone and osteoarthritis. Curr Opin Rheumatol. 2015;27(4):420–6.CrossRefPubMed
3.
go back to reference Mohan G, Perilli E, Parkinson IH, Humphries JM, Fazzalari NL, Kuliwaba JS. Pre-emptive, early, and delayed alendronate treatment in a rat model of knee osteoarthritis: effect on subchondral trabecular bone microarchitecture and cartilage degradation of the tibia, bone/cartilage turnover, and joint discomfort. Osteoarthritis Cartilage. 2013;21(10):1595–604.CrossRefPubMed Mohan G, Perilli E, Parkinson IH, Humphries JM, Fazzalari NL, Kuliwaba JS. Pre-emptive, early, and delayed alendronate treatment in a rat model of knee osteoarthritis: effect on subchondral trabecular bone microarchitecture and cartilage degradation of the tibia, bone/cartilage turnover, and joint discomfort. Osteoarthritis Cartilage. 2013;21(10):1595–604.CrossRefPubMed
4.
go back to reference Zhen G, Wen C, Jia X, Li Y, Crane JL, Mears SC, Askin FB, Frassica FJ, Chang W, Yao J, Carrino JA, Cosgarea A, Artemov D, Chen Q, Zhao Z, Zhou X, et al. Inhibition of TGF-beta signaling in mesenchymal stem cells of subchondral bone attenuates osteoarthritis. Nat Med. 2013;19(6):704–12.CrossRefPubMedPubMedCentral Zhen G, Wen C, Jia X, Li Y, Crane JL, Mears SC, Askin FB, Frassica FJ, Chang W, Yao J, Carrino JA, Cosgarea A, Artemov D, Chen Q, Zhao Z, Zhou X, et al. Inhibition of TGF-beta signaling in mesenchymal stem cells of subchondral bone attenuates osteoarthritis. Nat Med. 2013;19(6):704–12.CrossRefPubMedPubMedCentral
5.
go back to reference Roemer FW, Guermazi A, Javaid MK, Lynch JA, Niu J, Zhang Y, Felson DT, Lewis CE, Torner J, Nevitt MC. Change in MRI-detected subchondral bone marrow lesions is associated with cartilage loss: the MOST study. A longitudinal multicentre study of knee osteoarthritis. Ann Rheum Dis. 2009;68(9):1461–5.CrossRefPubMed Roemer FW, Guermazi A, Javaid MK, Lynch JA, Niu J, Zhang Y, Felson DT, Lewis CE, Torner J, Nevitt MC. Change in MRI-detected subchondral bone marrow lesions is associated with cartilage loss: the MOST study. A longitudinal multicentre study of knee osteoarthritis. Ann Rheum Dis. 2009;68(9):1461–5.CrossRefPubMed
6.
go back to reference Zhang LZ, Zheng HA, Jiang Y, Tu YH, Jiang PH, Yang AL. Mechanical and biologic link between cartilage and subchondral bone in osteoarthritis. Arthritis Care Res (Hoboken). 2012;64(7):960–7. Zhang LZ, Zheng HA, Jiang Y, Tu YH, Jiang PH, Yang AL. Mechanical and biologic link between cartilage and subchondral bone in osteoarthritis. Arthritis Care Res (Hoboken). 2012;64(7):960–7.
8.
go back to reference Zhou X, von der Mark K, Henry S, Norton W, Adams H, de Crombrugghe B. Chondrocytes transdifferentiate into osteoblasts in endochondral bone during development, postnatal growth and fracture healing in mice. PLoS Genet. 2014;10(12):e1004820.CrossRefPubMedPubMedCentral Zhou X, von der Mark K, Henry S, Norton W, Adams H, de Crombrugghe B. Chondrocytes transdifferentiate into osteoblasts in endochondral bone during development, postnatal growth and fracture healing in mice. PLoS Genet. 2014;10(12):e1004820.CrossRefPubMedPubMedCentral
9.
go back to reference Karsdal MA, Bay-Jensen AC, Lories RJ, Abramson S, Spector T, Pastoureau P, Christiansen C, Attur M, Henriksen K, Goldring SR, Kraus V. The coupling of bone and cartilage turnover in osteoarthritis: opportunities for bone antiresorptives and anabolics as potential treatments? Ann Rheum Dis. 2014;73(2):336–48.CrossRefPubMed Karsdal MA, Bay-Jensen AC, Lories RJ, Abramson S, Spector T, Pastoureau P, Christiansen C, Attur M, Henriksen K, Goldring SR, Kraus V. The coupling of bone and cartilage turnover in osteoarthritis: opportunities for bone antiresorptives and anabolics as potential treatments? Ann Rheum Dis. 2014;73(2):336–48.CrossRefPubMed
10.
go back to reference Pelletier JP, Roubille C, Raynauld JP, Abram F, Dorais M, Delorme P, Martel-Pelletier J. Disease-modifying effect of strontium ranelate in a subset of patients from the phase III knee osteoarthritis study SEKOIA using quantitative MRI: reduction in bone marrow lesions protects against cartilage loss. Ann Rheum Dis. 2015;74(2):422–9.CrossRefPubMed Pelletier JP, Roubille C, Raynauld JP, Abram F, Dorais M, Delorme P, Martel-Pelletier J. Disease-modifying effect of strontium ranelate in a subset of patients from the phase III knee osteoarthritis study SEKOIA using quantitative MRI: reduction in bone marrow lesions protects against cartilage loss. Ann Rheum Dis. 2015;74(2):422–9.CrossRefPubMed
11.
go back to reference Bertuglia A, Lacourt M, Girard C, Beauchamp G, Richard H, Laverty S. Osteoclasts are recruited to the subchondral bone in naturally occurring post-traumatic equine carpal osteoarthritis and may contribute to cartilage degradation. Osteoarthritis Cartilage. 2016;24(3):555–66.CrossRefPubMed Bertuglia A, Lacourt M, Girard C, Beauchamp G, Richard H, Laverty S. Osteoclasts are recruited to the subchondral bone in naturally occurring post-traumatic equine carpal osteoarthritis and may contribute to cartilage degradation. Osteoarthritis Cartilage. 2016;24(3):555–66.CrossRefPubMed
12.
go back to reference Beuf O, Ghosh S, Newitt DC, Link TM, Steinbach L, Ries M, Lane N, Majumdar S. Magnetic resonance imaging of normal and osteoarthritic trabecular bone structure in the human knee. Arthritis Rheum. 2002;46(2):385–93.CrossRefPubMed Beuf O, Ghosh S, Newitt DC, Link TM, Steinbach L, Ries M, Lane N, Majumdar S. Magnetic resonance imaging of normal and osteoarthritic trabecular bone structure in the human knee. Arthritis Rheum. 2002;46(2):385–93.CrossRefPubMed
13.
go back to reference Chiba K, Uetani M, Kido Y, Ito M, Okazaki N, Taguchi K, Shindo H. Osteoporotic changes of subchondral trabecular bone in osteoarthritis of the knee: a 3-T MRI study. Osteoporos Int. 2012;23(2):589–97.CrossRefPubMed Chiba K, Uetani M, Kido Y, Ito M, Okazaki N, Taguchi K, Shindo H. Osteoporotic changes of subchondral trabecular bone in osteoarthritis of the knee: a 3-T MRI study. Osteoporos Int. 2012;23(2):589–97.CrossRefPubMed
14.
go back to reference Chang G, Xia D, Chen C, Madelin G, Abramson SB, Babb JS, Saha PK, Regatte RR. 7T MRI detects deterioration in subchondral bone microarchitecture in subjects with mild knee osteoarthritis as compared with healthy controls. J Magn Reson Imaging. 2015;41(5):1311–7.CrossRefPubMed Chang G, Xia D, Chen C, Madelin G, Abramson SB, Babb JS, Saha PK, Regatte RR. 7T MRI detects deterioration in subchondral bone microarchitecture in subjects with mild knee osteoarthritis as compared with healthy controls. J Magn Reson Imaging. 2015;41(5):1311–7.CrossRefPubMed
15.
go back to reference Zuo J, Bolbos R, Hammond K, Li X, Majumdar S. Reproducibility of the quantitative assessment of cartilage morphology and trabecular bone structure with magnetic resonance imaging at 7 T. Magn Reson Imaging. 2008;26(4):560–6.CrossRefPubMed Zuo J, Bolbos R, Hammond K, Li X, Majumdar S. Reproducibility of the quantitative assessment of cartilage morphology and trabecular bone structure with magnetic resonance imaging at 7 T. Magn Reson Imaging. 2008;26(4):560–6.CrossRefPubMed
17.
go back to reference Bellamy N, Buchanan WW, Goldsmith CH, Campbell J, Stitt LW. Validation study of WOMAC: a health status instrument for measuring clinically important patient relevant outcomes to antirheumatic drug therapy in patients with osteoarthritis of the hip or knee. J Rheumatol. 1988;15(12):1833–40.PubMed Bellamy N, Buchanan WW, Goldsmith CH, Campbell J, Stitt LW. Validation study of WOMAC: a health status instrument for measuring clinically important patient relevant outcomes to antirheumatic drug therapy in patients with osteoarthritis of the hip or knee. J Rheumatol. 1988;15(12):1833–40.PubMed
18.
go back to reference Vasilic B, Wehrli FWA. Novel local thresholding algorithm for trabecular bone volume fraction mapping in the limited spatial resolution regime of in vivo MRI. IEEE Trans Med Imaging. 2005;24(12):1574–85.CrossRefPubMed Vasilic B, Wehrli FWA. Novel local thresholding algorithm for trabecular bone volume fraction mapping in the limited spatial resolution regime of in vivo MRI. IEEE Trans Med Imaging. 2005;24(12):1574–85.CrossRefPubMed
19.
go back to reference Gomberg BR, Saha PK, Song HK, Hwang SN, Wehrli FW. Topological analysis of trabecular bone MR images. IEEE Trans Med Imaging. 2000;19(3):166–74.CrossRefPubMed Gomberg BR, Saha PK, Song HK, Hwang SN, Wehrli FW. Topological analysis of trabecular bone MR images. IEEE Trans Med Imaging. 2000;19(3):166–74.CrossRefPubMed
20.
go back to reference Saha PK, Wehrli FW. Measurement of trabecular bone thickness in the limited resolution regime of in vivo MRI by fuzzy distance transform. IEEE Trans Med Imaging. 2004;23(1):53–62.CrossRefPubMed Saha PK, Wehrli FW. Measurement of trabecular bone thickness in the limited resolution regime of in vivo MRI by fuzzy distance transform. IEEE Trans Med Imaging. 2004;23(1):53–62.CrossRefPubMed
21.
go back to reference Sniekers YH, Intema F, Lafeber FP, van Osch GJ, van Leeuwen JP, Weinans H, Mastbergen SCA. Role for subchondral bone changes in the process of osteoarthritis; a micro-CT study of two canine models. BMC Musculoskelet Disord. 2008;9:20.CrossRefPubMedPubMedCentral Sniekers YH, Intema F, Lafeber FP, van Osch GJ, van Leeuwen JP, Weinans H, Mastbergen SCA. Role for subchondral bone changes in the process of osteoarthritis; a micro-CT study of two canine models. BMC Musculoskelet Disord. 2008;9:20.CrossRefPubMedPubMedCentral
22.
go back to reference Maerz T, Kurdziel M, Newton MD, Altman P, Anderson K, Matthew HW, Baker KC. Subchondral and epiphyseal bone remodeling following surgical transection and noninvasive rupture of the anterior cruciate ligament as models of post-traumatic osteoarthritis. Osteoarthritis Cartilage. 2016;24(4):698–708.CrossRefPubMed Maerz T, Kurdziel M, Newton MD, Altman P, Anderson K, Matthew HW, Baker KC. Subchondral and epiphyseal bone remodeling following surgical transection and noninvasive rupture of the anterior cruciate ligament as models of post-traumatic osteoarthritis. Osteoarthritis Cartilage. 2016;24(4):698–708.CrossRefPubMed
23.
go back to reference Yuan XL, Meng HY, Wang YC, Peng J, Guo QY, Wang AY, Bone-cartilage LSB. Interface crosstalk in osteoarthritis: potential pathways and future therapeutic strategies. Osteoarthritis Cartilage. 2014;22(8):1077–89.CrossRefPubMed Yuan XL, Meng HY, Wang YC, Peng J, Guo QY, Wang AY, Bone-cartilage LSB. Interface crosstalk in osteoarthritis: potential pathways and future therapeutic strategies. Osteoarthritis Cartilage. 2014;22(8):1077–89.CrossRefPubMed
24.
go back to reference Burr DB, Gallant MA. Bone remodelling in osteoarthritis. Nature reviews. Rheumatology. 2012;8(11):665–73.PubMed Burr DB, Gallant MA. Bone remodelling in osteoarthritis. Nature reviews. Rheumatology. 2012;8(11):665–73.PubMed
25.
go back to reference Chiba K, Nango N, Kubota S, Okazaki N, Taguchi K, Osaki M, Ito M. Relationship between microstructure and degree of mineralization in subchondral bone of osteoarthritis: a synchrotron radiation microCT study. J Bone Miner Res. 2012;27(7):1511–7.CrossRefPubMed Chiba K, Nango N, Kubota S, Okazaki N, Taguchi K, Osaki M, Ito M. Relationship between microstructure and degree of mineralization in subchondral bone of osteoarthritis: a synchrotron radiation microCT study. J Bone Miner Res. 2012;27(7):1511–7.CrossRefPubMed
26.
go back to reference Hunter DJ, Gerstenfeld L, Bishop G, Davis AD, Mason ZD, Einhorn TA, Maciewicz RA, Newham P, Foster M, Jackson S, Morgan EF. Bone marrow lesions from osteoarthritis knees are characterized by sclerotic bone that is less well mineralized. Arthritis Res Ther. 2009;11(1):R11.CrossRefPubMedPubMedCentral Hunter DJ, Gerstenfeld L, Bishop G, Davis AD, Mason ZD, Einhorn TA, Maciewicz RA, Newham P, Foster M, Jackson S, Morgan EF. Bone marrow lesions from osteoarthritis knees are characterized by sclerotic bone that is less well mineralized. Arthritis Res Ther. 2009;11(1):R11.CrossRefPubMedPubMedCentral
27.
go back to reference Driban JB, Tassinari A, Lo GH, Price LL, Schneider E, Lynch JA, Eaton CB, McAlindon TE. Bone marrow lesions are associated with altered trabecular morphometry. Osteoarthritis Cartilage. 2012;20(12):1519–26.CrossRefPubMedPubMedCentral Driban JB, Tassinari A, Lo GH, Price LL, Schneider E, Lynch JA, Eaton CB, McAlindon TE. Bone marrow lesions are associated with altered trabecular morphometry. Osteoarthritis Cartilage. 2012;20(12):1519–26.CrossRefPubMedPubMedCentral
28.
go back to reference Wolff J. The classic: on the significance of the architecture of the spongy substance for the question of bone growth: a preliminary publication. 1869. Clin Orthop Relat Res. 2011;469(11):3077–8.CrossRefPubMedPubMedCentral Wolff J. The classic: on the significance of the architecture of the spongy substance for the question of bone growth: a preliminary publication. 1869. Clin Orthop Relat Res. 2011;469(11):3077–8.CrossRefPubMedPubMedCentral
29.
go back to reference Ding M, Odgaard A, Hvid I. Changes in the three-dimensional microstructure of human tibial cancellous bone in early osteoarthritis. J Bone Joint Surg Br. 2003;85(6):906–12.PubMed Ding M, Odgaard A, Hvid I. Changes in the three-dimensional microstructure of human tibial cancellous bone in early osteoarthritis. J Bone Joint Surg Br. 2003;85(6):906–12.PubMed
30.
go back to reference Bobinac D, Spanjol J, Zoricic S, Maric I. Changes in articular cartilage and subchondral bone histomorphometry in osteoarthritic knee joints in humans. Bone. 2003;32(3):284–90.CrossRefPubMed Bobinac D, Spanjol J, Zoricic S, Maric I. Changes in articular cartilage and subchondral bone histomorphometry in osteoarthritic knee joints in humans. Bone. 2003;32(3):284–90.CrossRefPubMed
31.
32.
go back to reference Gomberg BR, Saha PK, Wehrli FW. Topology-based orientation analysis of trabecular bone networks. Med Phys. 2003;30(2):158–68.CrossRefPubMed Gomberg BR, Saha PK, Wehrli FW. Topology-based orientation analysis of trabecular bone networks. Med Phys. 2003;30(2):158–68.CrossRefPubMed
Metadata
Title
Quantitative evaluation of subchondral bone microarchitecture in knee osteoarthritis using 3T MRI
Authors
Chenglei Liu
Chang Liu
Xvhua Ren
Liping Si
Hao Shen
Qian Wang
Weiwu Yao
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Musculoskeletal Disorders / Issue 1/2017
Electronic ISSN: 1471-2474
DOI
https://doi.org/10.1186/s12891-017-1865-x

Other articles of this Issue 1/2017

BMC Musculoskeletal Disorders 1/2017 Go to the issue