Differences in tibial subchondral bone structure evaluated using plain radiographs between knees with and without cartilage damage or bone marrow lesions - the Oulu Knee Osteoarthritis study

Eur Radiol (2017) 27:4874–4882 DOI 10.1007/s00330-017-4826-8 MUSCULOSKELETAL Differences in tibial subchondral bone structure evaluated using plain radiographs between knees with and without cartilage damage or bone marrow lesions - the Oulu Knee Osteoarthritis study Jukka Hirvasniemi 1,2 & Jérôme Thevenot 1,3 & Ali Guermazi 4 & Jana Podlipská 1,3 & Frank W. Roemer 4,5 & Miika T. Nieminen 1,2,3,6 & Simo Saarakkala 1,2,3,6 Received: 3 October 2016 / Revised: 13 March 2017 / Accepted: 20 March 2017 / Published online: 24 April 2017 # The Author(s) 2017. This article is an open access publication Abstract Objectives To investigate whether subchondral bone structure from plain radiographs is different between subjects with and without articular cartilage damage or bone marrow lesions (BMLs). Methods Radiography-based bone structure was assessed from 80 subjects with different stages of knee osteoarthritis using entropy of Laplacian-based image (ELap) and local binary patterns (ELBP), homogeneity index of local angles (HIAngles,mean), and horizontal (FDHor) and vertical fractal dimensions (FDVer). Medial tibial articular cartilage damage and BMLs were scored using the magnetic resonance imaging osteoarthritis knee score. Level of statistical significance was set to p < 0.05. Results Subjects with medial tibial cartilage damage had significantly higher FDVer and ELBP as well as lower ELap and HIAngles,mean in the medial tibial subchondral bone region than subjects without damage. FDHor, FDVer, and ELBP were significantly higher, whereas ELap and HIAngles,mean were lower in the medial trabecular bone region. Subjects with medial tibial BMLs had significantly higher FDVer and ELBP as well as lower ELap and HIAngles,mean in medial tibial subchondral bone. FDHor, FDVer, and ELBP were higher, whereas ELap and HIAngles,mean were lower in medial trabecular bone. Conclusions Our results support the use of bone structural analysis from radiographs when examining subjects with osteoarthritis or at risk of having it. Key points • Knee osteoarthritis causes changes in articular cartilage and subchondral bone • Magnetic resonance imaging is a comprehensive imaging modality for knee osteoarthritis • Radiography-based bone structure analysis can provide additional information of osteoarthritic subjects * Jukka Hirvasniemi Simo Saarakkala Jérôme Thevenot 1 Research Unit of Medical Imaging, Physics and Technology, Faculty of Medicine, University of Oulu, POB 5000, FI-90014 Oulu, Finland Ali Guermazi 2 Medical Research Center Oulu, Oulu University Hospital and University of Oulu, Oulu, Finland 3 Infotech Oulu, University of Oulu, Oulu, Finland 4 Quantitative Imaging Center, Department of Radiology, Boston University School of Medicine, Boston, MA, USA 5 Department of Radiology, University of Erlangen-Nuremberg, Erlangen, Germany 6 Department of Diagnostic Radiology, Oulu University Hospital, Oulu, Finland Jana Podlipská Frank W. Roemer Miika T. Nieminen Eur Radiol (2017) 27:4874–4882 Keywords Radiography . Osteoarthritis . Bone . Structural Analysis . Knee Abbreviations BML bone marrow lesion ELap entropy of Laplacian-based image ELBP entropy of grouped Local Binary Patterns fractal dimension of horizontal structures FDHor fractal dimension of vertical structures FDVer FSA fractal signature analysis HI homogeneity index HIAngles HI for orientation of local patterns HIAngles,Perp HI perpendicularly to the bone trabeculae HIAngles,Paral HI along the trabeculae KL Kellgren–Lawrence LBP local binary patterns MOAKS MRI OA knee score MRI magnetic resonance imaging OA osteoarthritis PD proton density TSE turbo spin-echo ROI region of interest 2-D two-dimensional 3-D three-dimensional Introduction Bony changes, including osteophytes or subchondral cyst formation, are clearly seen on plain radiographs and are providing useful morphologic information in diseases affecting bone density and structure, such as osteoarthritis (OA) or osteoporosis. Although, the plain two-dimensional (2-D) radiograph is a projection (summation) through the actual threedimensional (3-D) structure, bone density and bone structure as depicted by plain radiographs is significantly related with the actual 3-D structure of bone [1–5]. Diagnosis of OA is based on a subject’s history and symptoms, physical findings, and characteristic changes on plain radiographs. Typically, the severity of OA is evaluated from radiographs using the Kellgren–Lawrence (KL) grading scale, which is based on the visual evaluation of joint space narrowing, subchondral bone sclerosis, presence of osteophytes, and deformation of bone ends [6]. As ordinal grading using the KL scale gives only a summary score of overall disease severity with varying intra- and inter-rater reliability [7–9], development of quantitative and userindependent image analysis algorithms that exploit additional radiographic information is important to potentially enhance the clinical value of plain radiographs in OA diagnostics. 4875 Joint space width is the most common parameter measured quantitatively from plain knee radiographs [10, 11]. Other parameters related to subchondral bone structure have also potential to be used as an additional measure in OA diagnostics and characterization with potential relevance for prediction of disease progression. Fractal analysis is the most popular method to assess bone structure from radiographs in OA research and a method called fractal signature analysis (FSA) has been shown to predict disease progression [12, 13]. Furthermore, it has been reported that bone structure assessed from plain radiographs using Laplacian-based method, local binary pattern (LBP)-based methods, and FSA is significantly related with the 3-D microstructure of bone [5]. Recently, subchondral and trabecular bone structures evaluated using LBP-based and Laplacian-based methods have shown to differ between subjects with different KL grades [14]. In that study, the KL grading and structure analysis of bone was made for the same images making the measurements dependent on each other to some extent, since features evaluated in the KL grading, for instance, bone sclerosis, affect the structural parameters as well. In order to study further the potential relevance of the radiography-based bone structural analysis methods, these should be compared with independent reference methods. Magnetic resonance imaging (MRI) is considered the most comprehensive imaging modality for assessment of knee OA in a research context [15]. Semi-quantitative scoring systems that evaluate features related with or altered in the knee OA process have been developed and used for the assessment of structural deterioration of tissues within the knee joint [16]. Among many different features, MRI enables direct evaluation of cartilage damage and subchondral bone marrow lesions (BMLs) that are known to be related with OA incidence and progression [17–21]. However, the (...truncated)