MRI Overestimates Articular Cartilage Thickness and Volume Compared to Synchrotron Radiation Phase-contrast Imaging
Suranjan Bairagi, Mohammad-Amin Abdollahifar, Oghenevwogaga J. Atake, William Dust, Sheldon Wiebe, George Belev, L. Dean Chapman, M. Adam Webb, Ning Zhu, David M. L. Cooper, B. Frank Eames
Accurate evaluation of morphological changes in articular cartilage are necessary for early detection of osteoarthritis (OA). 3T magnetic resonance imaging (MRI) has highly sensitive contrast resolution and is widely used clinically to detect OA. However, synchrotron radiation phase-contrast imaging computed tomography (SR-PCI) can also provide contrast to tissue interfaces that do not have sufficient absorption differences, with the added benefit of very high spatial resolution. Here, MRI was compared with SR-PCI for quantitative evaluation of human articular cartilage. Medial tibial condyles were harvested from non-OA donors and from OA patients receiving knee replacement surgery.
The most common cartilage disease is osteoarthritis (OA), where articular cartilage of the joint is destroyed either as a normal aging process or as a secondary disease from trauma [1, 2]. Given associated pain, swelling, and joint dysfunction, OA dramatically affects work and life productivity. Although destruction of articular cartilage is a gradual process, OA is hard to detect early, delaying diagnosis until significant patient symptoms exist and irreversible joint damage has occurred [1, 2]. As a result, most OA diagnoses are severe cases and are treated by replacing the joint surfaces with prosthetic components.
Materials and method
All tissues were obtained according to University of Saskatchewan-approved ethical protocol Bio 13–110. Healthy donor tissues were harvested through the Body Bequeathal Program of the Department of Anatomy, Physiology, and Pharmacology at the University of Saskatchewan. Osteoarthritic tissues were harvested from consenting patients receiving knee replacement surgery by orthopedic surgeons at Saskatoon City Hospital, Canada. All samples were stored in 10% formalin. For imaging protocols, samples were placed in a custom-designed, 3D printed sample holder (Fig 1) and submerged in phosphate-buffered saline (PBS). Imaging was performed on the medial tibial condyle of disarticulated human knee joints from four non-OA and four OA donors (Table 1). To avoid sex-dependent features that might provide unnecessary variance in our statistical analyses, only female tissues were used.
To confirm the status of articular cartilage in the medical school cadaveric (non-OA) and surgical patient (OA) samples of medial tibial condyles, gross anatomical analyses were performed by an orthopaedic surgeon. These analyses revealed that samples of the non-OA group had no obvious cartilage defects, while each sample in the OA group appeared to have severe OA with exposed subchondral bone and often cartilage fibrillation
Because insufficient biomarkers exist for the early diagnosis of OA, new imaging approaches to improve the diagnosis of OA are needed. Such improvements also will improve the ability to assess progression of this complex disease, predict final joint damage, and monitor the effectiveness of experimental therapies [1, 7].
Taken together, these findings clearly demonstrated that SR-PCI provided high-resolution images that may improve assessment of clinically relevant articular cartilage parameters, such as cartilage thickness and overall volume. In addition, SR-PCI can highlight fine details of the cartilage surface, interfaces between cartilage and bone, and even fine details of the subchondral bone structure. Comparing 3T MRI to SR-PCI, both MRI and SR-PCI revealed that the OA group had significantly lower average cartilage thickness and overall cartilage volume, compared to the non-OA group.
We thank the selfless donors of cadavers to the Body Bequeathal Program in the Department of Anatomy, Physiology, and Pharmacology, and also appreciate the donors of surgically removed OA tissues during total knee arthroplasty at City Hospital of Saskatoon. Thanks to Bianca Sarkis for helping prepare samples for histology and to Shreyas Jois, Aditya Manek, and the University of Saskatchewan College of Medicine Histology Core Facility.
Citation: Bairagi S, Abdollahifar M-A, Atake OJ, Dust W, Wiebe S, Belev G, et al. (2023) MRI overestimates articular cartilage thickness and volume compared to synchrotron radiation phase-contrast imaging. PLoS ONE 18(10): e0291757. https://doi.org/10.1371/journal.pone.0291757
Editor: Zhentian Wang, Tsinghua University, CHINA
Received: December 15, 2022; Accepted: September 5, 2023; Published: October 3, 2023
Copyright: © 2023 Bairagi et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: In order that others may replicate or extend our study findings, raw image files from all samples can be found at https://globus.usask.ca/file-manager?origin_id=ef36db6f-8e10-4b8b-93b5-ec8e895a7511&origin_path=%2F.
Funding: This study was supported by grants to BFE: Royal University Hospital (RUH) Foundation, the Saskatchewan Health Research Foundation (SHRF) Establishment Grant, and the Canadian Institutes of Health Research (CIHR) project grant 148683. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Part of the research described in this paper was performed at the Canadian Light Source, a national research facility of the University of Saskatchewan, which is supported by the Canada Foundation for Innovation (CFI), the Natural Sciences and Engineering Research Council (NSERC), the National Research Council (NRC), CIHR, the Government of Saskatchewan, and the University of Saskatchewan.
Competing interests: The authors have declared that no competing interests exist.