Improved Visualization of Cartilage Canals Using Quantitative Susceptibility Mapping

RESEARCH ARTICLE Improved Visualization of Cartilage Canals Using Quantitative Susceptibility Mapping Mikko J. Nissi1,2,3,4,5*, Ferenc Tóth6, Luning Wang1,2, Cathy S. Carlson6, Jutta M. Ellermann1 a11111 1 Center for Magnetic Resonance Research, Department of Radiology, University of Minnesota, Minneapolis, MN, United States of America, 2 Department of Orthopaedic Surgery, University of Minnesota, Minneapolis, MN, United States of America, 3 Research Group of Medical Imaging, Physics and Technology, Faculty of Medicine, University of Oulu, Oulu, Finland, 4 Medical Research Center Oulu, Oulu University Hospital and University of Oulu, Oulu, Finland, 5 Department of Applied Physics, University of Eastern Finland, Kuopio, Finland, 6 Department of Veterinary Population Medicine, College of Veterinary Medicine, University of Minnesota, St. Paul, MN, United States of America * Abstract OPEN ACCESS Citation: Nissi MJ, Tóth F, Wang L, Carlson CS, Ellermann JM (2015) Improved Visualization of Cartilage Canals Using Quantitative Susceptibility Mapping. PLoS ONE 10(7): e0132167. doi:10.1371/ journal.pone.0132167 Editor: Jung-Eun Kim, Kyungpook National University School of Medicine, REPUBLIC OF KOREA Received: December 8, 2014 Accepted: June 10, 2015 Purpose Cartilage canal vessels are critical to the normal function of epiphyseal (growth) cartilage and damage to these vessels is demonstrated or suspected in several important developmental orthopaedic diseases. High-resolution, three-dimensional (3-D) visualization of cartilage canals has recently been demonstrated using susceptibility weighted imaging (SWI). In the present study, a quantitative susceptibility mapping (QSM) approach is evaluated for 3-D visualization of the cartilage canals. It is hypothesized that QSM post-processing improves visualization of the cartilage canals by resolving artifacts present in the standard SWI post-processing while retaining sensitivity to the cartilage canals. Published: July 13, 2015 Copyright: © 2015 Nissi 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 Statement: All relevant data are within the paper and its Supporting Information files. Funding: This work was supported by National Institutes of Health (http://www.nih.gov/): grants T32 OD010993 (CSC), K18 OD010468 (CSC), P41 EB015894, S10 RR026783, R21 EB009138; Academy of Finland (http://www.aka.fi/): grant 260321; and W. M. Keck Foundation (http://www. wmkeck.org/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Methods Ex vivo distal femoral specimens from 3- and 8-week-old piglets and a 1-month-old human cadaver were scanned at 9.4 T with a 3-D gradient recalled echo sequence suitable for SWI and QSM post-processing. The human specimen and the stifle joint of a live, 3-week-old piglet also were scanned at 7.0 T. Datasets were processed using the standard SWI method and truncated k-space division QSM approach. To compare the post-processing methods, minimum/maximum intensity projections and 3-D reconstructions of the processed datasets were generated and evaluated. Results Cartilage canals were successfully visualized using both SWI and QSM approaches. The artifactual splitting of the cartilage canals that occurs due to the dipolar phase, which was present in the SWI post-processed data, was eliminated by the QSM approach. Thus, orientation-independent visualization and better localization of the cartilage canals was achieved PLOS ONE | DOI:10.1371/journal.pone.0132167 July 13, 2015 1 / 15 Improved Visualization of Cartilage Canals Using QSM Competing Interests: The authors have declared that no competing interests exist. with the QSM approach. Combination of GRE with a mask based on QSM data further improved visualization. Conclusions Improved and artifact-free 3-D visualization of the cartilage canals was demonstrated by QSM processing of the data, especially by utilizing susceptibility data as an enhancing mask. Utilizing tissue-inherent contrast, this method allows noninvasive assessment of the vasculature in the epiphyseal cartilage in the developing skeleton and potentially increases the opportunity to diagnose disease of this tissue in the preclinical stages, when treatment likely will have increased efficacy. Introduction Susceptibility-weighted imaging (SWI) is an MRI technique that utilizes subtle differences in magnetic susceptibility values between tissues to generate contrast [1–3]. SWI has been primarily used for imaging the brain, including anatomical features [3–5], the venous vasculature [1, 2], areas of hemorrhage and other brain lesions [6, 7], and quantification of iron content [8], areas of calcification [9], and oxygen saturation [10]. Typical SWI approaches rely on highpass filtering of the phase and subsequent generation and application of a phase mask to the magnitude data [11]. Potential drawbacks of the SWI technique, however, are that it is qualitative and suffers from artifacts due to the dipolar nature of phase accumulation between substances of different magnetic susceptibility [12, 13]. Quantitative susceptibility mapping (QSM) is an approach that attempts to calculate the underlying susceptibility distribution from the phase data [10, 13–16]. The non-uniform susceptibility distribution generates phase changes, from which the susceptibility can be derived by solving an ill-posed inverse problem [13–15, 17]. As the susceptibility distribution is revealed, the result is quantitative as opposed to the qualitative SWI data. Furthermore, the boundaries between susceptibility differences are better defined in the actual susceptibility maps than in the SWI data. Recently, the utilization of SWI for 3-D visualization of cartilage canal vasculature in the epiphyseal cartilage in the developing skeleton was introduced [12, 18] and its successful application was demonstrated [19]. The vasculature in the epiphyseal cartilage is confined to cartilage canals, structures composed of arteries, veins and capillaries embedded in a connective tissue matrix [20]. The diameter of the canals has been reported to range from 0.2 to 0.6 mm, with the confined vessels ranging from 0.01 to 0.16 mm in diameter in young piglets [12, 21]. While the imaging of cartilage canals was demonstrated using SWI with a detection limit roughly scaling with the imaging resolution (canals of approximately 100 μm were detected at 9.4 T at 100 μm isotropic resolution), this method was not free of artifacts [12]. Vessel splitting artifacts, apparent in the SWI data in planes parallel to B0, resulting from the dipolar phase pattern, hamper three-dimensional assessment and analysis. The purpose of this study was to explore the application of quant (...truncated)