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In Vitro MR Imaging of Hyaline Cartilage

Correlation with Scanning Electron Microscopy

¹ All authors: Department of Radiology, Dartmouth Medical School, Dartmouth Hitchcock Medical Center, One Medical Center Dr., Lebanon, NH 03756.

Received March 23, 1999; accepted after revision July 13, 1999.

 
Address correspondence to D. W. Goodwin.

Supported in part by the Radiological Society of North America Research and Education Fund seed grant.

Abstract

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OBJECTIVE. Our goal was to determine how the three-dimensional structure of hyaline cartilage affects its MR appearance and to correlate this appearance with detailed structural analysis using scanning electron microscopy and freeze-fracture sectioning techniques.

MATERIALS AND METHODS. In vitro 7-T spin-echo MR images of hyaline cartilage specimens from four patients undergoing above-knee amputations were obtained parallel and perpendicular to the main magnetic field. Specimens were imaged with low- and high-power scanning electron microscopy after freeze fracturing. The corresponding images from both techniques were analyzed with specific attention to the three-dimensional structure of the cartilage, collagen fibril orientation, and respective changes in the MR appearance.

RESULTS. Freeze fracturing of cartilage reveals a curved fracture plane. Expected changes in signal intensity predicted by the magic angle effect correlated with observed changes in signal intensity across the thickness of the sample. Changes in individual collagen fibril orientation did not correspond to MR layering.

CONCLUSION. The three-dimensional organization of collagen in cartilage has a strong influence on the MR appearance of cartilage. This influence is caused by the restriction of water mobility and the resulting magic angle effect caused by curvature of the collagen network, possibly because of the influence on proteoglycan orientation.

Introduction

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To maximize the usefulness of MR imaging of hyaline cartilage, one must understand the relationship between the complex structure of this tissue and the image. To date, such an understanding remains incomplete [1, 2, 3]. If the influence of structure on the MR image were comprehended, normal variation in structure could be distinguished from disorders; thus, the accuracy and clinical usefulness of this imaging technique would be significantly improved.

Matrix collagen within cartilage is organized in leaflike structures that radiate from the subchondral interface in a perpendicular orientation and then curve into the horizontal orientation at the articular surface [4] (Fig. 1). We believe this structure produces a characteristic orientation-dependent layered appearance that is the result of differences in the T2 decay of cartilage caused by the magic angle effect. To test this hypothesis, we have correlated MR images of human cartilage obtained at two orientations to the static magnetic field (B₀) with scanning electron microscopy performed after freeze-fracture sectioning in the plane of imaging. This histologic technique shows the three-dimensional structure of the collagen network and also allows visualization of individual collagen fibrils [4, 5, 6, 7].

View larger version (24K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1. — Drawing of collagen architecture shows leaves or layers consisting of mesh of collagen fibrils that curve into plane of articular surface. (Reprinted with permission from [4])

Materials and Methods

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Sample Preparation
Seven fresh cartilage samples were harvested from the femoral condyles of four patients who were 27-57 years old (average, 49 years). The knees were amputated for treatment of acute vascular occlusion (n = 1) or chronic vascular insufficiency (n = 3). Samples were cut from the knees with a bone saw with care to ensure that only healthy-appearing cartilage was included in the samples. All knees showed minimal degenerative changes present only at the tibial plateau and the patella. The samples were harvested within 3 days of amputation after routine examination by the pathology department. They were refrigerated in saline solution for no more than 3 additional days before imaging. Samples were prepared for imaging by cutting two scores in the subchondral bone at right angles and dividing the sample into quarters. These scores were filled with paraffin and used as fiducials for determining the plane of MR imaging. Subsequently, they were used to define the plane of fracture when samples were sectioned. For imaging, samples were placed in a sealed wax container filled with saline solution.

MR Imaging
MR images were obtained with a spectrometer (Surry Medical Imaging Systems; Guildford, United Kingdom) and a horizontal bore 7-T magnet (Magnex Scientific, Abington, United Kingdom). A 6-cm birdcage coil tuned to 300 MHz was used both to transmit and to receive. Spin-echo images were obtained with the following parameters: TR/TE, 1000/20 msec; field of view, 20-35 mm; bandwidth, 50 kHz; matrix size, 512 x 512; slice thickness, 1 mm; and excitations, 20. The readout gradient was oriented perpendicular to the articular surface so that the negative direction from cartilage toward bone shifted fat away from the cartilage.

Samples were first placed in the coil with the articular surface perpendicular to B₀ (0°). A scout image was obtained in the axial plane to visualize the fiducial cuts in the subchondral bone. Two images were then obtained of the fiducials at right angles in separate acquisitions. Subsequently, the sample was repositioned in the coil, this time with the articular surface parallel to B₀ (90°). Using fiducials to define the plane of imaging, we repeated the imaging with the same parameters. As a result, four images of each sample were obtained; two images were at right angles to one another, both at 0° and at 90° orientations to B₀.

Electron Microscopy
After imaging, we fixed samples in formalin. We subsequently demineralized them in 5% nitric acid for 48 hr and then rinsed them with saline solution. Using a scalpel, we extended the scores earlier cut in the bone to the subchondral bone to facilitate fracture sectioning. Care was taken not to extend the cut into the cartilage. Samples were then frozen and fractured into quarters. A partial proteoglycan digest was performed on three of the quarters from each specimen by placing samples in a 37°C bath of 40 mg of hyaluronidase type IV and 20 mg of trypsin type I in 20 ml of phosphate-buffered saline for 1 hr. Samples were first dehydrated through a graded series of ethanol; then they were dehydrated with 50% ethanol and 50% hexamethyldisilazane, followed by 100% hexamethyldisilazane. Samples were coated using a sputter-coater (Technics Hummer V; Anatech, Springfield, VA) with a gold and palladium target, and microscopy was performed with a scanning electron microscope (DSM-962; Zeiss USA, Thornwood, NY). Images were obtained at a variety of different magnifications. Large field-of-view low-magnification images were useful in showing the overall structure of the fracture plane. High-magnification images of individual collagen fibrils were also acquired. These images were obtained at the level of the deep, transitional, and surface layers, as defined on the MR image in each sample. The level of each MR layer was defined by measuring the dimensions of each layer and the layer's position relative to the surface and the subchondral bone. Measurements were made on the digital image with NIH Image (Wayne Rasband; National Institutes of Health, Bethesda, MD). With NIH Image, measurements on low-power scout scanning electron microscopy images were used to determine the level at which high-magnification images were obtained. This procedure ensured that high-power images were obtained within each MR layer.

Results

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MR imaging of cartilage revealed three poorly demarcated layers. When the surface was aligned perpendicular to B₀ (0°), a low-signal-intensity deep layer, a high-signal-intensity transitional layer, and a low-signal-intensity surface were seen in all seven samples (Fig. 2A). Signal intensity in the deep layer was not uniform. Instead, faint radially oriented striations and horizontal banding were present in this layer. In addition, a thin layer of higher signal intensity was occasionally observed at the interface between the subchondral bone and cartilage (Fig. 2A). The transition between layers was not well defined. Rather, these interfaces were irregular and, particularly at the inferior margin of the surface layer, one could visualize curvilinear low-signal-intensity extensions in the transitional layer below (Fig. 3A, 3B).

View larger version (70K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A. —55-year-old woman after above-knee amputation resulting from acute vascular occlusion of lower extremity. MR image of hyaline cartilage from femoral condyle imaged with surface perpendicular to the main magnetic field (B0, black arrow) shows surface (1), transitional (2), and deep (3) layers. Note thin high-signal-intensity layer (two white arrows) at border with subchondral bone. Also note score (arrowhead) cut in bone later used to fracture sample. Area displayed with electron microscopy in C is also marked (single white arrow).

View larger version (90K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3A. —55-year-old man after above-knee amputation for chronic vascular disease. MR image obtained with surface perpendicular to main magnetic field (B0, black arrow) shows three-layer appearance. High-signal-intensity transitional layer (white arrow) is present. Because surface is curved, influence of orientation is apparent. Increased signal intensity in deep layer and decreased signal intensity in superficial regions of transitional layer of cartilage are evident where sample is not perpendicular to B0.

View larger version (83K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3B. —55-year-old man after above-knee amputation for chronic vascular disease. MR image obtained with surface parallel to B0 (black arrow) shows increased signal intensity in deep layer, while decreasing signal intensity in superficial portion of transitional layer causes increase in thickness of surface layer. At this orientation, portions of transitional layer (white arrow) have low signal intensity.

Reproducible changes in the layered appearance of cartilage were created by changing the orientation of the sample relative to B₀. When imaged parallel to B₀ (90°), the thickness of the surface layer increased, while low signal extended deeper from the surface into the transitional layer (Fig. 3A, 3B). In this orientation, the width of the transitional layer also increased. Compared with the images obtained at 0°, the deep layer decreased in size. Because many of the samples had curved articular surfaces, the appearance of cartilage at a wide range of orientations relative to B₀ was observed (Fig. 3A, 3B). At orientations approximately 55° relative to B₀, the deepest regions of cartilage became universally high in signal intensity.

By fracturing frozen samples after decalcification, we were able to consistently show a characteristic curved plane of fracture (Fig 2B). Fractures extended perpendicularly from the subchondral bone and then curved into the horizontal plane. The depth of cartilage where this curve began varied among samples, but the perpendicular portion of the fracture plane extended beyond half the thickness of the sample in all cases. The curve was typically limited to the most superficial third of the cartilage. The most superficial level of cartilage was a thin film, which frequently separated from the underlying tissue during fracture. Beneath this film, the underlying collagen structure was oriented in the horizontal plane, parallel to the surface.

View larger version (158K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B. —55-year-old woman after above-knee amputation resulting from acute vascular occlusion of lower extremity. Scanning electron microscopy image reveals curvature of fracture plane (arrows).

In each sample, high-magnification images of the cartilage showing individual collagen fibrils were also obtained at depths corresponding to each of the visible MR layers. In all regions, in all samples, the orientation of individual collagen fibrils appeared random (Fig. 2C). No qualitative difference in the orientation of fibrils corresponding to the different layers seen on MR images was present. Specifically, we did not observe a transition from a highly ordered radial orientation in the deepest regions of cartilage to a more random orientation in the superficial regions.

View larger version (211K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2C. —55-year-old woman after above-knee amputation resulting from acute vascular occlusion of lower extremity. High-power scanning electron microscopy image from region of deep MR layer shows that individual collagen fibrils are not radially oriented.

MR images were correlated with the corresponding scanning electron microscopy image. In each sample, signal intensity was low when the fracture plane was parallel to B₀. As the fracture plane curved, the signal intensity of the cartilage in the corresponding image increased and subsequently decreased in a pattern consistent with the magic angle effect. Specifically, signal intensity was low when the fracture plane was parallel with B₀ and increased to a maximum when the plane of fracture was aligned at an angle approximately 55° from B₀.

Discussion

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Although the appearance of hyaline cartilage on MR images will vary with the sequence used, layers of different signal intensity can be seen [8, 9, 10, 11]. Three layers, a low-signal-intensity deep layer, a high-signal-intensity transitional layer, and a low-signal-intensity surface, are commonly described [9, 12, 13, 14, 15, 16, 17, 18]. Some authors also describe an additional thin high-signal-intensity layer between the deep layer and subchondral bone [10, 19]. These differences in signal intensity reflect regional differences in T2 decay [12, 13, 17, 18]. Specifically, T2 in the transitional layer is longer than in the deep and surface layers. This layering of cartilage, however, is not constant. Not surprisingly, given the influence of T2, we found layering of cartilage altered by changes in the TE [14]. In addition, cartilage shows orientation anisotropy [13, 17, 20, 21]; the appearance of cartilage on MR images will vary as the orientation relative to B₀ changes.

Such observations suggest that the MR appearance of cartilage is determined largely by the structure of the extracellular matrix through its influence on the mobility of water molecules and, therefore, on the T2 decay. Anisotropic arrangement of structural elements within cartilage should explain the observation of T2 anisotropy. Though some studies have asserted that variations in water or proteoglycan content determine layering [8, 22], most studies have argued that it is the regional variation of the orientation of collagen that is reflected in the MR image [9, 12, 13, 14, 20]. This explanation is compelling because three different zones, each characterized by different orientations of collagen fibrils, were described [23]. The radial zone in the deepest region of cartilage consists of radially oriented fibrils. Fibrils are oriented horizontally at the surface. Between the deepest regions and the surface is a transitional zone with randomly oriented fibrils. Studies suggest that regional differences in the orientation of individual collagen fibrils have a dominant influence on water mobility and image contrast [13, 20]. In such a model, radially oriented fibrils in the radial zone and horizontally oriented fibrils at the surface would explain orientation-dependent signal intensity in the deep and surface layers of the MR image. Random orientation of fibrils in the transitional zone would explain persistently high signal intensity and the lack of an observed orientation dependence in the transitional layer.

As compelling as this model is, correlation of MR imaging with collagen fibril orientation has been limited [20]. In fact, we did not observe regional differences in fibril orientation that corresponded to the layers seen on comparative MR images. Moreover, if the layers reflect transitions from an ordered arrangement of fibrils in the histologic, radial, and surface zones to randomness in the transitional zone, changes in orientation relative to B₀ would not be expected to change the dimensions of these layers. In our samples, the thickness of layers was different on images of cartilage obtained at different orientations. Other arguments can be made against the notion that individual fibril orientation is the main determinant of MR layering. Gründer et al. [21] noted that the fraction of water directly interacting with collagen fibrils is relatively small and unlikely to produce the observed effects on image contrast. They and others have suggested instead that matrix proteoglycans held in anisotropic orientation by the collagen network restrict water mobility and determine image contrast by influencing T2 decay [12, 21].

A complex structural organization of collagen and proteoglycans is, in fact, present within hyaline cartilage and is reflected in the curved plane of fracture produced by freeze-fracture sectioning [4, 5, 6, 7]. This three-dimensional organization of the collagen network can explain the appearance of cartilage on MR images. We believe that water mobility in cartilage is restricted by the collagen network, possibly through its influence on the orientation of proteoglycans. This restriction of mobility influences dipole-dipole interaction and provides an explanation for the observed changes in signal intensity and T2. When the surface of cartilage is perpendicular to B₀, the collagen network in the deepest regions of cartilage is aligned parallel with B₀. At this alignment, T2 decay is rapid. Tilting the sample out of plane results in prolongation of T2 decay and an increase in signal intensity within this zone. This effect is maximized at 55°, the magic angle. Just as the magic angle effect causes increased signal intensity in a curving tendon when its orientation relative to B₀ approaches 55°, the orientation of the collagen network would be expected to similarly influence the T2 and signal intensity of cartilage. Low signal intensity in the deep layer of cartilage reflects the radial orientation of the network at that level. The increased signal and prolonged T2 in the transitional layer can be explained by the curvature of the network, and, given the horizontal orientation of the network, we would expect a low-signal-intensity surface. Our results are consistent with this model.

By imaging the samples at 90° relative to B₀, we observed the orientation anisotropy characteristic of cartilage. Signal intensity changed in all layers in a fashion consistent with the magic angle effect. Moreover, the relative thickness of layers also changed when the orientation to B₀ was altered. This observation indicates that a gradual transition between layers occurs, as would be expected, with a curving structure. Such an effect would not be consistent with an abrupt change from an ordered arrangement of collagen fibrils to random orientation suggested as an explanation for MR layers in cartilage.

We were occasionally able to show a fourth thin layer of high signal intensity just above subchondral bone (Fig. 2A). Why this layer was not observed on all images is unclear. This deepest layer may be difficult to identify on our images because the TE was too long for optimal visualization. Although we did not specifically direct the electron microscopy portion of the study to investigate the cause of this layer, we did not identify any potential structural explanation at the bone-cartilage interface. Signal intensity within the deep layer was not uniform, and both horizontal banding and vertical striations were observed. Perhaps regional structural variation in the network, not well visualized in our study, or regional variation in cartilage biochemistry could explain these subtle variations in the three-layered MR appearance. Such a correlation is beyond the scope of this study and is worthy of further investigation.

Though to our knowledge correlation of MR imaging with the structure of the collagen network has not been performed before, earlier work supports our conclusions. The layering of cartilage has been well described and, though other influences on the MR appearance of cartilage, such as magnetization transfer, are present, it is apparent that regional variation in the T2 decay has a dominant influence on these layers [12, 13, 17, 18, 24]. Changes in signal intensity or T2 of cartilage in response to changes in orientation were also reported [12, 13, 17, 20, 21]. A study of T2 heterogeneity in cartilage and the influence of orientation by Xia et al. [13], however, appears to argue against our conclusions. Their inability to show an orientation effect in the transitional layer suggests that no relationship between structure and T2 is present at this level. We believe that the failure to show this expected orientation effect in the transitional layer is simply a reflection of the limitation of imaging techniques. In that study, images were obtained with a resolution of 14 x 14 x 1000 µm. The use of such asymmetric voxel dimensions could easily lead to averaging of T2 and signal intensity across the thickness of the image plane. If the depth of collagen curvature was not exactly the same across the thickness of the voxel, because of either sample positioning or a normal lack of uniformity in the curvature of the structure, imaging would imply randomness in the transitional layer. The influence of different curve orientations at various points across the slice thickness would be averaged. The small in-plane dimensions would actually exacerbate this effect. Plots of T2 versus depth of cartilage, obtained while imaging with the surface perpendicular to B₀ and published in the Xia et al. [13] study, actually support our model. These plots reveal a gradual increase in T2 at more superficial levels of the transitional layer, reaching a peak in the mid portion of the layer and decreasing toward the surface. This curve is exactly what one would predict with our model.

In our study, a certain degree of misregistration was unavoidable and, as a result, our correlation between MR layers and the curvature of the collagen network is somewhat qualitative. On MR images, the layers were not well defined. Though in one sense this lack of definition is a limitation of the study, it actually supports our hypothesis. If, as we believe, the curving collagen network influences T2 decay and signal intensity, poorly defined layers would be expected. Sharply defined layers would argue against the presence of a curving structure influencing image contrast. Sectioning of cartilage by fracture techniques is necessary for showing the collagen network but is also imprecise because the plane of fracture is often irregular. This potential misrepresentation was minimized by cutting a score in the subchondral bone to define both the plane of MR imaging and subsequent fracture sectioning.

In conclusion, the structure of the collagen network within hyaline cartilage, as revealed by electron microscopy after fracture sectioning, has a strong influence on the MR appearance of hyaline cartilage. We believe that the collagen network, possibly indirectly through its influence on proteoglycan orientation, limits water mobility. Curvature of the network produces predictable changes in signal intensity and T2 because of the magic angle effect. A layered appearance is the result. Understanding this relationship between the MR image and the underlying structure of the extracellular matrix of cartilage is of great importance in understanding the clinical image. Because the fibrous structure of cartilage is reflected in the MR image, it is possible to analyze the unique architecture of joint surfaces and to assess tissue integrity. Normal variation in the appearance of cartilage on MR images can be understood in terms of the complex interaction between cartilage structure and orientation relative to B₀ and distinguished from cartilage pathology.

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