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Published online before print October 29, 2004, 10.1148/radiol.2333031921
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(Radiology 2004;233:768-773.)
© RSNA, 2004

Experimental Studies

Cartilage Thickness in Cadaveric Ankles: Measurement with Double-Contrast Multi–Detector Row CT Arthrography versus MR Imaging1

Georges Y. El-Khoury, MD, Kyle J. Alliman, BS, Hannah J. Lundberg, BS, Melvin J. Rudert, PhD, Thomas D. Brown, PhD and Charles L. Saltzman, MD

1 From the Departments of Radiology (G.Y.E.) and Orthopaedics and Rehabilitation (K.J.A., H.J.L., M.J.R., T.D.B., C.L.S.), University of Iowa, Carver College of Medicine, 200 Hawkins Dr, Iowa City, IA 52242. From the 2003 RSNA scientific assembly. Received November 26, 2003; revision requested January 21, 2004; revision received February 12; accepted March 23. Supported by the National Institutes of Health Specialized Center for Research on Osteoarthritis (NIAMS) (award number: 5 P50 AR048939). Address correspondence to G.Y.E. (e-mail: george-el-khoury@uiowa.edu).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To test the accuracy of double-contrast multi–detector row computed tomographic (CT) arthrography for measurement of cartilage thickness in cadaveric ankles and to compare this technique with three-dimensional (3D) fat-suppressed spoiled gradient-echo in the steady state (FS-SPGR) magnetic resonance (MR) imaging.

MATERIALS AND METHODS: Five cadaveric ankles were used. In the ankle specimens, five to nine 1.5-mm-diameter holes were drilled across the joint traversing the tibial subchondral bone, tibial articular cartilage, talar dome cartilage, and talar subchondral bone. The ankle specimens were obtained and used according to institutional policies. Each ankle specimen was imaged first by using 3D FS-SPGR MR imaging with a 1.5-T magnet and then by using double-contrast arthrography followed by CT with a four–detector row scanner (ie, double-contrast multi–detector row CT arthrography). The section thickness used for CT scanning was 1.0 mm reconstructed in 0.5-mm intervals. The MR and CT images obtained in the five specimens were then downloaded to a workstation, where a measurement tool was used to measure the cartilage thickness at each hole. The physical measurement of cartilage thickness at each hole was used as the reference standard with which the MR imaging and CT measurements were compared. Linear regression and correlation analyses were performed by using a statistical computer program.

RESULTS: Double-contrast arthrography followed by multi–detector row CT, as compared with 3D FS-SPGR MR imaging, enabled more accurate measurement of the physical cartilage thickness in the ankle (P < .001).

CONCLUSION: In this study of five cadaveric ankles, multi–detector row CT arthrography was more accurate than 3D FS-SPGR MR imaging for measurement of articular cartilage thickness in the ankle.

© RSNA, 2004

Index terms: Ankle, arthrography, 461.1211, 461.122, 463.1211, 463.122 • Ankle, MR, 461.121412, 461.121415, 463.121412, 463.121415 • Arthritis, degenerative, 461.77, 463.77 • Cartilage, MR, 461.121412, 461.121415, 463.121412, 463.121415


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Recent advances in the treatment of articular cartilage abnormalities have prompted many investigators to explore a variety of imaging techniques for assessing the integrity of cartilage. In the clinical setting, articular cartilage thickness is indirectly evaluated on radiographs (1). Radiography, however, has been shown to be nonsensitive in the evaluation of early osteoarthritis (2). Arthrography and computed tomographic (CT) arthrography can yield more information about the status of the articular cartilage than radiography (3,4). These techniques, however, have been almost completely replaced by magnetic resonance (MR) imaging (5). The advantages of MR imaging include the absence of ionizing radiation, excellent soft-tissue contrast, and direct multiplanar capabilities (6).

The study results of Chan et al (7) showed that MR imaging is more sensitive than radiography and conventional CT (without arthrography) for assessment of the extent and severity of osteoarthritis in the knee. Intermediate- and T2-weighted MR imaging sequences have been shown clinically to perform well in the assessment of cartilage abnormalities (8,9). A variety of other MR imaging sequences also have been evaluated; however, three-dimensional (3D) fat-suppressed spoiled gradient-echo in the steady state (FS-SPGR) is currently accepted as the best sequence for imaging articular cartilage (6,10–16).

The disadvantages of using 3D FS-SPGR MR imaging include long acquisition times, increased magnetic susceptibility, and pronounced metal artifacts. The recent addition of water excitation to the 3D FS-SPGR sequence has effectively reduced the acquisition time by about one half. This sequence is likely to become the preferred method for MR imaging evaluation of articular cartilage. Very short cartilage sequences also are being developed and evaluated, but these are not yet widely available for clinical use (17,18).

With the advent of multi–detector row CT, there have been remarkable advances in musculoskeletal imaging. Multi–detector row CT can be used to acquire isotropic or near-isotropic data sets from which high-spatial-resolution multiplanar reformatted images can be generated. Another advantage of multi–detector row CT is that it enables the acquisition of diagnostic-quality images despite the presence of metal hardware. These capabilities motivated us to try performing double-contrast arthrography followed by multi–detector row CT (ie, double-contrast multi–detector row CT arthrography) in patients with posttraumatic osteoarthritis of the ankle.

The purpose of this study was to test the accuracy of double-contrast multi–detector row CT arthrography for the measurement of cartilage thickness in cadaveric ankles and to compare this technique with 3D FS-SPGR MR imaging.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Specimen Preparation
Five fresh-frozen normal cadaveric ankles from individuals aged 24–89 years at the time of death (mean age at death, 57 years) were resected approximately 5 cm above the ankle joint. Four cadavers were male, and one was female. Two specimens were right ankles, and three were left ankles. The ankle specimens were obtained and used according to institutional policies. An MR imaging–compatible support stand was constructed (by M.J.R., H.J.L.) entirely from acetyl plastic and designed to firmly hold the ankle and foot (Fig 1). To mount the specimen, the heel was fastened into a rectangular block of polymethylmethacrylate.



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  		Figure 1a. Specimen preparation. (a) The foot and ankle are mounted on an MR imaging-compatible support stand, which firmly holds the specimen in place. Arrow points to the drill guide inserted into the medullary space of the distal tibia. (b) Two views of the drill guide: one from above (top) showing nine holes, 1.5 mm in diameter each, and the other (bottom) showing a side view of the drill guide, which is cylindric.

 


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  		Figure 1b. Specimen preparation. (a) The foot and ankle are mounted on an MR imaging-compatible support stand, which firmly holds the specimen in place. Arrow points to the drill guide inserted into the medullary space of the distal tibia. (b) Two views of the drill guide: one from above (top) showing nine holes, 1.5 mm in diameter each, and the other (bottom) showing a side view of the drill guide, which is cylindric.

 
The cancellous bone in the medullary space above the ankle was reamed in preparation for insertion of a cylindric drill guide that was designed for accurate spatial registration of the drill holes (M.J.R., H.J.L.). The drill guide was 23 mm in diameter and 40 mm in length. It contained nine holes arranged in three rows, with each hole measuring 1.5 mm in diameter (Fig 1). The segment of the drill guide that protruded above the tibia was fastened with polymethylmethacrylate to an adjustable cross bar in the support stand that could be adjusted to apply compression or distraction across the ankle joint.

So that perfectly circular holes could be drilled, the tibial and talar articular surfaces were brought into close contact with each other during drilling. This close contact was accomplished by applying downward pressure on the tibia and was maintained by locking the cross bar on the support stand. A 1.5-mm-diameter drill bit powered by a hand drill (model 6626D; Makita, Tokyo, Japan) was introduced into the drill hole (by M.J.R. or H.J.L.), and drilling proceeded with use of saline irrigation while the drill bit was advanced by applying light pressure. Drilling continued until the drill bit crossed the tibial subchondral bone, tibial articular cartilage, talar dome articular cartilage, and talar subchondral bone. The drill stop was adjusted to limit penetration of the drill bit to approximately 1 cm into the talus.

Drilling was repeated for each of the remaining holes in the guide. After the drilling was concluded, the cross bar was released and the articular surfaces were distracted about 2.0 mm so that contrast material and air could be introduced for arthrography. Finally, the drill holes in the guide were plugged (by M.J.R. or H.J.L.) to maintain an airtight joint.

Imaging
The specimen, while fixed in the support stand, was placed in a quadrature transmit-receive coil and imaged by using a 1.5-T magnet (Signa System 5.4; GE Medical Systems, Milwaukee, Wis). The long axis of the foot was aligned parallel to the long axis of the magnet. A 3D FS-SPGR MR sequence was used to image the ankle in the coronal plane. The imaging parameters were those used in our clinical practice to evaluate articular cartilage: 52/10 (repetition time msec/echo time msec), a flip angle of 30°, a field of view of 12 cm, a section thickness of 1.5 mm, a matrix of 256 x 192, and 60 partitions. The imaging time was 12 minutes.

The ankle specimens were taken to a fluoroscopic suite, where the joints were injected, with fluoroscopic guidance, with about 0.7 mL of diatrizoate meglumine (Hypaque Meglumine 60%; Amersham Health, Princeton, NJ) followed by about 8 mL of room air. The radiologist (G.Y.E.) who performed the arthrographic examinations had 30 years experience performing arthrography. The specimens were then transferred to a CT unit, where they were scanned in the coronal plane (with the x-ray beam perpendicular to the long axis of the talus) by using a four–detector row CT scanner (Aquilion; Toshiba American Medical Systems, Tustin, Calif). Scanning parameters included 120 kVp, 75 mAs, 0.5-second gantry rotation, 3.5-mm table travel per rotation, 1-mm section thickness, and a 512 x 512 matrix with in-plane pixel dimensions of 0.3 x 0.3 mm. The images were reconstructed in 0.5-mm intervals.

Physical Measurement of Articular Cartilage Thickness
Each specimen was then removed from the support stand, and the ankle joint was disarticulated to expose the tibial and talar articular surfaces (Fig 2) (M.J.R., H.J.L.). A 5.3-mm modified trephine (Stryker Instruments, Kalamazoo, Mich) was used to harvest an osteochondral plug around each hole for physical measurements of articular cartilage thickness. The plug was harvested by introducing a central post 1.5 mm in diameter into the hole to guide the trephine and cut parallel to the hole. With saline irrigation, the trephine was used to cut a 5.3-mm-diameter core of articular cartilage, subchondral bone, and cancellous bone (Fig 2). In three ankles nine holes were drilled, but in two ankles, because of their small size and technical difficulties, we could only drill five holes in one ankle and six holes in the other. From all five ankles, a total of 76 cores were harvested from the tibial and talar sides.



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  		Figure 2. Harvesting a core of cartilage and bone around each drill hole. A, A disarticulated talar dome viewed from above has nine drill holes, 1.5 mm in diameter each. B, The same talar dome viewed from above after nine cores of cartilage and bone have been harvested. C, A harvested core of cartilage viewed from the side.

 
The cores were then bisected longitudinally, and the articular cartilage thickness was measured under a microscope (model 92718; Nikon, Tokyo, Japan) (Fig 3). Each core slice was mounted on a microscope stage, and an optical measuring grid was placed in the field of view at the same level as the cut surface of the slice. After the microscope lens was focused on the flat surface of the plug with the optical grid along the long axis of the plug, a digital image of the microscopic field was acquired at a magnification of x40. The image was downloaded to a computer (Dell Dimension 8200 PC; Dell, Round Rock, Tex), and the grid lines were used to calibrate the measurement tool in an Adobe Photoshop 7.0 program (Adobe Systems, San Jose, Calif). After calibration, the Adobe Photoshop measuring tool was then used to measure the cartilage thickness in each section.



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  		Figure 3. Bisected core shows cartilage at the top and bone at the bottom. Arrows point to the interphase between the articular cartilage and the subchondral bone.

 
An independent observer (K.J.A.) performed the cartilage measurements to the nearest 0.1 mm. Two measurements, one from each side of each hole, were taken, and these measurements were averaged (by K.J.A.) to yield a single value for the cartilage thickness at each of the 76 holes. The physical measurements, which served as the reference standards, were obtained a few days after the MR imaging and CT cartilage thickness measurements were performed.

MR Imaging and CT Measurements of Articular Cartilage Thickness
The MR and multi–detector row CT images obtained in the five ankle specimens were downloaded to an image processing workstation (Vitrea 3.1; Vital Images, Plymouth, Minn). The window width and window level for the images were standardized and set to equal the settings used in our clinical practice. Coronal images through the drill holes were displayed for measurement of the cartilage thickness. The measuring tool on the workstation was used to measure the cartilage thickness on both sides of the drill hole (Fig 4). The two measurements from each side of the hole were averaged (by K.J.A.) to yield a single thickness value for each drill hole. The MR imaging and CT measurements in each ankle were obtained during the same session but a few days before the physical measurements were obtained.



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  		Figure 4a. Coronal MR and CT images downloaded to the workstation in preparation for measurement of the cartilage thickness at each drill hole. (a) Three-dimensional FS-SPGR MR image (52/10, 30° flip angle, 12-cm field of view, 1.5-mm section thickness) obtained through the talar dome. (b) Reformatted coronal CT image obtained through the talar dome during measurement of the articular cartilage thickness with use of the measurement tool on the workstation.

 


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  		Figure 4b. Coronal MR and CT images downloaded to the workstation in preparation for measurement of the cartilage thickness at each drill hole. (a) Three-dimensional FS-SPGR MR image (52/10, 30° flip angle, 12-cm field of view, 1.5-mm section thickness) obtained through the talar dome. (b) Reformatted coronal CT image obtained through the talar dome during measurement of the articular cartilage thickness with use of the measurement tool on the workstation.

 
Statistical Analyses
Linear regression and correlation analyses were used to examine the relationships between measurements obtained with double-contrast arthrography followed by multi–detector row CT and physical measurements and between 3D FS-SPGR MR imaging measurements and physical measurements. Linear regression and correlation analyses were performed by using the biomedical program 6D (BMDP statistical software manual, volume 2 [to accompany release 7]; Dixon WJ, University of California, Berkeley, Calif).

A test for differences between dependent correlations was used to determine whether the correlation between thickness measured at multi–detector row CT and thickness at physical measurement was different from the correlation between MR imaging–measured thickness and physical thickness (19).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
Figure 5 is a scatterplot of the physical measurements as a function of the multi–detector row CT measurements of cartilage thickness at all sites in all five ankles (76 holes). The line of best fit constructed at regression analysis and the regression equation that describes that line also are shown. The closer the points are to the line of best fit, the more closely the physical measurement can be predicted on the basis of the multi–detector row CT measurements. This relationship is formally expressed by the R2 value, which is the proportion of variance in physical thickness accounted for by the multi–detector row CT–measured thickness. A related statistic, the Pearson product moment correlation coefficient, R, can be used to test the statistical significance of this relationship. The multi–detector row CT measurements were significantly correlated with the physical measurements (R = 0.91, P < .001).



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  		Figure 5. Scatterplot of physical measurements of cartilage thickness plotted against multi-detector row CT (MDCT) measurements of cartilage thickness at 76 holes. The line of best fit constructed at regression analysis and the corresponding regression equation also are shown. The R2 value of 0.81 is sufficiently high, and this indicates that the multi-detector row CT measurements are good predictors of the actual cartilage thickness values. (When the intercept equals 0 and the R2 value equals 1, the relationship between one measurement and the other measurement is perfect.) For plotting purposes and to prevent identical points from being superimposed, all points were modified by randomly adding selected values between –0.05 and +0.05.

 
Figure 6 is a scatterplot of the physical measurements as a function of the MR imaging measurements at all sites in all five ankles (76 holes). Again, the line of best fit and the corresponding regression equation are presented. On this scatterplot (Fig 6), the points are not as close to the line of best fit. Therefore, the prediction of the physical thickness based on the MR imaging–measured thickness is not as accurate as the prediction of the physical thickness based on the multi–detector row CT measurements. Note that the R2 value for this relationship is smaller than that for the CT measurement–physical measurement relationship. The correlation between MR imaging measurements and physical measurements was statistically significant (R = 0.70, P < .001). However, the test for differences between dependent correlations revealed a significantly higher correlation between multi–detector row CT–measured thickness and physical thickness than between MR imaging–measured thickness and physical thickness (t = 4.99, df = 73; P < .001).



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  		Figure 6. Scatterplot of physical measurements of cartilage thickness plotted against MR imaging measurements of cartilage thickness at 76 holes. The line of best fit and the corresponding regression equation also are shown. With an R2 value of 0.49, the results suggest that MR imaging is not as accurate as multi-detector row CT for predicting actual cartilage thickness. For plotting purposes and to prevent identical points from being superimposed, all points were modified by randomly adding selected values between –0.05 and +0.05.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
REFERENCES
 
The results of this study show that double-contrast arthrography followed by multi–detector row CT is an accurate method for measuring cartilage thickness in the ankle. We also found this technique to be better than 3D FS-SPGR MR imaging for assessment of cartilage thickness. The better performance of CT arthrography is attributed to the high spatial resolution and high temporal resolution, which were not possible with earlier CT scanners, achieved with multi–detector row CT. Because of the isotropic or near-isotropic data sets obtained with multi–detector row CT, the acquired multiplanar reformatted images have a spatial resolution that is almost equivalent to the spatial resolution of the in-plane images (20). With use of 16–detector row CT scanners, isotropic imaging probably will soon become the standard examination for data acquisition without the added penalty in radiation dose to the patient.

Double-contrast arthrography followed by multi–detector row CT is more invasive than MR imaging, but the invasiveness is compensated for by the added advantages of fast imaging times and high accuracy. In a previous study, Daenen et al (21) found arthrography followed by conventional CT to be superior to 3D fat-suppressed fast low-angle shot MR imaging—which is very similar to 3D FS-SPGR MR imaging—in depicting patellar cartilage surface abnormalities.

The majority of cartilage imaging studies have focused on the knee, especially the patellofemoral joint, where the articular surfaces do not fit tightly and the cartilage in the patella is thicker than that in any other joint. Only a limited number of studies have addressed cartilage abnormalities in the shoulder, hip, and ankle (22–27). Articular cartilage in the ankle is particularly difficult to study, whether with MR imaging or with CT arthrography (23). The talar dome fits tightly and completely within the mortise, leaving hardly any space between the articular surfaces, and the cartilage of the distal tibia and talar dome is relatively thin, measuring 0.4–2.1 mm, as compared with the cartilage of the patella, which is two to three times thicker (28,29). For patients undergoing multi–detector row CT arthrography of the ankle, we apply traction to the lower extremity to distract the articular surfaces.

A literature search yielded one MR imaging study focused on assessment of the articular cartilage thickness in the ankle (23), and in another study (27), CT arthrography was compared with MR arthrography for depicting focal cartilage lesions. Measuring cartilage thickness in the ankle with any imaging technique is challenging, and, to our knowledge, the use of multi–detector row CT arthrography for assessing cartilage thickness in the ankle had not been validated before the present study.

Conventional CT arthrography has been used intermittently to study articular cartilage for more than 21/2 decades (3,4,30–32). Impediments to the widespread use of this technique have been the long scanning times, which result in misregistration artifacts, and the relatively thick sections, which are unsuitable for the creation of high-spatial-resolution multiplanar images.

In the late 1970s, Horns (30) described the use of double-contrast arthrography for evaluation of the patellar articular surface. In 1982, Boven et al (3,4) introduced the use of double-contrast arthrography followed by conventional CT to study chondromalacia of the patella, and they were able to detect more cartilage lesions than they did with arthrography alone. Ihara (31) reported 97.1% sensitivity for the detection of fissures and fibrillation in the patellar cartilage with use this technique. Gagliardi et al (32) compared a variety of MR imaging sequences with MR arthrography and double-contrast CT arthrography for the detection of patellar lesions, with arthroscopy as the reference standard. They found that MR arthrography and double-contrast CT arthrography were more sensitive than T1-weighted, intermediate-weighted, and FS-SPGR MR imaging sequences in depicting intermediate grades of chondromalacia of the patella.

CT arthrography has continued to yield promising results; however, its clinical use in recent years has been limited because of its invasive nature and inability to generate high-spatial-resolution multiplanar reformatted images. Technologic advances in MR imaging eventually made it the dominant imaging technique for the evaluation of articular cartilage. Recent developments in CT technology led to the advent of multi–detector row CT, which yields isotropic or near-isotropic data sets. This capability results in high spatial resolution in all directions. To our knowledge, before the current study multi–detector row CT had not been used to assess cartilage thickness in the ankle.

In 2001, Vande Berg et al (33) used single-contrast arthrography followed by dual–detector row CT, the predecessor of multi–detector row CT, to study degenerative cartilage lesions in cadaveric knees and compared this technique with an intermediate-weighted MR imaging sequence. They found that in the detection of grade 2A lesions, grade 2B lesions, and lesions of higher grades (Noyes classification), CT performed slightly better than MR imaging. They attributed this to the multiplanar capability of dual–detector row CT and the improved spatial resolution, which exceeds the spatial resolution achieved with MR imaging. In a more recent study to compare the accuracy of MR arthrography with that of single-contrast single–detector row CT arthrography in the evaluation of focal cartilage lesions of the ankle, CT arthrography was also found to be more reliable than MR arthrography (27).

One minor drawback in our study was related to the fact that cartilage cores can show minimal changes in shape and dimension after they are harvested. Harvesting a cylindric cartilage core causes the release of residual mechanical stresses that existed when the cartilage core was part of a continuous articular surface (34). The tendency of the core to undergo dimensional and shape changes can contribute to a small disparity—usually of 5% or less—between the preharvest thickness measured at imaging and the postharvest physical thickness measurement. However, multi–detector row CT measurements and MR imaging measurements are affected similarly by these changes. We view this phenomenon more as a source of "noise" in the system rather than as a major systematic error.

In conclusion, our goal was to compare double-contrast arthrography followed by multi–detector row CT (with four detector rows) with a 3D FS-SPGR MR imaging sequence for the measurement of cartilage thickness in the ankle. In this cadaver study, multi–detector row CT arthrography was found to be more accurate than MR imaging for the measurement of ankle cartilage thickness.

Practical applications: Although multi–detector row CT arthrography of the ankle is more invasive, clinically, it may be particularly useful in patients with osteoarthritis, the underlying cause of which is posttraumatic in most cases. Such patients often either have or have had metal fixation devices in the vicinity of the ankle. An advantage of using multi–detector row CT arthrography rather than gradient-echo MR imaging sequences designed for cartilage imaging is that multi–detector row CT arthrography is capable of generating high-quality images despite the presence of metal. In a small subset of patients, MR imaging is contraindicated because of the presence of a pacemaker, a cochlear implant, certain types of aneurysm clips, or metal shrapnel in the orbit, and in such cases, multi–detector row CT arthrography can be an excellent substitute.


   ACKNOWLEDGMENTS
 
The authors thank Kevin S. Berbaum, PhD, and Stephen L. Hillis, PhD, for help with the statistical analyses; Thomas D. Baer, BA, and Douglas R. Pedersen, PhD, for help with graphics; and James A. Martin, PhD, for help with the physical measurements. We also thank Mary McBride for her secretarial help.


   FOOTNOTES
 
Abbreviations: FS-SPGR = fat-suppressed spoiled gradient echo in the steady state, 3D = three-dimensional

Authors stated no financial relationship to disclose.

Author contributions: Guarantors of integrity of entire study, G.Y.E., M.J.R., T.D.B., C.L.S.; study concepts and design, G.Y.E., C.L.S., M.J.R., T.D.B.; literature research, G.Y.E., M.J.R.; experimental studies, G.Y.E., M.J.R., H.J.L.; data acquisition, G.Y.E., K.J.A.; data analysis/interpretation, G.Y.E., K.J.A., H.J.L.; statistical analysis, G.Y.E., M.J.R., T.D.B., C.L.S.; manuscript preparation, definition of intellectual content, revision/review, and final version approval, G.Y.E., M.J.R., T.D.B., C.L.S.; manuscript editing, M.J.R., T.D.B., C.L.S.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 

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