Articular cartilage grading of the knee: diagnostic performance of fat-suppressed 3D volume isotropic turbo spin-echo acquisition (VISTA) compared with 3D T1 high-resolution isovolumetric examination (THRIVE)

Abstract

Background

Conventionally, two-dimensional (2D) fast spin-echo (FSE) sequences have been widely used for clinical cartilage imaging as well as gradient (GRE) sequences. Recently, three-dimensional (3D) volumetric magnetic resonance imaging (MRI) has been introduced with one 3D volumetric scan, and this is replacing slice-by-slice 2D MR scans.

Purpose

To evaluate the image quality and diagnostic performance of two 3D sequences for abnormalities of knee cartilage: fat-suppressed (FS) FSE-based 3D volume isotropic turbo spin-echo acquisition (VISTA) and GRE-based 3D T1 high-resolution isovolumetric examination (THRIVE).

Material and Methods

The institutional review board approved the protocol of this retrospective review. This study enrolled 40 patients (41 knees) with arthroscopically confirmed abnormalities of cartilage. All patients underwent isovoxel 3D-VISTA and 3D-THRIVE MR sequences on 3T MRI. We assessed the cartilage grade on the two 3D sequences using arthroscopy as a gold standard. Inter-observer agreement for each technique was evaluated with the intraclass correlation coefficient (ICC). Differences in the area under the curve (AUC) were compared between the 3D-THRIVE and 3D-VISTA.

Results

Although inter-observer agreement for both sequences was excellent, the inter-observer agreement for 3D-VISTA was higher than for 3D-THRIVE for cartilage grading in all regions of the knee. There was no significant difference in the diagnostic performance (P > 0.05) between the two sequences for detecting cartilage grade.

Conclusion

FSE-based 3D-VISTA images had good diagnostic performance that was comparable to GRE-based 3D-THRIVE images in the evaluation of knee cartilage, and can be used in routine knee MR protocols for the evaluation of cartilage.

Keywords

Knee magnetic resonance imaging (MRI)cartilage three-dimensional (3D) MRI

Introduction

The use of magnetic resonance imaging (MRI) for cartilage evaluation of the knee is clinically and radiologically important for patients with knee pain. Traditionally, two-dimensional (2D) intermediate-weighted and T2-weighted (T2W) fast spin-echo (FSE) sequences have been widely used for clinical cartilage imaging (1 –3). Although these standard clinical MRI sequences have good diagnostic performance, they also have relatively large slice thicknesses and interslice gaps, which can lead to partial volume artifacts.

Recently, three-dimensional (3D) volumetric MR images have been introduced with thin continuous slices, and they are replacing slice-by-slice 2D MR scans with one 3D volumetric scan. These 3D MR images are acquired with isotropic imaging which is becoming a routine sequence: Different isotropic imaging sequences exist, including volume isotropic turbo spin-echo acquisition (VISTA®, Philips Healthcare), sampling perfection with application-optimized contrasts using different flip angle evolution (SPACE®, Siemens Healthcare), and Cube® (GE Healthcare). Studies on 3D isovoxel images suggest that isovoxel 3D MR sequences could replace conventional 2D FSE images (4 –6).

In clinical practice, routine knee MR sequences combine FSE- and GRE-based 3D T1-weighted (T1W)/proton density (PD)-weighted MR sequences, including 3D FSE sequences, such as VISTA, SPACE, and Cube; and 3D GRE sequences, such as T1 high-resolution isovolumetric examination (THRIVE), Volume Interpolated Breathhold Examination (VIBE), and 3D fast spoiled gradient-echo sequence (FSPGR); however, different 3D sequences may differ in cartilage visualization. Few studies have compared the different sequences for 3D imaging of knee cartilage at 3.0T MR.

To our knowledge, a comparison of the performance of 3D-VISTA with that of 3D-THRIVE in the evaluation of cartilage has not been performed with an arthroscopic reference. The purpose of this study was to evaluate the image quality and diagnostic performance of two 3D sequences for cartilage grading compared with arthroscopic findings: fat-suppressed (FS) 3D-VISTA and 3D-THRIVE.

Material and Methods

Patient population

From November 2010 to August 2011, a total of 646 symptomatic patients underwent both 3D-THRIVE and fat-suppressed isovolumetric 3D-VISTA imaging; 117 of these patients were excluded due to a history of knee surgery. Of the remaining 529 patients, 40 underwent arthroscopic surgery after MRI examination. All arthroscopic knee surgeries were performed by a single orthopedic surgeon with 7 years of clinical experience. The retrospective study protocol was approved by the institutional review board at our institution.

MR protocol

All MRI examinations were performed on a 3T MR system (Achieva®, Philips Healthcare, Best, The Netherlands) with a dedicated 8-channel SENSE knee coil (Philips knee coil, Philips Healthcare). Patients were in the supine position with the knee slightly flexed. Post-contrast 3D-THRIVE MR images were taken after intravenously injecting gadoterate meglumine (Dotarem®, Guerbet, Roissy CdG Cedex, France) by hand injection (0.2 mL/kg/body weight). Details of the MR protocol are summarized in Table 1.

Table 1.

Parameters for MRI sequences.

Parameter	3D THRIVE	3D VISTA
Repetition time (ms)	7.7	1400
Echo time (ms)	3.8	32
Matrix size (cm)	256 × 256	320 × 320
FOV (cm)	14	16
Section thickness (mm)	1.5	0.5
Slice gap (mm)	0	0
Flip angle (°)	6	Variable (30–120)
ETL		63
NEX	1	1
Imaging time	3 min 40 s	7 min 5 s

ETL, echo train length; FOV, field of view; NEX, number of excitations, THRIVE, T1 high-resolution isovolumetric examination; VISTA, volume isotropic turbo spin echo acquisition.

Quantitative analyses of SNR and CNR

Typical regions of interest (ROIs) included more than 20 pixels for each tissue with a grossly normal structure. These ROIs were evaluated independently by two fellowship-trained musculoskeletal radiologists, one with 7 years of clinical experience and one with 1 year. The ROIs were drawn on an image of the center of each compartment of knee (medial femoral condyle, lateral femoral condyle, medial tibial plateau, lateral tibial plateau, patellar facet, and femoral trochlea), the synovial fluid, and the background. The drawings of the ROIs of the background were done at a distance of 1 cm from the prepatellar region to avoid a standard deviation of 0 resulting from image mask.

For quantitative assessment, the signal-to-noise ratio (SNR) and contrast-to-noise ratio (CNR) were calculated from the ROIs. The SNR of knee cartilage was calculated as the ratio of the mean signal intensity inside the cartilage to the standard deviation of the signal intensity in the background. The CNRs for synovial fluid were calculated as the difference in signal intensity between the cartilage and synovial fluid divided by the background noise. The average values SNR and CNR were used for comparison statistics.

Qualitative analyses of cartilage grading

Two fellowship-trained musculoskeletal radiologists, one with 7 years of clinical experience and one with 4 years, independently performed all cartilage grading of the MR images. The radiologists were blinded to the arthroscopic findings. Knee cartilage surfaces were divided into six regions: the medial femoral condyle, lateral femoral condyle, medial tibial plateau, lateral tibial plateau, femoral trochlea, and patellar facet.

We analyzed the cartilage with the two sequences. During the first review of the MR examinations, the radiologists used the 3D-THRIVE sequence in routine MR to grade each of the six articular surfaces of the knee joint using the Outerbridge classification system (7,8). We defined the cartilage grade: Grade 0, intact cartilage; grade 1, signal change on T2W MR images; grade 2, cartilage defect less than 50% of the depth; grade 3, cartilage defect 50% or more of the depth; and grade 4, full-thickness cartilage defect with exposure of subchondral bone. During the second review, the analyses of 3D-VISTA sequences were repeated with a 2-week interval between repeated analyses. When multiple cartilage lesions were present, the cartilage lesion with the highest grade was recorded.

Arthroscopic cartilage grading

The 40 patients underwent arthroscopic knee surgery within 6 months (range, 1–136 days; mean ± standard deviation, 37.4 ± 34.9 days) for a total of 41 knee arthroscopies. All arthroscopic knee surgeries were performed by a single orthopedic surgeon specializing in knee arthroscopy with 7 years of clinical experience.

The orthopedic surgeon graded each of the six articular surfaces of the knee joint during arthroscopy using the Noyes classification system (grade 0, normal; grade 1, cartilage softening; grade 2A, superficial partial-thickness cartilage lesion less than 50% of the total thickness of the articular surface; grade 2B, deep partial-thickness cartilage lesion greater than 50% of the total thickness of the articular surface; and grade 3, full-thickness cartilage lesion) (9). When multiple cartilage lesions were present, the cartilage lesion with the highest grade was recorded. For comparison with the Outerbridge classification-based MR grades of cartilage, we transformed the Noyes classification-based grade to the Outerbridge classification from the operation note and arthroscopic findings (7,8).

Statistical analysis

Paired t-tests were used to compare SNR and CNR between the two sequences. Inter-observer agreements for SNR/CNR and each technique were evaluated with the intraclass correlation coefficient (ICC). The cutoff point between normal and abnormal cartilage was set between grades 0 and 1. The sensitivity and specificity in each region of cartilage were calculated for both sequences. Differences in the area under the curve (AUC) were compared between the two sequences. All statistical analyses were performed in the R programming environment (R package version 2.3.1, R Foundation of Statistical Imaging, Vienna, Austria; http://cran.r-project.org). P values < 0.05 were considered statistically significant.

Results

This study included 40 patients (41 knee MR images) with a mean age of 47.1 years (range, 22–72 years). There were 22 men and 18 women. Of the 41 knee images, six compartments of the medial/lateral femoral condyle, medial/lateral tibial plateau, femoral trochlea, and patellar facet were included in the analysis. The distribution of arthroscopic cartilage grades is summarized in Table 2. The MR grades for cartilage compared to the arthroscopy grades are summarized in Table 3. Both over- and undergrading occurred more often with 3D-THRIVE than with 3D-VISTA.

Table 2.

Distribution of cartilage grades at arthroscopy.

Region	0	1	2	3	4
MFC	18 (43.9%)	3 (7.3%)	0 (0%)	12 (29.3%)	8 (19.5 %)
LFC	34 (82.9%)	0 (0%)	1 (2.4%)	6 (14.6%)	0 (0%)
TRO	21 (51.2%)	1 (2.4%)	3 (7.3%)	13 (31.7%)	3 (7.3%)
PAT	19 (46.3%)	0 (0%)	5 (12.2%)	14 (34.1%)	3 (7.3%)
MTP	29 (70.7%)	2 (4.9%)	2 (4.9%)	2 (4.9%)	6 (14.6%)
LTP	27 (65.9%)	1 (2.4%)	5 (12.2%)	8 (19.5%)	0 (0%)
Total	148	7	16	55	20

LFC, lateral femoral condyle; LTP, lateral tibial plateau; MFC, medial femoral condyle; MTP, medial tibial plateau; PAT, patellar facet; TRO, femoral trochlea.

Table 3.

MR grading of cartilage compared to arthroscopy: 3D-THRIVE (A) and 3D-VISTA (B).

	Arthroscopy
	Grade 0	Grade 1	Grade 2	Grade 3	Grade 4	Total
(A) 3D-THRIVE versus Arthroscopy
3D-THRIVE
Grade 0	137*	3	6	5	0	151
Grade 1	4	1*	1	2	0	8
Grade 2	6	2	6*	11	3	28
Grade 3	1	1	3	34*	4	43
Grade 4	0	0	0	3	13*	16
Total	148	7	16	55	20	246
(B) 3D-VISTA versus Arthroscopy
3D-VISTA
Grade 0	140*	4	4	4	0	152
Grade 1	1	0*	0	0	0	1
Grade 2	5	3	7*	2	0	17
Grade 3	2	0	5	48*	1	56
Grade 4	0	0	0	1	19*	20
Total	148	7	16	55	20	246

The numbers on the diagonal are the numbers of identical grading between MRI and arthroscopy, on the right of the diagonal are the numbers of undergraded interpretations, whereas on the left of the diagonal are the numbers of overgraded interpretations.

THRIVE, T1 high-resolution isovolumetric examination; VISTA, volume isotropic turbo spin echo acquisition.

In all six compartments of medial femoral condyle, lateral femoral condyle, medial tibial plateau, lateral tibial plateau, patellar facet, and femoral trochlea, the SNR for cartilage was significantly higher in 3D-THRIVE than that in 3D-VISTA (3D-THRIVE vs. 3D-VISTA; 118.0 vs. 201.1; 138.9 vs. 211.1; 109.5 vs. 193.3; 125.5 vs. 203.5; 139.0 vs. 206.6; 178.8 vs. 220.7; P < 0.05). However, the CNR of the cartilage-synovial fluid was significantly higher in 3D-VISTA than that in 3D-THRIVE (3D-VISTA vs. 3D-THRIVE; 170.9 vs. 61.1; 150.1 vs. 68.8; 179.5 vs. 61.2; 163.5 vs. 62.6; 150.0 vs. 64.3; 110.7 vs. 78.1; P < 0.05).

Although inter-observer agreement for both sequences was excellent, the inter-observer agreement for 3D-VISTA (ICC, 0.98; 95% confidence interval [CI], 0.979–0.988) was slightly higher than that for 3D-THRIVE (ICC, 0.97; 95% CI, 0.963–0.978) for cartilage grading in all regions of the knee. Detailed inter-observer agreements for each region are summarized in Table 4.

Table 4.

Inter-observer agreement of intraclass correlation (ICC) values at each cartilage surface of knee.

Region	3D-THRIVE	3D-VISTA
MFC	0.971 (0.946–0.985)	0.9579 (0.921–0.978)
LFC	0.916 (0.843–0.955)	0.9580 (0.921–0.978)
TRO	0.958 (0.922–0.978)	0.9870 (0.976–0.993)
PAT	0.899 (0.811–0.946)	0.9294 (0.868–0.962)
MTP	0.930 (0.868–0.964)	0.9921 (0.985–0.996)
LTP	0.696 (0.429–0.838)	0.7845 (0.596–0.885)

Data are means, with 95% confidence intervals in parentheses.

ICC, intraclass correlation; LFC, lateral femoral condyle; LTP, lateral tibial plateau; MFC, medial femoral condyle; MTP, medial tibial plateau; PAT, patellar facet; THRIVE, T1 high-resolution isovolumetric examination; TRO, femoral trochlea; VISTA, volume isotropic turbo spin echo acquisition.

Both 3D-THRIVE and 3D-VISTA showed high sensitivity and specificity in each region, except for the lateral tibial plateau (Figs. 1 –3, Table 5). The two sequences did not differ significantly in diagnostic performance for the detection of cartilage grade (P > 0.05; Tables 6 and 7).

Fig. 1.

A 61-year-old woman with grade 4 cartilage defect of the medial femoral condyle. The cartilage defect was visible on both T1 high-resolution isovolumetric examination (THRIVE) and volume isotropic turbo spin-echo acquisition (VISTA) images. (a) The contrast-enhanced THRIVE image showing a full-thickness cartilage defect and adjacent synovial enhancement (arrow). Corresponding subchondral bone signal change was also present. (b) The VISTA image at the same level also demonstrates a full-thickness cartilage defect (arrow). (c) Arthroscopic surgery showed a full-thickness cartilage lesion of the medial femoral condyle.

Table 5.

Sensitivity and specificity of 3D-THRIVE and 3D-VISTA of each region.

	3D-THRIVE vs. Arthroscopy		3D-VISTA vs. Arthroscopy
Region	Sensitivity	Specificity	Sensitivity	Specificity
MFC	95.0/100/95.0	95.2/95.2/95.2	95.2/95.0/95.0	90.5/85.7/85.7
LFC	100/100/100	88.2/88.2/91.2	100/100/100	94.1/91.2/94.1
TRO	94.7/94.7/89.5	90.9/90.9/90.9	94.7/94.7/94.7	95.5/95.5/95.5
PAT	95.2/95.2/90.5	89.5/78.9/84.2	95.2/95.2/95.2	84.2/84.2/89.5
MTP	90.0/90.0/90.0	96.8/93.5/100	100/100/88.9	96.8/96.8/100
LTP	46.2/38.5/38.5	96.4/92.9/96.4	61.5/69.2/61.5	89.3/85.7/89.3

The cell format is review1/review 2/overall.

LFC, lateral femoral condyle; LTP, lateral tibial plateau; MFC, medial femoral condyle; MTP, medial tibial plateau; PAT, patellar facet; THRIVE, T1 high-resolution isovolumetric examination; TRO, femoral trochlea; VISTA, volume isotropic turbo spin echo acquisition.

Table 6.

Comparison of AUC of 3D-THRIVE and 3D-VISTA.

Region	3D-THRIVE vs. Arthroscopy	3D-VISTA vs. Arthroscopy	P value
MFC	0.951 (0.835–0.994)	0.927 (0.801–0.985)	0.583
LFC	0.956 (0.841–0.995)	0.971 (0.864–0.999)	0.317
TRO	0.902 (0.768–0.972)	0.951 (0.834–0.994)	0.158
PAT	0.873 (0.730–0.957)	0.924 (0.794–0.984)	0.158
MTP	0.950 (0.833–0.994)	0.950 (0.833–0.994)	1.0
LTP	0.674 (0.510–0.812)	0.754 (0.595–0.875)	0.225

Data are means, with 95% confidence intervals in parentheses.

LFC, lateral femoral condyle; LTP, lateral tibial plateau; MFC, medial femoral condyle; MTP, medial tibial plateau; PAT, patellar facet; ROC, receiver operating characteristic; THRIVE, T1 high-resolution isovolumetric examination; TRO, femoral trochlea; VISTA, volume isotropic turbo spin echo acquisition.

Table 7.

Correlation between cartilage grading and the arthroscopic grades.

	3D-THRIVE vs. Arthroscopy		3D-VISTA vs. Arthroscopy
Region	Correlation coefficients	P value	Correlation coefficients	P value
MFC	0.954 (0.896–0.971)	<0.05	0.919 (0.853–0.957)	<0.05
LFC	0.845 (0.727–0.915)	<0.05	0.922 (0.857–0.958)	<0.05
TRO	0.921 (0.856–0.899)	<0.05	0.974 (0.952–0.986)	<0.05
PAT	0.817 (0.793–0.937)	<0.05	0.868 (0.765–0.928)	<0.05
MTP	0.885 (0.793–0.937)	<0.05	0.985 (0.971–0.992)	<0.05
LTP	0.459 (0.177–0.672)	0.003	0.534 (0.271–0.723)	0.003

Data are means, with 95% confidence intervals in parentheses.

Discussion

Cartilage evaluation of the knee is clinically important in patients with knee pain. Cartilage loss can cause knee pain, although the mechanisms involved in this process are not well understood (10,11). Promising cartilage treatments have been targeting patients with cartilage defects and the need to detect cartilage defects is increasing (12,13). MRI is a choice of diagnostic modality to evaluate articular cartilage because of its high spatial resolution and soft tissue contrast (14 –16). Recent studies have focused on the 3D MRI sequences for evaluating the knee cartilage (6,17 –20). Many studies have shown that 3D MR sequences have high sensitivity and specificity for detecting cartilage damage of the knee joint (10,20 –26), and cartilage evaluation with 3D MR sequences is promising (19,20,27). In volumetric evaluation for cartilage, the 3D sequences are useful: GRE-based 3D sequences, including 3D-THRIVE, 3D-VIBE, and 3D-FSPGR and FSE-based 3D sequences, including 3D-VISTA, 3D-SPACE, and 3D-CUBE. These sequences may differ somewhat in cartilage visualization. However, there are few reports on comparison of GRE-based 3D sequence and FSE-based 3D sequence in MRI evaluation of cartilage. Therefore, we compared the GRE-based 3D-THRIVE sequence of dark fluid and the FSE-based 3D-VISTA sequence of bright fluid.

In our assessment of six compartments of the knee, the CNR of cartilage-synovial fluid was significantly higher in 3D-VISTA than in in 3D-THRIVE, while the SNR of cartilage was higher in 3D-THRIVE than in 3D-VISTA. However, the diagnostic performance of 3D-THRIVE and 3D-VISTA was not significantly different despite the CNR differences. The CNR differences resulted from the signal intensity differences between the gradient-echo images and spin-echo images. We suggest that visualization of the cartilage and detection of cartilage defect can be accomplished with 3D-THRIVE or 3D-VISTA sequences (Fig. 1). Although diagnostic performance did not differ between the two sequences, in some cases, the cartilage defects were not clearly visualized on the 3D-THRIVE images, but were clearly visualized on the 3D-VISTA images (Fig. 2). This could have occurred due to the difference of FSE and GRE images.

Fig. 2.

A 47-year-old woman with grade 4 cartilage defect of the medial femoral condyle, demonstrating a discrepancy between the THRIVE and VISTA images. (a) The contrast-enhanced THRIVE image showing a signal change suggestive of a cartilage defect (arrow). The extent of the defect could not be clearly seen on the THRIVE image. (b) A VISTA image at the same level also demonstrates a clear cartilage defect to the level of the subchondral bone with high signal intensity (arrow). The adjacent cartilage, cartilage defect, joint fluid, and medial meniscus posterior horn were clearly visible. (c) Arthroscopic surgery showed cartilage defect of the deep partial-thickness cartilage lesion that was greater than 50% of the total thickness of the articular surface of the medial femoral condyle.

Fig. 3.

A 44-year-old woman with grade 2 cartilage defect of the lateral tibial plateau, demonstrating a false negative on both THRIVE and VISTA images. (a, b) Both contrast-enhanced THRIVE image and VISTA image showing no signal change suggestive of a cartilage defect. (c) Arthroscopic surgery showed cartilage defect of superficial partial-thickness cartilage lesion with less than 50% of the total thickness of the articular surface of the lateral tibial plateau.

With regards to cartilage grading, 3D-THRIVE and 3D-VISTA showed similar diagnostic performance, and both sequences showed high inter-observer agreement despite different SNR and different CNR. In cartilage defect of the lateral tibial plateau, the sensitivity and specificity was relatively lower despite the correlations of MR grades and arthroscopic grades were statistically significant (Table 7, Fig. 3).

In terms of undergrade or overgrade of cartilage, there was some differences between 3D-THRIVE and 3D-VISTA sequences. In arthroscopic correlation (Table 3), 3D-THRIVE showed 20 in right diagonal (i.e. undergrade) and 45 in left diagonal (i.e. overgrade) while 3D-VISTA showed 15 in right diagonal (i.e. undergrade) and 17 in left diagonal (i.e. overgrade). This suggest 3D-THRIVE tend to overgrade the cartilage defects despite statistically insignificantly difference. Therefore, radiologists should exercise caution in order to prevent over- or underestimation of the cartilage on 3D-THRIVE MR images. Furthermore, the insensitivity to surgical materials is one of the strengths of FSE-based MR sequences. With considering increasing cartilage surgery including microfracturing or cartilage graft, the FSE-based MR sequences would be better to minimize the surgery-related susceptibility artifact. In these reasons, we carefully suggest that 3D-VISTA is more suitable than 3D-THRIVE for cartilage grading.

In comparison with 3D-VISTA, we reviewed the contrast-enhanced 3D-THRIVE sequences instead of the pre-contrast 3D-THRIVE sequences. We chose this approach because the cartilage contour can be more clearly delineated on contrast-enhanced 3D-THRIVE images by the arthrographic effect due to diffusion of Gadolinium into joint (28,29). Future studies are needed to compare pre- and post-contrast 3D-THRIVE for the improvement of arthrographic effect in terms of diagnostic performance. Future studies are needed to compare pre- and post-contrast 3D-THRIVE, as well as other 3D sequences, such as VIBE, SPACE, 3D FSPGR, and CUBE. We suggest that GRE- and FSE-based 3D MR sequences are both good techniques for the qualitative evaluation of cartilage.

Our study has several limitations. First, we compared dark and bright fluid sequences (i.e. T1W and intermediate-weighted images), and we compared gradient-echo and fast spin-echo images. However, in clinical imaging, the combination of gradient-echo/spin-echo and T1W /intermediate-weighted 3D MR sequences is widely used, so a comparison of these sequences is appropriate. Second, the slice thickness of the MR sequences was not exactly the same. To improve the clinical usefulness of this study, we compared the MR images with MR parameters used for knee MR evaluation. Third, the arthroscopic surgeon might be aware of the MR imaging results, which could affect the arthroscopic cartilage grading. Finally, we compared the sequences of one manufacturer’s machine. Future studies will be needed to compare the corresponding sequences of other vendors.

In conclusion, FSE-based 3D-VISTA knee MR showed good diagnostic performance comparable to GRE-based 3D-THRIVE in the evaluation of knee cartilage, and it can be incorporated into routine knee MRI protocols for the evaluation of cartilage.

Footnotes

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This research was supported by Basic Science Research Program through the National Research Foundation of Korea(NRF) funded by the Ministry of Education, Science and Technology (2012R1A1A2042165).

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