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Purpose:
To develop and verify the accuracy of a rapid imaging protocol for delayed gadolinium-enhanced magnetic resonance (MR) imaging of cartilage that was based on threedimensional (3D) spoiled gradient-recalled acquisition in the steady state (SPGR) sequences with variable flip angles (FAs) (VFAs) and where a correction method for B1 field inhomogeneities was applied.
Materials and Methods:
The institutional research ethics board approved this study. Written informed consent was obtained from all subjects. A B1 field inhomogeneity correction method was applied to a 3D SPGR pulse sequence with VFAs (repetition time msec/echo time msec, 7.1/3.3; FAs, 2°, 5°, 10°, and 20°) and was used to perform delayed gadoliniumenhanced MR imaging of cartilage 3D T1 measurements at 1.5 T. The 3D T1 measurements were validated with the reference standard (the results of T1 mapping by using a single-section two-dimensional [2D] inversion-recovery [IR] fast spin-echo [SE] pulse sequence in vitro and in vivo) in six healthy volunteers.
Results:
T1 values calculated from 3D T1 maps were not significantly different from reference T1 values in vitro (P ⫽ .195) and in vivo (P ⫽ .52) when a B1 field inhomogeneity correction method was applied. In vivo T1 mapping of the articular surface of the whole femoropatellar joint, including data acquisition, was performed in approximately 8 minutes of acquisition time at a spatial resolution of 0.55 ⫻ 0.55 ⫻ 3.00 mm.
Conclusion:
Rapid T1 mapping by using 3D SPGR acquisitions with a VFA approach and a correction for B1 field inhomogeneities can be used for delayed gadolinium-enhanced MR imaging of cartilage. T1 measurements performed in vitro and in vivo by using this approach are highly accurate when compared with those performed by using standard 2D IR fast SE T1 mapping as a reference.
1
From the Department of Medical Imaging, Mount Sinai Hospital and the University Health Network (G.A., L.M.W., E.R.), Research Institute, the Hospital for Sick Children (Y.Y., H.L.M.C.), Department of Medical Biophysics (H.L.M.C.), and Department of Medical Imaging, Toronto General Hospital (M.S.S.), University of Toronto, Toronto, Ontario, Canada; Institute for Diagnostic Radiology, University Hospital Zu¨rich, Ra¨mistrasse 100, CH-8091 Zu¨rich, Switzerland (G.A.); and Ultrasound Diagnostic Imaging Department, Fourth Hospital of Hebei Medical University, Shijiazhuang, Hebei, China (Y.Y.). Received June 24, 2008; revision requested August 8; revision received March 1, 2009; accepted March 26; final version accepted April 14. Address correspondence to G.A. (e-mail:
[email protected] ).
娀 RSNA, 2009
姝 RSNA, 2009 Radiology: Volume 252: Number 3—September 2009 ▪ radiology.rsnajnls.org
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Gustav Andreisek, MD Lawrence M. White, MD Yi Yang, MD Emma Robinson, MD Hai-Ling Margaret Cheng, PhD Marshall S. Sussman, PhD
ORIGINAL RESEARCH
Delayed Gadolinium-enhanced MR Imaging of Articular Cartilage: Three-dimensional T1 Mapping with Variable Flip Angles and B1 Correction
TECHNICAL DEVELOPMENTS: MR Cartilage Measurement with T1 Mapping
D
elayed gadolinium-enhanced magnetic resonance (MR) imaging of cartilage is based on quantitative T1 mapping of articular cartilage subsequent to injection and penetration of gadopentetate dimeglumine (Magnevist; Berlex Imaging, Wayne, NJ) (1,2). After administration, gadopentetate dimeglumine is distributed in higher concentrations in cartilage areas, with lower glycoaminoglycan concentration resulting in lower T1 values. Such areas typically represent areas with pathologic cartilage composition and decreased glycoaminoglycan concentration content (3–5). For T1 mapping, most implementations of delayed gadolinium-enhanced MR imaging of cartilage use two-dimensional (2D) inversion recovery (IR) fast spin-echo (SE) pulse sequences (6–9). However, 2D IR fast SE acquisitions are limited by very long acquisition times of up to 30 minutes per single 2D section and do not achieve full joint coverage (10). These limitations severely hamper the widespread use of delayed gadolinium-enhanced MR imaging of cartilage in the clinic and for research and cannot be overcome by using interleaved multisection 2D acquisitions because of magnetization transfer effects, which introduce systematic errors in the T1 measurements, as well as the limitations of very long acquisition times (11,12). As a result, a number of faster imaging techniques for T1 mapping have been proposed and evaluated, and these include three-dimensional (3D) IR-prepared spoiled gradient-recalled acquisition in the steady state (SPGR) sequences (13) or the look-locker technique (14). In theory, these techniques allow whole-joint coverage with a section thickness and
Advance in Knowledge 䡲 Correction of B1 field inhomogeneities allows highly accurate T1 measurements when three-dimensional spoiled gradient recalled acquisition in the steady state pulse sequences with variable flip angles are used for T1 mapping. 866
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an in-plane resolution similar to those of single-section 2D IR fast SE acquisitions (14–16). However, the overall acquisition times are still about the same as those for a single-section 2D acquisition and range between 10 and 20 minutes. Recently, a newer approach for rapid 3D T1 mapping of cartilage implemented at 3.0-T MR imaging was reported (10). It allowed imaging of the whole knee joint in approximately 5 minutes and involved the acquisition of a fast low-angle shot sequence with variable flip angles (FAs) (VFAs) in combination with parallel imaging (generalized autocalibrating partially parallel acquisition). However, although this approach allowed fast 3D T1 mapping, differences in quantitative T1 results were observed when 3D fast low-angle shot T1 maps obtained with VFAs were compared with standard 2D IR fast SE T1 maps. The authors identified B1 field inhomogeneities as a possible source for these T1 inaccuracies (10). A possible solution to overcome these inaccuracy problems is to correct for B1 field inhomogeneities. This correction was recently demonstrated by Cheng and Wright (17), who used a rapid B1 field-mapping technique to obtain data for secondary correction of systematic errors in T1 mapping by using 3D SPGR sequences with a VFA. By using their technique, the authors were able to produce highly accurate T1 maps of the whole brain, even in the presence of severe B1 field inhomogeneities, within less than 4 minutes of acquisition time.
Implications for Patient Care 䡲 In this study, the delayed gadolinium-enhanced MR imaging of cartilage protocol allows rapid and precise determination of T1 of articular cartilage with wholejoint coverage. 䡲 Delayed gadolinium-enhanced MR imaging of cartilage may facilitate the clinical application of T1 mapping to assess articular cartilage.
We hypothesized that this technique also could be used for rapid and accurate T1 mapping of cartilage. We therefore aimed to develop and verify the accuracy of a rapid imaging protocol for delayed gadolinium-enhanced MR imaging of cartilage, which was based on 3D SPGR acquisitions with VFAs in which a correction method for B1 field inhomogeneities was applied.
Materials and Methods The research ethics board of University Health Network, Toronto, Ontario, Canada, approved this study. Written informed consent was obtained from all subjects.
MR Imaging Hardware All MR imaging experiments were performed with a 1.5-T MR unit (Signa Excite HD; GE Healthcare, Waukesha, Wis), equipped with high-performance gradients (amplitude, 40 mT/m; slew rate, 200 T/m/sec). An eight-channel transmit-receive knee
Published online before print 10.1148/radiol.2531081115 Radiology 2009; 252:865– 873 Abbreviations: FA ⫽ flip angle IR ⫽ inversion recovery SE ⫽ spin echo SPGR ⫽ spoiled gradient-recalled acquisition in the steady state T1(0) ⫽ baseline T1 T1(Gd) ⫽ contrast material– enhanced imaging T1 3D ⫽ three-dimensional 3D SPGR/VFA4 ⫽ 3D SPGR with four FAs 3D SPGR/VFA3 ⫽ 3D SPGR with three FAs 2D ⫽ two-dimensional VFA ⫽ variable FA Author contributions: Guarantors of integrity of entire study, G.A., L.M.W.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, G.A., L.M.W., E.R., H.L.M.C., M.S.S.; clinical studies, G.A.; experimental studies, all authors; statistical analysis, G.A., M.S.S.; and manuscript editing, all authors Authors stated no financial relationship to disclose.
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coil (Invivo, Orlando, Fla) placed in the isocenter of the MR unit was used for both in vitro and in vivo experiments.
MR Imaging Techniques Reference data for T1 measurements were acquired by using a standard singlesection 2D IR fast SE MR sequence (repetition time msec/echo time msec/inversion time msec, 2500/8/50, 180, 350, 650, 1200, and 1680; echo train length, five; readout bandwidth, 41.67 kHz; field of view, 140 ⫻ 140 mm; section thickness, 3 mm; number of sections, one; matrix, 256 ⫻ 256 pixels; in-plane resolution, 0.5 ⫻ 0.5 mm; number of signals acquired, two; and total acquisition time, 26 minutes 30 seconds [six acquisitions of 4 minutes 25 seconds each]). Data from this 2D IR fast SE acquisition were used to calculate T1 values, as discussed later in “T1 calculation,” which served as standard of reference for all in vitro and in vivo 3D T1 measurements. For 3D T1 data acquisitions, two SPGR sequences were adapted from Cheng and Wright (17). First, a 3D SPGR sequence with four FAs (3D SPGR/VFA4) was performed, with the following parameters: repetition time msec/echo time msec, 7.1/3.3; FAs, 2°, 5°, 10°, and 20°; bandwidth, 31.3 kHz; field of view, 140 ⫻ 140 mm; section thickness, 3 mm; number of sections, 12; matrix, 256 ⫻ 256 pixels; in-plane resolution, 0.55 ⫻ 0.55 mm; number of signals acquired, four; and total acquisition time, 7 minutes 12 seconds (four acquisitions of 1 minute 48 seconds each). Sequence parameters were chosen to allow whole femoropatellar joint coverage and high inplane resolution and signal-to-noise ratio while providing a short acquisition time. Second, a 3D SPGR sequence, in which the number of FAs was reduced from four to three (FAs of 2°, 10°, and 20°) (3D SPGR with three FAs [3D SPGR/VFA3]) and the number of signals acquired was reduced from four to one, was performed, allowing for a minimum possible acquisition time of 1 minute 21 seconds (three acquisitions of 27 sec-
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onds each). Data from these two 3D SPGR acquisitions were used to calculate T1 values, as discussed later in “T1 Calculation,” which were compared with standard reference T1 values. For B1 field inhomogeneity correction, first B1 field mapping was performed to gain data about B1 field inhomogeneities. Therefore, a rapid multisection 2D SE segmented echo-planar imaging sequence was performed. The sequence included two acquisitions at different excitation and refocusing angles. For the first acquisition, the excitation angle was 60° and the refocusing angle was 120°. For the second acquisition, the excitation angle was 120° and the refocusing angle was 240°. Other sequence parameters were as follows: 4000/21.5; readout bandwidth, 260 kHz; field of view, 140 ⫻ 140
mm; section thickness, 3 mm; number of sections, 12; matrix, 256 ⫻ 256 pixels; number of signals acquired, one; and acquisition time, 1 minute 12 seconds (two acquisitions of 36 seconds each). A segmented echo-planar imaging sequence was used rather than a conventional SE acquisition because of the much shorter acquisition time. Second, a postprocessing step was performed during which 3D SPGR T1 maps were corrected pixel by pixel for the measured B1 field inhomogeneities by using a data analysis routine (Matlab, release 7.3; MathWorks, Natick, Mass), which was developed by one author (H.L.M.C.) with 10 years of experience in MR imaging research. A detailed description of the theoretic and mathematic basis used was presented by Cheng and Wright (17).
Figure 1
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Figure 1: (a) Coronal 3D SPGR MR image (7.1/3.3) of phantom acquired at 10° FA. Numbers indicate concentration of gadopentetate dimeglumine in millimoles per liter in test tubes. (b) Coronal localizer MR image (5.3/1.5) illustrates position of 12 sections of SPGR acquisition. (c) Transaxial color-coded T1 map of phantom calculated from 3D SPGR data set by using B1 field inhomogeneity correction. Circular region of interest used for T1 measurements is shown in test tube with 0.25 mmol/L concentration.
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In Vitro Experiments For the in vitro experiments, a phantom that consisted of eight cylindrical 10-mL test tubes filled with physiologic saline (0.9% sodium chloride) doped with gadopentetate dimeglumine at concentrations of 0.1, 0.13, 0.19, 0.25, 0.38, 0.50, 0.75, and 1.0 mmol/L (Fig 1) was produced (13). To improve loading of the coil durFigure 2
Figure 2: Sagittal localizer MR image (5.3/1.5) illustrates position of 12 sections of 3D SPGR acquisition used in study subjects.
Figure 3
Figure 3: Transaxial 2D IR fast SE MR image (2500/8/1680) of patella in 32-year-old healthy male volunteer shows segmentation of articular cartilage surface into medial and lateral portions for evaluation of bulk T1(0) and T1(Gd) values (also referred to as delayed gadolinium-enhanced MR imaging of cartilage index). Border between medial and lateral regions of interest was defined by a line perpendicular to a line that was drawn parallel to axis between medial and lateral edges of patella, at level of most dorsal point of patellar cartilage surface. 868
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ing phantom measurements and to prevent susceptibility artifacts, test tubes were immobilized in a round 600-mL plastic container filled with physiologic saline. The phantom was imaged by using a standard single-section 2D IR fast SE sequence to acquire standard reference data for T1, the 3D SPGR/VFA3 and 3D SPGR/VFA4 sequences, and, for B1 mapping, the SE echo-planar imaging sequence. All imaging was performed at room temperature (24°C) in a transaxial plane perpendicular to the long axis of the phantom (Fig 1). The standard reference 2D IR fast SE sequence was a single-section acquisition. The 2D section location matched the location of the center section (section 7) of the 3D SPGR sequence.
In Vivo Experiments Six healthy volunteers were examined. These volunteers included four men and two women, with a mean and median age of 32.1 and 32.6 years, respectively (range, 23–38 years); a mean and median body weight of 81.7 and 78.5 kg, respectively (range, 55–120 kg); and a mean and median body mass index of 26.4 and 26.0 kg/m2 (range, 20.4 –36.2 kg/m2). The inclusion criterion was an age older than 18 years. Exclusion criteria were contraindications for MR imaging (eg, a pacemaker); pregnancy; or history of osteoarthritis, prior knee pain, disorders, or surgery. In two subjects, the left knee was imaged, and in four subjects, the right knee was imaged. In our study, we focused on the femoropatellar joint, specifically on the articular cartilage of the patella. Therefore, all in vivo MR imaging was performed in the transaxial plane. For reference T1 mapping, a 2D single-section IR fast SE sequence was performed. For 3D T1 mapping, SPGR/VFA4 was performed. Figure 2 illustrates the position of the individual sections of the 3D acquisition. It was not feasible to acquire more than one 2D IR fast SE section because of the long imaging time of 26 minutes 30 seconds per individual 2D single-section acquisition. Thus, we matched the position of the single 2D IR fast SE section to the position of the 3D SPGR section that best displayed
the center of the patella (section 7) by manually entering the coordinates of the appropriate 3D section. For B1 mapping, the SE segmented echo-planar imaging sequence was performed. MR imaging was performed at baseline and at 2 hours after the administration of 0.2 mmol/kg of gadopentetate dimeglumine (mean and median volume, 32.8 and 31.5 mL; range, 22– 48 mL of gadopentetate dimeglumine). To facilitate the transport of gadopentetate dimeglumine into cartilage, all subjects were asked to walk for at least 10 minutes following administration of the gadopentetate dimeglumine (12).
T1 Calculation For the calculation of T1 maps, data analysis software routines were developed by two authors (H.L.M.C. and M.S.S., with 10 and 15 years of experience in MR imaging research, respectively) by using previously published methods (17). Because of considerably long imaging times, in-plane motion correction was performed for 2D IR fast SE acquisitions by using a mutual information template-matching algorithm (18). In vitro, T1 was determined in circular regions of interest (mean size, 1 cm2 for in vitro and 0.6 cm2 for in vivo) placed in the center of the test tubes. To report in vivo T1 data, the metrics used were bulk baseline T1 (T1[0]) and contrast material– enhanced imaging T1 (T1[Gd]) (also referred to as the delayed gadolinium-enhanced MR imaging of cartilage index) values, both determined by averaging T1 across regions of interest in the patellar cartilage at baseline T1 (T1[0]) and at contrast material– enhanced imaging T1 (T1[Gd]). Separate T1(0) and T1(Gd) values were calculated for two regions of interest, one of which included the lateral and the other the medial aspect of the patellar articular cartilage (Fig 3). Regions of interest each had a mean size of 0.6 cm2, were placed by one author (G.A., a fellowship-trained radiologist with 5 years of experience in musculoskeletal MR imaging research), and included all cartilage from the cartilage-bone interface to the articular cartilage surface. For both in vitro and in vivo measure-
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Table 1 T1 Values of in Vitro Measurements 3D SPGR/VFA4 Phantom and Statistical Data
3D SPGR/VFA3
Without B1 Field With B1 Field Without B1 Field With B1 Field 2D IR Fast SE* Inhomogeneity Correction Inhomogeneity Correction Inhomogeneity Correction Inhomogeneity Correction
Gadopentetate dimeglumine concentration (mmol/L) 0.1 1280 ⫾ 129 0.13 1043 ⫾ 40 0.19 822 ⫾ 26 0.25 677 ⫾ 21 0.38 474 ⫾ 9 0.50 376 ⫾ 7 0.75 259 ⫾ 5 1.0 202 ⫾ 4 Mean difference† P value‡
1617 ⫾ 157 1218 ⫾ 78 997 ⫾ 58 811 ⫾ 39 569 ⫾ 26 448 ⫾ 19 305 ⫾ 12 225 ⫾ 9 132.1 (48.8, 215.4) .008
1276 ⫾ 148 1031 ⫾ 63 834 ⫾ 49 684 ⫾ 35 475 ⫾ 10 362 ⫾ 13 235 ⫾ 9 177 ⫾ 7 ⫺7.6 (⫺18.9, 3.7) .195
1614 ⫾ 298 1306 ⫾ 227 1056 ⫾ 125 852 ⫾ 92 620 ⫾ 61 506 ⫾ 52 348 ⫾ 34 256 ⫾ 26 177.9 (99.9, 255.8) .008
1321 ⫾ 231 1104 ⫾ 147 885 ⫾ 108 717 ⫾ 79 515 ⫾ 51 407 ⫾ 41 267 ⫾ 25 201 ⫾ 20 35.5 (16.8, 54.2) .016
Note.—All values are mean T1 values in milliseconds ⫾ standard deviations unless otherwise stated. The 3D data were acquired from central section of the 3D slab. * Standard of reference. †
Mean differences are those between 2D IR fast SE (standard of reference) and the 3D acquisitions. Numbers in parentheses are corresponding 95% confidence intervals.
‡
P values indicate significant differences between the standard of reference and the 3D acquisitions (the threshold significance level was .05).
ments, 3D T1 maps were calculated with and without correction for B1 field inhomogeneities.
Figure 4
Statistical Analysis Statistical analysis was performed by one author (G.A.) by using software (SPSS; SPSS, Chicago, Ill). In vitro and in vivo T1 data for standard reference 2D IR fast SE and 3D SPGR acquisitions are presented as means ⫾ standard deviations. Mean differences between standard reference 2D IR fast SE and each 3D acquisition method and 95% confidence intervals for the mean differences are provided for the in vitro data. In vitro and in vivo R2 values were calculated to evaluate the correlation between standard reference 2D IR fast SE and 3D SPGR T1 data. In addition, the Wilcoxon signed rank test was used to determine whether there were significant differences between the standard reference T1 values and T1 values calculated from 3D SPGR acquisitions. The threshold significance level was P ⫽ .05 (19). Linear regression analysis was performed to compare T1 data from 2D and 3D acquisitions. Results In Vitro T1 Measurements Mean reference T1 values, as determined by using single-section 2D IR fast SE T1
Figure 4: In vitro T1 data calculated from standard reference single-section 2D IR fast SE T1 maps and from T1 maps ofcorresponding3DSPGRsection(section7).Bestcorrelationbetweeninvitro3DSPGRand2DIRfastSET1measurementsisshownfor3DSPGR/VFA3 and3DSPGR/VFA4 acquisitionswhereB1 fieldinhomogeneitieswerecorrected. Uncorrected3DT1mapsshowdivergenceathigherT1values,resultinginsystematicoverestimationofT1.
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mapping, ranged from 202 msec ⫾ 4 (standard deviation) to 1280 msec ⫾ 129 for the gadopentetate dimeglumine concentrations in the phantom of 1.0 and 0.1 mmol/L, respectively (Table 1). Overall, all 3D SPGR/VFA3 and 3D SPGR/VFA4 maps with and without B1 field inhomogeneity correction showed a
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highly significant linear correlation with the reference data (R2 ⫽ 0.998 – 0.999, P ⬍ .001). However, regression analysis showed a systematic measurement error that was most pronounced for uncorrected T1 acquisitions, and the percentage error was similar at different T1 values (Fig 4).
Table 2 Percentage Error for Uncorrected and Corrected in Vitro 3D SPGR/VAF4 T1 Values across All 12 Sections of 3D Slab Compared with Standard Reference T1 Value Section 1 2 3 4 5 6 7 8 9 10 11 12
Without B1 Field Inhomogeneity Correction Mean T1 (msec)* Percentage Error† P Value‡ 161.4 389.3 617.8 600.3 738.7 763.1 761.6 774.0 726.5 733.0 566.5 161.5
⫺74.9 ⫺39.3 ⫺3.7 ⫺6.5 15.1 18.9 18.7 20.6 13.2 14.2 ⫺11.7 ⫺74.8
.012 .012 .484 .123 .012 .012 .012 .012 .012 .012 .012 .012
With B1 Field Inhomogeneity Correction Mean T1 (msec)* Percentage Error† P Value‡ 75.1 354.9 545.3 566.0 645.3 650.9 637.5 634.3 637.0 586.5 449.6 450.0
⫺88.3 ⫺44.7 ⫺15.1 ⫺11.9 0.5 1.4 ⫺0.7 ⫺1.2 ⫺0.8 ⫺8.6 ⫺30.0 ⫺30.0
.012 .012 .012 .575 .674 .484 .161 .484 .012 .012 .012 .012
* T1 values are mean values calculated from the individual T1 values at eight gadopentetate dimeglumine concentrations (0.1–1.0 mmol/L). The mean T1 value of the standard reference 2D IR fast SE acquisition was 642 msec. The percentage errors were calculated as follows: Percentage error ⫽ {[(T12D ⫺ T13D)/T12D] 䡠 ⫺1} 䡠 100, where T12D is the T1 value with 2D IR fast SE and T13D is the T1 value with 3D SPGR/VFA4.
SPGR/VFA3 maps with B1 field inhomogeneity correction, as well as SPGR/ VFA3 and SPGR/VFA4 maps without B1 field inhomogeneity correction, showed significant T1 differences from the reference standard 2D IR fast SE maps (P ⫽ .016, .008, and .008, respectively) (Table 1). Mean differences in T1 between the reference standard 2D IR fast SE and 3D SPGR/VFA4 maps with B1 field inhomogeneity correction were not significant (P ⫽ .195). The percentage errors in T1 between 2D IR fast SE and 3D SPGR/VAF4 acquisitions with B1 field inhomogeneity correction at the central five sections (sections 4 – 8) were less than 1.5% (Table 2). T1 values at sections 4, 5, 6, 7, and 8 (P ⫽ .575, .674, .484, .161, and .484, respectively) were not significantly different from the reference 2D IR fast SE T1 values. At the other sections of the 3D image volume, false-low T1 values were observed (Table 2). These T1 values were significantly lower than the reference 2D IR fast SE T1 values (P ⫽ .012). Percentage errors in T1 at the outer two sections on each side were greater than 30% and up to 88%.
†
In Vivo Experiment In vivo T1 mapping of the articular surface of the femoropatellar joint, including data acquisition, was performed in approximately 8 minutes of acquisition time
‡
P values indicate significant differences between the standard reference 2D IR fast SE value and the value with 3D acquisitions (threshold significance level was .05).
Table 3 T1 Values of in Vivo T1 Measurements at Center of Patella with 2D IR Fast SE T1 Mapping and 3D SPGR/VFA4 T1 Mapping with B1 Field Inhomogeneity Correction
Subject 1 2 3 4 5 6 Overall
2D IR Fast SE* Medial Lateral 903 ⫾ 95 840 ⫾ 90 862 ⫾ 91 914 ⫾ 129 813 ⫾ 88 842 ⫾ 121 863 ⫾ 102
820 ⫾ 78 787 ⫾ 91 855 ⫾ 117 856 ⫾ 133 826 ⫾ 84 828 ⫾ 94 829 ⫾ 99
At Baseline, T1(0) 3D SPGR/VFA4 Medial Lateral 882 ⫾ 93 877 ⫾ 110 899 ⫾ 93 910 ⫾ 127 924 ⫾ 168 821 ⫾ 149 886 ⫾ 123
783 ⫾ 122 750 ⫾ 117 907 ⫾ 134 861 ⫾ 91 882 ⫾ 143 825 ⫾ 145 834 ⫾ 125
Difference in Mean (%)†
2D IR Fast SE* Medial Lateral
2.4/4.5 ⫺4.3/4.8 ⫺4.2/⫺6.1 0.4/⫺0.6 ⫺13.6/⫺6.8 2.4/0.5 ⫺2.8/⫺0.6
586 ⫾ 46 584 ⫾ 122 634 ⫾ 53 526 ⫾ 66 702 ⫾ 96 579 ⫾ 53 602 ⫾ 73
At 2 Hours after Injection, T1(Gd) 3D SPGR/VFA4 Medial Lateral
501 ⫾ 79 595 ⫾ 53 644 ⫾ 56 523 ⫾ 60 706 ⫾ 76 628 ⫾ 66 599 ⫾ 65
507⫾36 613 ⫾ 97 619 ⫾ 97 544 ⫾ 107 793 ⫾ 173 570 ⫾ 78 608 ⫾ 98
529 ⫾ 79 622 ⫾ 58 662 ⫾ 90 572 ⫾ 82 806 ⫾ 80 665 ⫾ 80 642 ⫾ 78
Difference in Mean (%)† 13.5/⫺5.5 ⫺5.1/⫺4.6 2.4/⫺2.8 ⫺3.5/⫺9.4 ⫺12.9/⫺14.0 1.5/⫺5.9 ⫺0.7/⫺7.0
Note.—All values are mean T1 values in milliseconds ⫾ standards deviations unless otherwise stated. Raw data for uncorrected in vivo T1 measurements were omitted for clarity here but are shown in Figure 6. * The 2D IR fast SE acquisitions served as reference standard. The differences in mean values were calculated as follows: Difference in mean ⫽ [(AM2D ⫺ AM3D)/AM2D] 䡠 100, where AM2D is the average of mean values with 2D IR fast SE and AM3D is the average of mean values with 3D SPGR/VFA4. Data are difference in mean values for medial portion of cartilage of knee/difference in mean values for lateral portion of cartilage of knee.
†
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at a spatial resolution of 0.55 ⫻ 0.55 ⫻ 3.00 mm. Mean reference T1 values (2D IR fast SE) for the medial and lateral portions of the articular cartilage of the patella were 863 msec ⫾ 102 and 602 msec ⫾ 73 and 829 msec ⫾ 99 and 599 msec ⫾ 65, respectively, at baseline (T1[0]) and at 2 hours after the administration of gadopentetate dimeglumine (T1[Gd]), respectively (Table 3, Fig 5). Overall, for both the medial and lateral portions of the articular cartilage, correlation statistics showed a highly significant correlation between 2D and corrected 3D T1 mapping techniques (R2 ⫽ 0.977, P ⬍ .001). Correlation was still very high (R2 ⫽ 0.930) for uncorrected 3D T1 mapping, but statistical analysis results, similar to the results of in vitro experiments, showed a systematic error in T1 measurements with significantly false-high T1 values (P ⬍ .001), most noted at higher T1 values, which are representative for T1(0) measurements (Fig 6). There were no significant T1 differences between singlesection 2D IR fast SE and 3D SPGR/
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Figure 5
Figure 5: (a) Transaxial 2D IR fast SE MR image (2500/8) and color-coded (b) 3D and (c) standard reference 2D T1 maps of patella in 28-year-old female volunteer acquired 2 hours after intravenous administration of gadopentetate dimeglumine showed excellent agreement with respect to T1 values of articular cartilage. On 3D T1 map in b, slightly more artifacts are seen at bone-cartilage interface. These voxels were not included during segmentation process.
Figure 6
Figure 6: (a) In vivo T1 measurements before and 2 hours after gadopentetate dimeglumine administration showed excellent correlation between corrected 3D SPGR/VFA4 and reference 2D IR fast SE acquisition. (b) Uncorrected data showed a systematicoverestimationofT1athigherT1values,whicharerepresentativeforbaselineT1(0)measurements. Radiology: Volume 252: Number 3—September 2009 ▪ radiology.rsnajnls.org
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VFA4 maps with B1 field inhomogeneity correction (P ⫽ .52).
Discussion Correction of B1 field inhomogeneities is necessary in 3D SPGR/VFA T1 mapping approaches because variations in the B1 field can introduce systematic errors in T1 measurements of cartilage (10,20). These errors were shown to be accentuated at field strengths of 1.5 T or higher or when separate transmit-receive coil systems were used (21,22). In our study, we used an eight-channel transmit-receive knee coil, which allowed imaging with a high spatial resolution of 0.55 ⫻ 0.55 ⫻ 3.00 mm. Because it is known that such transmit-receive coils show, depending on the coil configuration, T1 deviations of up to 25% in certain regions of the field of view (23), a correction method needs to be applied. Our in vitro and in vivo results clearly confirmed the effects of B1 field inhomogeneities on the accuracy of 3D SPGR/VFA acquisitions. T1 maps calculated without correction for B1 field inhomogeneities resulted in less accurate T1 measurements when compared with reference T1 maps calculated with the 2D IR fast SE technique (eg, average error in vivo uncorrected up to 33% vs corrected less than 4.1%). More specifically, uncorrected data showed a divergence at higher T1 values. This can be explained by the fact that B1 effects result in a fixed percentage error in measured T1, which causes a systematic overestimation of T1 (17). In vitro, we performed two 3D SPGR sequences with three and four different FAs. We chose an acquisition with four FAs to allow whole femoropatellar joint coverage, high spatial resolution, and high signal-to-noise ratio, while providing a relatively short acquisition time, whereas we selected an acquisition with three FAs to minimize acquisition time while maintaining similar uniformity of T1 measurement precision across the T1 range of interest. Overall, the acquisitions with four FAs showed excellent accuracy when compared with the reference standard. Therefore, we decided to use the four-FA approach for 872
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our in vivo experiments where we were able to obtain highly precise (average error, ⬍ 4.1%) T1 maps of the articular cartilage of the patella in 8 minutes 24 seconds (7 minutes 12 seconds for the performance of the 3D SPGR/VFA4 sequence and 1 minute 12 seconds for B1 mapping). However, shorter acquisition times are possible through using either fewer signals acquired for the four-FA 3D SPGR/VFA sequence or a three-FA approach (acquisition time, 1 minute 21 seconds with one signal acquired). It remains, however, to be systematically determined in future studies whether fewer signals acquired or fewer FAs has a greater effect on T1 accuracy. Our results for the 3D SPGR/VFA acquisition with B1 field inhomogeneity correction showed that highly accurate T1 maps were produced only at the more central sections of the 3D slab. Similar observations were made by Li et al (20) who evaluated a VFA technique with two FAs without, however, the use of a B1 field inhomogeneity correction. Li et al observed in their study that, only in the central 60% of the 3D slab, T1 values correlated well with reference T1 values. In our study, inaccurate T1 measurements at the outer edges of the 3D slab occurred, despite correction for B1 field inhomogeneities. These inaccuracies are most likely caused by section profile effects. The SPGR sequence was a 3D acquisition in which a 3D slab is excited, while a section-selective 2D SE segmented echo-planar imaging sequence was used to acquire the B1 maps. Since section profile effects resulting from finite radiofrequency pulses are not corrected by field mapping, differences between 2D and 3D acquisitions, if substantial, will affect the accuracy of our T1 correction. Ideally, the pulses for both sequences should match. This will be a topic of our future studies. As a simple solution for now, we agree with Li et al (20), who recommended discarding information from the outer sections of each side of the 3D data set. This might then require performing more than one acquisition to cover the whole articular surface, because the exact location of abnormal areas of
articular cartilage usually is not known prior to the imaging study. Our study had several limitations. First, we investigated a limited number of different possible FAs for the SPGR acquisition. However, fundamental theoretical analyses for the optimal FAs have already been published (10,17). Thus, we limited our investigations on developing a clinically feasible protocol for delayed gadolinium-enhanced MR imaging of cartilage on the basis of these previous experiences. Second, we focused on the femoropatellar joint. Thus, only 12 sections were acquired, which was sufficient for T1 mapping of the entire patellar cartilage. For T1 mapping of the whole knee joint in the sagittal plane, however, the number of sections needs to be increased or two separate acquisitions of the medial and lateral portions of the knee need to be performed. Last, our in vivo experiments were performed only in healthy subjects. We did not include patients with osteoarthritis of the knee in this investigation because typically a larger variation in absolute T1 and in T1(Gd) over time can be observed in these patients. This would have hampered the direct comparison of 2D and 3D acquisitions. In conclusion, rapid T1 mapping by using 3D SPGR acquisitions with a VFA approach and a correction for B1 field inhomogeneities can be used for delayed gadolinium-enhanced MR imaging of cartilage. T1 measurements in vitro and in vivo by using this approach are highly accurate when compared with standard 2D IR fast SE T1 mapping as a reference.
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