Original Research

Ultrashort TE Spectroscopic Imaging (UTESI):Application to the Imaging of Short T2 RelaxationTissues in the Musculoskeletal System

Jiang Du, PhD,1* Atsushi M. Takahashi, PhD,2 and Christine B. Chung, MD1

Purpose: To investigate ultrashort TE spectroscopic imag-ing (UTESI) of short T2 tissues in the musculoskeletal(MSK) system.

Materials and Methods: Ultrashort TE pulse sequence isable to detect rapidly decaying signals from tissues with ashort T2 relaxation time. Here a time efficient spectroscopicimaging technique based on a multiecho interleaved variableTE UTE acquisition is proposed for high-resolution spectro-scopic imaging of the short T2 tissues in the MSK system. Theprojections were interleaved into multiple groups with thedata for each group being collected with progressively increas-ing TEs. The small number of projections in each groupsparsely but uniformly sampled k-space. Spectroscopic im-ages were generated through Fourier transformation of thetime domain images at variable TEs. T2* was quantifiedthrough exponential fitting of the time domain images or lineshape fitting of the magnitude spectrum. The feasibility of thistechnique was demonstrated in volunteer and cadaveric spec-imen studies on a clinical 3T scanner.

Results: UTESI was applied to six cadaveric specimens andfour human volunteers. High spatial resolution and con-trast images were generated for the deep radial and calci-fied layers of articular cartilage, menisci, ligaments, ten-dons, and entheses, respectively. Line shape fitting of theUTESI magnitude spectroscopic images show a short T2* of1.34 � 0.56 msec, 4.19 � 0.68 msec, 3.26 � 0.34 msec,1.96 � 0.47 msec, and 4.21 � 0.38 msec, respectively.

Conclusion: UTESI is a time-efficient method to image andcharacterize the short T2 tissues in the MSK system withhigh spatial resolution and high contrast.

Key Words: ultrashort TE; projection reconstruction; spec-troscopic imaging; short T2 species; deep layers of carti-lage; menisci; ligaments; tendons; entheses.J. Magn. Reson. Imaging 2009;29:412–421.© 2009 Wiley-Liss, Inc.

THE HUMAN MUSCULOSKELETAL (MSK) system con-tains a variety of tissues with relatively long T2 relax-ation components that can be visualized with conven-tional magnetic resonance imaging (MRI) techniques,as well as many tissues with short T2 components suchas the deep radial and calcified layers of articular car-tilage, menisci, ligaments, tendons, and entheses thatcannot be directly visualized (1–5). These short T2 tis-sues are crucial in the MSK system. For example, thecalcified cartilage is intimately associated with superfi-cial cartilage and subchondral bone and serves as tran-sition tissue between the compliant unmineralized su-perficial cartilage and the stiffer bone. It helps toprevent large stress concentrations at the interface ofthese two biomechanically diverse tissues (6,7). Recentstudies suggest that changes in the calcified layer couldcompromise the more superficial portion and cause it todegenerate (6–12). However, the deep radial and calci-fied layers of cartilage have been virtually unexploredusing MRI due to their short T2s, and the inability ofconventional clinical pulse sequences to acquire data inthis range (5). Knee menisci consist of concentricallyand radially arranged collagen fibers that play an im-portant role in absorbing impact load. Clinical se-quences can detect little or no signal from normal me-niscus. The interpretation of increased signal withinthe meniscus can be clinically challenging and may bea sign of a tear (1,4). Ligaments are short bands oftouch fibrous connective tissue composed mainly oflong, stringy collagen fibers, connecting the osseousstructures of a joint to afford stability. Tendons aretough bands of fibrous connective tissue attachingmuscles to bone, and normally appear as low signalwith clinical pulse sequences (1–3). Enthesis are min-eralized collagen fibers representing the point at whicha tendon inserts into bone. It is highly desirable toqualitatively and quantitatively evaluate these short T2tissues under a clinical MR system.

Chemical shift imaging (CSI) or spectroscopic imag-ing (SI) is a technique that combines acquisition ofspectral and spatial information in a single scan(13,14). In conventional CSI the spatial information isobtained through phase encoding, which is followed byfree induction decay (FID) sampling to generate spec-troscopic information. This spatial encoding scheme istime-consuming and makes it difficult to generate high-

1Department of Radiology, University of California, San Diego, California.2Global Applied Science Laboratory, GE Healthcare, Menlo Park, Cali-fornia.Contract grant sponsor: GE Healthcare.*Address reprint requests to: J.D., University of California, San Diego,Department of Radiology, 407 Dickinson St., San Diego, CA 92103-8756. E-mail: jiangdu@ucsd.eduReceived November 14, 2007; Accepted May 9, 2008.DOI 10.1002/jmri.21465Published online in Wiley InterScience (www.interscience.wiley.com).

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resolution images in vivo. Various fast spectroscopicimaging techniques have been proposed, includingspectroscopic FLASH (SFLASH) imaging, spectroscopicGRASE, fast gradient echo CSI, echo planar SI, multiplespin echo SI, spectroscopic RARE, and multiecho out-and-in spiral sampling (15–19). These techniques pro-vide higher signal-to-noise ratio (SNR) or spatial reso-lution for long T2 species with shorter scan times.However, spatial resolution is still limited, and the tech-niques are not suitable for short T2 tissues.

It is highly desirable to generate spectroscopic imagesof the short T2 tissues with high spatial resolution, highspectral resolution, and broad spectral bandwidth cov-erage. Projection reconstruction is more efficient inachieving high spatial resolution per unit time thanCartesian imaging (21). Spectral resolution can be in-creased by acquiring more images with longer TE delay.Another option to increase spectral resolution is to ac-quire multiecho images combined with variable TE de-lay, as is used in spiral spectroscopic imaging (20). Thetotal scan time can be reduced through angular under-sampling without spatial resolution degradation, whichhas been extensively investigated in contrast-enhancedtime-resolved MR angiography (22–26). The combina-tion of these techniques may provide a novel approachfor high-resolution spectroscopy imaging of short T2tissues.

In this study we devised a new approach termed ul-trashort TE spectroscopic imaging (UTESI) for tissueswith short T2s. We show that the combination of highlyundersampled interleaved projection reconstructionwith a multiecho UTE acquisition at progressively in-creasing TEs is able to provide high spatial resolutionspectroscopic imaging of short T2 tissues in the MSKsystem, including the deep radial and calcified layers ofcartilage, menisci, ligaments, tendons, and entheses.T2* was quantified through exponential signal decayfitting of the multiecho images, or line shape fitting ofthe magnitude UTESI images. This UTESI techniquewas validated through cadaveric specimen and in vivohealthy volunteer studies.

MATERIALS AND METHODS

We previously demonstrated that spectroscopic imag-ing of cortical bone can be realized through UTE acqui-sition at variable TE delays (27), where a single slicewas imaged with a single half pulse and a single echo,or free induction decay (FID). In this study we extendedthe original UTESI to multislice with multiecho acqui-sition and double half pulse excitation. Figure 1 showsthe revised UTESI pulse sequence, which is based on atwo-dimensional (2D) UTE pulse sequence and employsa double half radiofrequency (RF) pulse for signal exci-tation followed by radial ramp sampling (28–32). Radialramp sampling was started immediately after the end ofthe half RF pulse. Up to four echoes with an echo spac-ing (�TE) of 4–6 msec were collected after each half-pulse excitation. These were delayed progressively witha delay time (�t) of 120–300 �s. For each radial k-spaceline, two acquisitions with reversed slice selection gra-dient polarity were sampled and summed to form aselective 2D excitation (33).

The UTE sequence is sensitive to eddy currents thatmay cause out-of-slice signal excitation (34,35). Here adouble half pulse rather than a conventional single halfpulse was employed to improve slice profile of the longT2 components (32), which experience both half pulsesresulting in a conventional full pulse excitation. Theshort T2 signal mainly comes from the second halfpulse, since the excitation from the first half pulse isattenuated by the separation time (Tsep) between thetwo half pulses. It still requires the summation of twoacquisitions with reversed slice selection gradients toform a complete slice excitation for short T2 tissues.The double half pulse technique was first implementedby Josan et al (32) to improve half pulse slice profile formore accurate T2* measurement and temperaturemapping. In Josan et al’s initial approach, gradienttrapezoids with areas of 1, �2, 1 were used. RF wasplayed during the first up-ramp and flattop and duringthe last flattop and down-ramp with the RF waveformsreversed in time. In our double half pulse design, thesame half pulse RF waveform was repeated twice withthe bipolar trapezoidal pair of slice selection gradientreversed for the second half pulse. In this way the eddycurrents for the first and second half pulses will besimilar but opposite, resulting in reduced eddy cur-rents and improved slice profile.

The radial projections can be undersampled to re-duce the total scan time without spatial resolution deg-radation (23–27). In the UTESI sequence the radial halfprojections were highly undersampled and interleavedfor each TE. Figure 2 shows the acquisition scheme.The whole set of projections were interleaved into mul-tiple groups with each group at a progressively increas-ing TE delay which was a multiple of �t. For multiechoacquisition, all the echoes were shifted simultaneouslyby �t while keeping the echo spacing constant at �TE.The small number of projections in each group sparselybut uniformly sampled the k-space. Since the under-sampling streaks are in alignment with the half projec-tions, the oscillation pattern of the streaks can be con-trolled by adjusting the interleaving scheme. For

Figure 1. The UTE spectroscopic imaging pulse sequence em-ploys double half pulses (separated by separation time �T) forslice selective excitation followed by radial ramp sampling atvariable TEs, along with a minimal achievable TE of 8 �s.Single free induction decay (FID) or multiple gradient echoeswere sampled with variable TE delays to generate spectro-scopic information.

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simplicity, let us consider nine interleaved groups witheach group having 45 projections sparsely but uni-formly covering k-space. The nine interleaved groups ofhalf projections can be sampled in the following way: 1,4, 7, 2, 5, 8, 3, 6, and 9. In this way the high frequencyprojection data from neighboring interleaved groupsuniformly covers the periphery of k-space, and can beshared to reduce streak artifact (24–27). Meanwhile,the undersampling streaks oscillate periodically everythree groups, simulating signals with high temporalfrequency. Spectroscopic images were generatedthrough Fourier transformation of the time domain im-ages, which will shift all the streak artifacts to hightemporal frequencies, leaving streak artifact-free im-ages around the water peak (31).

Institutional Review Board permission was obtainedfor this study. UTE spectroscopic imaging was per-formed on six cadaveric specimens and four asymptom-atic volunteers. The fresh human knees and ankleswere harvested from nonembalmed cadavers. The spec-imens were immediately deep-frozen at �40°C (FormaBio-Freezer; Forma Scientific, Marietta, OH). The spec-imens were then allowed to thaw for 36 hours at roomtemperature prior to imaging. A 3-inch coil was used forcadaveric specimens. A quadrature knee coil was usedfor signal reception in volunteer studies. Typical acqui-sition parameters include: field of view (FOV) of 14–16cm for volunteers and 10 cm for cadaveric samples, TRsof 60–200 msec, an initial TE of 8 �s, and a TE delay of120–300 �s thereafter, one to four echoes with an echospacing of 4–6 msec, flip angle of 40–60°, bandwidth of�62.5 kHz, readout of 512 (actual sampling points �278), 3–8 slices, slice thickness of 2–3 mm, 1980–2025projections interleaved into 45–72 groups. The totalscan time was �8–13 minutes. The oblique sagittalplane was used to evaluate the calcified layer of carti-lage in the femorotibial joint. The oblique coronal planewas used to image the lateral collateral ligament. Theoblique sagittal and axial planes were used to interro-gate the Achilles tendon and enthesis. MR images werereviewed by a subspecialized musculoskeletal radiolo-gist to identify region of interest (ROI) placement innormal appearing calcified layer of the femorotibialjoint, the ligament, the meniscus, the Achilles tendon,

and enthesis. Normal calcified layer cartilage was iden-tified by its location just superficial to subchondralbone, its thin linear morphology and bright signal in-tensity. Normal-appearing meniscus was identified byits triangular morphology in the sagittal plane and theabsence of any regions of superimposed linear signalthat extended to an articular surface. Normal-appear-ing ligament, Achilles tendon, and enthesis were de-fined by its uniform signal and linear morphology.

Raw data were transferred to a Linux computer foroffline image reconstruction after the UTE spectro-scopic imaging data acquisition. The half projectiondata at each TE was regridded onto a 512 � 512 matrixfollowed by 2D fast Fourier transformation. Then thecomplex images at multiple TEs (45–144) were zero-padded to 512, yielding a spectroscopic imaging serieswith a matrix size of 512 � 512 � 512 after Fouriertransformation in the time domain. Voxel or ROI-basedspectra were generated by simply plotting the signalintensity across the 512 spectroscopic images. T2* wasderived through exponential fitting of the UTE imagesat progressively increasing TEs, or line shape fitting ofthe magnitude spectra using the following equation(27):

�S�r�,f� ��s0�r��

�� 1T2*

� 2

� 4�f � f02

[1]

where f0 is the peak resonance frequency, r� is thelocation in image space, s0�r� is the effective observableMR signal, and �s�r�,f � is the MR signal intensity atlocation r� and resonance frequency f.

To evaluate the accuracy of the T2* estimation usingtime domain exponential fitting and spectral domainline shape fitting, UTE images at progressively increas-ing TEs were acquired with full sampling for each TE. Intotal, 811 projections were acquired with a readoutmatrix of 512 and TEs ranging from 8 �s to 10 msec.Exponential fitting was performed to calculate T2* val-ues, which were used as a reference standard in eval-uating the accuracy of UTESI T2* quantification. De-scriptive statistical analysis was performed todetermine average T2* values in all cadaveric speci-mens and asymptomatic volunteers, interspecimenvariation, and variation between the UTESI and stan-dard UTE T2* quantification using constant TR andvarying TEs.

RESULTS

Figure 3 shows UTE spectroscopic images of the femo-rotibial articular cartilage and meniscus from a healthyvolunteer with a quadrature knee coil for signal recep-tion. The imaging FOV of 16 cm, readout of 512, and 3mm slice thickness resulted in an acquired voxel size of0.3 � 0.3 � 3.0 mm3, providing excellent depiction ofthe knee structure such as the superficial layers ofcartilage, deep radial, and calcified layers of cartilageand meniscus. The deep layers of cartilage appearbright over a broad range of spectrum, consistent withtheir short T2 relaxation time. Fat signal is shifted to

Figure 2. Interleaved variable TE UTE acquisition scheme di-vided the whole sets of half projections into multiple groupswith each group of half projections sparsely but uniformlycovering k-space with TE successively delayed by �t, whileecho spacing �TE was kept constant. Here TEij refers to theecho time for interleave i at echo j.

414 Du et al.

�420 Hz at 3T, suggesting that UTESI provides accu-rate fat water separation. The undersampling streakartifact was shifted to high spectral frequencies, leavingstreak artifact-free images near the water resonancefrequencies. Figure 4 shows the water peak imagesfrom two of eight slices. Both the articular cartilage andmeniscus are depicted with high spatial resolution,high SNR, and excellent fat suppression without anystreak artifact. However, the deep layers of cartilage arenot well depicted due to the poor contrast over thesuperficial layers of cartilage.

UTESI was also performed with fat signal suppres-sion using a long duration Gaussian pulse focused onfat resonance frequency. The image dynamic range wasincreased, providing high contrast for the cartilage andmeniscus in the time domain image series, as shown inFig. 5. The undersampling streak artifact is signifi-cantly reduced due to the view sharing reconstructionstrategy (31). However, the contrast between the super-ficial layers and deep layers of cartilage is quite limited.Fourier transformation of these time-domain image se-ries provides excellent spectroscopic images shown inFig. 6. The deep layers of cartilage (thin arrow) and

meniscus (thick arrow) appear bright over a broadrange of spectrum, suggesting its short T2 relaxationtime. Maximal contrast was achieved for the deep layersof cartilage at around �200 Hz away from the water

Figure 3. Selected UTE spectroscopic images of the humanknee from a healthy volunteer show clear definition of the deeplayers of cartilage (thin arrows), superficial cartilage, meniscus(thick arrows), as well as excellent fat water separation.

Figure 4. Selected water peak images from two of eight slicesshow excellent depiction of the articular cartilage (thin arrows)and meniscus (thick arrows) with a high spatial resolution of0.3 � 0.3 � 3 mm3 and high contrast with excellent fat signalsuppression. But there is little contrast between the deep lay-ers and superficial layers of cartilage.

Figure 5. Selected time-domain UTESI images of the knee withfat suppression provide excellent depiction of the articular carti-lage and meniscus (thick arrow). There is little contrast betweenthe deep layers of cartilage (short thin arrow) and superficiallayers of cartilage (long thin arrow). Streak artifact was sup-pressed by sharing high frequency projection data from neigh-boring interleaved groups during the image reconstruction.

Figure 6. Selected spectral domain UTESI images of the kneeshow excellent definition of the deep layers of cartilage (shortthin arrow), superficial layers of cartilage (long thin arrow),and menisci (thick arrow). The deep layers of cartilage havemuch shorter T2 than the superficial layers of cartilage, cre-ating increased contrast from 0 Hz up to �200 Hz. The streakartifact was shifted to high spectral frequencies due to theinterleaved acquisition scheme (the first and last images arerescaled in order to show the streaks better).

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peak resonance frequency, where the superficial layersof cartilage appear dark due to its long T2 relaxationtime and narrow spectrum. The spectroscopic imagesnear the peak resonance frequency did not show anystreak artifact that was shifted to high spectral frequen-cies due to the interleaved acquisition scheme.

Figure 7 shows typical UTE spectra from a small ROI(3 pixels) drawn in the deep layers of cartilage and alarge ROI (100 pixels) in meniscus, respectively. Lineshape fitting of the magnitude UTE spectrum of thedeep layers of cartilage shows a short T2* of 1.39 � 0.25msec, which was comparable with the value of 1.24 �0.19 msec derived from exponential signal decay fittingin the time domain. There is a significant signal fluctu-ation in the signal decay curve mainly due to the resid-ual undersampling streak artifact. Line shape fitting ofthe magnitude UTE spectrum of the meniscus shows ashort T2* of 4.96 � 0.35 msec. Exponential signal decayfitting shows a similar T2* value of 4.64 � 0.23 msec.

Figure 8 shows UTESI images of a meniscus samplein the time domain (upper row) and spectral domain(lower row). The imaging FOV of 10 cm, readout of 512,and 2 mm slice thickness resulted in a high spatialresolution of 0.2 � 0.2 � 2.0 mm3 (acquired voxel size),providing excellent depiction of the meniscus structure.

Figure 9 shows the corresponding exponential signaldecay curve and spectra from a small ROI. There aresome Gibbs ring artifacts at high spectral frequenciesthat can be suppressed by increasing spectral resolu-tion or applying lowpass filtering (20). The latter ap-proach is typically used in conventional spectroscopy.However, this filtering also leads to line broadening,increasing errors in T2 quantification through lineshape fitting, and thus not used in our analysis. Excel-lent line shape fitting was achieved for this UTE spec-trum, providing a T2* of 3.69 � 0.16 msec, which isslightly larger than the value of 3.58 � 0.13 msec de-rived through exponential signal decay fitting.

Figure 10 shows axial UTESI images of the Achillestendon in a cadaveric ankle specimen with a 3-inch coilfor signal reception. The imaging FOV of 10 cm, readoutof 512, and 2 mm slice thickness resulted in a highspatial resolution of 0.2 � 0.2 � 2.0 mm3 voxel size,providing excellent depiction of the tendon structure,including the fascicular pattern. Fat signal was shifted�456 Hz away from the water peak, providing robust fatsuppression in the tendon peak images. Figure 11shows the sagittal UTESI images of the same cadavericsample. Again, the tendon structure was demonstratedwith high spatial resolution, high SNR without anystreak artifact, and fat signal contamination.

Figure 12 shows T2* evaluation using three ap-proaches. The first approach is based on single compo-nent exponential signal decay fitting of fully sampled fatsaturated UTE images at a series of TEs ranging from0.1–10 msec (Fig. 12a), and shows a short T2* of 1.56 �0.06 msec. The second approach is based on two com-ponents (fat and tendon) exponential signal decay fit-ting of the UTESI images in time-domain, and shows acomparable short T2* of 1.59 � 0.15 msec. The thirdapproach employs line shape fitting of the magnitudeUTE spectrum from a small ROI drawn in tendon, andshows a short T2* of 1.66 � 0.24 msec.

Figure 8. Selected UTE images of a meniscus in vitro in thetime domain (upper row) and spectral domain (lower row) showexcellent depiction of the meniscus structure with a high spa-tial resolution of 0.2 � 0.2 � 2.0 mm3 (acquired), a highspectral resolution (29 Hz) and broad spectral bandwidth cov-erage of 5 kHz.

Figure 7. Line shape fitting of the magnitudeUTE spectra of the deep layers of cartilage (a)and meniscus (b) show a short T2* of 1.39 �0.25 msec and 4.96 � 0.35 msec, respectively.Exponential decay fitting of the multiple echoimages of the deep layers of cartilage (c) andmeniscus (d) shows similar values of 1.24 �0.19 msec and 4.64 � 0.23 msec, respectively.

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Figure 13 shows sagittal UTESI imaging of the enthe-sis in a cadaveric ankle specimen with a 3-inch coil forsignal reception. The imaging FOV of 10 cm, readout of512, and 2 mm slice thickness resulted in a high spatialresolution of 0.2 � 0.2 � 2.0 mm3 voxel size, providingexcellent depiction of the enthesis structure. All thestreak artifacts were shifted to high temporal frequen-cies, leaving high contrast enthesis images near thewater peak. Figure 14 shows the magnitude UTESIspectra from a small ROI drawn in the enthesis. Lineshape fitting shows that enthesis has a short T2* of4.63 � 0.26 msec.

Figure 15 shows coronal UTESI imaging of the lateralcollateral ligament in the knee joint from a 30-year-oldhealthy male volunteer with a 3-inch coil for signalreception. The imaging FOV of 14 cm, readout of 512,and 2 mm slice thickness resulted in a high spatialresolution of 0.27 � 0.27 � 2.0 mm3 voxel size, provid-ing excellent depiction of the ligament structure (shortarrows). Meanwhile, the deep layers of articular carti-lage are also well depicted (long arrows). Line shapefitting of the UTESI spectra from a small ROI drawn inthe ligament shows that lateral collateral ligament hasa short T2* of 3.44 � 0.18 msec.

Table 1 summarizes the mean and variation in T2*measurements for the deep layers of articular cartilage,menisci, ligaments, tendons, and entheses from fourhealthy volunteers and six cadaveric specimens. Allthese tissues have a short T2* of about 1–4 msec, pro-

viding little or low signal with conventional MR pulsesequences.

DISCUSSION

It has been demonstrated that the UTESI technique iscapable of producing high-resolution images of specieswith short T2 relaxation time. Examples shown hereinclude the deep radial and calcified layers of articularcartilage, which has never been imaged before withconventional pulse sequences. Also included are thetendons and menisci from both healthy volunteers andcadaveric samples, as well as ligaments, tendons, andentheses. The high-quality images of these short T2components were generated mainly due to the use of aminimal TE of 8 �s achieved through the combinationof half pulse excitation, VERSE, radial ramp sampling,and fast T/R switching (29–31). This TE is significantlyshorter than all previously reported sequences imple-mented on clinical MR systems, leading to significantlyreduced signal decay and increased SNR in both time-domain images and spectroscopic images. This singledigit TE also minimizes the undesirable baseline distor-tion which is a significant challenge in conventional CSIbased on FID acquisition method (13–20). UTESI pro-vides a spatial resolution on the order of 0.08–0.27mm3, which is much higher than that of the conven-tional spectroscopic imaging techniques (typically tens

Figure 10. Selected UTESI images of a cadaveric ankle spec-imen in the axial plane show excellent depiction of the Achillestendon with a high spatial resolution of 0.2 � 0.2 � 2.0 mm3

(acquired). Fat signals peaked at �456 Hz, leaving excellentimage contrast for the Achilles tendon around the water peak.

Figure 9. T2* estimation of the meniscus sam-ple using exponential signal decay fitting of theUTE images at variable TEs and line shapefitting of the magnitude spectrum show com-parable results of 3.58 � 0.13 msec and 3.69 �0.16 msec, respectively.

Figure 11. UTESI imaging of a cadaveric ankle specimen inthe sagittal plane shows excellent depiction of the tendon withaccurate fat water separation. The fibrous tissues in tendonare also well depicted (arrow).

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of mm3). This small voxel size may lead to a significantincrease in field homogeneity and T2* over the low-resolution acquisitions and lead to a less than linearloss in SNR with increasing resolution. Furthermore,the interleaved variable TE UTE acquisition strategysignificantly improved the spectral resolution and spec-tral bandwidth by acquiring a relatively large number ofimages at variable TEs within clinically acceptable scantimes. The highly undersampled acquisition producesstrong streak artifact at each TE. However, thesestreaks oscillate at variable TEs, simulating a high tem-poral frequency signal and are thus shifted to highspectral frequencies. As shown in Figs. 3–12, all theUTE spectroscopic images show minimal or no streaksnear the water resonance frequencies.

UTESI not only provides high-quality images in boththe time domain and spectral domain, it also providesfast estimation of T2* relaxation time. T2* values can bederived through exponential fitting of the UTE imagesat multiple echo times, as shown in Figs. 7, 9, and 12.The other approach is line shape fitting of the UTEspectroscopic images. We did not employ the conven-tional Lorentzian line shape fitting of the real spectra,which is susceptible to line broadening and distortiondue to field inhomogeneity, susceptibility, eddy cur-rents, and gradient anisotropy. A variety of algorithmshave been proposed to correct these phase errors andline shape distortion, which would be quite time-con-suming since UTESI contains a large number of spectra(here we have 512 � 512 � 262,144 spectra) (37,38).Further, it would be challenging to correct all the phaseerrors and line broadening effects since UTE imaging isespecially sensitive to these errors due to its half pulseexcitation and radial ramp sampling scheme (34,35).Instead, a modified Lorentzian line shape fitting shownin Eq. [1] was applied to the magnitude spectra, which

Figure 12. T2* estimation of Achilles tendon using single component exponential signal decay fitting of fully sampled UTEimages with fat suppression at progressively increasing TEs (a), two components exponential signal decay fitting of the UTESIimages without fat suppression in the time domain (b) and line shape fitting of the magnitude spectrum (c). Comparable T2*values were derived at 1.56 � 0.06 msec, 1.59 � 0.15 msec, and 1.66 � 0.24 msec, respectively.

Figure 13. UTE spectroscopic imaging of a cadaveric anklespecimen in the sagittal plane shows excellent depiction of theentheses (arrows).

Figure 14. Line shape fitting of the magnitude spectrumshows a relatively short T2* of 4.63 � 0.26 msec for the en-theses.

418 Du et al.

eliminates all the phase errors. T2* values generatedthrough line shape fitting of the magnitude spectrum isalmost completely unaffected by the undersamplingstreak artifact. Its accuracy in T2* estimation has beendemonstrated through comparison with fully sampledUTE acquisition at progressively increasing TEs, asshown in Fig. 12. Therefore, UTESI is a comprehensivetechnique that provides a wealth of information includ-ing time domain images with high spatial resolutionand SNR, spectroscopic domain images with moderatespectral resolution, and accurate fat/water separation,as well as fast estimation of T2* relaxation times.

Gold et al (1) proposed a projection reconstructionacquisition combined with half RF pulse excitation andvariable TE delays to generate imaging and spectro-scopic information of the short T2 tissues in the knee. Aminimum TE of 200 �s was used with the capacity todetect signals from tendon and menisci. Four to eightspectral interleaves were generated with a total scantime of 8 minutes and a relatively high spatial resolu-tion of 1–7.8 mm3, a moderate spectral resolution of61–120 Hz, and limited bandwidth coverage of 1330 Hz.Compared with the original spectroscopic imaging tech-nique proposed by Gold et al, the UTESI techniqueprovides a significant higher spatial resolution, spectralresolution, and spectral bandwidth coverage (1). Voxelsize was reduced from 0.5 � 0.5 � 3.5 mm3 in the oldapproach down to 0.3 � 0.3 � 3.0 to 0.2 � 0.2 � 2.0mm3 in the new approach. The number of acquiredmultiple echo images increased from 4 to 8 in the oldapproach, to 45 to 144 in the new approach, providingmore detailed spectroscopic images. The improved im-age quality in UTESI is partly due to the higher fieldstrength (3.0T over 1.5T), and stronger gradient system(4.0 G/cm vs. 2.2 G/cm), as well as the increasedchemical shift difference between water and fat (440 Hzat 3.0T vs. 220 Hz at 1.5T) (39).

Normal collagen-containing structures such as thedeep layers of cartilage, meniscus, ligament, tendon,

and enthesis appear as signal voids on conventional MRpulse sequences, and exhibit signal only with increasedT2 relaxation times due to injury of degenerativechanges or magic angle effects (1–4). UTESI allows di-rect imaging and quantification of these short T2 tis-sues, thus providing a novel approach for detection ofearlier or more subtle changes.

UTESI has great potential for evaluating the short T2tissues in the MSK system. It provides excellent fatwater separation, producing water only images withhigh spatial resolution, as shown in Figs. 3–6. Conven-tional fat suppression techniques based on a 90° satu-ration pulse centered on fat resonance frequency typi-cally provide imperfect suppression of fat signals due toB1 inhomogeneity, as well as off-resonance due to B0

field inhomogeneity, shimming, and susceptibility.UTESI generates images at a series of resonance fre-quencies, therefore providing robust fat water separa-tion. UTESI allows short T2 imaging without long-T2suppression pulses that may partly saturate short T2signals. High contrast can be generated for short T2tissues, such as the deep layers of cartilage, at certainranges of off-resonance frequencies where water and fathave very low signal because of their long T2 and nar-row spectrum, while the short T2 tissues still haverelatively high signal because of their short T2 andbroad spectrum. However, efficient suppression of longT2 tissues is still helpful in increasing the dynamicrange since many short T2 tissues, especially corticalbone, have a proton density much lower than that of thesurrounding long T2 tissues, such as muscle and fat(27). The anti-aliasing property of radial sampling al-lows small FOV imaging without aliasing artifact, whichis another advantage of UTESI over the conventionalCartesian imaging. Furthermore, UTESI has potentialfor fat quantification since both fat and water spectraare generated for each voxel. The integration of the fatpeak and water gives an estimation of fat content aswell as fat distribution.

Figure 15. UTE spectroscopic imaging of theknee of a 30-year-old male volunteer in theoblique coronal plane shows excellent depic-tion of the lateral collateral ligament (short ar-row) and deep layers of articular cartilage (longarrow).

Table 1T2* Relaxation Times for the Deep Radial and Calcified Layers of Articular Cartilage, Menisci, Ligaments, Tendons, and EnthesesMeasured Through Line Shape Fitting of the Magnitude UTESI Spectra

TissuesDeep Radial and

CalcifiedCartilage

Menisci Ligaments Tendons Entheses

T2* (ms) 1.34 � 0.56 4.19 � 0.68 3.26 � 0.34 1.96 � 0.47 4.21 � 0.38

Ultrashort TE Spectroscopic Imaging 419

Table 1 shows quite a big variation in T2* quantifica-tion of the short T2 tissues in the MSK system, espe-cially for the deep layers of articular cartilage, which arevery thin (�100 �m) and subject to significant partialvolume effect. Magic angle effect further complicatesthe T2* measurement. Collagen fibers in menisci, liga-ments, tendons, and entheses are highly ordered. Theprotons within the bound water are subject to dipolarinteractions whose strength depends on the orientationof the fibers to the static magnetic field B0. These dipo-lar interactions cause a rapid dephasing of the MRsignal, and are dependent on 3cos2�-1, where � is theangle of the fibers relative to B0. When 3cos2�-1 � 0, or� � 55°, 125°, etc, dipolar interactions are minimized,resulting in an increase of T2 as well as MR signal.Fullerton et al (40) reported an increase in T2 of Achillestendon from 0.6 at 0° to B0 to 22 msec at 55°. Henkel-man et al (41) described an increase from 7 to 23 msecwhen the orientation of the tendon to B0 was changedfrom 0° to 55°. All these studies were performed on asmall bore spectrometer using small tendon samples.UTESI sequence is able to depict signal from short T2tissues, enabling magic angle imaging and quantifica-tion of the whole knee of cadaveric sample or healthyvolunteers/patients on a clinical system. Our next stepwill focus on a systematic study of the magic angleeffect using UTESI, and measure their baseline T2*values (at 0°C).

One of the major technical challenges for UTESI isrelated to gradient distortion (34–36). UTE sequencesemploy two half pulse excitations with opposite sliceselective gradient polarities (33,42). Distortion in sliceselection gradient results in slice profile broadening.The double half pulse scheme employed here improvesthe slice profile for long T2 tissues, but the short T2tissues still suffer from slice profile broadening (32).Distortion in readout gradients results in sampling tra-jectory errors, leading to suboptimal image reconstruc-tion. Errors can be reduced by measuring the sliceselection gradient followed by precompensation, andmeasuring the readout gradient and using it for regrid-ding (34–36).

There are some Gibbs ring artifacts in the UTE spec-trum, which can be suppressed by applying a temporalfilter. MR spectroscopy typically employs a Hanningfiltering and zero filling before FFT in the time domain,which is effective in improving the perceived spectralresolution and reducing noise level. However, Hanningfiltering also affects the spectral line shape, thereforeintroducing some errors in T2 estimation based on lineshape fitting. We did not therefore apply any temporalfiltering. Furthermore, signal from short T2 tissues de-cays very rapidly. UTESI appears to be less affected byGibbs ringing than long T2 spectroscopic imaging. Fig-ure 12 confirms that the Gibbs ringing artifacts do notsignificantly affect the accuracy in T2 quantification.The UTESI technique is also able to estimate T2 of longT2 tissues, such as these from the superficial layers ofcartilage. But a longer TE delay or more echoes aredesirable for more accurate estimation. A conventionalpulse sequence may be more suitable since ultrashortTE based on half pulse excitation is not necessary forlong T2 tissues, and thus eliminates the scan time

penalty due to two NEX acquisitions associated withhalf pulse excitation.

In conclusion, spectroscopic imaging of the short T2tissues in the MSK system can be generated using thenovel UTESI sequence, which employs a multislice mul-tiecho UTE acquisition combined with an interleavedvariable TE acquisition scheme. This technique pro-vides images with high spatial resolution and moderatespectral resolution, together with T2* estimation androbust fat water separation in a single scan.

ACKNOWLEDGMENT

The authors thank Graeme Bydder for helpful discus-sion.

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