Saeed Jerban1, Michael Song2, Amir M Afsahi1, Dina Moazamian1, Michael Carl2, Yajun Ma1, Alecio Lombardi1, Christine B Chung1, Eric Y Chang1,3, and Jiang Du1
1Department of Radiology, University of California, San Diego, San Diego, CA, United States, 2General Electric Healthcare, San Diego, CA, United States, 3Radiology Service, VA San Diego Healthcare System, San Diego, CA, United States
Synopsis
High susceptibility levels at the marrow/bone
interface may significantly reduce T2* of marrow, leading to trabecular bone
volume overestimation when imaged using conventional MRI sequences. The
presence of fat in bone marrow further complicates trabecular bone imaging due
to chemical shift artifacts. In this study, an ultrashort echo time MRI
(UTE-MRI) technique focused on the fat peak frequency was investigated to image
trabecular bone ex vivo and in vivo. This technique was shown to improve trabecular
bone imaging by minimizing chemical shift artifacts as well as susceptibility
related short T2* effects, thereby providing more accurate estimation of
trabecular bone structure.
INTRODUCTION
Bone has an extremely short apparent
transverse relaxation time (T2*) and is typically rendered “invisible” when imaged
using conventional pulse sequences with echo times (TEs) of a few milliseconds (1). High resolution MRI (e.g., voxel
size~0.2mm) can indirectly visualize trabecular bone as dark regions surrounded
by marrow. With data post-processing, it is possible to obtain the 3D
architecture of trabecular bone (2). Such visualization has been used to
track bone structure changes in response to medical treatments (3–5) as well as for finite element
analysis-driven mechanical competence assessment (6).
High
susceptibility at the marrow/bone interface together with multiple fat peaks may
significantly reduce marrow T2*, resulting in trabecular bone volume
overestimation. Ultrashort echo time MRI (UTE-MRI) allows acquiring signals from
tissues with short T2* such as bone and its neighboring marrow, which could potentially
avoid bone volume overestimation. However, UTE-MRI is sensitive to chemical
shift artifacts, which may lead to strong spatial blurring of bone structures. Alternatively,
MR imaging at the fat peak frequency is hypothesized to minimize marrow-related
chemical shift artifacts. Bone is expected to be off-resonance in fat-centered
imaging. However, bone signal, while detectable with UTE-MRI, is much lower than
marrow signal due to its low proton density and short T2*, leading to
negligible water-associated off-resonance artifact. This study aimed to investigate
the feasibility of using UTE-MRI at the fat peak frequency for more accurate
depiction of the trabecular bone structure in the human calcaneus ex vivo and
in vivo at 3T.METHODS
Ex
vivo study: Whole ankle specimens and sectioned distal
tibial samples (n=11) were scanned at room temperature on a 3T clinical scanner
(MR750, GE Healthcare Technologies, WI). The following four 3D MR sequences
were performed: 1) 3D gradient echo (GRE) sequence (TR=20, TE=4.4 ms) at the
water peak frequency; 2) 3D-UTE-Cones sequence (TR=7.6, TE=0.032 ms) at the
water peak frequency; 3) 3D-UTE-Cones sequence (TR=7.6, TE=0.032 ms) at the fat
peak frequency; and 4) 3D-UTE-Cones at the fat peak frequency with five
different TEs (TE=0.032, 1.1, 2.2, 3.3, 4.4 ms). Typical imaging parameters
included: Field-of-view (FOV)=8 cm, acquisition matrix=384×384, slice thickness=0.6mm,
voxel size=0.2×0.2×0.6mm3, slices=84-160, scan time=5-10 minutes, respectively.
In vivo study: The ankle
of a 43-year-old man was scanned using
the setup described above, with only minor differences to shorten the scan time
by limiting the number of slices to 84 with a slice thickness of 1mm.
Zero-interpolation was used during image reconstruction, resulting in a
reconstructed nominal voxel size of 0.2×0.2×0.5 mm3 under 5.5
minutes scan time.Results
Figure
1 shows high-resolution imaging of a sectioned distal tibia sample. Strong
chemical shift artifacts were observed in 3D-UTE-Cones imaging at the water
peak, leading to obscured trabecular structures within the sample. In contrast,
3D-UTE-Cones imaging at the fat peak shows high signal for marrow fat, with excellent
depiction of trabecular bone structures. Longer TEs led to more signal loss in
marrow fat, likely due to the susceptibility-related T2* shortening. 3D-GRE
sequence showed excellent depiction of marrow fat, but with more signal loss
compared with the UTE-Cones images at the water peak.
Figure
2 shows 3D-UTE-Cones and GRE imaging of a whole ankle specimen from a
65-year-old male donor. UTE-Cones at the water peak shows strong chemical shift
artifacts (red arrows), which are greatly reduced in UTE-Cones imaging at the
fat peak. The clinical GRE sequence showed excellent contrast, but with obvious
trabecular bone overestimation. Figure 3 shows 3D-UTE-Cones imaging of the same
whole ankle specimen at different TEs, again with more marrow signal loss at
longer TEs.
Figure
4 demonstrates in vivo calcaneal trabecular bone images of a 43-year-old male
volunteer. Trabeculae were seen with higher contrast in images acquired at the
fat peak frequency and greater marrow signal loss was observed in images
acquired at longer TEs.DISCUSSION
The
feasibility of the UTE-MRI sequence at the fat peak frequency in trabecular
bone imaging was examined ex vivo and in vivo. The 3D-UTE-Cones sequence at the
fat peak frequency improved the contrast in visualizing the trabeculae while minimizing
the fat-to-water chemical shift artifact. Potential chemical shift artifact from
bone (off-resonance in fat-centered imaging) was not observed due to the low
proton density of water in bone. Bone volume was apparently higher in images
performed at higher TEs, likely due to the marrow’s shortened T2* caused by the
susceptibility phenomenon at the marrow/bone interface. More accurate depiction
of trabecular bone structure also allows more reliable finite element analysis
of its mechanical properties. Nevertheless, the accuracy of the visualized bone
volume needs to be investigated in future studies comparing MRI and microcomputed tomography data. CONCLUSION
The proposed UTE-Cones
sequence at the fat peak frequency was shown to improve trabecular bone imaging
by enhancing the contrast between bone and marrow, in addition to avoiding the
potential bone overestimation caused by chemical shift artifacts and the high
level of susceptibility at the marrow-bone interface.Acknowledgements
The authors acknowledge grant support from the NIH
(R01AR068987, R01AR062581, and R01AR075825), Veterans Affairs
(I01RX002604 and I01CX001388), and GE Healthcare. References
1. Du J, Bydder GM.
Qualitative and quantitative ultrashort-TE MRI of cortical bone. NMR Biomed.
2013;26:489–506 doi: 10.1002/nbm.2906.
2. Wehrli FW, Song HK, Saha PK, Wright AC. Quantitative MRI for the
assessment of bone structure and function. NMR Biomed. 2006;19:731–764 doi:
10.1002/nbm.
3. Zhang XH, Liu XS, Vasilic B, et al. In vivo μMRI-based finite element
and morphological analyses of tibial trabecular bone in eugonadal and
hypogonadal men before and after testosterone treatment. J. Bone Miner. Res.
2008;23:1426–1434 doi: 10.1359/jbmr.080405.
4. Wehrli FW, Rajapakse CS, Magland JF, Snyder PJ. Mechanical implications
of estrogen supplementation in early postmenopausal women. J. Bone Miner. Res.
2010;25:1406–1414 doi: 10.1002/jbmr.33.
5. Rajapakse CS, Leonard MB, Bhagat YA, Sun W, Magland JF, Wehrli FW.
Micro-MR imaging-based computational biomechanics demonstrates reduction in
cortical and trabecular bone strength after renal transplantation. Radiology
2012;262:912–920 doi: 10.1148/radiol.11111044.
6. Rajapakse CS, Kobe EA, Batzdorf AS, Hast MW, Wehrli FW. Accuracy of
MRI-based finite element assessment of distal tibia compared to mechanical
testing. Bone 2018;108:71–78 doi: 10.1016/j.bone.2017.12.023.
7. Liney GP, Bernard CP, Manton DJ, Turnbull LW, Langton CM. Age, gender,
and skeletal variation in bone marrow composition: A preliminary study at 3.0
Tesla. J. Magn. Reson. Imaging 2007;26:787–793 doi: 10.1002/jmri.21072.
8. Du J, Chiang AJT, Chung CB, et al. Orientational analysis of the
Achilles tendon and enthesis using an ultrashort echo time spectroscopic
imaging sequence. Magn. Reson. Imaging 2010;28:178–184 doi: 10.1016/j.mri.2009.06.002.
9. Du J, Carl M, Bydder M, Takahashi A, Chung CB, Bydder GM. Qualitative
and quantitative ultrashort echo time (UTE) imaging of cortical bone. J. Magn.
Reson. 2010;207:304–311 doi: 10.1016/j.jmr.2010.09.013
10. Ma YJ, Zhu Y, Lu X, Carl M, Chang EY, Du J. Short T 2 imaging using a
3D double adiabatic inversion recovery prepared ultrashort echo time cones (3D
DIR-UTE-Cones) sequence. Magn. Reson. Med. 2017;00:1–9 doi: 10.1002/mrm.26908.
11. Ma Y, Shao H, Du J, Chang EY. Ultrashort echo time magnetization
transfer (UTE-MT) imaging and modeling: magic angle independent biomarkers of
tissue properties. NMR Biomed. 2016;29:1546–1552 doi: 10.1002/nbm.3609.
12. Ma Y, Lu X, Carl M, et al. Accurate T 1 mapping of short T 2 tissues
using a three-dimensional ultrashort echo time cones actual flip angle
imaging-variable repetition time (3D UTE-Cones AFI-VTR) method. Magn. Reson.
Med. 2018;80:598–608 doi: 10.1002/mrm.27066.