UTE MRI of Tendons, Ligaments & Meniscus
Akshay Chaudhari1

1Stanford University, United States

Synopsis

Tissues in the musculoskeletal system such as menisci, tendons, and ligaments typically have short-T2 relaxation times, which makes imaging them with high signal-to-noise (SNR) ratio challenging. This presentation covers novel concepts based on the development of ultrashort echo time (UTE) sequences to image and quantify potential biomarkers of disease activity in these short-T2 tissues. A brief description of the potential biomarkers that can be acquired with UTE sequences is provided along with a description of technical considerations important in practical implementation of these methods.

Introduction

Tissues in the musculoskeletal system comprise of a multitude of MRI relaxation parameters due to variations in hydration levels and the extent and orientation of the collagen and proteoglycan content. Such tissues, namely the articular cartilage, menisci, tendons, and ligaments are of particular interest because of their potential role in diseases such as osteoarthritis (OA). While the articular cartilage has been extensively studied in the past, studying the menisci, tendons, and ligaments is challenging due to their short T2 relaxation time. Compared to articular cartilage which can have a relaxation of time of 30-40ms, the T2 relaxation time of the meniscus is approximately 10-12ms, that of tendons is approximately 5-6ms, and that of ligaments is between 5-10ms (1–5). Performing quantitative imaging of such tissues may be beneficial for evaluating potential biomarkers of OA activity.

Many conventional MRI sequences cannot generate an echo-time (TE) short enough to accurately characterize such tissues. As a result, there is interest in the development of pulse sequences that can produce ultrashort TE’s (UTE) of approximately less than 100μs in order to image and characterize the meniscus, tendons, and ligaments.

Objectives

The objective of this talk is to present an overview of performing UTE imaging in the musculoskeletal system. Specifically, this presentation will cover:

1. Understanding the acquisition of the UTE signal

2. Utilizing UTE sequences to generate potentially useful biomarkers in OA

3. Technical considerations in implementing UTE sequences

UTE Acquisition

Contrary to the acquisition of parallel lines in k-space that is common with Cartesian pulse sequences, UTE sequences typically acquire k-space information using non-Cartesian trajectories. Cartesian sequences utilize a dephaser gradient prior to data sampling, which requires a substantial duration before the center of k-space is acquired. In contrast, non-Cartesian trajectories start sampling directly from the center of k-space. As a result, the minimum achievable TE for UTE sequences is only limited by the switching of the radiofrequency electronics of the MRI scanner from transmit to receive mode, and is on the order of 10’s of microseconds. 2D non-Cartesian UTE sequences usually sample the k-space with spiral or radial trajectories, while 3D UTE sequences usually sample k-space with radial or cones trajectories (6–8).

Biomarkers with UTE Sequences

The primary benefit of utilizing UTE sequences is the additional SNR that they can provide for imaging short-T2 tissues such as the menisci, ligaments, and tendons. Since quantitative MRI parameters are extremely sensitive to variations in SNR, UTE sequences increase the opportunity to perform accurate and repeatable quantitative imaging.

Specifically, UTE sequences have primarily been used to measure T2, T2*, and T1ρ relaxation times for menisci, tendons, and ligaments. T2 and T2* are thought to correlate to hydration and collagen level in tissues, while T1ρ is thought to be sensitive to proteoglycan content. T2* measurements of the meniscus are amongst the most widely utilized quantitative MR parameter for short-T2 tissues. Increases in T2* of the meniscus in-vivo have been shown to indicate sub-clinical meniscal degeneration, changes in the meniscus following joint injuries, and sensitivity to zonal variations in the meniscus structure in vitro, all using 3D UTE cones readouts (9–11). Measurement of T2* relaxation times of the tendons has similarly been shown to vary during loading cycles, during varying physical activity, and in patients with patellar tendinopathy (12–14).

While T2* can be measured with multi-echo gradient echo sequences, measurement of T2 is typically limited to spin-echo-type sequences that refocus magnetic field inhomogeneities. However, this refocusing increases the TE of the acquisitions, which lowers the image SNR and makes it challenging to accurately measure tissue T2. In such cases, pulse sequences such as UTE double-echo steady-state (UTEDESS) have been used to measure the T2 of tendons, ligaments, and menisci while simultaneously producing multi-contrast and isotropic resolution images (3,15).

Recent developments have also expanded to include the use of T1ρ in UTE sequences. 3D UTE cones sequences have been utilized to measure the T1ρ of cartilage, menisci, tendons, and ligaments in a single acquisition in healthy volunteers(16,17). It should be noted that UTE methods are not strictly required for measuring meniscus T2 and T1ρ, and that Cartesian methods have also been used previously (18–20). However, such Cartesian methods may be more sensitive to image SNR, which could be a consideration in choosing optimal sequences for short-T2 biomarker quantification (4,21).

In addition to modeling tissues undergoing relaxation as a monoexponential decay, UTE sequences have been used to treat the signal from a single voxel as a signal that is undergoing biexponential decay (12,22–24). In such scenarios where there is a fast-decaying component along with a slow-decaying component, the presence a UTE echo (or a TE around 1ms) is beneficial to accurately characterize the fast-decaying component.

Additional biomarkers such as UTE magnetization transfer and delayed gadolinium enhanced magnetic resonance imaging may also be beneficial for musculoskeletal applications (25,26).

Technical Considerations

With quantitative measurements of short-T2 tissues, careful tuning of sequence parameters is necessary in order to overcome inherent SNR limitations. Even simple operations such as coil-combination for multi-channel data and fat saturation methods may bias quantitative measurements (3,27). The duration of spin-lock pulses can also affect quantitative T1ρ measurements, so comparisons between different studies should take into account sequence variations. Intrinsic effects such as magic angle can also affect quantification of T2 and T1ρ values spatially, depending on the orientation of the tissue to that of the main magnetic field (28,29). While UTE sequences provide a considerable TE shortening, the non-Cartesian acquisitions have to contend with gradient timing delays, eddy currents, and long reconstruction durations (30,31). Additional technical details can be found in previous review articles (32,33).

Conclusion

The development of new UTE methods has enabled imaging and quantification of tissues with short-T2 relaxation times in the musculoskeletal system. With careful planning of sequence parameters and processing of the raw-data, a variety of biomarkers can now be obtained, which makes it important to implement such methods clinically and in research studies to evaluate their true utility in detecting pathologies.

Acknowledgements

No acknowledgement found.

References

1. Trattnig S, Mamisch TC, Welsch GH, Glaser C, Szomolanyi P, Gebetsroither S, Stastny O, Horger W, Millington S, Marlovits S. Quantitative T2 mapping of matrix-associated autologous chondrocyte transplantation at 3 Tesla: an in vivo cross-sectional study. Invest Radiol 2007;42:442–448. doi: 10.1097/01.rli.0000262088.67368.49.

2. Baum T, Joseph GB, Karampinos DC, Jungmann PM, Link TM, Bauer JS. Cartilage and meniscal T2 relaxation time as non-invasive biomarker for knee osteoarthritis and cartilage repair procedures. Osteoarthritis Cartilage 2013;21:1474–84. doi: 10.1016/j.joca.2013.07.012.

3. Chaudhari AS, Sveinsson B, Moran CJ, McWalter EJ, Johnson EM, Zhang T, Gold GE, Hargreaves BA. Imaging and T2 relaxometry of short-T2 connective tissues in the knee using ultrashort echo-time double-echo steady-state (UTEDESS). Magn. Reson. Med. 2017;78:2136–2148. doi: 10.1002/mrm.26577.

4. Chaudhari AS, Black MS, Eijgenraam S, Wirth W, Maschek S, Sveinsson B, Eckstein F, Oei EHG, Gold GE, Hargreaves BA. Five-minute knee MRI for simultaneous morphometry and T2 relaxometry of cartilage and meniscus and for semiquantitative radiological assessment using double-echo in steady-state at 3T. J. Magn. Reson. Imaging 2017. doi: 10.1002/jmri.25883.

5. Zarins ZA, Bolbos RI, Pialat JB, Link TM, Li X, Souza RB, Majumdar S. Cartilage and meniscus assessment using T1rho and T2 measurements in healthy subjects and patients with osteoarthritis. Osteoarthr. Cartil. 2010;18:1408–1416. doi: 10.1016/j.joca.2010.07.012.

6. Kijowski R, Blankenbaker DG, Klaers JL, Shinki K, De Smet AA, Block WF. Vastly undersampled isotropic projection steady-state free precession imaging of the knee: diagnostic performance compared with conventional MR. Radiology 2009;251:185–194. doi: 10.1148/radiol.2511081133.

7. Gurney PT, Hargreaves B a, Nishimura DG. Design and analysis of a practical 3D cones trajectory. Magn. Reson. Med. 2006;55:575–82. doi: 10.1002/mrm.20796.

8. Qian Y, Boada FE. Acquisition-weighted stack of spirals for fast high-resolution three-dimensional ultra-short echo time MR imaging. Magn. Reson. Med. 2008;60:135–45. doi: 10.1002/mrm.21620.

9. Chu CR, Williams AA, West R V, Qian Y, Fu FH, Do BH, Bruno S. Quantitative Magnetic Resonance Imaging UTE-T2* Mapping of Cartilage and Meniscus Healing After Anatomic Anterior Cruciate Ligament Reconstruction. Am. J. Sports Med. 2014;42:1847–56. doi: 10.1177/0363546514532227.

10. Williams a., Qian Y, Golla S, Chu CR. UTE-T2* mapping detects sub-clinical meniscus injury after anterior cruciate ligament tear. Osteoarthr. Cartil. 2012;20:486–494. doi: 10.1016/j.joca.2012.01.009.

11. Koff MF, Shah P, Pownder S, Romero B, Williams R, Gilbert S, Maher S, Fortier LA, Rodeo SA, Potter HG. Correlation of meniscal T2* with multiphoton microscopy, and change of articular cartilage T2 in an ovine model of meniscal repair. Osteoarthr. Cartil. 2013;21:1083–91. doi: 10.1016/j.joca.2013.04.020.

12. Kijowski R, Wilson JJ, Liu F. Bicomponent ultrashort echo time T2* analysis for assessment of patients with patellar tendinopathy. J. Magn. Reson. Imaging 2017;46:1441–1447. doi: 10.1002/jmri.25689.

13. Chang EY, Du J, Iwasaki K, Biswas R, Statum S, He Q, Bae WC, Chung CB. Single- and Bi-component T2* analysis of tendon before and during tensile loading, using UTE sequences. J. Magn. Reson. Imaging 2015;42:114–20. doi: 10.1002/jmri.24758.

14. Grosse U, Springer F, Hein T, Grözinger G, Schabel C, Martirosian P, Schick F, Syha R. Influence of physical activity on T1 and T2* relaxation times of healthy Achilles tendons at 3T. J. Magn. Reson. Imaging 2015;41:193–201. doi: 10.1002/jmri.24525.

15. Sveinsson B, Chaudhari A, Gold G, Hargreaves B. A simple analytic method for estimating T2 in the knee from DESS. Magn. Reson. Imaging 2017;38:63–70. doi: 10.1016/j.mri.2016.12.018.

16. Ma Y-J, Carl M, Searleman A, Lu X, Chang EY, Du J. 3D adiabatic T1ρprepared ultrashort echo time cones sequence for whole knee imaging. Magn. Reson. Med. 2018. doi: 10.1002/mrm.27131.

17. Ma Y-J, Carl M, Shao H, Tadros AS, Chang EY, Du J. Three-dimensional ultrashort echo time cones T1ρ(3D UTE-cones-T1ρ) imaging. NMR Biomed. 2017;30. doi: 10.1002/nbm.3709.

18. Stehling C, Luke A, Stahl R, Baum T, Joseph G, Pan J, Link TM. Meniscal T1rho and T2 measured with 3.0T MRI increases directly after running a marathon. Skelet. Radiol 2011;40:725–735. doi: 10.1007/s00256-010-1058-2.

19. Rauscher I, Stahl R, Cheng J, Li X, Huber MB, Luke A, Majumdar S, Link TM. Meniscal measurements of T1rho and T2 at MR imaging in healthy subjects and patients with osteoarthritis. Radiology 2008;249:591–600. doi: 10.1148/radiol.2492071870.

20. Knox J, Pedoia V, Wang A, Tanaka M, Joseph GB, Neumann J, Link TM, Li X, Ma CB. Longitudinal changes in MR T1ρ/T2 signal of meniscus and its association with cartilage T1p/T2 in ACL-injured patients. Osteoarthr. Cartil. 2018. doi: 10.1016/j.joca.2018.02.001.

21. Raya JG, Dietrich O, Horng A, Weber J, Reiser MF, Glaser C. T2 measurement in articular cartilage: impact of the fitting method on accuracy and precision at low SNR. Magn Reson Med 2010;63:181–193. doi: 10.1002/mrm.22178.

22. Juras V, Apprich S, Zbyn S, Zak L, Deligianni X, Szomolanyi P, Bieri O, Trattnig S. Quantitative MRI analysis of menisci using biexponential T2* fitting with a variable echo time sequence. Magn Reson Med 2014;71:1015–1023. doi: 10.1002/mrm.24760.

23. Juras V, Apprich S, Szomolanyi P, Bieri O, Deligianni X, Trattnig S. Bi-exponential T2 analysis of healthy and diseased Achilles tendons: an in vivo preliminary magnetic resonance study and correlation with clinical score. Eur Radiol 2013;23:2814–2822. doi: 10.1007/s00330-013-2897-8.

24. Liu F, Kijowski R. Assessment of different fitting methods forin-vivobi-component T2*analysis of human patellar tendon in magnetic resonance imaging. Muscles. Ligaments Tendons J. 7:163–172. doi: 10.11138/mltj/2017.7.1.163.

25. Krishnan N, Shetty SK, Williams A, Mikulis B, McKenzie C, Burstein D. Delayed gadolinium-enhanced magnetic resonance imaging of the meniscus: an index of meniscal tissue degeneration? Arthritis Rheum. 2007;56:1507–11. doi: 10.1002/art.22592.

26. Ma Y-J, Chang EY, Carl M, Du J. Quantitative magnetization transfer ultrashort echo time imaging using a time-efficient 3D multispoke Cones sequence. Magn. Reson. Med. 2018;79:692–700. doi: 10.1002/mrm.26716.

27. Carl M, Nazaran A, Bydder GM, Du J. Effects of fat saturation on short T2 quantification. Magn. Reson. Imaging 2017;43:6–9. doi: 10.1016/j.mri.2017.06.007.

28. Xia Y. Magic-angle effect in magnetic resonance imaging of articular cartilage: a review. Invest Radiol 2000;35:602–621.

29. Shao H, Pauli C, Li S, Ma Y, Tadros AS, Kavanaugh A, Chang EY, Tang G, Du J. Magic angle effect plays a major role in both T1rho and T2 relaxation in articular cartilage. Osteoarthr. Cartil. 2017;25:2022–2030. doi: 10.1016/j.joca.2017.01.013.

30. Brodsky EK, Klaers JL, Samsonov AA, Kijowski R, Block WF. Rapid measurement and correction of phase errors from B0 eddy currents: impact on image quality for non-Cartesian imaging. Magn. Reson. Med. 2013;69:509–15. doi: 10.1002/mrm.24264.

31. Atkinson IC, Lu A, Thulborn KR. Characterization and correction of system delays and eddy currents for MR imaging with ultrashort echo-time and time-varying gradients. Magn. Reson. Med. 2009;62:532–7. doi: 10.1002/mrm.22016.

32. Robson MD, Gatehouse PD, Bydder M, Bydder GM. Magnetic resonance: an introduction to ultrashort TE (UTE) imaging. J Comput Assist Tomogr 2003;27:825–846.

33. Tyler DJ, Robson MD, Henkelman RM, Young IR, Bydder GM. Magnetic resonance imaging with ultrashort TE (UTE) PULSE sequences: technical considerations. J. Magn. Reson. Imaging 2007;25:279–89. doi: 10.1002/jmri.20851.

Proc. Intl. Soc. Mag. Reson. Med. 26 (2018)