Correlation of Mono-exponential and Bi-exponential UTE-T2* Analyses and Biomechanics in Human Achilles Tendons
Eric Y Chang1,2, Robert M Healey3, Reni Biswas2, Sheronda Statum2, Betty Tran2, Kenyu Iwasaki4, Jiang Du2, Won C Bae2, and Christine B Chung1,2

1Radiology Service, VA San Diego Healthcare System, San Diego, CA, United States, 2Department of Radiology, University of California, San Diego Medical Center, San Diego, CA, United States, 3Department of Orthopaedic Surgery, University of California, San Diego Medical Center, San Diego, CA, United States, 4Department of Orthopaedic Surgery, Kyushu University, Fukuoka, Japan

Synopsis

In this pilot study, we sought to determine if mono-exponential T2, mono-exponential UTE-T2*, or bi-exponential UTE-T2* correlated with biomechanical properties in human Achilles tendons. We found very high and significant correlation coefficients between mono-exponential T2* (rho = 0.90, p = 0.002) and bi-exponential T2* fractions (rho = -0.97, p < 0.001) obtained using the UTE-Cones sequence and ultimate tensile strain. Ultimate tensile strain represents the percentage change in tendon length prior to failure and high strains have been previously associated with tendon degeneration. Our results suggest that non-invasive MRI of the Achilles tendon may serve as a surrogate measure.

Purpose

To determine if mono-exponential T2, mono-exponential UTE-T2*, or bi-exponential UTE-T2* correlate with biomechanical properties in human Achilles tendons.

Materials and Methods

Samples: Five human cadaveric ankles (donor age 81 ± 16.5 years, mean ± standard deviation) were used for this study.

Protocol: Whole, intact Achilles tendons were scanned on a 3T clinical scanner (Discovery MR 750; GE Healthcare, Milwaukee, WI) using an 8-channel transmit-receive extremity coil with tendon orientation parallel to B0. Our quantitative MR protocol consisted of a 2D-CPMG sequence (TR = 2000 ms, TE = 10, 20, 30, 40, 50, 60, 70, 80 ms, FOV 10 cm, matrix = 320 x 256, slice thickness = 1 mm, scan time ~8.5 min per tendon, Fig 1A) and 5 sets of an isotropic, dual-echo 3D-UTE-Cones sequence covering 10 echoes (TR = 20 ms, TE = 0.03, 0.1, 0.2, 0.4, 0.6, 0.8, 2, 4, 10, 15, 20, 30 ms, FOV 10 cm, matrix = 168 x 168, slice thickness 0.6 mm, scan time ~5 min per set/~25 min per tendon, Fig 1B). Thereafter 15 cm of Achilles tendons were dissected with the calcaneal attachment maintained. The tendons were bluntly separated along physiologic planes when possible, yielding anterior (soleus) and posterior (gastrocnemius) halves (Fig 1C). Dissected tendons were then imaged using an isotropic 3D-FSE sequence (0.4 mm3) from which cross-sectional area measurements were made for biomechanical analyses.

Image Analysis: Using mid-sagittal images, a fellowship trained musculoskeletal radiologist manually drew regions of interests over the entire tendon (global analysis) as well as the proximal, mid, and distal thirds of each tendon (regional analysis). Mono-exponential T2, mono-exponential UTE-T2*, and bi-exponential UTE-T2* values were calculated using a semi-automated MATLAB (The Mathworks Inc., Natick, MA) routine as previously described (Fig 1D-G)1.

Biomechanics: The calcanei were potted into a low melting point alloy (Cerrobend, Satterlee Co., Minneapolis, MN), allowing for bone fixation at an appropriate testing angle without heat damage during fixation. Tendons were marked at the surface using India ink and the proximal free end was freeze-clamped using liquid nitrogen cooled grips (Fig 2A) inside a material testing device (Instron model 1122; Norwood, MA). Tendons were preconditioned to reduce the effects of hysteresis before being tensilde loaded to failure. Multi-angle high definition recorded video was used for strain measurements and determination of the precise location of failure (Figs 2B-D). Ultimate tensile strain (%), ultimate tensile stress (MPa), elastic modulus (MPa) and energy to failure (J) were determined2.

Statistics: Descriptive statistics were calculated. Spearman correlation was performed between multi-parametric values and biomechanical measures using both global analysis values and regional analysis values at locations of failure.

Results

Eight separate halves were imaged and tested. For two Achilles tendons no physiologic plane was discernable between the soleus and gastrocnemius tendons at dissection and the Achilles was tested as a whole. Mean T2 value was 12.3 ± 4.8 ms and mean mono-exponential UTE-T2* value was 3.5 ± 2.0 ms. Mean short T2* was 2.2 ± 1.0 ms and mean short fraction was 85%. Mean tendon failure was 5.8 ± 3.1 cm above the center of the calcaneal insertion. Mean ultimate tensile strain was 14 ± 4%, mean ultimate tensile stress was 15.6 ± 6.6 MPa, mean elastic modulus was 113.4 ± 40 MPa, and mean energy to failure was 5473.1 ± 2916.7 J. Spearman correlations were significant for ultimate tensile strain and global mono-exponential UTE-T2* values (rho = 0.90, p = 0.002, Fig 3A), global short/long T2* fractions (rho = -0.97 and 0.97, respectively, p < 0.001, Fig 3B), and regional mono-exponential UTE-T2* values (rho = 0.93, p = 0.001). CPMG T2 demonstrated no significant correlations with biomechanical measures (p > 0.3). Stress, elastic modulus, and energy to failure demonstrated no significant correlations with MR measures (p > 0.2).

Discussion

In this pilot study, very high and significant correlation coefficients were seen between mono-exponential T2* and bi-exponential T2* fractions obtained using the UTE-Cones sequence and ultimate tensile strain. Ultimate tensile strain represents the percentage change in tendon length prior to failure and high strains have been previously associated with tendon degeneration3. Our results suggest that non-invasive MRI of the Achilles tendon may serve as a surrogate measure. Specifically, the larger the UTE-T2* value (positive correlation), the larger the long T2* fraction (positive correlation), or the smaller the short T2* fraction (negative correlation), the more deformation can occur in the tendon prior to failure.

Acknowledgements

The authors gratefully acknowledge funding from the VA Clinical Science R&D Service (Career Development Award-2, 5IK2CX000749).

References

(1) 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 Jul;42(1):114-20.

(2) Leek BT, Tasto JP, Tibor LM, Healey RM, Freemont A, Linn MS, Chase DE, Amiel D. Augmentation of tendon healing with butyric acid-impregnated sutures: biomechanical evaluation in a rabbit model. Am J Sports Med. 2012 Aug;40(8):1762-71.

(3) Jung HJ, Fisher MB, Woo SL. Role of biomechanics in the understanding of normal, injured, and healing ligaments and tendons. Sports Med Arthrosc Rehabil Ther Technol. 2009 May 20;1(1):9.

Figures

Fig 1. Imaging and Analysis of Achilles Tendons. (A) Spin-echo (TE 10 ms), (B) UTE-Cones (TE 0.03 ms), and (C) gross images of the Achilles tendon of a specimen. (D and E) Regional mono-exponential T2* and (F and G) bi-exponential T2* analyses of the mid-third of the anterior half of a tendon. Source images are of high quality and there is smaller residual signal using bi-exponential analysis.

Fig 2. Achilles Tensile Testing. (A) Image of testing apparatus with calcaneus potted into Cerrobend and proximal tendon freeze-clamped with liquid nitrogen cooled grips. (B-D) Images of specimens after failure, which occurred after up to 1605 N (361 pounds) of tensile force was applied.

Fig 3. Correlations Between Quantitative MRI and Biomechanics. (A) Very strong, positive correlation between mono-exponential T2* analysis and ultimate tensile strain (rho =0.90, p = 0.002). (B) Very strong, negative correlation between bi-exponential T2* fraction and ultimate tensile strain (rho = -0.97, respectively, p < 0.001).



Proc. Intl. Soc. Mag. Reson. Med. 24 (2016)
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