Magnetization Transfer in Human Achilles Tendon Assessed by a 3D Ultrashort Echo Time Sequence: Quantitative Examinations in Healthy Volunteers at 3T

Zusammenfassung

Ziel: Magnetisierungstransfer-Kontrast(MTC)-Bildgebung ermöglicht die Einsicht in die Interaktionen zwischen freiem und gebundenem Wasser. Neu entwickelte Ultrashort-echo-time(UTE)-Sequenzen für Ganzkörper-MRT erlauben MTC-Bildgebung in Gewebearten mit extrem schnellem Signalzerfall, wie Sehnen. Ziel dieser Studie war die Entwicklung einer Methodik, die es erlaubt, den MT-Effekt gesunder Achillessehnen in vivo bei 3 T quantitativ zu bestimmen. Material und Methoden: 16 gesunde Sehnen von Probanden ohne anamnestische Tendinopathie wurden mit einer 3-D-UTE-Sequenz mit einem rechteckförmigen On-Resonanz-Anregepuls und einem Fermi-förmigen Off-Resonanz-MT-Präparationspuls untersucht. Die Frequenz des MT-Pulses variierte von 1 bis 5 kHz. MT-Effekte wurden als MT-Ratio (MTR) zwischen Messungen mit und ohne MT-Präparation berechnet. Direkte Sättigungseffekte der MT-Präparation auf die Signalintensität wurden mit numerischen Simulationen der Blochgleichungen ermittelt. Ein Patient mit Tendinopathie wurde untersucht, um beispielhaft zu zeigen, wie sich die MTR verändert. Ergebnisse: Die Berechnung von MTR-Daten war in allen Fällen möglich und zeigte für die gesunden Probanden einen Abfall von 0,53 ± 0,05 auf 0,25 ± 0,03 (1 kHz bis 5 kHz). Die Untersuchung der Varianz bezüglich Geschlecht und Knöcheldominanz ergab keine signifikanten Differenz (p > 0,05). Hingegen zeigte der Tendinosepatient MTR-Werte zwischen 0,36 (1 kHz) und 0,19 (5 kHz). Schlussfolgerung: MT-Effekte in menschlichen Achillessehnen können zuverlässig in vivo mittels einer 3-D-UTE-Sequenz bei 3 T gemessen werden. Alle gesunden Sehnen zeigten ähnliche MTR-Werte (Variationskoeffizient 10,0 ± 1,2 %). Die untersuchten degenerierten Sehnen zeigten vermutlich aufgrund der veränderten Mikrostruktur bei Tendinopathie einen deutlich unterschiedlichen MT-Effekt.

Abstract

Purpose: Magnetization transfer contrast (MTC) imaging provides insight into interactions between free and bounded water. Newly developed ultrashort echo time (UTE) sequences implemented on whole-body magnetic resonance (MR) scanners allow MTC imaging in tissues with extremely fast signal decay such as tendons. The aim of this study was to develop a technique for the quantification of the MT effect in healthy Achilles tendons in-vivo at 3 Tesla. Materials and Methods: 16 normal tendons of volunteers with no history of tendinopathy were examined using a 3D-UTE sequence with a rectangular on-resonant excitation pulse and a Fermi-shaped off-resonant MT preparation pulse. The frequency of the MT pulse was varied from 1 to 5 kHz. MT effects were calculated in terms of the MT ratio (MTR) between measurements without and with MT preparation. Direct saturation effects of MT preparation on the signal intensity were evaluated using numerical simulation of Bloch equations. One patient with tendinopathy was examined to exemplarily show changes of MTR under pathologic conditions. Results: Calculation of MTR data was feasible in all examined tendons and showed a decrease from 0.53 ± 0.05 to 0.25 ± 0.03 (1 kHz to 5 kHz) for healthy volunteers. Evaluation of variation with gender and dominance of ankle revealed no significant differences (p > 0.05). In contrast, the patient with confirmed tendinopathy showed MTR values between 0.36 (1 kHz) and 0.19 (5 kHz). Conclusion: MT effects in human Achilles tendons can be reliably assessed in-vivo using a 3D UTE sequence at 3 T. All healthy tendons showed similar MTR values (coefficient of variation 10.0 ± 1.2 %). The examined patient showed a clearly different MT effect revealing a changed microstructure in the case of tendinopathy.

Key words

ankle - tendons - MR imaging - tissue characterization - magnetization transfer

References

• 1 Wolff S D, Balaban R S. Magnetization transfer contrast (MTC) and tissue water proton relaxation in vivo.  Magn Reson Med. 1989;  10 135-144
• 2 Balaban R S, Ceckler T L. Magnetization transfer contrast in magnetic resonance imaging.  Magn Reson Q. 1992;  8 116-137
• 3 Vahlensieck M, Traber F, Schild H. Magnetization transfer contrast imaging (MTC): its fundamentals, technics and applications [Review].  Fortschr Röntgenstr. 1998;  169 3-10
• 4 Henkelman R M, Stanisz G J, Graham S J. Magnetization transfer in MRI: a review.  NMR Biomed. 2001;  14 57-64
• 5 Petrella J R, Grossman R I, McGowan J C et al. Multiple sclerosis lesions: relationship between MR enhancement pattern and magnetization transfer effect.  AJNR Am J Neuroradiol. 1996;  17 1041-1049
• 6 Runge V M, Wells J W, Williams N M et al. Detectability of early brain meningitis with magnetic resonance imaging.  Invest Radiol. 1995;  30 484-495
• 7 Schick F, Stern W, Forster J et al. Magnetization transfer contrast of hepatic lesions in breath-hold gradient-echo images of different T 1 weighting.  J Magn Reson Imaging. 1997;  7 280-285
• 8 Vahlensieck M, Gieseke J, Traber F et al. Magnetization transfer contrast (MTC) – which is the most MTC-sensitive MRI sequence?.  Fortschr Röntgenstr. 1998;  169 195-197
• 9 Horng A, Raya J, Zscharn M et al. Locoregional deformation pattern of the patellar cartilage after different loading types – high-resolution 3D-MRI volumetry at 3T in-vivo.  Fortschr Röntgenstr. 2011;  183 432-440
• 10 Du J, Pak B C, Znamirowski R et al. Magic angle effect in magnetic resonance imaging of the Achilles tendon and enthesis.  Magn Reson Imaging. 2009;  27 557-564
• 11 Hayes C W, Parellada J A. The magic angle effect in musculoskeletal MR imaging.  Top Magn Reson Imaging. 1996;  8 51-56
• 12 Li T, Mirowitz S A. Manifestation of magic angle phenomenon: comparative study on effects of varying echo time and tendon orientation among various MR sequences.  Magn Reson Imaging. 2003;  21 741-744
• 13 Du J, Chiang A J, Chung C B et al. Orientational analysis of the Achilles tendon and enthesis using an ultrashort echo time spectroscopic imaging sequence.  Magn Reson Imaging. 2009;  28 178-184
• 14 Gatehouse P D, Thomas R W, Robson M D et al. Magnetic resonance imaging of the knee with ultrashort TE pulse sequences.  Magn Reson Imaging. 2004;  22 1061-1067
• 15 Robson M D, Bydder G M. Clinical ultrashort echo time imaging of bone and other connective tissues.  NMR Biomed. 2006;  19 765-780
• 16 Robson M D, Gatehouse P D, Bydder M et al. Magnetic resonance: an introduction to ultrashort TE (UTE) imaging.  J Comput Assist Tomogr. 2003;  27 825-846
• 17 Adler R S, Swanson S D, Doi K et al. The effect of magnetization transfer in meniscal fibrocartilage.  Magn Reson Med. 1996;  35 591-595
• 18 Paavola M, Kannus P, Jarvinen T A et al. Achilles tendinopathy.  J Bone Joint Surg Am. 2002;  84-A 2062-2076
• 19 Riley G. The pathogenesis of tendinopathy. A molecular perspective.  Rheumatology. 2004;  43 131-142
• 20 Ceckler T L, Balaban R S. Field dispersion in water-macromolecular proton magnetization transfer.  J Magn Reson B. 1994;  105 242-248
• 21 Springer F, Martirosian P, Machann J et al. Magnetization transfer contrast imaging in bovine and human cortical bone applying an ultrashort echo time sequence at 3 Tesla.  Magn Reson Med. 2009;  61 1040-1048
• 22 Astrom M, Gentz C F, Nilsson P et al. Imaging in chronic achilles tendinopathy: a comparison of ultrasonography, magnetic resonance imaging and surgical findings in 27 histologically verified cases.  Skeletal Radiol. 1996;  25 615-620
• 23 Fornage B D, Rifkin M D. Ultrasound examination of tendons.  Radiol Clin North Am. 1988;  26 87-107
• 24 Gibbon W W, Cooper J R, Radcliffe G S. Distribution of sonographically detected tendon abnormalities in patients with a clinical diagnosis of chronic achilles tendinosis.  J Clin Ultrasound. 2000;  28 61-66
• 25 Grassi W, Filippucci E, Farina A et al. Sonographic imaging of tendons.  Arthritis Rheum. 2000;  43 969-976
• 26 Hartgerink P, Fessell D P, Jacobson J A et al. Full- versus partial-thickness Achilles tendon tears: sonographic accuracy and characterization in 26 cases with surgical correlation.  Radiology. 2001;  220 406-412
• 27 Maffulli N. Rupture of the Achilles tendon.  J Bone Joint Surg Am. 1999;  81 1019-1036
• 28 Maffulli N, Waterston S W, Squair J et al. Changing incidence of Achilles tendon rupture in Scotland: a 15-year study.  Clin J Sport Med. 1999;  9 157-160
• 29 Pang B S, Ying M. Sonographic measurement of achilles tendons in asymptomatic subjects: variation with age, body height, and dominance of ankle.  J Ultrasound Med. 2006;  25 1291-1296
• 30 Halasi T, Kynsburg A, Tallay A et al. Development of a new activity score for the evaluation of ankle instability.  Am J Sports Med. 2004;  32 899-908
• 31 Chen T M, Rozen W M, Pan W R et al. The arterial anatomy of the Achilles tendon: anatomical study and clinical implications.  Clin Anat. 2009;  22 377-385
• 32 Ohberg L, Lorentzon R, Alfredson H. Eccentric training in patients with chronic Achilles tendinosis: normalised tendon structure and decreased thickness at follow up.  Br J Sports Med. 2004;  38 8-11 ; discussion
• 33 Springer F, Steidle G, Martirosian P et al. Effects of in-pulse transverse relaxation in 3D ultrashort echo time sequences: analytical derivation, comparison to numerical simulation and experimental application at 3 T.  J Magn Reson. 2010;  206 88-96
• 34 Oatridge A, Herlihy A H, Thomas R W et al. Magnetic resonance: magic angle imaging of the Achilles tendon.  Lancet. 2001;  358 1610-1611
• 35 Allen G M, Wilson D J. Ultrasound in sports medicine – a critical evaluation.  Eur J Radiol. 2007;  62 79-85
• 36 Khan K M, Forster B B, Robinson J et al. Are ultrasound and magnetic resonance imaging of value in assessment of Achilles tendon disorders? A two year prospective study.  Br J Sports Med. 2003;  37 149-153
• 37 Weber C, Wedegartner U, Maas L C et al. MR Imaging of the Achilles Tendon: Evaluation of Criteria for the Differentiation of Asymptomatic and Symptomatic Tendons.  Fortschr Röntgenstr. 2011;  183 631-640
• 38 Rominger M B, Bachmann G, Schulte S et al. Value of ultrasound and magnetic resonance imaging in the control of the postoperative progress after Achilles tendon rupture.  Fortschr Röntgenstr. 1998;  168 27-35
• 39 Rees J D, Wilson A M, Wolman R L. Current concepts in the management of tendon disorders.  Rheumatology. 2006;  45 508-521
• 40 Emerson C, Morrissey D, Perry M et al. Ultrasonographically detected changes in Achilles tendons and self reported symptoms in elite gymnasts compared with controls – an observational study.  Man. Ther;  15 37-42
• 41 Fahlstrom M, Alfredson H. Ultrasound and Doppler findings in the Achilles tendon among middle-aged recreational floor-ball players in direct relation to a match.  Br J Sports Med. 2010;  44 140-143
• 42 Fredberg U, Bolvig L, Andersen N T. Prophylactic training in asymptomatic soccer players with ultrasonographic abnormalities in Achilles and patellar tendons: the Danish Super League Study.  Am J Sports Med. 2008;  36 451-460
• 43 Syha R, Peters M, Birnesser H et al. Computer-based quantification of the mean Achilles tendon thickness in ultrasound images: effect of tendinosis.  Br J Sports Med. 2007;  41 897-902 ; discussion
• 44 Du J, Carl M, Diaz E et al. Ultrashort TE T 1rho (UTE T 1rho) imaging of the Achilles tendon and meniscus.  Magn Reson Med. 2010;  64 834-842
• 45 Hodgson R J, Evans R, Wright P et al. Quantitative magnetization transfer ultrashort echo time imaging of the Achilles tendon.  Magn Reson Med. 2011;  65 1372-1376
• 46 Kallinen M, Suominen H. Ultrasonographic measurements of the Achilles tendon in elderly athletes and sedentary men.  Acta Radiol. 1994;  35 560-563
• 47 Cook J L, Bass S L, Black J E. Hormone therapy is associated with smaller Achilles tendon diameter in active post-menopausal women.  Scand J Med Sci Sports. 2007;  17 128-132
• 48 Tumia N, Kader D, Arena B et al. Achilles tendinopathy during pregnancy.  Clin J Sport Med. 2002;  12 43-45