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Erschienen in: Skeletal Radiology 1/2021

08.07.2020 | Scientific Article

Ultrashort echo time (UTE) imaging reveals a shift in bound water that is sensitive to sub-clinical tendinopathy in older adults

verfasst von: Isaac F. Loegering, Sarah C. Denning, Kevin M. Johnson, Fang Liu, Kenneth S. Lee, Darryl G. Thelen

Erschienen in: Skeletal Radiology | Ausgabe 1/2021

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Abstract

Objective

Use ultrashort echo time (UTE) magnetic resonance imaging to quantify bound water components of asymptomatic older Achilles tendons and investigate the relationship between UTE findings and imaging assessment of sub-clinical tendinopathy.

Materials and methods

Thirteen young (age 25 ± 4.8) and thirteen older (age 67 ± 4.7) adults were tested. A UTE sequence was used to quantify the transverse relaxation times of bound (\( {T}_{2,s}^{\ast } \)) and free (\( {T}_{2,l}^{\ast } \)) water and the bound water fraction (Fs) in the Achilles tendon. Anatomical images were collected and graded by a musculoskeletal radiologist to identify signs of sub-clinical tendinopathy. Two-sample t tests were used to compare \( {T}_{2,s}^{\ast } \), \( {T}_{2,l}^{\ast } \), and Fs between age groups and between adults with and without sub-clinical tendinopathy.

Results

Older tendons exhibited a 60% longer \( {T}_{2,s}^{\ast } \) (p = 0.004), similar \( {T}_{2,l}^{\ast } \) (p = 0.86), and 5% smaller Fs (p = 0.048) than young tendons. Seven older adult tendons exhibited tendon thickening and increased signal intensity indicative of sub-clinical tendinopathy. This subset of tendons exhibited a 7% smaller bound water fraction (p = 0.02) and significantly longer \( {T}_{2,s}^{\ast } \) (p < 0.001) than the normal tendons from young and older adults.

Conclusion

Older adult tendons exhibited unique UTE signatures that are consistent with disruption of the collagen fiber network and changes in macromolecular content. UTE imaging metrics were sensitive to early indicators of tissue degeneration identified on anatomical images and hence could provide a quantitative biomarker by which to track changes in tissue health resulting from injury, disease, and treatment.
Literatur
1.
Zurück zum Zitat Tuite DJ, Renström P, O’Brien M. The aging tendon. Scand J Med Sci Sports. 1997;7:72–7.CrossRef Tuite DJ, Renström P, O’Brien M. The aging tendon. Scand J Med Sci Sports. 1997;7:72–7.CrossRef
2.
Zurück zum Zitat Moore MJ, De Beaux A. A quantitative ultrastructural study of rat tendon from birth to maturity. J Anat. 1987;153:163–9.PubMedPubMedCentral Moore MJ, De Beaux A. A quantitative ultrastructural study of rat tendon from birth to maturity. J Anat. 1987;153:163–9.PubMedPubMedCentral
3.
Zurück zum Zitat Almekinders LC, Deol G. The effects of aging, antiinflammatory drugs, and ultrasound on the in vitro response of tendon tissue. Am J Sports Med. 1999;27:417–21.CrossRef Almekinders LC, Deol G. The effects of aging, antiinflammatory drugs, and ultrasound on the in vitro response of tendon tissue. Am J Sports Med. 1999;27:417–21.CrossRef
4.
Zurück zum Zitat Ippolito E, Natali PG, Postacchini F, Accinni L, De CM. Morphological, immunochemical, and biochemical study of rabbit Achilles tendon at various ages. J Bone Joint Surg Am. 1980;62:583–98.CrossRef Ippolito E, Natali PG, Postacchini F, Accinni L, De CM. Morphological, immunochemical, and biochemical study of rabbit Achilles tendon at various ages. J Bone Joint Surg Am. 1980;62:583–98.CrossRef
5.
Zurück zum Zitat Vailas AC, Pedrini VA, Pedrini-Mille A, Holloszy JO. Patellar tendon matrix changes associated with aging and voluntary exercise. J Appl Physiol. 1985;58:1572–6.CrossRef Vailas AC, Pedrini VA, Pedrini-Mille A, Holloszy JO. Patellar tendon matrix changes associated with aging and voluntary exercise. J Appl Physiol. 1985;58:1572–6.CrossRef
6.
Zurück zum Zitat Honda T, Katagiri K, Kuroda A, Matsunaga E, Shinkai H. Age-related changes of the dermatan sulfate containing small proteoglycans in bovine tendon. Coll Relat Res. 1987;7:171–84.CrossRef Honda T, Katagiri K, Kuroda A, Matsunaga E, Shinkai H. Age-related changes of the dermatan sulfate containing small proteoglycans in bovine tendon. Coll Relat Res. 1987;7:171–84.CrossRef
7.
Zurück zum Zitat Rigozzi S, Müller R, Stemmer A, Snedeker JG. Tendon glycosaminoglycan proteoglycan sidechains promote collagen fibril sliding—AFM observations at the nanoscale. J Biomech. 2013;46:813–8.CrossRef Rigozzi S, Müller R, Stemmer A, Snedeker JG. Tendon glycosaminoglycan proteoglycan sidechains promote collagen fibril sliding—AFM observations at the nanoscale. J Biomech. 2013;46:813–8.CrossRef
8.
Zurück zum Zitat Menard D, Stanish WD. The aging athlete. Am J Sports Med. 1989;17:187–96.CrossRef Menard D, Stanish WD. The aging athlete. Am J Sports Med. 1989;17:187–96.CrossRef
9.
Zurück zum Zitat Frey C, Shereff M, Greenidge N. Vascularity of the posterior tibial tendon. J Bone Joint Surg Am. 1990;72:884–8.CrossRef Frey C, Shereff M, Greenidge N. Vascularity of the posterior tibial tendon. J Bone Joint Surg Am. 1990;72:884–8.CrossRef
10.
Zurück zum Zitat Kvist M. Achilles tendon injuries in athletes. Sports Med. 1994;18:173–201.CrossRef Kvist M. Achilles tendon injuries in athletes. Sports Med. 1994;18:173–201.CrossRef
11.
Zurück zum Zitat Khan KM, Cook JL, Taunton JE, Bonar F. Overuse tendinosis, not tendinitis: part 1: a new paradigm for a difficult clinical problem. Phys Sportsmed. 2000;28:38–48.CrossRef Khan KM, Cook JL, Taunton JE, Bonar F. Overuse tendinosis, not tendinitis: part 1: a new paradigm for a difficult clinical problem. Phys Sportsmed. 2000;28:38–48.CrossRef
12.
Zurück zum Zitat Albers IS, Zwerver J, Diercks RL, Dekker JH, Van den Akker-Scheek I. Incidence and prevalence of lower extremity tendinopathy in a Dutch general practice population: a cross sectional study. BMC Musculoskelet Disord. 2016;17:16.CrossRef Albers IS, Zwerver J, Diercks RL, Dekker JH, Van den Akker-Scheek I. Incidence and prevalence of lower extremity tendinopathy in a Dutch general practice population: a cross sectional study. BMC Musculoskelet Disord. 2016;17:16.CrossRef
13.
Zurück zum Zitat Aström M, Rausing A. Chronic Achilles tendinopathy. A survey of surgical and histopathologic findings. Clin Orthop Relat Res. 1995:151–64. Aström M, Rausing A. Chronic Achilles tendinopathy. A survey of surgical and histopathologic findings. Clin Orthop Relat Res. 1995:151–64.
14.
Zurück zum Zitat Riley GP, Goddard MJ, Hazleman BL. Histopathological assessment and pathological significance of matrix degeneration in supraspinatus tendons. Rheumatology. 2001;40:229–30.CrossRef Riley GP, Goddard MJ, Hazleman BL. Histopathological assessment and pathological significance of matrix degeneration in supraspinatus tendons. Rheumatology. 2001;40:229–30.CrossRef
15.
Zurück zum Zitat Kannus P, NIITTYMÄKI S, JÄRVINEN M, LEHTO M. Sports injuries in elderly athletes: a three-year prospective, controlled study. Age Ageing. 1989;18:263–70.CrossRef Kannus P, NIITTYMÄKI S, JÄRVINEN M, LEHTO M. Sports injuries in elderly athletes: a three-year prospective, controlled study. Age Ageing. 1989;18:263–70.CrossRef
16.
Zurück zum Zitat Du J, Diaz E, Carl M, Bae W, Chung CB, Bydder GM. Ultrashort echo time imaging with bicomponent analysis. Magn Reson Med. 2012;67:645–9.CrossRef Du J, Diaz E, Carl M, Bae W, Chung CB, Bydder GM. Ultrashort echo time imaging with bicomponent analysis. Magn Reson Med. 2012;67:645–9.CrossRef
17.
Zurück zum Zitat Koff MF, Pownder SL, Shah PH, Yang LW, Potter HG. Ultrashort echo imaging of cyclically loaded rabbit patellar tendon. J Biomech. 2014;47:3428–32.CrossRef Koff MF, Pownder SL, Shah PH, Yang LW, Potter HG. Ultrashort echo imaging of cyclically loaded rabbit patellar tendon. J Biomech. 2014;47:3428–32.CrossRef
18.
Zurück zum Zitat Chang EY, Du J, Statum S, Pauli C, Chung CB. Quantitative bi-component T2* analysis of histologically normal Achilles tendons. Muscles Ligaments Tendons J. 2015;5:58.CrossRef Chang EY, Du J, Statum S, Pauli C, Chung CB. Quantitative bi-component T2* analysis of histologically normal Achilles tendons. Muscles Ligaments Tendons J. 2015;5:58.CrossRef
19.
Zurück zum Zitat Juras V, Zbyn S, Pressl C, Valkovic L, Szomolanyi P, Frollo I, et al. Regional variations of T2* in healthy and pathologic achilles tendon in vivo at 7 Tesla: preliminary results. Magn Reson Med. 2012;68:1607–13.CrossRef Juras V, Zbyn S, Pressl C, Valkovic L, Szomolanyi P, Frollo I, et al. Regional variations of T2* in healthy and pathologic achilles tendon in vivo at 7 Tesla: preliminary results. Magn Reson Med. 2012;68:1607–13.CrossRef
20.
Zurück zum Zitat Chang EY, Du J, Iwasaki K, Biswas R, Statum S, He Q, et al. Single-and bi-component T2* analysis of tendon before and during tensile loading, using UTE sequences. J Magn Reson Imaging. 2015;42:114–20.CrossRef Chang EY, Du J, Iwasaki K, Biswas R, Statum S, He Q, et al. Single-and bi-component T2* analysis of tendon before and during tensile loading, using UTE sequences. J Magn Reson Imaging. 2015;42:114–20.CrossRef
21.
Zurück zum Zitat Takamiya H, Kusaka Y, Seo Y, Noguchi M, Ikoma K, Morimoto T, et al. Characteristics of proton NMR T2 relaxation of water in the normal and regenerating tendon. Jpn J Physiol. 2000;50:569–76.CrossRef Takamiya H, Kusaka Y, Seo Y, Noguchi M, Ikoma K, Morimoto T, et al. Characteristics of proton NMR T2 relaxation of water in the normal and regenerating tendon. Jpn J Physiol. 2000;50:569–76.CrossRef
22.
Zurück zum Zitat Diaz E, Chung CB, Bae WC, Statum S, Znamirowski R, Bydder GM, et al. Ultrashort echo time spectroscopic imaging (UTESI): an efficient method for quantifying bound and free water. NMR Biomed. 2012;25:161–8.CrossRef Diaz E, Chung CB, Bae WC, Statum S, Znamirowski R, Bydder GM, et al. Ultrashort echo time spectroscopic imaging (UTESI): an efficient method for quantifying bound and free water. NMR Biomed. 2012;25:161–8.CrossRef
23.
Zurück zum Zitat 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;23:2814–22.CrossRef 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;23:2814–22.CrossRef
24.
Zurück zum Zitat Kijowski R, Wilson JJ, Liu F. Bicomponent ultrashort echo time analysis for assessment of patients with patellar tendinopathy. J Magn Reson Imaging. 2017;46:1441–7.CrossRef Kijowski R, Wilson JJ, Liu F. Bicomponent ultrashort echo time analysis for assessment of patients with patellar tendinopathy. J Magn Reson Imaging. 2017;46:1441–7.CrossRef
25.
Zurück zum Zitat Larson PEZ, Gurney PT, Nishimura DG. Anisotropic field-of-views in radial imaging. IEEE Trans Med Imaging IEEE. 2007;27:47–57.CrossRef Larson PEZ, Gurney PT, Nishimura DG. Anisotropic field-of-views in radial imaging. IEEE Trans Med Imaging IEEE. 2007;27:47–57.CrossRef
27.
Zurück zum Zitat Erickson SJ, Prost RW, Timins ME. The “magic angle” effect: background physics and clinical relevance. Radiology. 1993;188:23–5.CrossRef Erickson SJ, Prost RW, Timins ME. The “magic angle” effect: background physics and clinical relevance. Radiology. 1993;188:23–5.CrossRef
28.
Zurück zum Zitat Liu F, Kijowski R. Assessment of different fitting methods for in-vivo bi-component T2* analysis of human patellar tendon in magnetic resonance imaging. Muscles Ligaments Tendons J. CIC Edizioni Internazionali. 2017;7:163. Liu F, Kijowski R. Assessment of different fitting methods for in-vivo bi-component T2* analysis of human patellar tendon in magnetic resonance imaging. Muscles Ligaments Tendons J. CIC Edizioni Internazionali. 2017;7:163.
31.
32.
Zurück zum Zitat Petersen W, Pufe T, Zantop T, Paulsen F. Blood supply of the flexor hallucis longus tendon with regard to dancer’s tendinitis: injection and immunohistochemical studies of cadaver tendons. Foot Ankle Int. SAGE Publications Inc. 2003;24:591–6. Available from: https://doi.org/10.1177/107110070302400804. Petersen W, Pufe T, Zantop T, Paulsen F. Blood supply of the flexor hallucis longus tendon with regard to dancer’s tendinitis: injection and immunohistochemical studies of cadaver tendons. Foot Ankle Int. SAGE Publications Inc. 2003;24:591–6. Available from: https://​doi.​org/​10.​1177/​1071100703024008​04.
33.
Zurück zum Zitat Kannus P, Paavola M, Józsa L. Aging and degeneration of tendons. Tendon Inj Springer. 2005:25–31. Kannus P, Paavola M, Józsa L. Aging and degeneration of tendons. Tendon Inj Springer. 2005:25–31.
34.
Zurück zum Zitat Cook JL, Khan KM, Kiss ZS, Purdam CR, Griffiths L. Prospective imaging study of asymptomatic patellar tendinopathy in elite junior basketball players. J Ultrasound Med. 2000;19:473–9.CrossRef Cook JL, Khan KM, Kiss ZS, Purdam CR, Griffiths L. Prospective imaging study of asymptomatic patellar tendinopathy in elite junior basketball players. J Ultrasound Med. 2000;19:473–9.CrossRef
35.
Zurück zum Zitat Grosse U, Springer F, Hein T, Grözinger G, Schabel C, Martirosian P, et al. Influence of physical activity on T1 and T2* relaxation times of healthy Achilles tendons at 3T. J Magn Reson Imaging. 2015;41:193–201.CrossRef Grosse U, Springer F, Hein T, Grözinger G, Schabel C, Martirosian P, et al. Influence of physical activity on T1 and T2* relaxation times of healthy Achilles tendons at 3T. J Magn Reson Imaging. 2015;41:193–201.CrossRef
36.
Zurück zum Zitat Qiao Y, Tao H-Y, Ma K, Wu Z-Y, Qu J-X, Chen S. UTE-analysis of diseased and healthy achilles tendons and correlation with clinical score: an in vivo preliminary study. Biomed Res Int. 2017;2017. Qiao Y, Tao H-Y, Ma K, Wu Z-Y, Qu J-X, Chen S. UTE-analysis of diseased and healthy achilles tendons and correlation with clinical score: an in vivo preliminary study. Biomed Res Int. 2017;2017.
37.
Zurück zum Zitat Klein S, Staring M, Murphy K, Viergever MA, Pluim JPW. Elastix: a toolbox for intensity-based medical image registration. IEEE Trans Med Imaging. 2010;29:196.CrossRef Klein S, Staring M, Murphy K, Viergever MA, Pluim JPW. Elastix: a toolbox for intensity-based medical image registration. IEEE Trans Med Imaging. 2010;29:196.CrossRef
Metadaten
Titel
Ultrashort echo time (UTE) imaging reveals a shift in bound water that is sensitive to sub-clinical tendinopathy in older adults
verfasst von
Isaac F. Loegering
Sarah C. Denning
Kevin M. Johnson
Fang Liu
Kenneth S. Lee
Darryl G. Thelen
Publikationsdatum
08.07.2020
Verlag
Springer Berlin Heidelberg
Erschienen in
Skeletal Radiology / Ausgabe 1/2021
Print ISSN: 0364-2348
Elektronische ISSN: 1432-2161
DOI
https://doi.org/10.1007/s00256-020-03538-1

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