Skip to main content
SpringerLink
Log in

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

  • Scientific Article
  • Published:
Skeletal Radiology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Tuite DJ, Renström P, O’Brien M. The aging tendon. Scand J Med Sci Sports. 1997;7:72–7.

    Article  CAS  Google Scholar 

  2. Moore MJ, De Beaux A. A quantitative ultrastructural study of rat tendon from birth to maturity. J Anat. 1987;153:163–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  3. 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.

    Article  CAS  Google Scholar 

  4. 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.

    Article  CAS  Google Scholar 

  5. 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.

    Article  CAS  Google Scholar 

  6. 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.

    Article  CAS  Google Scholar 

  7. 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.

    Article  CAS  Google Scholar 

  8. Menard D, Stanish WD. The aging athlete. Am J Sports Med. 1989;17:187–96.

    Article  CAS  Google Scholar 

  9. Frey C, Shereff M, Greenidge N. Vascularity of the posterior tibial tendon. J Bone Joint Surg Am. 1990;72:884–8.

    Article  CAS  Google Scholar 

  10. Kvist M. Achilles tendon injuries in athletes. Sports Med. 1994;18:173–201.

    Article  CAS  Google Scholar 

  11. 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.

    Article  CAS  Google Scholar 

  12. 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.

    Article  Google Scholar 

  13. Aström M, Rausing A. Chronic Achilles tendinopathy. A survey of surgical and histopathologic findings. Clin Orthop Relat Res. 1995:151–64.

  14. Riley GP, Goddard MJ, Hazleman BL. Histopathological assessment and pathological significance of matrix degeneration in supraspinatus tendons. Rheumatology. 2001;40:229–30.

    Article  CAS  Google Scholar 

  15. 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.

    Article  CAS  Google Scholar 

  16. 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.

    Article  Google Scholar 

  17. 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.

    Article  Google Scholar 

  18. 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.

    Article  Google Scholar 

  19. 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.

    Article  Google Scholar 

  20. 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.

    Article  Google Scholar 

  21. 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.

    Article  CAS  Google Scholar 

  22. 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.

    Article  Google Scholar 

  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;23:2814–22.

    Article  Google Scholar 

  24. 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.

    Article  Google Scholar 

  25. Larson PEZ, Gurney PT, Nishimura DG. Anisotropic field-of-views in radial imaging. IEEE Trans Med Imaging IEEE. 2007;27:47–57.

    Article  Google Scholar 

  26. Xu Y, Murrell GAC. The basic science of tendinopathy. Clin Orthop Relat Res. 2008;466:1528–38. Available from: https://doi.org/10.1007/s11999-008-0286-4.

  27. Erickson SJ, Prost RW, Timins ME. The “magic angle” effect: background physics and clinical relevance. Radiology. 1993;188:23–5.

    Article  CAS  Google Scholar 

  28. 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.

    Google Scholar 

  29. Corps AN, Robinson AHN, Movin T, Costa ML, Hazleman BL, Riley GP. Increased expression of aggrecan and biglycan mRNA in Achilles tendinopathy. Rheumatology. 2005;45:291–4. Available from: https://doi.org/10.1093/rheumatology/kei152.

  30. Carr AJ, Norris SH. The blood supply of the calcaneal tendon. J Bone Joint Surg BrThe British Editorial Society of Bone & Joint Surgery. 1989;71-B:100–1. Available from: https://doi.org/10.1302/0301-620X.71B1.2914976.

  31. Macnab I. Rotator cuff tendinitis. Ann R Coll Surg Engl. Royal College of Surgeons of England. 1973;53:271.

    CAS  PubMed  PubMed Central  Google Scholar 

  32. 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.

  33. Kannus P, Paavola M, Józsa L. Aging and degeneration of tendons. Tendon Inj Springer. 2005:25–31.

  34. 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.

    Article  CAS  Google Scholar 

  35. 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.

    Article  Google Scholar 

  36. 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. 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.

    Article  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge the contributions of Ana Ebrahimi, Sara John, Kelli Hellenbrand, Marti Garcia, Jenelle Grogan, Haley Cilliers, and Oliver Wieben.

Funding

National Institutes of Health AG051748.

Author information

Authors and Affiliations

  1. Department of Biomedical Engineering, University of Wisconsin-Madison, 1513 University Ave, Madison, WI, 53706, USA

    Isaac F. Loegering & Sarah C. Denning

  2. Department of Medical Physics, University of Wisconsin-Madison, 1111 Highland Ave, Madison, WI, 53705, USA

    Kevin M. Johnson

  3. Department of Radiology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, 02114, USA

    Fang Liu

  4. University of Wisconsin School of Medicine & Public Health, 600 Highland Avenue, Madison, WI, 53792, USA

    Kenneth S. Lee

  5. Department of Mechanical Engineering, University of Wisconsin-Madison, 1513 University Ave, Madison, WI, 53706, USA

    Darryl G. Thelen

Authors
  1. Isaac F. Loegering
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sarah C. Denning
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kevin M. Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kenneth S. Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Darryl G. Thelen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Darryl G. Thelen.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Informed consent

The study was approved by the institutional review board of the University of Wisconsin-Madison, and written consent was obtained from each subject prior to participation.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Loegering, I.F., Denning, S.C., Johnson, K.M. et al. Ultrashort echo time (UTE) imaging reveals a shift in bound water that is sensitive to sub-clinical tendinopathy in older adults. Skeletal Radiol 50, 107–113 (2021). https://doi.org/10.1007/s00256-020-03538-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00256-020-03538-1

Keywords

Search

Navigation