Korean Journal of Radiology

The Korean Society of Radiology (대한영상의학회)
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The Association between the Magnetic Resonance Imaging Findings of Adhesive Capsulitis and Shoulder Muscle Fat Quantification Using a Multi-Echo Dixon Method

  • Yoon, Min A (Department of Radiology, Korea University Guro Hospital, Korea University College of Medicine) ;
  • Hong, Suk-Joo (Department of Radiology, Korea University Guro Hospital, Korea University College of Medicine) ;
  • Hong, Sun (Department of Radiology, Korea University Guro Hospital, Korea University College of Medicine) ;
  • Kang, Chang Ho (Department of Radiology, Korea University Anam Hospital, Korea University College of Medicine) ;
  • Kim, Baek Hyun (Department of Radiology, Korea University Ansan Hospital, Korea University College of Medicine) ;
  • Kim, In Seong (Siemens Healthcare)
  • Received : 2017.02.20
  • Accepted : 2017.07.24
  • Published : 2018.02.01
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Abstract

Objective: To investigate the association between the magnetic resonance imaging (MRI) findings of adhesive capsulitis and shoulder muscle fat percentages using a multi-echo Dixon method. Materials and Methods: Twenty-four patients with clinical diagnoses of adhesive capsulitis and either intact rotator cuffs or Ellman grade 1 partial tears as indicated by MRI scans were included. Two radiologists independently evaluated MRI scans of adhesive capsulitis as follows: presence or absence of axillary recess capsular and extracapsular hyperintensities; thickness of the coracohumeral ligament; thickness of abnormal rotator interval soft tissue; and thickness of glenoidal/humeral axillary recess capsules. Fat quantifications of the supraspinatus, infraspinatus, teres minor, subscapularis, teres major and posterior deltoid muscles were performed using multi-echo Dixon imaging at three locations. Inter-rater agreement was assessed. Differences in fat percentages were assessed and correlations between fat percentages and quantitative measurements were evaluated. Results: The fat percentage of the supraspinatus was significantly higher in patients with extracapsular hyperintensity (present, $3.00{\pm}1.74%$; absent, $1.81{\pm}0.80%$; p = 0.022). There were positive correlations between the fat percentage of the teres minor and the thicknesses of the abnormal rotator interval soft tissue (r = 0.494, p = 0.014) and the glenoidal axillary recess capsule (r = 0.475, p = 0.019). After controlling for the effects of age, sex and clinical stage, the relationship between the teres minor fat percentage and the thickness of the abnormal rotator interval soft tissue was statistically significant (r = 0.384, p = 0.048). Inter-rater agreement was almost perfect for fat quantification (intraclass correlation coefficients [ICC] > 0.9) and qualitative analyses (k = 0.824), but were variable for quantitative measurements (ICC, 0.170-0.606). Conclusion: Several MRI findings of adhesive capsulitis were significantly related to higher fat percentages of shoulder muscles.

Keywords

References

  1. Huang SW, Lin JW, Wang WT, Wu CW, Liou TH, Lin HW. Hyperthyroidism is a risk factor for developing adhesive capsulitis of the shoulder: a nationwide longitudinal population-based study. Sci Rep 2014;4:4183
  2. Neviaser JS. Adhesive capsulitis and the stiff and painful shoulder. Orthop Clin North Am 1980;11:327-331
  3. Neviaser AS, Hannafin JA. Adhesive capsulitis: a review of current treatment. Am J Sports Med 2010;38:2346-2356 https://doi.org/10.1177/0363546509348048
  4. Emig EW, Schweitzer ME, Karasick D, Lubowitz J. Adhesive capsulitis of the shoulder: MR diagnosis. Am J Roentgenol 1995;164:1457-1459 https://doi.org/10.2214/ajr.164.6.7754892
  5. Mengiardi B, Pfirrmann CW, Gerber C, Hodler J, Zanetti M. Frozen shoulder: MR arthrographic findings. Radiology 2004;233:486-492 https://doi.org/10.1148/radiol.2332031219
  6. Gondim Teixeira PA, Balaj C, Chanson A, Lecocq S, Louis M, Blum A. Adhesive capsulitis of the shoulder: value of inferior glenohumeral ligament signal changes on T2-weighted fatsaturated images. Am J Roentgenol 2012;198:W589-W596 https://doi.org/10.2214/AJR.11.7453
  7. Connell D, Padmanabhan R, Buchbinder R. Adhesive capsulitis: role of MR imaging in differential diagnosis. Eur Radiol 2002;12:2100-2106 https://doi.org/10.1007/s00330-002-1349-7
  8. MacDougall JD, Elder GC, Sale DG, Moroz JR, Sutton JR. Effects of strength training and immobilization on human muscle fibres. Eur J Appl Physiol Occup Physiol 1980;43:25-34 https://doi.org/10.1007/BF00421352
  9. Lin HC, Li JS, Lo SF, Shih YF, Lo CY, Chen SY. Isokinetic characteristics of shoulder rotators in patients with adhesive capsulitis. J Rehabil Med 2009;41:563-568 https://doi.org/10.2340/16501977-0378
  10. Rawat P, Eapen C, Seema KP. Effect of rotator cuff strengthening as an adjunct to standard care in subjects with adhesive capsulitis: A randomized controlled trial. J Hand Ther 2017;30:235-241.e8 https://doi.org/10.1016/j.jht.2016.10.007
  11. Agten CA, Rosskopf AB, Gerber C, Pfirrmann CW. Quantification of early fatty infiltration of the rotator cuff muscles: comparison of multi-echo Dixon with single-voxel MR spectroscopy. Eur Radiol 2016;26:3719-3727 https://doi.org/10.1007/s00330-015-4144-y
  12. Fischer MA, Nanz D, Shimakawa A, Schirmer T, Guggenberger R, Chhabra A, et al. Quantification of muscle fat in patients with low back pain: comparison of multi-echo MR imaging with single-voxel MR spectroscopy. Radiology 2013;266:555-563 https://doi.org/10.1148/radiol.12120399
  13. Ellman H. Diagnosis and treatment of incomplete rotator cuff tears. Clin Orthop Relat Res 1990:64-74
  14. Hannafin JA, Chiaia TA. Adhesive capsulitis. A treatment approach. Clin Orthop Relat Res 2000:95-109
  15. Zhong X, Nickel MD, Kannengiesser SA, Dale BM, Kiefer B, Bashir MR. Liver fat quantification using a multi-step adaptive fitting approach with multi-echo GRE imaging. Magn Reson Med 2014;72:1353-1365 https://doi.org/10.1002/mrm.25054
  16. Meyer DC, Hoppeler H, von Rechenberg B, Gerber C. A pathomechanical concept explains muscle loss and fatty muscular changes following surgical tendon release. J Orthop Res 2004;22:1004-1007 https://doi.org/10.1016/j.orthres.2004.02.009
  17. Park S, Lee DH, Yoon SH, Lee HY, Kwack KS. Evaluation of adhesive capsulitis of the shoulder with fat-suppressed T2- weighted MRI: Association between clinical features and MRI findings. Am J Roentgenol 2016;207:135-141 https://doi.org/10.2214/AJR.15.15200
  18. Ackland DC, Pak P, Richardson M, Pandy MG. Moment arms of the muscles crossing the anatomical shoulder. J Anat 2008;213:383-390 https://doi.org/10.1111/j.1469-7580.2008.00965.x
  19. Nardo L, Karampinos DC, Lansdown DA, Carballido-Gamio J, Lee S, Maroldi R, et al. Quantitative assessment of fat infiltration in the rotator cuff muscles using water-fat MRI. J Magn Reson Imaging 2014;39:1178-1185 https://doi.org/10.1002/jmri.24278
  20. Ahn KS, Kang CH, Oh YW, Jeong WK. Correlation between magnetic resonance imaging and clinical impairment in patients with adhesive capsulitis. Skeletal Radiol 2012;41:1301-1308 https://doi.org/10.1007/s00256-012-1391-8
  21. Walch G, Boulahia A, Calderone S, Robinson AH. The 'dropping' and 'hornblower's' signs in evaluation of rotator-cuff tears. J Bone Joint Surg Br 1998;80:624-628 https://doi.org/10.1302/0301-620X.80B4.8651
  22. Jung JY, Jee WH, Chun HJ, Kim YS, Chung YG, Kim JM. Adhesive capsulitis of the shoulder: evaluation with MR arthrography. Eur Radiol 2006;16:791-796 https://doi.org/10.1007/s00330-005-0020-5
  23. Goutallier D, Postel JM, Bernageau J, Lavau L, Voisin MC. Fatty muscle degeneration in cuff ruptures. Pre- and postoperative evaluation by CT scan. Clin Orthop Relat Res 1994:78-83
  24. Fuchs B, Weishaupt D, Zanetti M, Hodler J, Gerber C. Fatty degeneration of the muscles of the rotator cuff: assessment by computed tomography versus magnetic resonance imaging. J Shoulder Elbow Surg 1999;8:599-605 https://doi.org/10.1016/S1058-2746(99)90097-6
  25. Tae SK, Oh JH, Kim SH, Chung SW, Yang JY, Back YW. Evaluation of fatty degeneration of the supraspinatus muscle using a new measuring tool and its correlation between multidetector computed tomography and magnetic resonance imaging. Am J Sports Med 2011;39:599-606 https://doi.org/10.1177/0363546510384791
  26. Fox PT. Physiological ROI definition by image subtraction. J Cereb Blood Flow Metab 1991;11:A79-A82 https://doi.org/10.1038/jcbfm.1991.41
  27. Oh JH, Kim SH, Choi JA, Kim Y, Oh CH. Reliability of the grading system for fatty degeneration of rotator cuff muscles. Clin Orthop Relat Res 2010;468:1558-1564 https://doi.org/10.1007/s11999-009-0818-6
  28. Slabaugh MA, Friel NA, Karas V, Romeo AA, Verma NN, Cole BJ. Interobserver and intraobserver reliability of the Goutallier classification using magnetic resonance imaging: proposal of a simplified classification system to increase reliability. Am J Sports Med 2012;40:1728-1734 https://doi.org/10.1177/0363546512452714
  29. Lesage P, Maynou C, Elhage R, Boutry N, Herent S, Mestdagh H. [Reproducibility of CT scan evaluation of muscular fatty degeneration. Intra- and interobserver analysis of 56 shoulders presenting with a ruptured rotator cuff muscles]. Rev Chir Orthop Reparatrice Appar Mot 2002;88:359-364
  30. Yoo YH, Kim HS, Lee YH, Yoon CS, Paek MY, Yoo H, et al. Comparison of multi-echo Dixon methods with volume interpolated breath-hold gradient echo magnetic resonance imaging in fat-signal fraction quantification of paravertebral muscle. Korean J Radiol 2015;16:1086-1095 https://doi.org/10.3348/kjr.2015.16.5.1086
  31. Reeder SB, Robson PM, Yu H, Shimakawa A, Hines CD, McKenzie CA, et al. Quantification of hepatic steatosis with MRI: the effects of accurate fat spectral modeling. J Magn Reson Imaging 2009;29:1332-1339 https://doi.org/10.1002/jmri.21751
  32. Yamaguchi K, Tetro AM, Blam O, Evanoff BA, Teefey SA, Middleton WD. Natural history of asymptomatic rotator cuff tears: a longitudinal analysis of asymptomatic tears detected sonographically. J Shoulder Elbow Surg 2001;10:199-203 https://doi.org/10.1067/mse.2001.113086
  33. Reilly P, Macleod I, Macfarlane R, Windley J, Emery RJ. Dead men and radiologists don‘t lie: a review of cadaveric and radiological studies of rotator cuff tear prevalence. Ann R Coll Surg Engl 2006;88:116-121
  34. Needell SD, Zlatkin MB, Sher JS, Murphy BJ, Uribe JW. MR imaging of the rotator cuff: peritendinous and bone abnormalities in an asymptomatic population. Am J Roentgenol 1996;166:863-867 https://doi.org/10.2214/ajr.166.4.8610564