Three-dimensional quantitative measurements of atrophy and fat infiltration in sub-regions of the supraspinatus muscle show heterogeneous distributions: a cadaveric study

Abstract

Introduction

Rotator cuff tears are common in the older population. Atrophy and fat infiltration develop un-evenly in torn supraspinatus (SSP) muscles leading to pre- and post-surgical complications. The purpose of the current study was twofold: first, to implement a volumetric and quantitative magnetic resonance imaging (MRI) approach to quantify the degree of muscle atrophy and fat infiltration within the SSP muscle and its four sub-regions (AS, PS, AD, and PD); second to compare 3-D MRI outcomes to the standard 2-D assessment and investigate their relationship with tear size.

Materials and methods

Fifteen cadaveric shoulders were obtained and MRI performed. Quantitative 3-D outcomes included SSP muscle volume, fossa volume, fat-free muscle volume, and fat fraction for the whole SSP muscle and its four sub-regions. 2-D and qualitative measurements included tear size, 2-D fat infiltration using the Goutallier classification, tangent sign, and occupation ratio.

Results

Linear regression outcomes with tear size were not significant for both cross-sectional area (r = − 0.494, p = 0.061) and occupation ratio (r = − 0.011, p = 0.969). Tear size negatively correlated with fat-free muscle volume for both AS and PS sub-regions (AS: r = − 0.78, p < 0.001; PS: r = − 0.68, p = 0.005, respectively) while showing no significant correlation with fat fraction outcomes. AD and PD sub-regions positively correlated with tear size and fat fraction outcomes (AD: r = 0.70, p = 0.017; PD: r = 0.52, p = 0.045, respectively), while no significant correlation was observed between tear size and fat-free muscle volumes.

Conclusion

Quantitative 3-D volumetric assessment of muscle degeneration resulted in better outcomes compared to the standard 2-D evaluation. The superficial supraspinatus muscle sub-regions primarily presented muscle atrophy, while the deep sub-regions were mainly affected by fat infiltration. 3-D assessments could be used pre-surgically to determine the best course of treatment and to estimate the muscles’ regenerative capacity and function.

This is a preview of subscription content, access via your institution.

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

References

  1. 1.

    Chung SW, Kim JY, Kim MH, Kim SH, Oh JH (2013) Arthroscopic repair of massive rotator cuff tears: outcome and analysis of factors associated with healing failure or poor postoperative function. Am J Sports Med 41(7):1674–1683

    Article  Google Scholar 

  2. 2.

    Fabis J, Danilewicz M, Omulecka A (2001) Rabbit supraspinatus tendon detachment: effects of size and time after tenotomy on morphometric changes in the muscle. Acta Orthop Scand 72(3):282–286

    CAS  Article  Google Scholar 

  3. 3.

    Fuchs B, Weishaupt D, Zanetti M, Hodler J, Gerber C (1999) Fatty degeneration of the muscles of the rotator cuff: assessment by computed tomography versus magnetic resonance imaging. J Shoulder Elbow Surg 8(6):599–605

    CAS  Article  Google Scholar 

  4. 4.

    Fukuta S, Tsutsui T, Amari R, Wada K, Sairyo K (2016) Tendon retraction with rotator cuff tear causes a decrease in cross-sectional area of the supraspinatus muscle on magnetic resonance imaging. J Shoulder Elbow Surg 25(7):1069–1075

    Article  Google Scholar 

  5. 5.

    Gerber C, Schneeberger AG, Hoppeler H, Meyer DC (2007) Correlation of atrophy and fatty infiltration on strength and integrity of rotator cuff repairs: a study in thirteen patients. J Shoulder Elbow Surg 16(6):691–696

    Article  Google Scholar 

  6. 6.

    Giambini H, Hatta T, Krzysztof GR et al (2017) Intramuscular fat infiltration evaluated by magnetic resonance imaging predicts the extensibility of the supraspinatus muscle. Muscle Nerve 57(1):129–135

    Article  Google Scholar 

  7. 7.

    Giambini H, Hatta T, Rezaei A, An KN (2018) Extensibility of the supraspinatus muscle can be predicted by combining shear wave elastography and magnetic resonance imaging-measured quantitative metrics of stiffness and volumetric fat infiltration: a cadaveric study. Clin Biomech (Bristol, Avon) 57:144–149

    Article  Google Scholar 

  8. 8.

    Gladstone JN, Bishop JY, Lo IK, Flatow EL (2007) Fatty infiltration and atrophy of the rotator cuff do not improve after rotator cuff repair and correlate with poor functional outcome. Am J Sports Med 35(5):719–728

    Article  Google Scholar 

  9. 9.

    Goutallier D, Postel JM, Bernageau J, Lavau L, Voisin MC (1994) Fatty muscle degeneration in cuff ruptures. Pre- and postoperative evaluation by CT scan. Clin Orthop Relat Res 304:78–83

    Google Scholar 

  10. 10.

    Hatta T, Giambini H, Uehara K et al (2015) Quantitative assessment of rotator cuff muscle elasticity: reliability and feasibility of shear wave elastography. J Biomech 48(14):3853–3858

    Article  Google Scholar 

  11. 11.

    Horiuchi S, Nozaki T, Tasaki A et al (2017) Reliability of MR quantification of rotator cuff muscle fatty degeneration using a 2-point Dixon technique in comparison with the Goutallier classification: validation study by multiple readers. Acad Radiol 24(11):1343–1351

    Article  Google Scholar 

  12. 12.

    Initiative USBaJ (2014) Burden of musculoskeletal diseases in the United States: prevalence, societal and economic cost(ed)^(eds), Rosemont, IL

  13. 13.

    Jo CH, Shin JS (2013) Changes in appearance of fatty infiltration and muscle atrophy of rotator cuff muscles on magnetic resonance imaging after rotator cuff repair: establishing new time-zero traits. Arthroscopy 29(3):449–458

    Article  Google Scholar 

  14. 14.

    Kikukawa K, Ide J, Kikuchi K, Morita M, Mizuta H, Ogata H (2014) Hypertrophic changes of the teres minor muscle in rotator cuff tears: quantitative evaluation by magnetic resonance imaging. J Shoulder Elbow Surg 23(12):1800–1805

    Article  Google Scholar 

  15. 15.

    Kim SY, Bleakney RR, Rindlisbacher T, Ravichandiran K, Rosser BW, Boynton E (2013) Musculotendinous architecture of pathological supraspinatus: a pilot in vivo ultrasonography study. Clin Anat 26(2):228–235

    Article  Google Scholar 

  16. 16.

    Kim SY, Boynton EL, Ravichandiran K, Fung LY, Bleakney R, Agur AM (2007) Three-dimensional study of the musculotendinous architecture of supraspinatus and its functional correlations. Clin Anat 20(6):648–655

    Article  Google Scholar 

  17. 17.

    Kim SY, Sachdeva R, Li Z, Lee D, Rosser BW (2015) Change in the pathologic supraspinatus: a three-dimensional model of fiber bundle architecture within anterior and posterior regions. Biomed Res Int 2015:564825

    PubMed  PubMed Central  Google Scholar 

  18. 18.

    Lee S, Lucas RM, Lansdown DA et al (2015) Magnetic resonance rotator cuff fat fraction and its relationship with tendon tear severity and subject characteristics. J Shoulder Elbow Surg 24(9):1442–1451

    Article  Google Scholar 

  19. 19.

    Lippe J, Spang JT, Leger RR, Arciero RA, Mazzocca AD, Shea KP (2012) Inter-rater agreement of the Goutallier, Patte, and Warner classification scores using preoperative magnetic resonance imaging in patients with rotator cuff tears. Arthroscopy 28(2):154–159

    Article  Google Scholar 

  20. 20.

    Matsumura N, Oguro S, Okuda S et al (2017) Quantitative assessment of fatty infiltration and muscle volume of the rotator cuff muscles using 3-dimensional 2-point Dixon magnetic resonance imaging. J Shoulder Elbow Surg 26(10):e309–e318

    Article  Google Scholar 

  21. 21.

    Meyer DC, Hoppeler H, von Rechenberg B, Gerber C (2004) A pathomechanical concept explains muscle loss and fatty muscular changes following surgical tendon release. J Orthop Res 22(5):1004–1007

    Article  Google Scholar 

  22. 22.

    Meyer DC, Pirkl C, Pfirrmann CW, Zanetti M, Gerber C (2005) Asymmetric atrophy of the supraspinatus muscle following tendon tear. J Orthop Res 23(2):254–258

    Article  Google Scholar 

  23. 23.

    Minagawa H, Yamamoto N, Abe H et al (2013) Prevalence of symptomatic and asymptomatic rotator cuff tears in the general population: from mass-screening in one village. J Orthop 10(1):8–12

    Article  Google Scholar 

  24. 24.

    Nardo L, Karampinos DC, Lansdown DA et al (2014) Quantitative assessment of fat infiltration in the rotator cuff muscles using water-fat MRI. J Magn Reson Imaging 39(5):1178–1185

    Article  Google Scholar 

  25. 25.

    Nozaki T, Tasaki A, Horiuchi S et al (2015) Quantification of fatty degeneration within the supraspinatus muscle by using a 2-point Dixon method on 3-T MRI. AJR Am J Roentgenol 205(1):116–122

    Article  Google Scholar 

  26. 26.

    Post M, Silver R, Singh M (1983) Rotator cuff tear. Diagnosis and treatment. Clin Orthop Relat Res 173:78–91

    Google Scholar 

  27. 27.

    Roh MS, Wang VM, April EW, Pollock RG, Bigliani LU, Flatow EL (2000) Anterior and posterior musculotendinous anatomy of the supraspinatus. J Shoulder Elbow Surg 9(5):436–440

    CAS  Article  Google Scholar 

  28. 28.

    Rulewicz GJ, Beaty S, Hawkins RJ, Kissenberth MJ (2013) Supraspinatus atrophy as a predictor of rotator cuff tear size: an MRI study utilizing the tangent sign. J Shoulder Elbow Surg 22(6):e6-10

    Article  Google Scholar 

  29. 29.

    Safran O, Schroeder J, Bloom R, Weil Y, Milgrom C (2011) Natural history of nonoperatively treated symptomatic rotator cuff tears in patients 60 years old or younger. Am J Sports Med 39(4):710–714

    Article  Google Scholar 

  30. 30.

    Schaefer O, Winterer J, Lohrmann C, Laubenberger J, Reichelt A, Langer M (2002) Magnetic resonance imaging for supraspinatus muscle atrophy after cuff repair. Clin Orthop Relat Res 403:93–99

    Article  Google Scholar 

  31. 31.

    Shin SJ, Chung J, Lee J, Ko YW (2016) Recovery of muscle strength after intact arthroscopic rotator cuff repair according to preoperative rotator cuff tear size. Am J Sports Med 44(4):972–980

    Article  Google Scholar 

  32. 32.

    Thomazeau H, Rolland Y, Lucas C, Duval JM, Langlais F (1996) Atrophy of the supraspinatus belly. Assessment by MRI in 55 patients with rotator cuff pathology. Acta Orthop Scand 67(3):264–268

    CAS  Article  Google Scholar 

  33. 33.

    Trevino JH 3rd, Gorny KR, Gomez-Cintron A, Zhao C, Giambini H (2019) A quantitative alternative to the Goutallier classification system using Lava Flex and Ideal MRI techniques: volumetric intramuscular fatty infiltration of the supraspinatus muscle, a cadaveric study. MAGMA 32(6):607–615

    CAS  Article  Google Scholar 

  34. 34.

    Vidt ME, Santago AC 2nd, Tuohy CJ et al (2016) Assessments of Fatty infiltration and muscle atrophy from a single magnetic resonance image slice are not predictive of 3-dimensional measurements. Arthroscopy 32(1):128–139

    Article  Google Scholar 

  35. 35.

    Williams MD, Ladermann A, Melis B, Barthelemy R, Walch G (2009) Fatty infiltration of the supraspinatus: a reliability study. J Shoulder Elbow Surg 18(4):581–587

    Article  Google Scholar 

  36. 36.

    Yamamoto A, Takagishi K, Osawa T et al (2010) Prevalence and risk factors of a rotator cuff tear in the general population. J Shoulder Elbow Surg 19(1):116–120

    Article  Google Scholar 

  37. 37.

    Yuri T, Kuwahara Y, Fujii H, Kiyoshige Y (2017) Functions of the subregions of the supraspinatus muscle. Clin Anat 30(3):347–351

    Article  Google Scholar 

  38. 38.

    Yuri T, Mura N, Yuki I, Fujii H, Kiyoshige Y (2018) Contractile property measurement of the torn supraspinatus muscle using real-time tissue elastography. J Shoulder Elbow Surg 27(9):1700–1704

    Article  Google Scholar 

Download references

Acknowledgements

This study was supported by the University of Texas at San Antonio. A co-author, Takuma Yuri, is funded by a Grant-in-Aid for JSPS fellows (Grant number 19J10699). We would like to thank Dr. Hiromi Fujii.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Hugo Giambini.

Ethics declarations

Conflict of interest

The authors declare they have no conflicts of interest.

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

Verify currency and authenticity via CrossMark

Cite this article

Trevino III, J.H., Yuri, T., Hatta, T. et al. Three-dimensional quantitative measurements of atrophy and fat infiltration in sub-regions of the supraspinatus muscle show heterogeneous distributions: a cadaveric study. Arch Orthop Trauma Surg (2021). https://doi.org/10.1007/s00402-021-03765-8

Download citation

Keywords

  • Rotator cuff tear
  • Fat infiltration
  • Goutallier classification
  • Muscle sub-region
  • Occupation ratio
  • Atrophy