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

      Highlights

      • Shoulders with rotator cuff tears showed high fat fraction outcomes.
      • Negative correlation between extensibility and Shear Wave Elastography-measured moduli.
      • Extensibility of the muscle was correlated to quantitative muscle quality metrics.
      • Elastography and Magnetic Resonance Imaging outcomes could help prevent repair re-tear.

      Abstract

      Background

      A torn rotator cuff tendon will retract over time causing changes in muscle properties and decreasing its extensibility, or deformation. During surgery, large tensile loads are applied to bring the torn tendon to the footprint. Poor muscle extensibility and large tensile stresses at the repair might lead to gap formation or re-tear of the repair. A quantitative evaluation of muscle properties could be used to predict the extensibility of the supraspinatus (SSP) muscle.

      Method

      Magnetic resonance imaging (MRI)-measured volumetric fat fraction and shear wave elastography (SWE)-measured elastic modulus of the SSP muscle were obtained on seventeen cadaveric shoulders. Experimental extensibility and stiffness were then measured by axially pulling the tendon up-to 60 N. Univariate and multivariate analyses were used to determine the correlation and contribution of fat fraction and elastic modulus to experimental outcomes.

      Findings

      SWE moduli negatively correlated with SSP muscle extensibility (r = 0.54–0.58, P ≤ 0.0259); fat fraction resulted in a positive correlation (r = 0.69, P = 0.0021). SWE measurements, solely, explained up to 34% and 33% of the variability in measured extensibility and stiffness, respectively. Fat Fraction, solely, explained 48% of the variability in extensibility and 36% of the variability in stiffness. These methods combined predicted up to 62% of the musculotendinous extensibility.

      Interpretation

      This study showed a comprehensive quantitative assessment of SSP muscle properties using SWE to estimate stiffness and MRI to measure fatty infiltration. The extensibility of the detached muscle/tendon unit was highly correlated to material properties of the muscle when these methods were used in combination.

      Keywords

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      References

        • Andersson T.
        • Romu T.
        • Karlsson A.
        • Noren B.
        • Forsgren M.F.
        • Smedby O.
        • Kechagias S.
        • Almer S.
        • Lundberg P.
        • Borga M.
        • Leinhard O.D.
        Consistent intensity inhomogeneity correction in water-fat MRI.
        J. Magn. Reson. Imaging. 2015; 42: 468-476
        • Bartl C.
        • Kouloumentas P.
        • Holzapfel K.
        • Eichhorn S.
        • Wortler K.
        • Imhoff A.
        • Salzmann G.M.
        Long-term outcome and structural integrity following open repair of massive rotator cuff tears.
        Int. J. Shoulder Surg. 2012; 6: 1-8
        • Berth A.
        • Neumann W.
        • Awiszus F.
        • Pap G.
        Massive rotator cuff tears: functional outcome after debridement or arthroscopic partial repair.
        J. Orthop. Traumatol. 2010; 11: 13-20
        • Bouillard K.
        • Nordez A.
        • Hug F.
        Estimation of individual muscle force using elastography.
        PLoS One. 2011; 6: e29261
        • Caldwell G.L.
        • Warner J.P.
        • Miller M.D.
        • Boardman D.
        • Towers J.
        • Debski R.
        Strength of fixation with transosseous sutures in rotator cuff repair.
        J. Bone Joint Surg. Am. 1997; 79: 1064-1068
        • Eby S.F.
        • Cloud B.A.
        • Brandenburg J.E.
        • Giambini H.
        • Song P.
        • Chen S.
        • Lebrasseur N.K.
        • An K.N.
        Shear wave elastography of passive skeletal muscle stiffness: influences of sex and age throughout adulthood.
        Clin. Biomech. (Bristol, Avon). 2015; 30: 22-27
        • 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 Elb. Surg. 1999; 8: 599-605
        • Gazielly D.F.
        • Gleyze P.
        • Montagnon C.
        Functional and anatomical results after rotator cuff repair.
        Clin. Orthop. Relat. Res. 1994; : 43-53
        • Gerber C.
        • Meyer D.C.
        • Schneeberger A.G.
        • Hoppeler H.
        • von Rechenberg B.
        Effect of tendon release and delayed repair on the structure of the muscles of the rotator cuff: an experimental study in sheep.
        J. Bone Joint Surg. Am. 2004; 86-A: 1973-1982
        • Gerber C.
        • Schneeberger A.G.
        • Hoppeler H.
        • Meyer D.C.
        Correlation of atrophy and fatty infiltration on strength and integrity of rotator cuff repairs: a study in thirteen patients.
        J. Shoulder Elb. Surg. 2007; 16: 691-696
        • Giambini H.
        • Hatta T.
        • Krzysztof G.R.
        • Widholm P.
        • Karlsson A.
        • Leinhard O.D.
        • Adkins M.C.
        • Zhao C.
        • An K.N.
        Intramuscular fat infiltration evaluated by magnetic resonance imaging predicts the extensibility of the supraspinatus muscle.
        Muscle Nerve. 2017; 57: 129-135
        • Gladstone J.N.
        • Bishop J.Y.
        • Lo I.K.
        • Flatow E.L.
        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. 2007; 35: 719-728
        • Goutallier D.
        • Postel J.M.
        • Bernageau J.
        • Lavau L.
        • Voisin M.C.
        Fatty muscle degeneration in cuff ruptures. Pre- and postoperative evaluation by CT scan.
        Clin. Orthop. Relat. Res. 1994; : 78-83
        • Goutallier D.
        • Postel J.M.
        • Gleyze P.
        • Leguilloux P.
        • Van Driessche S.
        Influence of cuff muscle fatty degeneration on anatomic and functional outcomes after simple suture of full-thickness tears.
        J. Shoulder Elb. Surg. 2003; 12: 550-554
        • Gumucio J.P.
        • Korn M.A.
        • Saripalli A.L.
        • Flood M.D.
        • Phan A.C.
        • Roche S.M.
        • Lynch E.B.
        • Claflin D.R.
        • Bedi A.
        • Mendias C.L.
        Aging-associated exacerbation in fatty degeneration and infiltration after rotator cuff tear.
        J. Shoulder Elb. Surg. 2014; 23: 99-108
        • Harryman 2nd, D.T.
        • Mack L.A.
        • Wang K.Y.
        • Jackins S.E.
        • Richardson M.L.
        • Matsen 3rd, F.A.
        Repairs of the rotator cuff. Correlation of functional results with integrity of the cuff.
        J. Bone Joint Surg. Am. 1991; 73: 982-989
        • Hatta T.
        • Giambini H.
        • Uehara K.
        • Okamoto S.
        • Chen S.
        • Sperling J.W.
        • Itoi E.
        • An K.N.
        Quantitative assessment of rotator cuff muscle elasticity: reliability and feasibility of shear wave elastography.
        J. Biomech. 2015; 48: 3853-3858
        • Hatta T.
        • Giambini H.
        • Uehara K.
        • Okamoto S.
        • Chen S.
        • Sperling J.W.
        • Itoi E.
        • An K.N.
        Quantitative assessment of rotator cuff muscle elasticity: reliability and feasibility of shear wave elastography.
        J. Biomech. 2015; 48: 3853-3858
        • Hatta T.
        • Giambini H.
        • Hooke A.W.
        • Zhao C.
        • Sperling J.W.
        • Steinmann S.P.
        • Yamamoto N.
        • Itoi E.
        • An K.N.
        Comparison of passive stiffness changes in the supraspinatus muscle after double-row and knotless transosseous-equivalent rotator cuff repair techniques: a cadaveric study.
        Arthroscopy. 2016; 32: 1973-1981
        • Hatta T.
        • Giambini H.
        • Zhao C.
        • Sperling J.W.
        • Steinmann S.P.
        • Itoi E.
        • An K.N.
        Biomechanical effect of margin convergence techniques: quantitative assessment of supraspinatus muscle stiffness.
        PLoS One. 2016; 11: e0162110
        • Hatta T.
        • Giambini H.
        • Itoigawa Y.
        • Hooke A.W.
        • Sperling J.W.
        • Steinmann S.P.
        • Itoi E.
        • An K.N.
        Quantifying extensibility of rotator cuff muscle with tendon rupture using shear wave elastography: a cadaveric study.
        J. Biomech. 2017; 61: 131-136
        • Hersche O.
        • Gerber C.
        Passive tension in the supraspinatus musculotendinous unit after long-standing rupture of its tendon: a preliminary report.
        J. Shoulder Elb. Surg. 1998; 7: 393-396
        • Hug F.
        • Tucker K.
        • Gennisson J.L.
        • Tanter M.
        • Nordez A.
        Elastography for muscle biomechanics: toward the estimation of individual muscle force.
        Exerc. Sport Sci. Rev. 2015; 43: 125-133
        • Iannotti J.P.
        • Deutsch A.
        • Green A.
        • Rudicel S.
        • Christensen J.
        • Marraffino S.
        • Rodeo S.
        Time to failure after rotator cuff repair: a prospective imaging study.
        J. Bone Joint Surg. Am. 2013; 95: 965-971
        • Itoigawa Y.
        • Sperling J.W.
        • Steinmann S.P.
        • Chen Q.
        • Song P.
        • Chen S.
        • Itoi E.
        • Hatta T.
        • An K.N.
        Feasibility assessment of shear wave elastography to rotator cuff muscle.
        Clin. Anat. 2015; 28: 213-218
        • Kim H.M.
        • Dahiya N.
        • Teefey S.A.
        • Keener J.D.
        • Galatz L.M.
        • Yamaguchi K.
        Relationship of tear size and location to fatty degeneration of the rotator cuff.
        J. Bone Joint Surg. Am. 2010; 92: 829-839
        • Kim H.M.
        • Galatz L.M.
        • Lim C.
        • Havlioglu N.
        • Thomopoulos S.
        The effect of tear size and nerve injury on rotator cuff muscle fatty degeneration in a rodent animal model.
        J. Shoulder Elb. Surg. 2012; 21: 847-858
        • Kutner M.H.
        • Nachtsheim C.
        • Neter J.
        Applied Linear Regression Models.
        McGraw-Hill/Irwin, 2004
        • Lohr J.F.
        • Uhthoff H.K.
        The microvascular pattern of the supraspinatus tendon.
        Clin. Orthop. Relat. Res. 1990; : 35-38
        • Meyer D.C.
        • Jacob H.A.
        • Nyffeler R.W.
        • Gerber C.
        In vivo tendon force measurement of 2-week duration in sheep.
        J. Biomech. 2004; 37: 135-140
        • Meyer D.C.
        • Lajtai G.
        • von Rechenberg B.
        • Pfirrmann C.W.
        • Gerber C.
        Tendon retracts more than muscle in experimental chronic tears of the rotator cuff.
        J. Bone Joint Surg. (Br.). 2006; 88: 1533-1538
        • Milgrom C.
        • Schaffler M.
        • Gilbert S.
        • van Holsbeeck M.
        Rotator-cuff changes in asymptomatic adults. The effect of age, hand dominance and gender.
        J. Bone Joint Surg. (Br.). 1995; 77: 296-298
        • Minagawa H.
        • Yamamoto N.
        • Abe H.
        • Fukuda M.
        • Seki N.
        • Kikuchi K.
        • Kijima H.
        • Itoi E.
        Prevalence of symptomatic and asymptomatic rotator cuff tears in the general population: from mass-screening in one village.
        J. Orthop. 2013; 10: 8-12
        • Post M.
        • Silver R.
        • Singh M.
        Rotator cuff tear. Diagnosis and treatment.
        Clin. Orthop. Relat. Res. 1983; : 78-91
        • Rathbun J.B.
        • Macnab I.
        The microvascular pattern of the rotator cuff.
        J. Bone Joint Surg. (Br.). 1970; 52: 540-553
        • Rydell J.
        • Knutsson H.
        • Pettersson J.
        • Johansson A.
        • Farneback G.
        • Dahlqvist O.
        • Lundberg P.
        • Nystrom F.
        • Borga M.
        Phase sensitive reconstruction for water/fat separation in MR imaging using inverse gradient.
        in: Med Image Comput Comput Assist Interv. 10. 2007: 210-218
        • Schwartz C.
        • Croisier J.L.
        • Rigaux E.
        • Denoel V.
        • Bruls O.
        • Forthomme B.
        Dominance effect on scapula 3-dimensional posture and kinematics in healthy male and female populations.
        J. Shoulder Elb. Surg. 2014; 23: 873-881
        • Ward S.R.
        • Hentzen E.R.
        • Smallwood L.H.
        • Eastlack R.K.
        • Burns K.A.
        • Fithian D.C.
        • Friden J.
        • Lieber R.L.
        Rotator cuff muscle architecture: implications for glenohumeral stability.
        Clin. Orthop. Relat. Res. 2006; 448: 157-163
        • Wu G.
        • van der Helm F.C.
        • Veeger H.E.
        • Makhsous M.
        • Van Roy P.
        • Anglin C.
        • Nagels J.
        • Karduna A.R.
        • McQuade K.
        • Wang X.
        • Werner F.W.
        • Buchholz B.
        • International Society of, B
        ISB recommendation on definitions of joint coordinate systems of various joints for the reporting of human joint motion–part II: shoulder, elbow, wrist and hand.
        J. Biomech. 2005; 38: 981-992
        • Yamamoto A.
        • Takagishi K.
        • Osawa T.
        • Yanagawa T.
        • Nakajima D.
        • Shitara H.
        • Kobayashi T.
        Prevalence and risk factors of a rotator cuff tear in the general population.
        J. Shoulder Elb. Surg. 2010; 19: 116-120
        • Yushkevich P.A.
        • Piven J.
        • Hazlett H.C.
        • Smith R.G.
        • Ho S.
        • Gee J.C.
        • Gerig G.
        User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability.
        NeuroImage. 2006; 31: 1116-1128
        • Zumstein M.A.
        • Jost B.
        • Hempel J.
        • Hodler J.
        • Gerber C.
        The clinical and structural long-term results of open repair of massive tears of the rotator cuff.
        J. Bone Joint Surg. Am. 2008; 90: 2423-2431