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Editorial Commentary: Monitoring Tendon and Muscle Recovery After Rotator Cuff Repair Using Diagnostic Ultrasound Demonstrates that Early Repair is Beneficial for Many Patients With Reparable Tears

      Abstract

      Rotator cuff repair is performed to effect healing of the enthesis; to restore shoulder comfort, strength, and function; to prevent tear propagation; and to prevent progression of atrophic muscle changes (fatty degeneration, fatty infiltration, and fatty atrophy) that eventually occur. Non-retracted and moderately retracted rotator cuff tears usually heal after repair, and muscle atrophy may recover over time. It follows that early rotator cuff repair is beneficial for many patients with chronic but reparable rotator cuff tears. Diagnostic ultrasound can provide quantitative information about the recovery of both muscle and tendon and represents a viable alternative to magnetic resonance imaging for evaluating healing after rotator cuff repair.
      Rotator cuff repair is performed to restore shoulder comfort, strength, and function, but also to prevent tear propagation and progression of the atrophic muscle changes that eventually occur. These atrophic changes are characterized as fatty degeneration, fatty infiltration, and fatty atrophy and are often used interchangeably.
      • Kuzel B.R.
      • Grindel S.
      • Papandrea R.
      • Ziegler D.
      Fatty infiltration and rotator cuff atrophy.
      Both muscle atrophy and fatty infiltration are independently associated processes
      • Barry J.J.
      • Lansdown D.A.
      • Cheung S.
      • Feeley B.T.
      • Ma C.B.
      The relationship between tear severity, fatty infiltration, and muscle atrophy in the supraspinatus.
      and independent predictors of outcome after rotator cuff repair.
      • 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.
      Mechanical unloading of the rotator cuff muscles that occurs with chronic tears has also been shown to increase the pennation angle of muscle fibers.
      • Kuzel B.R.
      • Grindel S.
      • Papandrea R.
      • Ziegler D.
      Fatty infiltration and rotator cuff atrophy.
      ,
      • Tomioka T.
      • Minagawa H.
      • Kijima H.
      • et al.
      Sarcomere length of torn rotator cuff muscle.
      As the myotendinous unit retracts, the muscle fibers reorient, and interstitial fat and fibrous tissue gradually occupy the spaces between the reoriented muscle fibers
      • Meyer D.C.
      • Hoppeler H.
      • von Rechenberg B.
      • Gerber C.
      A pathomechanical concept explains muscle loss and fatty muscular changes following surgical tendon release.
      , although the muscle fibers themselves do not degenerate.
      • Kuzel B.R.
      • Grindel S.
      • Papandrea R.
      • Ziegler D.
      Fatty infiltration and rotator cuff atrophy.
      Suprascapular nerve injury has also been implicated in the pathogenesis of atrophic muscle changes that occur with chronic rotator cuff tears. Retracted supraspinatus tears increase tension on the suprascapular nerve at the suprascapular notch,
      • Albritton M.J.
      • Graham R.D.
      • Richards II, R.S.
      • Basamania C.J.
      An anatomic study of the effects on the suprascapular nerve due to retraction of the supraspinatus muscle after rotator cuff tear.
      ,
      • Mallon W.J.
      • Wilson R.J.
      • Basamania C.J.
      The association of suprascapular neuropathy with massive rotator cuff tears. A preliminary report.
      and combined supraspinatus and infraspinatus tears may cause suprascapular nerve injury at the spinoglenoid notch.
      • Costouros J.G.
      • Porramatikul M.
      • Lie D.T.
      • Warner J.J.
      Reversal of supracapular neuropathy following arthroscopic repair of massive supraspinatus and infraspinatus rotator cuff tears.
      Additionally, suprascapular nerve recovery has been demonstrated following rotator cuff repair.
      • Costouros J.G.
      • Porramatikul M.
      • Lie D.T.
      • Warner J.J.
      Reversal of supracapular neuropathy following arthroscopic repair of massive supraspinatus and infraspinatus rotator cuff tears.
      Despite these benefits of rotator cuff repair, the classic teaching has been that repair does not predictably reverse rotator cuff muscle atrophy or fatty infiltration.
      • 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.
      ,
      • Deniz G.
      • Kose O.
      • Tugay A.
      • Guler F.
      • Turan A.
      Fatty degeneration and atrophy of the rotator cuff muscles after arthroscopic repair: does it improve, halt or deteriorate?.
      ,
      • Hata Y.
      • Saitoh S.
      • Murakami N.
      • Kobayashi H.
      • Kaito T.
      • Kato H.
      Volume changes of supraspinatus and infraspinatus muscles after supraspinatus tendon repair: A magnetic resonance imaging study.
      ,
      • 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.
      Instead, the progression of muscle atrophy can be slowed or stopped in some cases by successful healing following repair.
      • Fabbri M.
      • Ciompi A.
      • Lanzetti R.M.
      • et al.
      Muscle atrophy and fatty infiltration in rotator cuff tears: Can surgery stop muscular degenerative changes?.
      ,
      • Liem D.
      • Lichtenberg S.
      • Magosch P.
      • Habermeyer P.
      Magnetic resonance imaging of arthroscopic supraspinatus tendon repair.
      Fabbri et al. demonstrated that patients who underwent arthroscopic rotator cuff repair had no muscle atrophy progression, as compared to patients undergoing long-term nonoperative treatment.
      • Fabbri M.
      • Ciompi A.
      • Lanzetti R.M.
      • et al.
      Muscle atrophy and fatty infiltration in rotator cuff tears: Can surgery stop muscular degenerative changes?.
      However, the irreversibility of the progressive atrophic muscle changes associated with chronic rotator cuff tears has been challenged by several studies that have reported on varying degrees of reversal of muscle atrophy following successful rotator cuff repair.
      • Thomazeau H.
      • Rolland Y.
      • Lucas C.
      • Duval J.M.
      • Langlais F.
      Atrophy of the supraspinatus belly: Assessment by MRI in 55 patients with rotator cuff pathology.
      • 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.
      • Gerber C.
      • Fuchs B.
      • Hodler J.
      The results of repair of massive tears of the rotator cuff.
      • Lhee S.-H.
      • Singh A.K.
      • Lee D.Y.
      Does magnetic resonance imaging appearance of supraspinatus muscle atrophy change after repairing rotator cuff tears?.
      A recent study found that preoperative tendon retraction was the most important predictor of improvement in muscle atrophy following repair, although patient age was important as well.
      • Lhee S.-H.
      • Singh A.K.
      • Lee D.Y.
      Does magnetic resonance imaging appearance of supraspinatus muscle atrophy change after repairing rotator cuff tears?.
      Other factors, such as tear acuity, location, and size, and patient factors, such as general health and compliance with postoperative exercise, may also play a role.
      Magnetic resonance imaging (MRI) is the standard-of-care imaging modality for evaluating the rotator cuff myotendinous unit.
      • Ma J.
      • Sahoo S.
      • Imrey P.B.
      • et al.
      Inter-rater agreement of rotator cuff tendon and muscle MRI parameters evaluated preoperatively and during the first postoperative year following rotator cuff repair. J Shoulder Elbow Surg.
      MRI is used to evaluate tear location, thickness (partial or full), tear size, and degree of retraction. MRI is also used for evaluating muscle quality, including fatty infiltration and atrophy, and for evaluating associated and adjacent soft tissue, cartilage, and bony lesions. The degree of muscle atrophy can be defined by the tangent sign, or by the occupation radio, which is the ratio of the cross-sectional area of the supraspinatus muscle to that of the entire supraspinatus fossa, at a standardized location, typically the most lateral sagittal oblique MRI image, where the scapular spine contacts the scapular body.
      • Kuzel B.R.
      • Grindel S.
      • Papandrea R.
      • Ziegler D.
      Fatty infiltration and rotator cuff atrophy.
      A recent study has demonstrated good to excellent agreement in rating muscle atrophy and cross-sectional area, but less agreement for fatty infiltration.
      • Ma J.
      • Sahoo S.
      • Imrey P.B.
      • et al.
      Inter-rater agreement of rotator cuff tendon and muscle MRI parameters evaluated preoperatively and during the first postoperative year following rotator cuff repair. J Shoulder Elbow Surg.
      Ultrasound is another diagnostic tool for evaluating rotator cuff disorders. Benefits of diagnostic ultrasound include affordability, portability, lack of ionizing radiation, and ease of use. Additionally, ultrasound is a dynamic study that can provide real-time feedback to patients regarding their pathoanatomy.
      • Kuzel B.R.
      • Grindel S.
      • Papandrea R.
      • Ziegler D.
      Fatty infiltration and rotator cuff atrophy.
      Diagnostic ultrasound has been found to have similar specificity and sensitivity to non-contrast enhanced MRI for both partial and full-thickness rotator cuff tears.
      • de Jesus J.O.
      • Parker L.
      • Frangos A.J.
      • Nazarian L.N.
      Accuracy of MRI, MR arthrography, and ultrasound in the diagnosis of rotator cuff tears: A meta-analysis.
      Limitations of diagnostic ultrasound are that it is highly operator-dependent and requires substantial experience and technical skill.
      • Kuzel B.R.
      • Grindel S.
      • Papandrea R.
      • Ziegler D.
      Fatty infiltration and rotator cuff atrophy.
      Ultrasound has typically been used mostly to evaluate rotator cuff tendons rather than their muscles. Additionally, shoulder surgeons lack confidence in the ability of diagnostic ultrasound to quantify rotator cuff muscle atrophy and fatty infiltration, as well as tendon retraction, medial to the acromion.
      • Kruse K.K.
      • Dilisio M.F.
      • Wang W.L.
      • Schmidt C.C.
      Do we really need to order magnetic resonance imaging? Shoulder surgeon ultrasound practice patterns and beliefs.
      Recently, several studies have demonstrated the utility of diagnostic ultrasound for evaluating rotator cuff muscle atrophy and fatty infiltration and have concluded that it may be comparable to MRI.
      • Kuzel B.R.
      • Grindel S.
      • Papandrea R.
      • Ziegler D.
      Fatty infiltration and rotator cuff atrophy.
      ,
      • de Jesus J.O.
      • Parker L.
      • Frangos A.J.
      • Nazarian L.N.
      Accuracy of MRI, MR arthrography, and ultrasound in the diagnosis of rotator cuff tears: A meta-analysis.
      ,
      • Apostolopoulos A.P.
      • Angelis S.
      • Yallapragada R.K.
      • et al.
      The sensitivity of magnetic resonance imaging and ultrasonography in detecting rotator cuff tears.
      ,
      • Okoroha K.R.
      • Mehran N.
      • Duncan J.
      • et al.
      Characterization of rotator cuff tears: Ultrasound versus magnetic resonance imaging.
      Khoury et al. evaluated 45 shoulders in 39 patients and determined that muscle occupation ratios had a correlation of .90 when measured using both MRI and ultrasound.
      • Khoury V.
      • Cardinal E.
      • Brassard P.
      Atrophy and fatty infiltration of the supraspinatus muscle: Sonography versus MRI.
      The authors also evaluated fatty infiltration using ultrasound to grade echogenicity as mild or marked and to qualitatively grade muscle pennation pattern as normal, effaced, or absent.
      • Kuzel B.R.
      • Grindel S.
      • Papandrea R.
      • Ziegler D.
      Fatty infiltration and rotator cuff atrophy.
      ,
      • Khoury V.
      • Cardinal E.
      • Brassard P.
      Atrophy and fatty infiltration of the supraspinatus muscle: Sonography versus MRI.
      The authors could distinguish mild from severe fatty infiltration but were unable to distinguish moderate from severe fatty infiltration.
      • Khoury V.
      • Cardinal E.
      • Brassard P.
      Atrophy and fatty infiltration of the supraspinatus muscle: Sonography versus MRI.
      In the study entitled “Diagnostic Ultrasound Shows Reversal of Supraspinatus Muscle Atrophy Following Arthroscopic Rotator Cuff Repair” authors Pagán-Conesa, García-Ortiz, Emilio José Salmerón-Martínez, Moya-Martínez, and López-Prats report on using diagnostic ultrasound to evaluate and quantify supraspinatus muscle atrophy, and to determine whether there is any relationship between supraspinatus repair and eventual recovery of the myotendinous unit.
      • Pagán-Conesa A.
      • García-Ortiz M.T.
      • Salmerón-Martínez E.J.
      • Moya-Martínez A.
      • López-Prats F.
      Diagnostic ultrasound shows reversal of supraspinatus muscle atrophy following arthroscopic rotator cuff repair.
      The authors develop and use various quantitative ultrasound-based measures to conclude that atrophic muscle changes can be reversed following supraspinatus repair.
      • Pagán-Conesa A.
      • García-Ortiz M.T.
      • Salmerón-Martínez E.J.
      • Moya-Martínez A.
      • López-Prats F.
      Diagnostic ultrasound shows reversal of supraspinatus muscle atrophy following arthroscopic rotator cuff repair.
      Specifically, the measures comprise the occupation ratio previously described by Thomazeau,
      • Thomazeau H.
      • Rolland Y.
      • Lucas C.
      • Duval J.M.
      • Langlais F.
      Atrophy of the supraspinatus belly: Assessment by MRI in 55 patients with rotator cuff pathology.
      a representative histogram of supraspinatus muscle pixilation as a marker of atrophy, a histogram ratio that normalizes pixel distribution to that of the trapezius muscle, echogenicity reduction following repair, muscle pennate pattern, and pennation angle changes following repair. Other studies have reported on echogenicity,
      • Khoury V.
      • Cardinal E.
      • Brassard P.
      Atrophy and fatty infiltration of the supraspinatus muscle: Sonography versus MRI.
      but measures such as the histogram and histogram ratio are novel and have not yet been validated. Pennation angle is thought be a marker for fatty infiltration. Some studies have measured changes in pennation angle following repair.
      • Hayashi I.
      • Enokida M.
      • Nagira K.
      • et al.
      Change in the pennation angle of the supraspinatus muscle after rotator cuff tear repair.
      However, it remains unclear how often pennation angle can be determined precisely. It is also unclear how often muscle visualization by ultrasound is obscured by acromion shadowing, although this may be less of an issue for the supraspinatus than for the posterior cuff muscles.
      • Kim S.
      • Bleakney R.
      • Boynton E.
      • Ravichandiran K.
      • Rindlisbacher T.
      • McKee N.
      • Agur A.
      Investigation of the static and dynamic musculotendinous architecture of supraspinatus.
      The authors stress that one advantage of these quantitative measures is that they are obtained in a semiautomated manner that minimizes operator dependency.
      • Pagán-Conesa A.
      • García-Ortiz M.T.
      • Salmerón-Martínez E.J.
      • Moya-Martínez A.
      • López-Prats F.
      Diagnostic ultrasound shows reversal of supraspinatus muscle atrophy following arthroscopic rotator cuff repair.
      The authors demonstrate that Patte II rotator cuff tears,
      • Patte D.
      Classification of rotator cuff lesions.
      with intermediate retraction to the level of the humeral head, had the greatest improvements after repair, as demonstrated by diagnostic ultrasound. Patte III tears demonstrate less muscle recovery after repair, and Patte I tears typically did not have muscle atrophy preoperatively, so there was little room for improvement. The authors suggest that more timely repairs produced better clinical and ultrasound-based results, irrespective of whether single or double repair was carried out. Conversely, larger more retracted tears demonstrated inferior clinical and ultrasound-based results.
      Concerns have been raised that two-dimensional assessment of muscle, such as from a single MRI slice or from diagnostic ultrasound, does not predict muscle volume and is of limited use for quantifying muscle atrophy or fatty infiltration.
      • Vidt M.E.
      • Santago 2nd, A.C.
      • Tuohy C.J.
      • et al.
      Assessments of fatty infiltration and muscle atrophy from a single magnetic resonance image slice are not predictive of 3-dimensional measurements.
      The rotator cuff muscles are fusiform so that a smaller preoperative muscle cross-sectional area may simply reflect retraction of the myotendinous unit. Consequently, lateralization of the supraspinatus muscle following repair may falsely increase the occupation ratio and change the portion of the muscle being evaluated for fatty infiltration.
      • Kuzel B.R.
      • Grindel S.
      • Papandrea R.
      • Ziegler D.
      Fatty infiltration and rotator cuff atrophy.
      ,
      • Sasaki T.
      • Shitara H.
      • Yamamoto A.
      • et al.
      What is the appropriate reference for evaluating the recovery of supraspinatus muscle atrophy after arthroscopic rotator cuff repair? The occupation ratio of the supraspinatus may change after rotator cuff repair without volumetric improvement.
      Some authors have suggested that immediate postoperative imaging should be used as a baseline because this corrects for the effect of myotendinous retraction.
      • Sasaki T.
      • Shitara H.
      • Yamamoto A.
      • et al.
      What is the appropriate reference for evaluating the recovery of supraspinatus muscle atrophy after arthroscopic rotator cuff repair? The occupation ratio of the supraspinatus may change after rotator cuff repair without volumetric improvement.
      ,
      • Mascarenhas R.
      • Verma N.K.
      Editorial Commentary: Muscle atrophy after arthroscopic rotator cuff repair—Reversible?.
      Jo et al. examined the effect of arthroscopic rotator cuff repair on rotator cuff muscle atrophy at various time points, including preoperatively, immediately postoperatively, and 1 year postoperatively.
      • Jo C.H.
      • Park J.W.
      • Shin J.S.
      Changes of muscle atrophy according to the immediate postoperative time point in magnetic resonance imaging after arthroscopic rotator cuff repair.
      They found that rotator cuff muscle atrophy typically improves after arthroscopic repair, but that increased atrophy is seen 1 year postoperatively as compared with immediately postoperatively. Hamano et al. found that muscle atrophy and fatty infiltration improved after rotator cuff repair, but they compared MRI-based measures at 2 years to those at 2 weeks postoperative to eliminate any effects related to medial tendon retraction.
      • Hamano N.
      • Yamamoto A.
      • Shitara H.
      • et al.
      Does successful rotator cuff repair improve muscle atrophy and fatty infiltration of the rotator cuff? A retrospective magnetic resonance imaging study performed shortly after surgery as a reference.
      Kim et al. compared MRI findings at 6 months following supraspinatus repair to those obtained 1-2 days following MRI and found that the supraspinatus cross-sectional area decreased significantly, whereas the Goutallier stage and Thomazeau grade remained similar.
      • Kim H.B.
      • Yoo J.C.
      • Jeong J.Y.
      Evaluation of muscular atrophy and fatty infiltration using time-zero magnetic resonance imaging as baseline data, after rotator cuff repair.
      Additionally, there remains the possibility that some of the intact repairs in the study by Pagán-Conesa et al. may have been retears with continuity,
      • McCarron J.A.
      • Derwin K.A.
      • Bey M.J.
      • et al.
      Failure with continuity in rotator cuff repair "healing".
      in which the repair is characterized by a distinctive continuity of nontendinous tissue from the footprint to the retracted tendinous portion.
      • Youn S.M.
      • Rhee Y.G.
      • Rhee S.M.
      Nontendinous healing after repairing of retracted rotator cuff tear: An imaging study. J Shoulder Elbow Surg.
      This has been described previously using MRI,
      • McCarron J.A.
      • Derwin K.A.
      • Bey M.J.
      • et al.
      Failure with continuity in rotator cuff repair "healing".
      ,
      • Youn S.M.
      • Rhee Y.G.
      • Rhee S.M.
      Nontendinous healing after repairing of retracted rotator cuff tear: An imaging study. J Shoulder Elbow Surg.
      but it is unclear whether these retears with continuity are identified accurately by ultrasound or whether the authors entertained this possible outcome following repair. Previous study has demonstrated that retracted tears are a risk factor for retears with continuity.
      • Weir T.B.
      • Gilotra M.N.
      • Foster M.J.
      • et al.
      Preoperative tendon retraction, not smoking, is a risk factor for failure with continuity after rotator cuff repair.
      The myotendinous junction retracts in these retears with continuity, which would obviously influence pennation angle and cross-sectional area measures.
      Overall, the authors focused on differences between preoperative and 12 months postoperative ultrasound, but as noted above, the improvements may relate to lateralization of supraspinatus muscle following repair. The authors chose to omit the discussion of the 1-month and 6-month postoperative findings because their statistical analysis did not reveal any differences. I am surprised by their decision because if the authors could demonstrate that muscle atrophy did not progress between 1 month and 12 months, then this would represent an even more important finding and would demonstrate that repair prevents progression of atrophic muscle changes. The authors conceded that they could not measure reproducibly sagittal cross-sectional area by ultrasound, so they could not demonstrate any increase in muscle volume following rotator cuff repair.
      • Pagán-Conesa A.
      • García-Ortiz M.T.
      • Salmerón-Martínez E.J.
      • Moya-Martínez A.
      • López-Prats F.
      Diagnostic ultrasound shows reversal of supraspinatus muscle atrophy following arthroscopic rotator cuff repair.
      Using preoperative measures, rather than immediate postoperative measures as the baseline and failing to quantify volumetric muscle changes are the two principal limitations of their study.
      Despite these limitations and concerns regarding the use of diagnostic ultrasound for quantifying muscle recovery following rotator cuff repair, the study by Pagán-Conesa et al. reinforces our understanding that early repair of supraspinatus tendon tears that are not severely retracted leads to tendon healing in most cases, substantial clinical improvement, and the potential for some muscle recovery.
      • Pagán-Conesa A.
      • García-Ortiz M.T.
      • Salmerón-Martínez E.J.
      • Moya-Martínez A.
      • López-Prats F.
      Diagnostic ultrasound shows reversal of supraspinatus muscle atrophy following arthroscopic rotator cuff repair.
      Additionally, the study extends previous work on using diagnostic ultrasound to evaluate both rotator cuff tendons and muscles. Finally, this study should spawn additional studies into the utility of ultrasound for evaluating muscle atrophy and fatty infiltration and explore ultrasound’s potential role as a tool to evaluate biological and other repair strategies that may promote tendon and muscle healing and recovery.

      Supplementary Data

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