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Background: The role of degenerative changes in rotator cuff musculature with respect to the functional outcomes of rotator
cuff repair have only recently been recognized and are still not well understood. In addition, the reversibility of these changes
with repair of the tendons is questionable.
Hypothesis: Poorer preoperative muscle quality negatively affects outcome, and a successful outcome (in terms of a healed
repair) might demonstrate improvements in fatty infiltration and muscle atrophy.
Study Design: Cohort study; Level of evidence, 2.
Methods: Thirty-eight patients (mean age, 62 years) were prospectively evaluated with preoperative and 1-year postoperative
clinical examination and appropriate magnetic resonance image sequencing to determine grades of muscle atrophy and fatty
infiltration of the supraspinatus and infraspinatus muscles. American Shoulder and Elbow Society (ASES), Constant, and pain
scores were determined as well as strength measurements. The retear rate and progression of muscle degeneration were also
evaluated. Independent predictors of outcome measurements and cuff integrity were determined.
Results: The overall clinical outcome, including ASES, Constant, and pain scores, improved significantly (P < .0001). Strength in for-
ward elevation improved significantly (P < .006), while external rotation strength did not. There was a strongly negative correlation
between muscle quality and outcome results in most cases. When the results were adjusted for multivariate effect, muscle atrophy
and fatty infiltration of the infraspinatus muscle were the only independent predictors of ASES and Constant scores (P < .03). Tear
size and rotator cuff healing did not play an independent role. Tear size, however, was the only independent predictor of ultimate cuff
integrity (P = .002). Both atrophy and fatty infiltration progressed significantly over the course of the study. In cases in which the ten-
don had re-torn, the progression was found to be more significant than when the repair proved successful (P < .003).
Conclusion: Muscle atrophy and fatty infiltration of the rotator cuff muscles, particularly of the infraspinatus, play a significant
role in determining functional outcome after cuff repair. Tear size appears to have the most influential effect on repair integrity. A
successful repair did not lead to improvement or reversal of muscle degeneration and a failed repair resulted in significantly more
progression. In general, healed repairs demonstrated minimal progression. These findings suggest that repairs should be per-
formed, if possible, before more significant deterioration in the cuff musculature in order to optimize outcomes, and that under-
standing the degree of muscle atrophy and fatty infiltration before surgery can help guide patient expectations.
Keywords: rotator cuff tears; rotator cuff repair outcomes; muscle atrophy; fatty infiltration
719
720 Gladstone et al The American Journal of Sports Medicine
muscle quality (fatty infiltration and muscle atrophy) have Outcome Assessment
been implicated as predictors of outcome and repair
integrity, relatively few studies have analyzed the direct The preoperative and postoperative evaluation consisted of
effect of these variables on outcomes. Goutallier et al9 were a patient-based questionnaire and physical examination
one of the first groups to demonstrate a highly negative cor- performed by an independent examiner (our shoulder fel-
relation between fatty infiltration of the infraspinatus mus- low). The examination included measurement of range of
cle and outcome. Thomazeau et al18 and Gerber et al7 showed motion and strength testing with the use of a dynamome-
a direct correlation between increasing muscle atrophy and ter in both forward elevation and external rotation.
retearing of a repair. In these 2 studies, atrophy had a chance Forward elevation strength was assessed with the
to improve if the repair remained healed. Fatty infiltration, patient’s arm abducted 90° in the scapular plane, with the
on the other hand, never regressed, even with a successful elbow extended and forearm pronated. Resistance was
repair. To our knowledge, no study has used a regression applied at the wrist and the measurement recorded in
analysis model to determine the independent effect of vari- pounds. External rotation was measured with the arm at
ables such as initial tear size, muscle quality, and tendon the side, the elbow flexed 90°, and the wrist in neutral
integrity on outcome. rotation. Resistance was applied at the wrist and meas-
In this study, we analyzed the effect of muscle quality on ured in pounds. These evaluations allowed the calculation
measures of functional outcome including American of several standard shoulder-specific scores, including the
Shoulder and Elbow Society (ASES) and Constant scores, Constant score, the ASES survey, and a visual analog scale
pain, strength, and the structural integrity of the repair. In (VAS) pain score.
addition, we evaluated the progression (or regression) of
fatty infiltration and muscle atrophy during the study
interval. We hypothesized that poorer preoperative muscle Radiographic Assessment
quality would negatively affect outcome, and that a suc-
Because many of the patients brought their MRI scans to
cessful outcome (in terms of a healed repair) might demon-
their first office visit, only the postoperative MRI was
strate improvements in fatty infiltration and muscle
standardized. The protocol for the postoperative MRI con-
atrophy. A clearer understanding of these factors would
sisted of coronal images in both T1 and inversion recovery
allow better preoperative counseling and decision-making
(IR) format with 3-mm slices, sagittal oblique images in IR
as to the most appropriate treatment plan.
format with 3-mm slices, and axial images in T1 format
with 4-mm slices. Rotator cuff integrity, fatty infiltration,
MATERIALS AND METHODS and muscular atrophy were evaluated and graded by 2
independent examiners and, if necessary, a consensus
Patient Enrollment agreement was reached. Any tendon defect on the T2-
weighted sequence that filled with fluid was considered
Thirty-eight patients were enrolled in this study. The a retear. No attempt was made to compare defect size at
patients were a subset of a larger prospective, Institu- follow-up with the preoperative tear size.
tional Review Board–approved study using postoperative Fatty infiltration was evaluated using the criteria estab-
MRI to evaluate rotator cuff integrity at a minimum of 1 lished by Goutallier et al9 on the basis of fatty streaks within
year after repair. The larger study was conducted to eval- the muscle belly. This classification system, originally
uate the functional outcome and repair integrity in open described for CT, was applied to the T1-weighted coronal MRI
rotator cuff repairs compared with arthroscopic repairs.3 sequences in this study: grade 0, no fat; grade 1, thin streaks
Patients were included in this study if both the preoper- of fat; grade 2, less fat than muscle; grade 3, equal amounts of
ative and postoperative MRI scans permitted appropriate fat and muscle; and grade 4, more fat than muscle. Previous
evaluation of fatty infiltration and, in particular, were studies have found that this staging system can be appropri-
medial enough on the T1-weighted sagittal oblique view ately applied to MRI.5,20 Additionally, for some of the statisti-
to allow determination of muscle atrophy. All patients cal analyses, the grades were dichotomized into none to mild
had full-thickness rotator cuff tears diagnosed by MRI fatty infiltration (grades 0 and 1) and moderate to severe fatty
preoperatively and then confirmed at the time of surgery. infiltration (grades 2 through 4). This dichotimization has
Patients had either an open rotator cuff repair (15 clinical implications because studies have indicated that
patients) or an arthroscopic repair (23 patients) per- grades 0 or 1 are found in both unaffected shoulders as well
formed by one surgeon (E.L.F.), with the open subset as shoulders with rotator cuff tears, while grades 2 or higher
occurring before the use of arthroscopic repair tech- appear only in patients with rotator cuff tears.16,18,21
niques. Patients with concomitant disorders such as Muscle atrophy was graded according to the scale pro-
glenohumeral arthritis, fracture, or osteonecrosis were posed by Warner et al20 (Figure 1), based on an oblique
excluded. All patients had complete clinical and MRI sagittal plane image where the coracoid and scapular
examinations preoperatively and at minimum follow-up spine meet the scapular body. On this view, both the
of 1 year (range, 12 to 15 months), which was part of the supraspinatus and infraspinatus muscle can be seen.
larger study protocol. Atrophy was graded as none, mild, moderate, or severe. For
Vol. 35, No. 5, 2007 Fatty Infiltration and Atrophy After Rotator Cuff Repair 721
TABLE 2
Correlation of Functional Outcome, Tear Size, and Symptom Duration to Muscle Qualitya
Muscle quality P value corr coeff P value corr coeff P value corr coeff P value corr coeff
Supraspinatus fat .17 –0.231 .16 –0.236 .007 –0.457 .012 –0.415
Infraspinatus fat .027 –0.364 .029 –0.359 .0001 –0.637 .001 –0.546
Supraspinatus atrophy .034 –0.354 .015 –0.402 .005 –0.482 .0001 –0.599
Infraspinatus atrophy .014 –0.401 .006 –0.44 .0001 –0.58 .001 –0.6
TABLE 3
Independent Predictors of Functional Outcome, P Valuesa
Supraspinatus Infraspinatus
TABLE 4 100
Correlation of Muscle Quality and 90
Cuff Integrity at Follow-upa 80 70 67
70
Re-tear Rate%
Tendon Repair
60
50
Muscle Healed Retorn P value
40 29
Supraspinatus MA 0.65 1.73 .002 30 22
FI 0.57 1.73 .007 20
Infraspinatus MA 0.30 0.87 .012 10
FI 0.39 0.87 .076 0
None/Mild Mod/Severe None/Mild Mod/Severe
a FI FI MA MA
Comparison of preoperative muscle atrophy (MA) and fatty
infiltration (FI) in the group with a healed rotator cuff repair com- Figure 2. Effect of clinically insignificant versus significant mus-
pared with the retorn group. cle atrophy (MA) and fatty infiltration (FI) on retear rate (P < .05).
TABLE 5
Progression of Fatty Infiltration and Muscle Atrophy Overall, and Differentiating Those With
an Intact Versus Retorn Rotator Cuff
Figure 4. Intact repair with no progression at 1-year follow-up. A, preoperative T1-weighted MRI coronal sequence through the
supraspinatus demonstrating grade 2 fatty infiltration. B, preoperative T1-weighted MRI sagittal sequence demonstrating mini-
mal muscle atrophy of the supraspinatus. C, no progression of supraspinatus fatty infiltration postoperatively. D, no change in
muscle atrophy postoperatively.
the reasons for a poorer outcome have focused on factors of these factors may allow for better preoperative counsel-
such as retear rates, chronicity, and size of tear. Although ing of patients as to expected functional results, and per-
these factors are important, the inherent quality of the haps a clearer indication as to which severely involved
muscle whose tendon is to be repaired may play as criti- tendons should have a repair be attempted.
cal a role in determining the ultimate outcome of a cuff This study demonstrates, as have others,8-10,13,14 the crit-
repair. More recent studies have begun to analyze the ical role muscle quality plays in the outcome of rotator cuff
effect of fatty infiltration and atrophy of the rotator cuff repairs. There is a strongly negative correlation between
musculature on functional outcome after rotator cuff increasing muscle degeneration and poorer functional
repair.7,9,12,14,18,20 These studies have generally focused on outcomes in both assessment scores and strength meas-
the effect of either fatty infiltration9 or muscle atro- urements (Table 2). More interesting, perhaps, is the find-
phy7,18,20 without considering the 2 together, or performing ing that when a regression analysis model is used, both
a regression analysis to distinguish the independent pre- fatty infiltration and muscle atrophy come out as inde-
dictors of functional outcome and repair integrity. In addi- pendent predictors of outcome, apparently overriding the
tion, if muscle degeneration is a determining factor in effect of tear size or repair integrity, both of which were
functional outcome, its regression or progression with a entered into the analysis as variables. While our analysis
cuff repair would be of importance to document. Our study and others15,17,18 have shown a very strong relationship
sought not only to analyze the effect of muscle quality on between fatty infiltration, muscle atrophy, and tear size,
functional outcomes and structural integrity of the repair, these results demonstrate that they cannot be considered
but also to determine the progression, or regression, of interchangeable. Furthermore, these findings stress the
fatty infiltration and atrophy in a group of prospectively importance of appropriately performed MRI to best assess
followed rotator cuff repairs. An enhanced understanding the muscle degeneration in rotator cuff tears preoperatively.
726 Gladstone et al The American Journal of Sports Medicine
Appropriate MRI requires a T1-weighted sequence in both Supraspinatus atrophy only independently affected for-
coronal and sagittal orientations, and cuts sufficiently ward elevation strength, while supraspinatus fatty infil-
medial to evaluate muscle atrophy. tration was an independent predictor of external rotation
The infraspinatus independently predicted functional strength along with fatty infiltration of the infraspinatus.
outcome—atrophy predicted ASES and Constant scores, The seemingly greater importance of the infraspinatus
while fatty infiltration also predicted ASES score. toward function may be because those tears that extend
Interestingly, the supraspinatus did not independently into or involve the infraspinatus are much larger.
predict outcome, and even when the individual unadjusted Additionally, an ineffective infraspinatus, either through
results were considered, supraspinatus fatty infiltration rupture or muscle degeneration, can offset the biomechan-
did not correlate with functional outcome scores. ics of the glenohumeral joint,12,19 thus leading to poorer
Vol. 35, No. 5, 2007 Fatty Infiltration and Atrophy After Rotator Cuff Repair 727
outcomes. Conversely, patients with a torn supraspinatus atrophy7,18 and fatty infiltration9 in cases of successfully
and an intact anterior-posterior force-couple can maintain repaired tendons. While Goutallier et al9 showed that the
good function and strength. Another possible explanation fatty infiltration of the infraspinatus never regressed, even
for greater influence of the infraspinatus may be that with a healed repair, they showed that fatty degeneration
chronic retraction or atrophy of the supraspinatus can of the supraspinatus can reverse and improve, leading to a
cause traction on the suprascapular nerve and subsequent recommendation to operate on wide tears before the
degeneration of the infraspinatus, even in the absence of a appearance of irreversible muscle damage. Gerber et al7
tear of the infraspinatus, as postulated by Albritton et al.1 found that infraspinatus atrophy progressed and was
Goutallier et al9 showed that degeneration of the infra- unaffected by repair integrity, while supraspinatus atro-
spinatus was more of a negative predictor of outcome and phy increased only if the repair failed. In those patients
function than the supraspinatus, even after a successful with a successful repair, there was an improvement in the
rotator cuff repair. Jost et al,12 when evaluating preopera- cross-sectional area of the supraspinatus. Fatty infiltra-
tive and postoperative fatty infiltration of the infraspina- tion, on the other hand, systematically progressed, but sig-
tus and supraspinatus in 20 reruptures of the rotator cuff, nificantly less so when the repair was successful. These
showed that only the amount of postoperative fatty infil- findings were consistent with ours. Thomazeau et al18 also
tration of the infraspinatus was significantly correlated to reported a reversal of supraspinatus atrophy in more than
postoperative Constant scores. half of their intact cuff repairs; however, no reversal was
Cuff integrity after rotator cuff repair was directly influ- seen in those with a failed repair. These data, along with
enced by the degree of muscle degeneration when individ- our results showing the higher rate of progression in those
ual correlations were examined. The only independent with moderate to severe atrophy, support the belief that
predictor of healing of a repair, however, was preoperative rotator cuff repair should occur before irreversible histo-
tear size. This finding is in keeping with the conclusions of logic and electromyographic changes occur.14 In addition,
several historical studies11 emphasizing the correlation of an attempt at the strongest repair possible should always
higher retear rates with a larger preoperative tear size. be undertaken, as the progression rate is greater in cuff
These studies, however, did not examine the effect of mus- muscles with failed repairs.
cle degeneration on healing potential or functional out- There are several limitations to this study, in particular
come. In more recent studies, the effect of muscle quality the small number of patients enrolled. Because many of
on cuff integrity was evaluated, but regression analyses our patients came to their initial visit with MRI scans,
were not performed to determine independent predictors. potential study participants were excluded because of
Thomazeau et al18 found that muscle atrophy of the inadequate preoperative image sequences to allow for ade-
supraspinatus correlated with the severity of rotator cuff quate muscle belly assessment. We did not have a control
disease, and they reported higher retear rates with group in which only a wide bursectomy and débridement
increasing grades of atrophy. They concluded that preoper- without repair was performed. This would have allowed a
ative supraspinatus atrophy was the main predictive fac- comparison of the progression of fatty infiltration and
tor for a retear. Goutallier et al9 found that retears muscular atrophy in muscles where no attempt at rotator
correlated with fatty infiltration of both the supraspinatus cuff repair was undertaken and those in which one was
and infraspinatus, and that infraspinatus degeneration performed, whether the repair ultimately failed or
had a highly negative influence on the outcome of remained intact. Furthermore, because the natural history
supraspinatus repairs. Interestingly, in our study infra- of the progression (or reversal) of muscle atrophy and fatty
spinatus fatty degeneration was the only variable that had infiltration is not fully understood, a follow-up time of 1
no effect on retear rate. Their supraspinatus retear rate year may not be sufficient to observe the full effects. Also,
was 50% when the infraspinatus fatty degeneration was the quantification of atrophy and fatty infiltration was
stage 2 or greater. We found retear rates of 70% and 67% based on interpretation of 2-dimensional magnetic reso-
when patients had stage 2 or greater fatty infiltration and nance images at 1 specific cut through the muscle belly
muscle atrophy, respectively. (either on coronal or sagittal sequences). This may not give
If muscle degeneration equates negatively to functional as accurate a measurement as a volumetric analysis.
outcome and retear rates, then it would stand to reason Finally, the effect of stretching the muscle in the process of
that progression of fatty infiltration and muscle atrophy repairing it may also affect its appearance on postopera-
portends poorly for the patient’s well-being. Our study did tive MRI and has not been studied. We did not record the
not show reversal of these characteristics (except for 1 size of the retear compared with the original tear. Looking
case, 2.6%), even in the face of successful repairs. In fact, at this factor in relation to the preoperative amounts and
each variable showed statistically significant progression subsequent progression of fatty infiltration and muscular
of degeneration during the course of the study. Higher atrophy may have provided useful information.
grades (2 and greater) of degeneration progressed more In conclusion, our analysis reveals that fatty infiltration
significantly (70% vs 25%), and rotator cuffs that retore and muscle atrophy of the infraspinatus and supraspinatus
also progressed more significantly than those that healed. significantly affect the functional outcome after rotator cuff
In general, there was minimal to no progression with suc- repair even though pain is consistently relieved. Outcome
cessful repairs. These findings are in contradistinction to appears to be mostly affected by the condition of the infra-
other studies that have shown improvement in muscle spinatus, and the likelihood of a retear is affected by tear
728 Gladstone et al The American Journal of Sports Medicine
size. Neither fatty infiltration nor muscular atrophy 7. Gerber C, Fuchs B, Hodler J. The results of repair of massive tears of
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