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Fatty Infiltration and Atrophy

of the Rotator Cuff Do Not Improve


After Rotator Cuff Repair and
Correlate With Poor Functional Outcome
James N. Gladstone,*† MD, Julie Y. Bishop,‡ MD, Ian K.Y. Lo,§ MD, and Evan L. Flatow,† MD

From the Shoulder Service, Department of Orthopaedic Surgery, Mount Sinai Medical Center,

New York, New York, The Ohio State University, Department of Orthopaedic Surgery,
§
Columbus, Ohio, and the University of Calgary, Department of Surgery, Calgary,
Alberta, Canada

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

*Address correspondence to James N. Gladstone, MD, Department of


Rotator cuff repair is a successful procedure, both objectively
Orthopaedic Surgery, Mount Sinai Medical Center, 5 East 98th Street, Box and subjectively, with regard to pain relief and functional
1188, New York, NY 10029 (e-mail: james.gladstone@mountsinai.org). outcome. This appears to be the case even when the repair
No potential conflict of interest declared. itself subsequently fails. However, investigators have docu-
mented significantly better functional results when the
The American Journal of Sports Medicine, Vol. 35, No. 5
DOI: 10.1177/0363546506297539 repair remains intact.7,11,12,18 Although variables such as
© 2007 American Orthopaedic Society for Sports Medicine tear size, number of tendons involved, tear chronicity, and

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

(Mitek Worldwide, Westwood, Mass) when bone quality


was compromised.
All patients used a sling for 6 weeks and were allowed
only passive range of motion during this time period. At 6
weeks, gradual full active motion was instituted, progress-
ing to resistive strengthening, which was continued for a
total of 3 to 4 months.

Surgical Technique: Arthroscopic Rotator Cuff Repair

Our technique for arthroscopic rotator cuff repair closely


Figure 1. Grading for muscle atrophy based on a T1-weighted parallels our open technique with respect to capsular and
oblique sagittal plane magnetic resonance image. The amount interval releases for tendon mobilization.4 A radiofre-
of muscle above or below a line drawn from the tip of the cora- quency probe was used to perform the arthroscopic
coid to the tip of the scapular spine determines the grade. releases. Medial retraction, as well as the length of the tear
(Reprinted from Warner JJP, Higgins L, Parsons IM 4th, Dowdy from anterior to posterior, was measured with use of a cal-
P. Diagnosis and treatment of anterosuperior rotator cuff tears. ibrated probe.
J Shoulder Elbow Surg. 2001;10:37-46 with permission from Once the rotator cuff was adequately mobilized, the ten-
The Journal of Shoulder and Elbow Surgery Board of Trustees.) don was repaired to the prepared greater tuberosity with
suture anchors placed laterally. The number of anchors
and sutures used depended on the size of the rotator cuff
statistical analysis, none was given a score of 0; mild, 1; mod- tear. A medially placed tendon-transfixing device
erate, 2; and severe, 3. As part of the analysis, the grades (CuffTack, Mitek Worldwide or Suretac, Smith & Nephew,
were also dichotomized to none/mild (grades 0 and 1) and Andover, Mass) was used to supplement fixation. We no
moderate/severe (grades 2 and 3). longer use these devices and now use 2 rows of anchors,
medial and lateral. An attempt was always made to fix the
Statistics cuff tendon to the lateral aspect of the tuberosity, if tension
allowed, to maximize the surface area for healing.
All statistical analyses were performed by a biostatistician. Postoperative care was similar to that described above
Analysis was performed using Spearman’s correlation coef- for open and mini-open repairs.
ficient to determine correlation of muscle atrophy and fatty
infiltration to outcome measures, strength, pain, tear size,
RESULTS
and cuff integrity. To determine independent predictors of
these measures, a stepwise linear regression analysis was Overall Outcomes
used. The effect of variables on cuff integrity was deter-
mined using a stepwise logistic regression analysis. A χ2 test Fifteen patients underwent open rotator cuff repair and 23
was used to examine muscle degeneration with respect to underwent arthroscopic rotator cuff repair, for a total of 38
healed and retorn tendons. Progression of fatty infiltration patients. All patients were followed up a minimum of 1
and muscle atrophy was evaluated using the Wilcoxon year postoperatively (range, 12 to 15 months) with MRI
signed rank test. The McNemar test analyzed progression and a clinical examination. The mean patient age was 62
based on dichotomized preoperative grades. In all analyses, years (range, 36 to 78 years). The mean symptom duration
P < .05 was considered statistically significant. was 10.5 months (range, 2 weeks to 51 months). The aver-
age tear size was 2.59 cm (range, 0.5 to 5 cm).
Surgical Technique: Mini-Open There was a statistically significant improvement in the
or Open Rotator Cuff Repair ASES (from 47.3 ± 20.4 to 88.2 ± 13.8), Constant (58 ± 16.7
to 82 ± 13.8), and pain (5.6 ± 2.8 to 0.86 ± 1.7) scores (all
Our surgical technique for open rotator cuff repairs has values mean ± standard deviation) in all patients (P <
been previously described2 and will not be restated except .0001 for all). Forward elevation strength improved signif-
as it relates to this study. Whether using the mini-open or icantly from 7.65 ± 6.4 lb to 13.5 ± 8.1 lb (P < .0006) after
open technique, the rotator cuff tendon was repaired in a cuff repair, while external rotation strength increased, but
similar fashion in all cases. Tear size was measured with a not significantly (P = .01), from 12.1 ± 8.9 lb to 15 ± 8.4 lb
ruler. Bursal, capsular, and interval releases for tendon (Table 1).
mobilization were performed with a Mayo scissors in an
attempt to obtain a repair without tension. Correlation of Functional Outcome to Muscle Quality
Once adequately mobilized, the rotator cuff was repaired
to the prepared greater tuberosity with sutures placed in a Table 2 summarizes the correlation of fatty infiltration and
modified Mason-Allen fashion and passed through bone muscle atrophy with outcomes. These values are presented
tunnels reinforced with Cuff Link bone tunnel devices as an overview. However, it must be noted that they are
722 Gladstone et al The American Journal of Sports Medicine

TABLE 1 repair, regardless of the degree of muscle atrophy or fatty


Functional Outcome Resultsa infiltration.
To determine independent predictors of functional outcome,
Measurement Preoperative Postoperative P value a stepwise linear regression analysis was performed. This
model takes into account the potential effect of the analyzed
ASES score 47.3 88.2 .0001
Constant score 58 82 .0001
variables on each other. The variables analyzed were fatty
Pain score 5.6 0.9 .0001 infiltration of the supraspinatus and infraspinatus, muscle
Forward elevation 7.7 13.5 .0006 atrophy of the supraspinatus and infraspinatus, tear size, and
strength (lb) whether the tendon had healed (intact or retorn). Table 3
External rotation 12.1 15 .01 summarizes the results. Infraspinatus atrophy is an inde-
strength (lb) pendent predictor of ASES score (P = .001), Constant score
a
(P = .033), and forward elevation strength (P = .04).
ASES = American Shoulder and Elbow Society. Supraspinatus atrophy independently predicts forward eleva-
tion (P = .013). Infraspinatus fatty infiltration independently
unadjusted results; that is to say, they do not take into predicted ASES score (P = .01) and external rotation strength
account the effect one has on the other. For example, in the (P = .004). Supraspinatus fatty infiltration also independently
unadjusted model, fatty infiltration of the infraspinatus affected external rotation strength (P = .04). Using this
(r = –.359, P < .03) and muscle atrophy of the supraspinatus regression analysis model, tear size and postoperative healing
(r = –0.402, P < .02) both appear to negatively influence the of the rotator cuff repair were not found to be independent
Constant score. This does not account for the interrelated- predictors of functional outcome or strength.
ness of these variables. To determine independent predictors
of outcome, a regression analysis is required (see below). Effect of Muscle Quality and
In almost every case, atrophy and fatty degeneration have Tear Size on Cuff Integrity
a strongly negative effect on assessment score, strength
parameters, and cuff repair integrity. There is also a strongly Overall, 61% of the rotator cuff repairs had healed at follow-
positive correlation with initial tear size. Table 2 shows that up and 39% were retorn. Preoperative variables of fatty
supraspinatus fatty infiltration did not affect the outcome infiltration and muscle atrophy were analyzed to determine
measures of ASES (r = –.231, P = .17) and Constant (r = –.236, their effect on postoperative cuff integrity.
P = .16) scores, while the 3 other variables, supraspinatus and Preoperative muscle atrophy (P = .001) and fatty infiltra-
infraspinatus muscle atrophy as well as infraspinatus fat, cor- tion (P = .008) of the supraspinatus and atrophy of the
relate significantly. There was no relationship between mus- infraspinatus (P = .041) were significantly correlated to post-
cle quality and pain scores (P > .2 in all cases); pain improved operative cuff integrity. Atrophy of the supraspinatus aver-
significantly in all cases with the performance of a rotator cuff aged 0.65 (range, 0 to 3, on a 4-point scale) in patients with

TABLE 2
Correlation of Functional Outcome, Tear Size, and Symptom Duration to Muscle Qualitya

ASES Score Constant Score Strength ER Strength FE

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

Symptom Duration Cuff Integrity Tear Size

P value corr coeff P value corr coeff P value corr coeff

Supraspinatus fat .3 –0.2 .005 –0.457 .0001 0.745


Infraspinatus fat .086 –0.33 .076 –0.3 .0001 0.712
Supraspinatus atrophy .057 –0.371 .001 –0.53 .0001 0.819
Infraspinatus atrophy .035 –0.399 .01 –0.425 .0001 0.651
a
Spearman’s rho correlation coefficients (corr coeff) and corresponding P values are listed to show any correlations between preoperative
fatty infiltration and muscular atrophy and the preoperative rotator cuff tear size and patient’s symptom duration, the postoperative
American Shoulder and Elbow Society (ASES), Constant, and strength scores, as well as postoperative rotator cuff integrity. Significant cor-
relations are in bold. ER, external rotation; FE, forward elevation.
Vol. 35, No. 5, 2007 Fatty Infiltration and Atrophy After Rotator Cuff Repair 723

TABLE 3
Independent Predictors of Functional Outcome, P Valuesa

Supraspinatus Infraspinatus

Outcome Atrophy Infiltration Atrophy Infiltration Tear Size Cuff Integrity

ASES score - - P = .001 P = .01 - - - -


Constant score - - P = .033 - - - - -
FE strength P = .013 - P = .04 - - - - -
ER strength - P = .04 - P = .004 - - - -
a
Results of stepwise linear regression analysis to determine independent predictors of functional outcome. Tear size and cuff integrity at
follow-up were not independent predictors of any of the outcome measures. ASES, American Shoulder and Elbow Society; FE, forward ele-
vation; ER, external rotation.

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).

an intact cuff at follow-up versus 1.73 (range, 0 to 3) in those


with a retear (P = .002). Infraspinatus atrophy averaged 0.30 Progression
(range, 0 to 3) in the intact group, while those with a retear
averaged 0.87 (range, 0 to 3; P = .012). Fatty infiltration of the No reversal of muscle atrophy or fatty infiltration was noted
supraspinatus was similarly greater in the retear group during the time of this study. In fact, in all but 1 case, muscle
(1.73; range, 0 to 4, on a 5-point scale) compared with those degeneration either remained the same or progressed. In each
with an intact cuff repair (0.57; range, 0 to 4; P = .007). category, supraspinatus atrophy (P < .001) and fatty infiltra-
Although fatty infiltration of the infraspinatus was greater tion (P = .001) as well as infraspinatus atrophy (P =0.015) and
in the retorn group (0.87; range, 0 to 4 vs 0.39; range, 0 to 4), fatty infiltration (P = .001), the progression was statistically
this only approached significance (P = .076) (Table 4). significant (Table 5). The greater the preoperative degree of
The magnitude of effect on cuff integrity is highlighted muscle degeneration, the more progression was noted at the
when the variables are further analyzed in terms of clini- time of follow-up.
cally significant (> grade 2) versus clinically insignificant Twenty-three patients had no or mild muscle atrophy
(grades 0 to 1) preoperative muscle degeneration. A statis- and 8 of them (35%) progressed (7 progressed 1 grade and
tically significant (P < .05) difference in healing rate was 1 patient progressed 2 grades). Of the 15 patients who had
found between the dichotomized groups. Of the 28 patients moderate to severe atrophy preoperatively, 10 (67%) pro-
with clinically insignificant fatty infiltration, 8 (29%) had gressed from grade 2 to grade 3 (Figures 3, 4, and 5). Four
retorn, while 7 of the 10 patients with clinically significant patients progressed in the supraspinatus, 2 in the infra-
fatty infiltration had not healed (70%). With respect to pre- spinatus, and 4 in both. The only exception was in 1 patient
operative muscle atrophy, those with no to minimal atro- whose atrophy improved from a moderate to mild grade
phy failed in 22% of cases (5 of 23 patients), whereas the (grade 2 to 1) with a successful repair of the supraspinatus.
failure rate with moderate to severe atrophy increased to When we looked at the progression of fatty infiltration in
67% (10 of 15 patients) (Figure 2). individual patients, none showed an improvement during the
Interestingly, a stepwise logistic regression analysis, preoperative to postoperative period. Of the 28 patients with
including the variables of muscle atrophy, fatty infiltra- no or mild fatty infiltration, 7 (25%) progressed. Of the 10
tion, and tear size, demonstrated that tear size (P = .002) patients with moderate to severe fatty infiltration preopera-
was the only independent predictor of postoperative rota- tively, 7 (70%) progressed (4 in both the supraspinatus and
tor cuff integrity. infraspinatus and 3 in the infraspinatus alone). Four
724 Gladstone et al The American Journal of Sports Medicine

TABLE 5
Progression of Fatty Infiltration and Muscle Atrophy Overall, and Differentiating Those With
an Intact Versus Retorn Rotator Cuff

P value for Degree


of Progression,
Overall Healed Retorn Retorn vs. Intacta

Supraspinatus fatty infiltration Preoperative 1.03 0.57 1.73 .003


Postoperative 1.61 0.86 2.67
P value .001 .06 .007
Degree of progression 0.58 0.29 0.94
Infraspinatus fatty infiltration Preoperative 0.58 0.39 0.87 .001
Postoperative 1.28 0.52 2.33
P value .001 .16 .003
Degree of progression 0.7 0.13 1.46
Supraspinatus atrophy Preoperative 1.08 0.65 1.73 .31
Postoperative 1.47 0.79 2.33
P value .001 .02 .007
Degree of progression 0.39 0.14 0.60
Infraspinatus atrophy Preoperative 0.53 0.27 0.86 .001
Postoperative 0.53 0.30 1.67
P value .02 1.00 .014
Degree of progression 0.33 -0.05 0.80
Average tear size (cm) 2.8 2.1 3.8 .001
a
P value < .05 represents a significantly greater degree of progression in the retorn group than in the intact group.

100 Association of Fatty Infiltration,


90 Muscle Atrophy, and Tear Size
80 70 67
Progression %

70 The amount of preoperative fatty infiltration of the


60 supraspinatus correlated highly with the amount of preop-
50 35
erative muscle atrophy of the supraspinatus (r = .714, P <
40
25
.001) and the infraspinatus (r = .422, P < .009), and the
30 amount of fatty infiltration in the infraspinatus (r = .573,
20 P < .0001). Preoperative fatty infiltration of the infra-
10 spinatus correlated highly with muscle atrophy of the
0 infraspinatus (r = .881, P < .001), and also with atrophy of
None/Mild Mod/Severe None/Mild Mod/Severe the supraspinatus (r = .575, P < .0001). Finally, the amount
FI FI MA MA
of preoperative muscle atrophy of the supraspinatus and
Figure 3. Effect of clinically insignificant versus significant infraspinatus correlated significantly with each other (r =
muscle atrophy (MA) and fatty infiltration (FI) on progression .551, P < .0001).
(P < .05). Tear size correlated strongly with fatty infiltration of the
supraspinatus (r = .673, P < .001) and infraspinatus (r =
.728, P < .001) as well as with muscle atrophy of the
supraspinatus (r = .807, P < .001) and infraspinatus (r =
patients progressed 1 grade, while the other 3 progressed
.666, P < .001). When fatty infiltration and muscle atrophy
by 2 grades.
were dichotomized, there was a significant difference in
Overall, the amounts of fatty infiltration and muscular
mean tear size between the none to mild group and the
atrophy progressed regardless of cuff integrity. Although
moderate to severe group in each case.
the progression of fatty infiltration of both the supraspina-
tus and infraspinatus and atrophy of the supraspinatus
were found to be minimal when the cuff remained intact, DISCUSSION
there was no overall reversal. Nonetheless, progression
was significantly less in those tendons that healed than in Rotator cuff repairs typically lead to clinical improvement
those in which repair failed (atrophy of the infraspinatus, for patients from both a pain and functional standpoint,
P = .001; fatty infiltration of the supraspinatus P = .003 regardless of the integrity of the repair at follow-up.12
and infraspinatus P = .001). This did not apply in the case Nonetheless, numerous studies have shown even better
of supraspinatus muscle atrophy (P = .31) (Table 5). outcomes with a maintained repair.6,7,11,12,18 Historically,
Vol. 35, No. 5, 2007 Fatty Infiltration and Atrophy After Rotator Cuff Repair 725

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

Figure 5. Failure of repair at 1 year with progression of mus-


cle changes. A, T2-weighted coronal sequence demonstrating
retear of the supraspinatus. B, T1-weighted coronal sequence
showing no preoperative fatty infiltration of the supraspinatus.
C, T1-weighted sagittal sequence showing mild supraspinatus
atrophy preoperatively. D, postoperative supraspinatus with
progression to grade 3 fatty infiltration. E, postoperative
supraspinatus with progression to moderate muscle atrophy.

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
reverses after surgery, even with a successful outcome, and the rotator cuff. J Bone Joint Surg Am. 2000;82:505-515.
8. Goutallier D, Bernageau J, Patte D. Assessment of the trophicity of
in moderate to severe cases progression is significantly
the muscles of the ruptured rotator cuff by CT scan. In: Post M,
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phy and fatty infiltration can be expected to increase more Mosby Year Book; 1990:11-13.
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challenge ahead will be to figure out whether this point can
atrophy before and after repair of the rotator cuff. Fifth International
be determined, and thus allow for intervention in a timely Conference of Surgery of the Shoulder. Paris, France; 1992:50.
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ACKNOWLEDGMENT ure of rotator cuff repairs. J Bone Joint Surg Am. 2000;82:304-314.
13. Nakagaki K, Ozaki J, Tomita Y, Tamai S. Fatty degeneration in the
We sincerely appreciate the efforts and support provided to supraspinatus muscle after rotator cuff tear. J Shoulder Elbow Surg.
us for the statistical analysis in this manuscript by our bio- 1996;5:194-200.
14. Nakagaki K, Ozaki J, Tomita Y, Tamai S. Function of supraspinatus
statistician, John Doucette, Associate Professor,
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Department of Community Medicine at the Mount Sinai Orthop Relat Res. 1995;318:144-151.
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