Changes of Supraspinatus Muscle Volume and Fat Fraction After Successful or Failed Arthroscopic Rotator Cuff Repair

Abstract

Background:

Muscle atrophy and fatty infiltration are limiting factors for successful rotator cuff (RC) repair. Quantitative data regarding these hallmarks of degenerative muscle changes after RC repair in humans are scarce. By utilizing a new application of the 6-point Dixon magnetic resonance imaging technology, 3-dimensional volume and fat fraction analysis of the whole RC muscle have become possible.

Purpose:

Quantitative analysis of atrophy and fatty infiltration of the supraspinatus muscle after healed and failed RC tendon-to-bone repair.

Study Design:

Cohort study; Level of evidence, 3.

Methods:

Muscle volume and fat fraction were measured preoperatively and at 3 and 12 months postoperatively in 19 failed and 21 healed arthroscopic supraspinatus tendon repairs, with full muscle volume segmentation and magnetic resonance Dixon sequences.

Results:

In both groups, the muscle volume initially decreased 3 months after RC repair by –3% in intact (P = .140) and –10% in failed repair (P = .004) but recovered between 3 and 12 months to 103% (P = .274) in intact and 92% (P = .040) in failed repairs when compared with the preoperative volume (difference of change between groups, preoperative to 12 month: P = .013). The supraspinatus muscle’s fat fraction did not significantly change after successful repair (6.5% preoperative, 6.6% after 3 months, and 6.7% after 12 months; all nonsignificant). There was, however, a significant increase from 7.8% to 10.8% at 3 months (P = .014) and 11.4% at 12 months (P = .020) after failed repair (difference between groups at 3- and 12-month follow-up: P = .018 and P = .001, respectively).

Conclusion:

After successful arthroscopic repair, RC tendon tear–induced fatty infiltration can be almost stopped, and muscle atrophy can even be slightly reversed. In case of a failed repair, however, these changes are further pronounced during the first 3 postoperative months but seem to stabilize thereafter.

Keywords

arthroscopic rotator cuff repair muscle volume muscle degeneration fatty infiltration Dixon

Chronic tears of the rotator cuff (RC) tendons are associated with muscle degeneration, which is structurally characterized by atrophy and fatty infiltration.^8,11,23 There are essentially no quantitative data in the available literature related to these muscle changes after RC repair.^7,17,24 This is mainly related to technical limitations of the currently available magnetic resonance imaging (MRI) hardware and software: clinically available MRI is often unable to cover the entire RC muscles from medial to lateral or quantify the muscular fat content.^1,17,23 Therefore, muscle atrophy is currently either graded with the tangent sign³³ or analyzed on a single cross-sectional image,¹³ which has been proven to be less valid than a 3-dimensional (3D) analysis.^1,31 Fatty infiltration is mostly graded by MRI adaptations of the classification of Goutallier,^6,11 which is influenced by the retraction of the myotendinous unit²³ and has not demonstrated better-than-moderate interreader reliability.^6,15

If nonoperative management fails, arthroscopic RC repair is the gold standard for the treatment of symptomatic full-thickness RC tears. A healed tendon-to-bone repair is associated with not only a better overall clinical state and higher postoperative strength but also a better outcome than if the repair has failed to heal.^14,27

Quantitative data comparing the degenerative muscle changes after successful or failed RC repair in humans are scarce, and semiquantitative data are controversial: There are some authors who report irreversible muscle degeneration,^10,21,24 while others report recovery from atrophy^1,9 or even fatty infiltration.^13,32

Recent technological developments in MRI permit 3D analysis of the entire RC muscle,^8,18,22 including quantitative analysis of its fat fraction.^{8,15,18-20,22} It was the purpose of this investigation to quantitatively and longitudinally analyze supraspinatus muscle atrophy and fatty infiltration before and after arthroscopic supraspinatus repair and compare the results of repairs that healed with those that ultimately failed to heal using full muscle volume MRI segmentation and magnetic resonance (MR) Dixon sequences for quantitative analysis of intramuscular fat content.

We hypothesized that muscle volume will increase after successful and decrease after failed RC repair, whereas the degree of fatty infiltration will not be reversible in successful RC repairs but will increase in failed repairs.

Methods

Between May 2014 and March 2017, 115 patients (116 shoulders) were enrolled in this prospective institutional review board–approved study. All patients had a full-thickness tear of at least the supraspinatus tendon, as documented with MR arthrography. The tear was associated with no more than stage 2 fatty infiltration of the supraspinatus muscle,^6,11 and all patients underwent arthroscopic RC repair. Excluded were patients with previous operations, osteoarthritis of the glenohumeral joint, inflammatory rheumatoid diseases, or use of oral steroids or immunosuppressive drugs. Patients gave informed consent for detailed clinical assessment, including Constant score and subjective shoulder value,^3,5 and imaging assessment, including standardized MRI preoperatively and at 3 and 12 months postoperatively. They also consented to have tendon, capsule, and muscle biopsy specimens harvested during arthroscopic RC repair (analyses in process). Preoperative MR arthrography was performed at a mean 4 days before surgery (minimum 1 day, maximum 35 days), which defined the preoperative diagnostic imaging elements. The final MRI examinations at 12 months postoperatively determined structural healing (Sugaya I and II³⁰) or failure of structural healing (“retears”: Sugaya IV and V³⁰). All shoulders with failed repairs were matched for sex, age (±10 years), and preoperative tear size (Patte and Cofield classification)^2,26 to at least 1 but preferably 2 healed shoulders, which served as controls.

Surgical Technique

All surgical procedures were performed arthroscopically with the patient in the beach-chair position under regional or general anesthesia. Subacromial debridement and tenotomy or tenodesis of the long head of the biceps were performed as a routine. Joint fluid was aspirated, and tissue biopsy specimens were harvested with an arthroscopic biopsy clamp of the joint capsule and the torn supraspinatus tendon and muscle. The RC tendon-to-bone repair was thereafter performed with double-loaded 6.5-mm titanium screw-in anchors (Karl Storz SE & Co KG). Postoperatively, the shoulders were immobilized in an abduction brace and passively mobilized under the control of a physical therapist for the first 6 weeks. Between weeks 7 and 12, active-assistive range of motion exercises were allowed, and gentle strengthening of the repaired RC muscles was started thereafter.

Clinical Assessment

All patients were clinically assessed with the Constant score³ and subjective shoulder value⁵ before surgery as well as 3 months (without strength measurements) and 12 months postoperatively by a trained research nurse (S.W.) not otherwise involved in the patients’ treatment.

MRI and Evaluation

All patients underwent MRI of the shoulder in a 1.5-T scanner (MAGNETOM Avanto Fit; Siemens Healthcare) with a dedicated 16-channel phased-array shoulder coil.

The MRI protocol was identical for all patients and for all 3 imaging time points. The protocol consisted of 4 standard imaging planes (coronal oblique proton density weighted with fat saturation, sagittal oblique T1, sagittal oblique short tau inversion recovery, axial T2 Trufi 3D [true fast imaging with steady-state free precession]) and 1 sagittal oblique 6-point Dixon sequence. Based on the latter sequence, fat signal fraction maps were generated on the scanner’s console for subsequent intramuscular fat quantification.^4,12 Detailed imaging parameters are listed in Table 1.

Table 1

Detailed Magnetic Resonance Imaging Parameters^a

Parameter	Coronal Oblique PDfs	Sagittal Oblique T1	Sagittal Oblique STIR	Axial T2 Trufi 3D	Sagittal Oblique 6-Point Dixon
TR, ms	2200	450	4000	11.2	20
TE, ms	34	11	47	4.84	1.70, 4.76, 7.82, 10.88, 13.94, 17.00
Slices, n	20	29	23	52	64
Slice thickness, mm	4	4	4	1.7	3
Spacing, mm	4.8	4.8	4.8	—	—
Matrix	384 x 384	384 x 307	256 x 256	512 x 256	192 x 192
FOV, mm²	159 x 159	159 x 159	170 x 170	180 x 180	174 x 174
TA, min:s	3:40	1:11	3:32	3:41	3:19

FOV, field of view; PDfs, proton density weighted with fat saturation; STIR, short-tau inversion recovery; TA, acquisition time; TE, echo time; TR, repetition time; Trufi, true fast imaging with steady-state free precession. Dashes signify no spacing between slices.

All MR images were evaluated by a fellowship-trained musculoskeletal radiologist (L.F., 6 years of experience) who was blinded to clinical data (eg, pain, shoulder function) but not to the imaging at each time point.

On preoperative MR images, the following parameters were assessed:

Tear size according to the Cofield classification²: small (<1 cm), medium (1-3 cm), large (>3-5 cm), massive (>5 cm)

Tear location: anterior part, posterior part, or both (supraspinatus); superior part, inferior part, or both (infraspinatus and subscapularis)

Tendon retraction according to the Patte classification²⁶: type 1 (proximal stump close to bony insertion), type 2 (proximal stump at level of humeral head), type 3 (proximal stump at glenoid level)

Evaluation of fatty muscle infiltration (separate for supraspinatus, infraspinatus, and subscapularis): qualitatively according to Fuchs et al⁶ based on the Goutallier classification¹¹ and quantitatively by placing freehand regions of interest on fat signal fraction maps on the most lateral slice where the scapular Y was still visible (Figure 1)^8,18,33

Postoperative 3- and 12-month follow-up scans were evaluated as follows:

Cuff integrity according to the Sugaya classification³⁰(separately for supraspinatus, infraspinatus, and subscapularis): type I (repaired cuff of sufficient thickness, homogeneously low signal intensity), type II (sufficient thickness, partial high-signal intensity area), type III (insufficient thickness without discontinuity), type IV (minor discontinuity in >1 section, suggestive of a small tear), type V (major discontinuity in each image, suggestive of a medium-to-large tear)

Evaluation of fatty muscle infiltration: qualitatively and quantitatively as described for the preoperative data

Volume Measurement

For volumetric analysis, the MRI data were taken from the picture archiving and communication system (Phoenix-PACS) and stored anonymously as Digital Imaging and Communications in Medicine files.

The MR images were used to measure the volume, length, and smallest enveloping box of the supraspinatus muscle. The out-of-phase qDixon sequences (ie, Eco0) were imported into MeVisLab (MeVis Medical Solutions AG) and 3 mm–thick sectional planes (segments) of the cross section of the supraspinatus muscle were manually outlined in sagittal projections with the freehand CSO module of MeVisLab. The resulting segmented voxel data were converted into a 3D model with the generated WEM module and stored as an STL file (Standard Tessellation Language) (Figures 2 and 3).

The created 3D model was imported in the CASPA program (Computer Assisted Surgery Planning Application; Balgrist CARD AG) to determine the muscle volumes.

The study was approved by the cantonal ethical committee (BASEC NR: PB_2017-00372), and all patients signed an informed consent form before enrollment.

Statistical Analysis

Statistical analysis was performed under the supervision of a professional biostatistician. Initial data inspection revealed various outcome variables to have a nonnormal distribution, as assessed with Kolmogorov-Smirnov tests. Therefore, nonparametric inference tests were used for statistical analysis. The analysis was conducted with SPSS statistical software (v 24.0; IBM Corp). The Mann-Whitney U test was used to test for differences between intact repairs and failed repairs. Significance was set at α < .05. Correlation between supraspinatus muscle volume and supraspinatus fat fraction was performed with Pearson and Spearman correlations.

Results

Of the 115 patients who were primarily enrolled in the ongoing prospective database, 14 dropped out or were lost to follow-up. At the time of this analysis, 95 patients had completed all clinical and radiological follow-up examinations and were therefore available for this study. Of those patients, 19 (20%), with a mean ± SD age of 62 ± 7 years, had an MRI-confirmed retear (Sugaya IV, n = 9; Sugaya V, n = 10) of the reconstructed RC and were included in the study group. Using our matching criteria, we were able to identify and include 21 patients with a mean age of 60 ± 6 years in the control group with a healed RC (Sugaya I, n = 6; Sugaya II, n = 15).

Demographics, clinical data, and RC tear patterns are presented in Table 2.

Table 2

Intergroup Comparison of Patients’ Demographics, Clinical Data, and Rotator Cuff Tear Pattern (Cofield and Patte Classification) and Muscle Degeneration According to Goutallier^a

	Intact		Failure
	n^b	%	n^b	%	P Value
Patients	21		19
Sex					.57
Female	5	24	4	21
Male	16	76	15	79
Side					.50
Right	11	52	9	47
Left	10	48	10	53
Dominance					.73
Right	20	95	18	95
Left	1	5	1	5
Age,^c y	60 ± 6		62 ± 7		.34
BMI^c	28 ± 5		27 ± 4		.42
Cofield					.21
Medium	12	57	6	32
Large	5	24	9	47
Massive	4	19	4	21
Goutallier SSP					.13
Grade 0	11	52	6	32
Grade 1	9	43	10	53
Grade 2	1	5	3	16
Goutallier ISP					.47
Grade 0	11	52	7	37
Grade 1	8	38	11	58
Grade 2	2	10	1	5
Goutallier SSC					.05
Grade 0	17	81	10	53
Grade 1	4	19	7	37
Grade 2	0	0	2	11
Patte SSP					.53
Grade 1	6	29	5	26
Grade 2	14	67	11	58
Grade 3	1	5	3	16
Occurrence					.41
Acute	5	24	2	10
Chronic	16	76	17	89
Tear pattern					.78
Involving SSC	14	67	12	63
Involcing ISP	12	57	13	68

BMI, body mass index; ISP, infraspinatus; SSC, subscapularis; SSP, supraspinatus.

Absolute number.

Mean ± SD.

Clinical Outcome

The mean preoperative absolute Constant score was comparable in both groups (failures, 61 ± 14; intact controls, 59 ± 18; P≥ .999), decreased at 3 months to 51 ± 16 for failures and 57 ± 8 for intact (P = .73) (no strength measurements), and increased to 70 ± 18 after failed and to 79 ± 6 after successful repairs (P = .19) at 12-month follow-up (Table 3, Figure 4). Differences in Constant score subvalues (pain, force, and range of movement) between groups after 12 months are depicted in Table 4.

Table 3

Absolute and Relative Preoperative and 3- and 12-Month Postoperative Constant Scores With Intergroup Comparison

	Intact (n = 21)					Failures (n = 19)
Constant Score	Mean	SD	Median	Min	Max	Mean	SD	Median	Min	Max	P Value
Preoperative
Absolute	59	18	63	25	83	61	14	64	20	78	≥.999
Relative	69	19	74	33	95	71	15	70	30	88	.84
Postoperative 3 mo^a
Absolute	57	8	57	45	79	51	16	57	15	70	.73
Relative	65	9	64	54	88	60	18	65	15	78	.88
Postoperative 12 mo
Absolute	79	6	81	67	87	70	18	78	32	86	.19
Relative	90	8	92	71	99	81	20	90	34	99	.22

No strength measurements at postoperative 3 months.

Table 4

Subvalues of 12-Month Constant Score With Intergroup Comparison

	Intact (n = 21)					Failures (n = 19)
Constant Score	Mean	SD	Median	Min	Max	Mean	SD	Median	Min	Max	P Value
Pain, points	14.6	0.9	15.0	12.0	15.0	12.8	3.7	15.0	5.0	15.0	.130
Force, kg	4.8	1.4	4.4	1.5	7.5	3.9	2.5	4.9	0.0	8.4	.350
Flexion, deg	146	12	140	130	170	130	39	140	35	170	.583
Abduction, deg	156	14	160	130	180	133	41	150	50	170	.102
External rotation, deg	49	15	50	20	83	39	17	40	0	70	.035

Muscle Volume

In both groups, the supraspinatus muscle volume decreased in the first 3 months after repair. Muscle atrophy was significantly greater in failed (–10%; P = .004 vs preoperatively) than successful repairs (–3%; P = .140 vs preoperatively). This process stopped after 3 months and even slightly recovered in the intact repairs until 12 months. After 12 months, the volume was 103% (P = .274) in intact repairs but decreased to 92% (P = .04) of the preoperative volume in the failed repairs (difference between the groups at 12 months, P = .440; difference of change preoperatively to 12 months between groups, P = .013) (Figure 5).

Fat Fraction

The fat content of the supraspinatus muscle did not significantly change in patients with intact repairs (from 6.5% preoperatively to 6.6% after 3 months and 6.7% after 12 months; P = .696, P = .680). Conversely, there was a significant and substantial increase of fat content from 7.8% to 10.8% at 3 months (P = .014) and to 11.4% at 12 months (P = .020 vs preoperative) in the failed repairs (difference between the groups, P = .018 at 3 months and P = .001 at 12 months follow-up) (Figure 6).

There was a moderate negative correlation between supraspinatus volume and fat fraction (Pearson correlation coefficient, –0.439; Spearman correlation coefficient, –0.519) (Figure 7).

Absolute (Contractile) Muscle Mass

When analyzing the absolute muscle mass (volume minus fat content), we found an even larger difference than with muscle volume alone. Whereas the decrease of mean contractile volume was 11.6% after 3 months and 10% after 12 months in retears, it had decreased only by 0.9% after 3 months but increased by 3.7% after 12 months in intact repairs. These changes of contractile volume were significantly different between the groups (P = .046 after 3 and P = .030 after 12 months).

In a subgroup analysis (Sugaya IV or V vs intact), we could not document a significant difference in the progression of atrophy between Sugaya IV failures and intact repairs. Conversely, the volume change from presurgery to 3 and 12 months between intact repairs and Sugaya V failures was statistically significant (P = .011 and P = .001) (Figure 8).

The subgroup analysis of the supraspinatus muscle fat fraction was not significantly different between Sugaya IV and V (all nonsignificant) (Figure 9).

Discussion

The most important finding of this investigation was that RC tendon tear–induced fatty infiltration can be stopped and muscle atrophy can even be minimally reversed after successful arthroscopic RC repair. If repairs fail to heal, the degenerative muscle changes increase substantially in the first 3 postoperative months but seem to stabilize thereafter. Therefore, both our hypotheses could mainly be confirmed. The observation, however, that muscle atrophy and fatty infiltration do not significantly increase in retears between 3 and 12 months was unexpected.

To our knowledge, this is the first quantitative longitudinal 3D RC muscle segmentation analysis after successful and failed arthroscopic RC repair. Even Chung and colleagues,¹ who reported 3D muscle volume measurements, did not assess the whole supraspinatus muscle, only 1 or 2 cm–thick muscle volume slices, and provided no fat fraction analysis. Their data, which indicated that the muscle area and volume can increase after successful repair, could have been caused by lateralization of the muscle volume by successful repair. Our measurements confirm that repair failure is associated with a significant volume loss of the respective muscle, as opposed to successful repair, which is definitely not associated with further volume loss and possible recovery of preexisting atrophy.

Our failure rate of 20% is comparable with other imaging-controlled RC repair outcome studies.^14,27 In agreement with previous observations is the fact that not only the patients with successful repairs but, to a lesser degree, also those with failed repairs showed significant clinical improvement.^14,28

The further decrease of the muscle volume not only after failed but also after successful RC repair may be related to the prudent postoperative rehabilitation protocol, as patients were not allowed to activate their shoulder muscles for 6 weeks nor start their strengthening program before 3 months after surgery. These findings are in accordance with our experimental data in sheep, where we found further 10% muscle atrophy 6 weeks after successful RC repair.⁸

It is interesting and not fully understood that not only the processes of fatty infiltration but also muscle atrophy seems to stop after a period of approximately 3 months even if the repair fails to heal. A potential explanation is that small retears still provide some mechanical force transmission or that a side-to-side healing occurs at 3 months so that the muscle does act against some resistance. This hypothesis is supported by the subgroup analysis, which showed comparable muscle volume regeneration behavior of Sugaya IV reruptures and intact repairs as opposed to larger retears (Sugaya V).

Despite our prospective study design, there remain potential limitations. We did not perform immediate postoperative baseline MRI as suggested by Chung et al.¹ Such postoperative baseline MRI seems to be useful for 2-dimensional muscle area analysis (ie, Goutallier, cross-sectional muscle area, Tangent sign), as the lateralization of the myotendinous unit through repair influences these measurements,^13,16,29 but it should influence neither 3D volume analysis nor intramuscular fat fraction. We did not further analyze the potential effect of age and sex on RC muscle volume, but we tried to avoid this potential bias by including these factors as matching criteria. We matched patients according to posterosuperior tear size as well as possible. The matching resulted in a control group that was overall comparable but had slightly but significantly less fatty infiltration of the subscapularis muscle. Whether minimally increased fatty infiltration of the subscapularis is a risk factor for supraspinatus repair is not currently known. The focus of this investigation, however, was not primarily the cause of the failure of healing but the quantitative and precise analysis of changes of the muscle affected by a tear of its tendon and its successful or unsuccessful repair. We believe that the answer given regarding the study question is not invalidated by this preoperative difference, but in view of retear risk, this clearly merits further investigation. Also, we still do not exactly know how fast the RC muscle atrophies and degenerates after tendon tears, as baseline MR images (ie, before RC tear) are not available for these patients and the first postoperative MRI was taken at 3 months. Experiments with sheep documented that muscle atrophy occurs rapidly after tendon release (80% atrophy after 6 weeks) but remains stable until 16 weeks (78%).⁸ Even bigger cohort studies will not be able to answer this question in the human, and comparative analysis of pathologic (RC tear) and healthy contralateral shoulders in the same patient might give further insight.

The fact that our results showed a significant difference between healed and Sugaya V failures for atrophy but no significant difference between healed and Sugaya IV may be due to the small sample size, but it may also be due to Sugaya IV failures leading indeed to less atrophy than Sugaya V. This possibility is not excluded with the insignificant difference of Sugaya IV and V failures and may deserve further attention in future studies.

With a mean of 7% and a maximum of 19%, the degree of fatty infiltration in our patient cohort does not seem very severe, but these are typical candidates for successful RC repair, according to the mentioned inclusion criteria. Our data concerning fatty infiltration are compatible with recent information from other studies with Dixon-based quantification of fat fraction.¹⁹ These authors also reported relatively mild preoperative fatty infiltration of the supraspinatus muscle: 7% in isolated supraspinatus tendon tears and 11% in multitendon tears, which increased during the first 6 months from 7% to 9% in intact repairs and from 9% to 14% in failed repairs.

Besides the main topic of the study, it seems interesting that the post hoc analysis by the fellowship-trained radiologist revealed 4 cases that showed preoperative Goutallier stage 3, which should per definition have about 50% fat in the muscle. This was obviously not the case, as Dixon analysis showed a maximum fatty infiltration of 19% and indicated that the Goutallier grading on sagittal MR images according to Fuchs et al⁶ can overestimate the amount of fatty infiltration^15,25 but is strongly correlated with myotendinous retraction.²³ Given the relatively small differences in fat content—which, however, were very distinct and significant between intact and failed repairs—it appears justified and even necessary to use such precise and quantitative measurement techniques such as the Dixon sequence, especially when answering basic research questions about RC muscle degeneration and regeneration.

Conclusion

Our data document that RC tendon tear–induced fatty infiltration can nearly be arrested and muscle atrophy potentially even partially reversed after successful arthroscopic RC tendon repair. If the repair fails to heal, however, degenerative changes occur rapidly and substantially within 3 months; thereafter, neither substantial progression nor any signs of reversal of these muscular changes can be observed.

Footnotes

One or more of the authors has declared the following potential conflict of interest or source of funding: C.G. is a developer for Zimmer Inc and consultant for Karl Storz. AOSSM checks author disclosures against the Open Payments Database (OPD). AOSSM has not conducted an independent investigation on the OPD and disclaims any liability or responsibility relating thereto.

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