Abstract
Introduction
Sizable rotator cuff defects with limited muscle atrophy and fat replacement may represent acute traumatic ruptures that are less likely to recur after surgery to close the defect, while closure of defects with poor quality muscle are associated with defect recurrence. These distinct lesions are both referred to as tears. We analyzed the relationship between rotator cuff defect size and muscle quality to determine the relative proportion of sizable defects associated with good muscle and factors associated with muscle deterioration.
Material and methods
A cohort of 230 consecutive shoulder MRIs in patients with full-thickness rotator cuff tendon defects, limited acromioclavicular arthrosis (to avoid hindrance of defect measurement), and a duration of symptoms in the radiology report from a large urban center in the United States was evaluated for the measured distance between the supraspinatus tendon edge and the greater tuberosity medial to lateral (coronal plane defect size), anterior to posterior (sagittal plane defect width), and fatty infiltration (Goutallier classification), and atrophy (Warner classification) of the supraspinatus. We sought factors independently associated with fatty infiltration and muscle atrophy in multivariable logistic regression analyses.
Results
Forty-nine of 109 shoulders (45%) with a coronal plane defect >20 mm had reasonable muscle quality as defined by Goutallier grade less than 2 and Warner grade less than 2. Both greater fatty infiltration of the supraspinatus muscle and greater supraspinatus muscle atrophy were associated with older age and greater coronal plane defect size.
Conclusion
The observation that supraspinatus muscle health deteriorates with age and defect size, but nearly half of the largest defects had good muscle, suggests an important distinction between relatively recent traumatic ruptures and old untreated rupture or gradual attrition that may be obfuscated by referring to all lesions as tears.
Level of evidence
Level III; Retrospective diagnostic cohort.
Keywords: Rotator cuff tendinopathy, Shoulder, Magnetic resonance imaging, MRI, Tendinopathy, Tear, Defect
1. Introduction
Most humans develop rotator cuff tendinopathy as they age and most rotator cuff defects seem to result from age-appropriate changes rather than injury or an acute event.1, 2, 3, 4, 5, 6, 7 Acute rotator cuff ruptures tend to be large, involving more than one tendon. Fatty infiltration of rotator cuff muscles reflects longstanding rotator cuff muscle dysfunction related either to gradual attrition or untreated acute ruptures.8,9 In both situations, the tendon defect leads to mechanical unloading of muscle which then deteriorates, atrophies, and is replaced by fat.10 The observation that greater fatty infiltration is associated with larger defect size, defect location, and older age is consistent with the evidence that rotator cuff defects often result from attrition of the rotator cuff tendons with age rather than an acute event or injury.11, 12, 13, 14 Also consistent with this conceptualization of rotator cuff tendinopathy, the degree of fatty infiltration correlates with extent of muscle atrophy, physician-appraised outcome scores after surgery to close a rotator cuff defect, inability to completely close the defect during surgery, the status of the anterior-most part of the supraspinatus tendon, and recurrence of the defect documented on ultrasound or MRI after surgery.13, 14, 15, 16, 17, 18, 19, 20, 21, 22 While relative sparing of the anterior supraspinatus might occasionally maintain muscle quality in attritional defect,20, 21, 22 and some poor muscle quality may be related to remote acute ruptures, the evidence points to a potentially useful distinction between acute traumatic ruptures and age-related attritional defects.
New shoulder symptoms, particularly after a specific event, can be misinterpreted as new pathology or even an injury. Amongst the subset of people with an attritional defect of the rotator cuff, description of the lesion as a “tear” has the potential to reinforce that misconception.23 Misinterpretation of a new pain as an injury or vulnerability is associated with greater symptom intensity and magnitude of incapability, more so when there are also feelings of worry or despair.24,25 In other words, reinforcing a sense of injury harms health. This is another reason we might want to consider a clear distinction between large defects with good muscle (likely acute ruptures), large defects with poor muscle (either old ruptures or long-standing attritional changes), and smaller attritional defects that are not large enough for the muscle to deteriorate. Additional analysis of the relationship between rotator cuff defect size and muscle quality may help refine how we conceptualize rotator cuff pathology.
We assessed the relationship between rotator cuff tendon defect size and the extent of fatty infiltration accounting for other factors. We also measured the relationship between supraspinatus muscle atrophy and fatty infiltration. Finally, we calculated the relative percentage of full thickness defects that were above a specific size with reasonable muscle quality.
2. Materials & methods
2.1. Study design
After institutional review board approval of this retrospective study, we obtained 4634 radiology reports for all shoulder MRIs taken from one regional radiology service that provides most of the imaging services in the region. We identified 616 shoulders who had a shoulder MRI with diagnosis of a full-thickness rotator cuff defect involving the supraspinatus, infraspinatus, or subscapularis over the past 3 years. MRI signal changes in the rotator cuff tendons without a full-thickness defect were excluded. We excluded 144 shoulders with prominent osteophytes secondary to acromioclavicular osteoarthritis as one of the authors thought the osteophytes sterically hindered accurate measurements of the rotator cuff in 2 planes. We included 237 shoulders for whom duration of symptoms was recorded in the radiology report, intending to use this information in the analysis, but we found this data unreliable. After excluding 5 shoulders that did not have supraspinatus defects and 2 shoulders with a fracture, we analyzed 230 radiology reports.
2.2. Measures
Our primary outcomes were categories of supraspinatus muscle fat infiltration (Goutallier) and atrophy (Warner) in the MRI report. The Goutallier classification has five levels: grade 0 is defined as completely normal muscle, without any fatty streak; grade 1 as muscle containing some fatty streaks; grade 2 as less than 50% of muscle being involved; grade 3 as 50% of muscle involvement; and grade 4 as greater than 50% muscle involvement.19 The Warner classification has four levels: no atrophy is defined as muscle completely filling its fossa; mild atrophy as the muscle's outer contour being flat compared with its fossa; moderate atrophy as the muscle's outer contour being concave into the fossa; and severe atrophy as the muscle being barely apparent in its fossa.20 We assigned no atrophy “grade 0”, mild atrophy “grade 1”, moderate atrophy “grade 2”, and severe atrophy as “grade 3”. One author classified Goutallier and Warner classifications using imaging software. Other explanatory variables were the coronal plane defect size (the distance between the supraspinatus tendon edge and the greater tuberosity; often referred to as “retraction”) and the sagittal plane defect size measured on MR images, patient age, and time of presentation after onset of symptoms. One author quantified the maximum distance from tendon edge to the greater tuberosity on coronal oblique images (coronal plane defect size) and sagittal plane (anterior to posterior) defect size).
2.3. Study population
The mean age of the sample was 64 ± 10 years (Table 1). The mean coronal plane size of the defect for the entire sample was 21 ± 10 mm (mm). The mean coronal plane size of the defect for the entire sample was 18 ± 8 mm. Sixty-three people (27%) had Goutallier grade 0, 85 (37%) grade 1, 55 (24%) grade 2, 13 (6%) grade 3, and 14 (6%) grade 4 fatty muscle infiltration. One hundred four people (45%) had Warner grade 0, 68 (30%) grade 1, 35 (15%) grade 2, and 23 (10%) grade 3 atrophy of the supraspinatus muscle.
Table 1.
Data characteristics.
| Variables | N = 230 |
|---|---|
| Patient age in years | 64 ± 10 |
| Mean retraction (mm) | 21 ± 10 |
| Mean width (mm) | 18 ± 8 |
| Goutallier classification | |
| Grade 0 | 63 (27) |
| Grade 1 | 85 (37) |
| Grade 2 | 55 (24) |
| Grade 3 | 13 (6) |
| Grade 4 | 14 (6) |
| Warner classification | |
| Grade 0 | 104 (45) |
| Grade 1 | 68 (30) |
| Grade 2 | 35 (15) |
| Grade 3 | 23 (10) |
| Time of presentation | |
| <1 week | 4 (2) |
| 1 week - 1 month | 60 (26) |
| 1 month - 6 months | 85 (37) |
| 6 months - 1 year | 26 (11) |
| >1 year | 55 (24) |
Continuous variables as mean ± standard deviation (range); Discrete variables as number (percentage).
2.4. Statistical analysis
Continuous variables are presented as mean ± standard deviation (SD) and discrete data as proportions. We used chi-squared tests for trend to assess relationships between discrete variables and Spearman rank correlation coefficient tests to assess relationships between discrete and continuous variables. Our primary dependent variables (Goutallier and Warner classifications of the supraspinatus muscle) were ordinal and were used for bivariate and multivariable analysis. We created two multivariable ordinal logistic regression models to assess factors independently associated with Goutallier and Warner classifications. We included all variables with P < 0.10 on bivariate analysis in the final model (Table 2, Table 3). Statistical significance was defined as P < 0.05 for all tests.
Table 2.
Bivariate analyses of factors associated with Goutallier classification.
| Variables | Goutallier |
P value | ||||
|---|---|---|---|---|---|---|
| 0 | 1 | 2 | 3 | 4 | ||
| Patient age | 59 ± 9 | 63 ± 8 | 69 ± 9 | 68 ± 11 | 73 ± 11 | <0.001 |
| Patient sex | 0.56 | |||||
| Male | 25 (40) | 39 (46) | 27 (49) | 9 (69) | 4 (29) | |
| Female | 38 (60) | 46 (54) | 28 (51) | 4 (31) | 10 (71) | |
| Retraction (mm) | 14 ± 7 | 21 ± 10 | 24 ± 10 | 20 ± 10 | 35 ± 8 | <0.001 |
| Width (mm) | 15 ± 6 | 18 ± 8 | 21 ± 9 | 20 ± 7 | 25 ± 9 | <0.001 |
Bold indicates statistically significant difference; Continuous variables as mean ± standard deviation; Discrete variables as number (percentage).
Table 3.
Bivariate analyses of factors associated with Warner classification.
| Variables | Warner |
P value | |||
|---|---|---|---|---|---|
| 0 | 1 | 2 | 3 | ||
| Patient age | 60 ± 9 | 68 ± 9 | 68 ± 9 | 67 ± 11 | <0.001 |
| Patient sex | 0.4 | ||||
| Male | 41 (39) | 36 (53) | 17 (49) | 10 (43) | |
| Female | 63 (61) | 32 (47) | 18 (51) | 13 (57) | |
| Retraction (mm) | 18 ± 10 | 21 ± 9 | 23 ± 10 | 30 ± 10 | <0.001 |
| Width (mm) | 16 ± 7 | 19 ± 9 | 19 ± 8 | 23 ± 7 | <0.001 |
Bold indicates statistically significant difference; Continuous variables as mean ± standard deviation; Discrete variables as number (percentage).
3. Results
3.1. Relative percentage of full thickness defects that were above a specific size with reasonable muscle quality
Using a cut-off of 20 mm in an attempt to identify potential large acute ruptures, fifty-seven of the 230 shoulders (25%) had a coronal plane defect greater than 20 mm in combination with Goutallier grade less than 2, suggesting either relative sparing of the anterior supraspinatus, or relatively recent large defects more likely to be traumatic ruptures. Sixty-nine shoulders (30%) had a coronal plane defect greater than 20 mm and Warner grade less than 2. Forty-nine of 109 shoulders (45%) with a coronal plane defect >20 mm had reasonable muscle quality as defined by Goutallier grade less than 2 and Warner grade less than 2.
3.2. Factors associated with supraspinatus fatty infiltration and muscle atrophy
Accounting for potential confounding in multivariable analyses, greater fatty infiltration of the supraspinatus muscle categorized according to Goutallier was associated with older age (Odds ratio [OR] 1.1, 95% confidence interval [CI] 1.1 to 1,1; P < 0.001) and greater coronal plane defect size (OR 1.1, 95% CI 1.0 to 1.1; P < 0.001; Table 4).
Table 4.
Multivariable ordinal logistic regression analysis of factors associated with Goutallier and Warner classifications.
| Dependent variables | Independent variables | Regression coefficient [β] (95% CI) | Standard error (SE) | P value | VIF | Semipartial R2 | Adjusted R2 |
|---|---|---|---|---|---|---|---|
| Goutallier | Patient age in years | 0.08 (0.05–0.11) | 0.01 | <0.001 | 1.06 | 0.1 | 0.13 |
| Retraction (mm) | 0.08 (0.05–0.12) | 0.02 | <0.001 | 1.85 | 0.08 | ||
| Width (mm) | −0.00 (−0.04 to 0.04) | 0.02 | 0.922 | 1.88 | |||
| Warner | Patient age in years | 0.06 (0.03–0.09) | 0.01 | <0.001 | 1.06 | 0.05 | 0.08 |
| Retraction (mm) | 0.06 (0.02–0.09) | 0.02 | 0.001 | 1.85 | 0.05 | ||
| Width (mm) | −0.01 (−0.05 to 0.03) | 0.02 | 0.771 | 1.88 |
Bold indicates statistically significant difference; * Only the semipartial R2 of significant variables is reported; VIF = Variance inflation factor.
Greater supraspinatus muscle atrophy categorized according to Warner was also associated with older age (OR 1.1, 95% CI 1.0 to 1.1; P < 0.001) and coronal plane defect size (OR 1.1, 95% CI 1.0 to 1.1; P = 0.001; Table 4) in multivariable analyses.
3.3. Relationship between supraspinatus fatty infiltration and muscle atrophy
There is a strong correlation between supraspinatus fatty infiltration categorized according to Goutallier and supraspinatus muscle atrophy categorized according to Warner (ρs = 0.74; P < 0.001; Table 5).
Table 5.
Bivariate analysis of Goutallier versus Warner Classification.
| Variables | Goutallier |
P value | ||||
|---|---|---|---|---|---|---|
| 0 | 1 | 2 | 3 | 4 | ||
| Warner | <0.001 | |||||
| 0 | 57 (90) | 42 (49) | 5 (9) | 0 (0) | 0 (0) | |
| 1 | 6 (10) | 31 (36) | 28 (51) | 2 (15) | 1 (7) | |
| 2 | 0 (0) | 12 (14) | 17 (31) | 4 (31) | 2 (14) | |
| 3 | 0 (0) | 0 (0) | 5 (9) | 7 (54) | 11 (79) | |
Bold indicates statistically significant difference; Discrete variables as number (percentage).
4. Conclusion
Evidence to date suggests there may be utility in distinguishing various classes of rotator cuff pathology that are obscured by referring to all defects as tears. We analyzed a large number of MRIs of shoulders with full thickness rotator cuff defects and found that nearly half of the largest defects had good muscle quality suggesting they were traumatic ruptures, but for the entire group muscle atrophy and fat replacement correlated with age and defect size suggesting a distinct pathological process of attritional defect formation with age. This supports conceptualizing some rotator cuff defects as ruptures and others as defects rather than describing all of them as tears.
This study has some limitations. First, the exclusion of notable acromioclavicular arthrosis (which would contribute to a younger cohort) and reports that don't mention a duration of symptoms (which might represent a higher proportion of acute, more likely traumatic ruptures) might overrepresent the relative prevalence of defects that were sizable (>20 mm) with good muscle. The rates of various types of defects in the MRIs selected in this study are probably not representative of the rates that would be observed in population-based data, but the relationships between age and defect size and muscle quality and the clear distinction of a subset of large defects without muscle deterioration are likely consistent in other samples. Second, we used duration of symptoms to select patients and found it unreliable. Given that the information is likely recorded by radiology technologists and not orthopaedic surgeons, we decided we could not rely on these to study the relationship between duration of symptoms and severity of rotator cuff pathology. Third, there were technical variations in the MRIs (e.g. 1.5 vs. 3.0 Tesla magnet) that might have affected the results, although the quality of the scans was very good overall. Finally, although the measurement of rotator cuff fatty infiltration and muscle atrophy are well-established in the literature, interobserver agreement for them is poor to moderate, with Lippe et al. reporting kappa values of 0.53 and 0.28 for Goutallier and Warner classifications, respectively.21 Nevertheless, we feel confident that similar relationships would be identified by other observers.
The observation that defect size and age are correlated with supraspinatus atrophy and fatty infiltration, which correlate with each other, is consistent with the weight of current evidence14,26 and supports the conceptualization of a large proportion of rotator cuff tendinopathy as an age-appropriate attritional process.2,4, 5, 6, 7 Evidence suggests that acute, traumatic full-thickness rotator cuff tears comprise 5% or less of operatively treated rotator cuff defects.1,3 On the other hand, as many as 88% of patients with symptoms from rotator cuff tendinopathy regard the onset of new shoulder symptoms as representing new pathology and often as an injury mistakenly ascribed to a specific event.27, 28, 29, 30, 31, 32, 33, 34 In other words, perceived injury is likely much more common than true injury. While acute traumatic ruptures are likely over-represented in our sample because of the way patients were selected and perhaps because MRIs are obtained largely for planning surgery in our setting, the observation of distinct classes suggestive of distinct traumatic and attritional pathologies is consistent with current best evidence. It is confusing to refer to both of these pathologies as tears.
Given the lines of evidence summarized in this paper, combined with the evidence from the current experiment, we feel it may be worthwhile to consider changing the nomenclature regarding rotator cuff defects. Traumatic defects tend to be large, involving more than one tendon.35,36 Gradual onset degenerative pathophysiology is often misinterpreted as new pathology and even as an injury.37, 38, 39 There is much to learn about the treatment of atraumatic defects. And, to date, there is limited evidence that closure of single tendon, relatively small and likely attritional/degenerative rotator cuff defects alters either 1) Comfort or incapability relative to non-operative treatment or 2) The natural history of the progression to rotator cuff arthropathy. One randomized trial by Moosmeyer et al. involving people with rotator cuff defects less than 3 cm and with good muscle quality found small gains in shoulder function with surgical management that increased over the course of 10 years compared to nonsurgical management.40, 41, 42 Another randomized trial by Kukkonen et al. involving people with small (averaging around 10 mm) symptomatic atraumatic full-thickness supraspinatus defects showed no differences at 1, 2, and 5 years.43, 44, 45 More experimental evidence is needed to demonstrate a benefit to defect closure.
The weight of evidence, including this study, suggests that rotator cuff defects are best conceptualized as either age-appropriate tendon senescence or acute traumatic rupture. The word “tear” might be replaced with the word “defect” and “repair” with “closure” in the setting of rotator cuff attrition. For acute defects, the word rupture might be more appropriate as rupture connotes injury, while the jargon “tear” has come to be used misleadingly to refer to both traumatic and atraumatic defects. These word choices are important as they may contribute to unhealthy and inaccurate interpretation of symptoms (unhelpful thoughts), reinforcement of the misconceptions that surgery is necessary for repair, and false hopes that surgery can cure attrition of the rotator cuff.
Funding/sponsorships
This research did not receive any specific grant from funding agencies in the public, commercial or not-for-profit sectors.
Institutional ethical committee approval
This study received approval from the Institutional Review Board of the University of Texas at Austin. This study has been performed in accordance with the ethical standards in the 1964 Declaration of Helsinki. This study has been carried out in accordance with relevant regulations of the US Health Insurance Portability and Accountability Act (HIPAA). The study number assigned to this study is 2019–01-0148.
Author contributions
EK: Conceptualization, Methodology, Software, Validation, Formal analysis, Investigation, Data Curation, Writing – Original Draft, Writing – Review & Editing, Visualization BK: Investigation, Data Curation, Formal Analysis, Writing – Review & Editing JK: Methodology, Software, Validation, Formal analysis, Investigation, Resources, Writing – Review & Editing AJ: Writing – Review & Editing, Supervision DR: Conceptualization, Methodology, Resources, Writing – Review & Editing, Supervision, Project administration.
Declaration of competing interest
One of the authors (DR) received royalties from Wright Medical (Memphis, TN, USA) for elbow plates in the amount of less than USD 10,000 per year and from Skeletal Dynamics for an internal joint stabilizer elbow in the amount of between 10,000 and 100,000 USD per year. One of the authors certifies that he (DR) is a Deputy Editor for Hand and Wrist, Journal of Orthopaedic Trauma, and Clinical Orthopaedics and Related Research® and has received or may receive payments or benefits in the amount of USD 5000 per year. One of the authors certifies that he (DR) received honoraria from meetings of the AO North America (Wayne, PA, USA), AO International (Davos, Switzerland), and various hospitals and universities. All other authors report no conflict of interest.
Acknowledgements
None.
Contributor Information
Eugene Kim, Email: eskim@utexas.edu.
Benjamin Kopp, Email: Bjkopp@ascension.org.
Joost T.P. Kortlever, Email: kortlever.joost@gmail.com.
Anthony Johnson, Email: aj.johnson@austin.utexas.edu.
David Ring, Email: david.ring@austin.utexas.edu.
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