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Introduction

  1. Top of page
  2. Introduction
  3. Pathophysiology of FI
  4. Imaging of fatty changes
  5. Clinical relevance of FI
  6. Reversibility of changes
  7. Discussion
  8. AUTHOR CONTRIBUTIONS
  9. REFERENCES

Rotator cuff (RC) pathology is a common and challenging musculoskeletal condition to manage. The prevalence of RC tears is estimated between 15% and 51%, with higher rates at age >50 years (1). While RC repair is an effective procedure for relieving pain and improving function, high retear and/or failure-to-heal rates persist despite technical improvements. Furthermore, poorer outcomes are associated with failures and recurrent defects compared to intact repairs, although some tears are painless and associated with good function (2).

RC tendon research has primarily focused on changes at the tendon–bone interface. However, muscle physiology may require greater understanding, as the presence of fatty infiltration (FI) of the muscle following tears is also likely to influence the mechanics and biologic milieu of the RC tendons, and may predict and/or affect the results of RC repair. Fatty muscle infiltration influences several clinical parameters, as it is associated with higher failure rates and loss of muscle strength (3). Preoperative assessment of FI of any of the RC muscles, in addition to tear size and degree of retraction, may play an increasing role in planning surgical management and for counseling patient expectation. Both partial- and full-thickness RC tears are associated with increased FI, which has been shown to be more extensive in larger tears (4). This review explores the prevalence, pathophysiology, and clinical implications of fatty changes of the RC. Muscle atrophy is an important related topic, but beyond the scope of this review.

Significance & Innovations

  • Rotator cuff tendon tears are a prevalent musculoskeletal disorder, with high failure rates following repair despite advances in techniques.

  • There is increasing evidence that muscle physiology influences clinical outcomes, in particular fatty infiltration, as it is associated with higher failure rates and loss of muscle strength.

  • Evidence regarding the reversibility of fatty infiltration remains inconclusive, although surgical repair has been reported to prevent progression of fatty changes.

  • Preoperative assessment of fatty infiltration may play an increasing role in surgical planning and managing patient expectations regarding outcomes.

Pathophysiology of FI

  1. Top of page
  2. Introduction
  3. Pathophysiology of FI
  4. Imaging of fatty changes
  5. Clinical relevance of FI
  6. Reversibility of changes
  7. Discussion
  8. AUTHOR CONTRIBUTIONS
  9. REFERENCES

Deposition of fat within muscles is termed FI. It is unclear whether FI of muscles occurs as part of the normal degeneration process, or is indicative of a failed repair mechanism that predisposes to tears.

Fatty changes can occur in multiple locations. Following massive tears, FI was found in the muscle belly within the interstitial (intramuscular) and epimysial (extramuscular) compartments, as well as within the torn tendon (5). Within the muscle, FI is associated with increased interstitial connective tissue, which may impair tendon physiology and mechanics (6). Accumulation of fat has been noted at the muscle surface, as well as within the sarcoplasm of type I muscle fibers (7).

A number of theories have been proposed to explain the pathophysiology of FI in the healing environment following tears. Distal supraspinatus detachment with muscular retraction and loss of muscle load or tension may alter the tendon physiology and increase susceptibility to changes that induce FI. Animal models of RC tears with FI have demonstrated decreased tendon mechanical properties (8). Gerber et al demonstrated in an ovine model that detachment and retraction of infraspinatus muscles resulted in a significant increase in FI and decreased cross-sectional area (9). Traction was then applied to increase the muscle–tendon unit length following RC repair, which prevented progression of fatty changes. However, it was noted that preexisting muscle FI remained unchanged. The pennation angle, which typically increases with cross-sectional area, did not vary significantly compared to controls.

Increased lipid deposition within the tendon may impair tendon elasticity (6), increasing the likelihood that the tendon–muscle complex will remain retracted following tears. However, it was noted in an ovine model that despite the presence of FI, there was no degeneration or changes in muscle fiber composition, and vascularization and intramuscular pressures remained unaffected (6). Changes in tendon compliance due to lipid deposition may make tendon mobilization for repair more difficult.

Suprascapular neuropathy may contribute to FI, as supported by both animal models and small clinical studies (10, 11). Albritton et al proposed that supraspinatus retraction might place excessive tension or traction on the suprascapular nerve, which may subsequently contribute to both infraspinatus and supraspinatus degeneration (12). Decreased propagation of action potentials at the neuromuscular junction may reduce muscle contraction and result in architectural changes and FI.

Tear size and vascularity may influence the extent of FI. Larger tears were found to have an increased association with lipid accumulation, as well as an increased number of blood vessels and mitochondria (13). These changes may reflect increased aerobic metabolism in muscle fibers associated with larger tears. Furthermore, inducers of neoangiogenesis may play an important role in the pathogenesis of fatty changes. Immunohistologic analysis of biopsy samples taken from 33 patients with medium-sized tears suggested that FI was associated with increased expression of hypoxia-inducible factor 1 and vascular endothelial growth factor (14).

At the intracellular level, preexisting adipocytes are suggested to proliferate in torn tendons, rather than simply accumulating increased triglyceride content. Matsumoto et al noted that despite increased fatty accumulation in torn RC tendons, the size of tendon adipocytes remained the same as in control tendons (7). Peroxisome proliferator–activated receptor α may help to regulate fatty acid catabolism. FI in larger tears has been shown to result in decreased muscle fiber size and absolute myofibril volume, rather than fiber death (13).

Imaging of fatty changes

  1. Top of page
  2. Introduction
  3. Pathophysiology of FI
  4. Imaging of fatty changes
  5. Clinical relevance of FI
  6. Reversibility of changes
  7. Discussion
  8. AUTHOR CONTRIBUTIONS
  9. REFERENCES

Goutallier initially proposed a 5-stage grading system for FI of RC tears using computerized tomography (CT) with contrast that could be used to predict outcomes and from which tears were likely to be irreparable (15) (Table 1). This was modified by Fuchs et al to form a 3-stage classification (16). The axial CT plane is reported to produce the most consistent results (17). Currently, a modified magnetic resonance imaging (MRI) grading system is widely used clinically to assess FI of the RC (Figure 1).

Table 1. Outlining different classification systems for assessment of fatty infiltration of rotator cuff muscles (7, 13)
 Rotator cuff pathology
Goutallier et al staging 
 0Muscle without fatty streak (i.e., no fatty deposits). This represents completely normal muscle
 1Rotator cuff muscle contains some fatty streaks but the majority is still normal muscle tissue
 2Fatty infiltration is present but there is still more muscle present than fat
 3Equal amounts of muscle and fat are observed
 4The majority is fat rather than muscle
Fuchs et al staging 
 Grade 0 and 1Represents normal muscle
 Grade 2Moderately pathologic muscle
 Grade 3 and 4Advance degeneration
thumbnail image

Figure 1. A, Magnetic resonance imaging (MRI; coronal proton-density image) of the right shoulder demonstrating a chronic supraspinatus tear with fatty infiltration, tendon retraction, and severe muscle atrophy. B, MRI (sagittal proton-density image) of the right shoulder. Severe fatty infiltration of the supraspinatus and infraspinatus muscles is visible.

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Questions persist about the reproducibility of imaging assessment of FI. Lesage et al graded FI using CT and reported a good interobserver agreement (r2 = 0.75), which was improved by increased experience (r2 = 0.78) (18). Interobserver agreement for MRI Goutallier staging is reported to be poor, although this may be a reflection of imaging experience. In a recent study, the observed agreement between 10 fellowship-trained orthopedic surgery shoulder specialists for determining muscle quality and Goutallier grade was 0.36, with a kappa value of just 0.1 (19). A comparison of CT versus MRI assessment of fatty changes found only a fair to moderate correlation (16). Another study compared interpretation of 75 CT arthrography and MRI arthrography images by 2 radiologists and 3 fellowship-trained orthopedic surgeons (20). A higher correlation coefficient was reported for MRI arthrography (95% confidence interval [95% CI] 0.6–0.72) compared to CT arthrography (95% CI 0.43–0.6), and was higher for radiologists (95% CI 0.58–0.78) than surgeons (95% CI 0.32–0.68). No difference was found between the reliability of the Goutallier and Fuchs grading systems.

Ultrasound is an alternative assessment modality that is cheaper, less time consuming, and has greater availability at some institutions, although it is technician dependent. In a study of 45 shoulders from 39 patients, high comparability in the accuracy of MRI and ultrasound was suggested, with a reported correlation coefficient of 0.90 (21). Ultrasound had 94.4% sensitivity and 91.3% specificity in diagnosing supraspinatus FI, with lower levels for the infraspinatus.

Clinical relevance of FI

  1. Top of page
  2. Introduction
  3. Pathophysiology of FI
  4. Imaging of fatty changes
  5. Clinical relevance of FI
  6. Reversibility of changes
  7. Discussion
  8. AUTHOR CONTRIBUTIONS
  9. REFERENCES

A number of clinical studies have reported the effect of FI on clinical outcomes, and are outlined in Table 2. In an ultrasound study of 251 shoulders with full-thickness supraspinatus or infraspinatus tears, FI prevalence of 34.7% was measured (4). Based on a retrospective analysis of 377 shoulder MRIs, the prevalence of FI of the infraspinatus muscle (Goutallier grade 2 or higher) was estimated at 66.7% of full-thickness tears (22). The discrepancy in prevalence rates may be due to greater MRI sensitivity in detecting fatty changes. FI is not limited to RC tears, and in one series was shown to occur in the absence of tears in 18.1% of cases (22).

Table 2. Summary of clinical studies related to fatty infiltration and muscle atrophy of rotator cuff muscles*
Author, year (ref.)Muscles involvedStudy designPurposeConclusionGrading systemLimitations
  • *

    LOE = level of evidence; FI = fatty infiltration; US = ultrasound; NA = not applicable; MRI = magnetic resonance imaging; CT = computed tomography; OA = osteoarthritis.

Kim et al, 2010 (4)Supraspinatus, infraspinatusRetrospective review (251 shoulders assessed for tears) LOE: 3Investigate the relationship between tear geometry and muscle FI in shoulder rotator cuff tears using USIntegrity of the anterior supraspinatus tendon is important to the development of FI, and patients with tears that extend through this specific area may benefit from early surgical interventionNAUS is less commonly used as an imaging modality to assess fatty degeneration than is MRI or CT Accuracy of US for the detection of FI in rotator cuff muscles has yet to be validated by institution of study Data for interobserver and intraobserver reliability of those who performed US were not available
Tae et al, 2010 (33)Supraspinatus, infraspinatusCohort study (61 patients with full-thickness rotator cuff tears) LOE: 2Introduce new method (multidetector CT) to evaluate fatty degenerationThis form of quantitative measuring of FI was rather reliable and correlated well with both the preexisting grade of fatty degeneration and cuff tear sizeGoutallier systemCorrelates well with only a specific oblique sagittal image when compared to MRI There may be some pathology not assessed with this method
Goutallier et al, 2010 (34)Supraspinatus, infraspinatus, deltoidProspective study (29 shoulders without OA) LOE: 4Evaluate the functional level of influence of an intact rotator cuff on unweighted Constant scoreOther than the rotator cuff, there seems to be other muscles in the shoulder involved in “basic” shoulder function representing 60% of the unweighted Constant score A lower fatty degeneration index is correlated with more function of an intact repaired cuff, which improves a “basic function level”Goutallier systemDespite long-term followup and high negative correlation between compared groups and the relatively small size of the series of sutured cuffs, it is difficult to definitely confirm the validity of this method
Oh et al, 2009 (35)Supraspinatus, infraspinatus, subscapularisProspective study (366 with disorders of the shoulder) LOE: 3Determine the role of vitamin D as a factor accounting for fatty degeneration and muscle function in the rotator cuffVitamin D level has a significant negative correlation with fatty degeneration of torn cuff musclesGoutallier systemCould not demonstrate relationship between fatty degeneration of subscapularis and vitamin D No normal control group
Oh et al, 2010 (20)Supraspinatus, infraspinatus, subscapularisRetrospective study (review of 75 full-thickness tears) LOE: 3To validate reliability of rotator cuff grading systemsReported data from system of Goutallier et al should be interpreted carefully because of relatively low reliabilityGoutallier system, Fuchs systemUsed different modalities preoperatively and postoperatively Included only rotator cuff tears in the study and observers were not blinded May be a bias when evaluating postoperative CT among observers
Burkhart et al, 2007 (26)Supraspinatus, infraspinatus, subscapularisRetrospective study (22 patients with massive rotator cuff tears) LOE: 4Determine the functional results of arthroscopic repair of massive rotator cuff tears in patients with stage 3 and 4 FIArthroscopic rotator cuff repair in patients with grade 3 or 4 fatty degeneration, specifically with 50–70%, show much greater improvement than those with >75% fatty degenerationGoutallier systemRelatively small number of patients
Goutallier et al, 2003 (23)Supraspinatus, infraspinatus, subscapularisProspective study (221 shoulders with rotator cuff tear) LOE: 4Assess whether the severity of presurgical fatty degeneration had an influence on anatomic and functional outcomesEvaluating the degree of fatty degeneration prior to surgery of infraspinatus or subscapularis muscles had an influence on supraspinatus tendon outcome and is an important prognostic factor in rotator cuff surgeryGoutallier systemDue to the fact that sagittal CT section reconstruction was not performed, the study was unable to examine the potential influence of supraspinatus atrophy on the likelihood of tear recurrence
Goutallier et al, 1999 (3)Supraspinatus, infraspinatus, subscapularisProspective study (74 patients operated for rotator cuff rupture) LOE: 4Assess whether fatty degeneration has an influence on anatomic and clinical results after surgical repair of rotator cuffFatty degeneration of supraspinatus and infraspinatus is an important prognostic factor of functional results after surgical repair of the rotator cuff Concludes that it is probably better to operate on rotator cuff tears before the appearance of irreversible muscular damageGoutallier systemCertain satisfactory results in the series could not be explained properly by the occurrence of retears, the presence of important muscle degeneration, a lesion of the subscapularis, or by a neglected tendon cleavage
Fuchs et al, 1999 (16)Supraspinatus, infraspinatusProspective study (41 patients underwent CT and MRI of affected shoulder) LOE: 3Evaluate whether fatty degeneration of rotator cuff muscles could reproducibly be assessed by CT or MRI and if grading by 2 methods was comparableGoutallier grading system of FI is reproducible as well on CT as on MRI No evidence that either grading by MRI or CT accurately reflects the true degree of fatty degeneration or infiltration of graded muscleGoutallier system, Fuchs systemParasagittal imaging used for MRI, whereas horizontal sections were used for CT, which could lead to examination of different muscular regions
Goutallier et al, 1994 (15)Supraspinatus, infraspinatus, subscapularisProspective study (63 patients) LOE: 4To determine whether FI progressively increases over time, decreases after repair, and is accompanied by muscle weaknessTendinous cuff tears induce muscle degeneration over time FI, particularly of the infraspinatus, can be correlated with severe functional impairment Degree of severity of FI correlates with poor functional outcomesGoutallier systemMeasurement of shoulder cuff muscles areas or volumes could not be reliably or easily performed with a CT scan

Goutallier grading can potentially play a role in managing RC tears. The measured Goutallier grade can be used to estimate both retear rates and clinical outcomes following RC repairs, and thus give surgeons an indication as to tendon reparability and help to counsel patients regarding their likely outcomes. A study using both CT and MRI assessment of 220 shoulders found that a Goutallier grade of greater than 1 predicts higher retear rates for RC repairs (23). Postoperative American Shoulder and Elbow Surgeons and Constant scores also reportedly correlate with Goutallier grading (5, 24). Postoperative (and not preoperative) infraspinatus FI (Goutallier grade 2 or less as measured on MRI) was found to predict postoperative outcomes, as assessed by both MRI and University of California, Los Angeles (UCLA) scores (25). However, the grading system is not without its limitations. Clinical improvement has been reported in a small series of repairs involving massive tears with grade 3 or 4 FI of the infraspinatus that were predicted likely to fail by the Goutallier grade (26).

A correlation has been described between the preoperative global fatty degeneration index, which measures the mean value of the Goutallier grades for the supraspinatus, infraspinatus, and subscapularis muscles, and the recurrence of tears at up to 9 years (23).

The presence and degree of muscular FI have been found to be associated with increasing age and significantly larger cuff tear width and length; in fact, these latter 2 factors were found to be the most important predictors of infraspinatus FI (4). FI was also associated with a significantly shorter tear distance posteriorly from the biceps, and thus this distance has been proposed as an important predictor of supraspinatus FI.

Rapid progression of FI and muscle atrophy has been reported following tears. One study reported that 50% of cases with FI progressed within 6 months (27). A retrospective analysis of 1,688 patients with RC tears involving preoperative CT or MRI evaluation of the supraspinatus and infraspinatus found that FI appeared at an average of 3 years after symptom onset in moderate cases, and after 5 years in cases with severe FI (28). Progression of FI was noted to be more rapid following infraspinatus tears, with intermediate infiltration occurring after 3 years and severe infiltration taking 4 years (29). For both tendons, more severe FI appeared to involve a longer time course. The rate of progression of FI is affected by whether or not repairs remain intact. Gladstone et al reported a higher rate of progression of changes in repairs that fail to heal compared to intact repairs (24).

A correlation between fatty changes in specific RC muscles and cuff tears has been suggested, as FI in intact infraspinatus muscles was found to be predictive of supraspinatus tears. FI of the infraspinatus and subscapularis muscles reportedly influences supraspinatus tendon repair outcomes, and muscular atrophy is likely to be greater if more than one muscle is involved (15). Therefore, fatty changes in all RC muscles may need to be considered preoperatively.

In a prospective cohort study of 38 patients, FI and muscle atrophy predicted poorer functional outcomes (24). However, FI and atrophy were not found to be predictive of cuff integrity, although a correlation was found with tear size. Intact repairs were associated with a significantly slower rate of progression of FI and muscle atrophy compared to failed repairs. For reasons that are not fully understood, supraspinatus changes, unlike infraspinatus changes, were not found to correlate with outcomes in this study. Higher repair failure rates of the supraspinatus have been reported to correlate with increased preoperative FI of the supraspinatus and infraspinatus muscles in a series of 57 patients with a mean followup of 17.7 months (15). A larger series following 74 patients had demonstrated that FI of the infraspinatus more than the supraspinatus correlated with decreased strength and range of motion, particularly impaired active external rotation (3).

Supraspinatus retear rates as high as 50–70% have been reported in association with Goutallier grade 2 or greater FI, and 67% for muscle atrophy (15, 24). A strong correlation between FI and increased tear size and higher repair failure rates has been demonstrated (24, 30). In contrast, Jost el al found that neither preoperative supraspinatus nor infraspinatus FI predicted clinical outcomes, but postoperative FI could be used to predict clinical outcomes (31). Significant clinical improvement assessed using UCLA scores has been reported following arthroscopic repairs of tears associated with even severe fatty changes, although greater improvement is seen if FI affects 50–75%, rather than more than 75%, of the tendon (26).

Reversibility of changes

  1. Top of page
  2. Introduction
  3. Pathophysiology of FI
  4. Imaging of fatty changes
  5. Clinical relevance of FI
  6. Reversibility of changes
  7. Discussion
  8. AUTHOR CONTRIBUTIONS
  9. REFERENCES

Some uncertainty exists regarding the reversibility of fatty changes after surgical repair, and a number of animal studies have tried to address this. Evidence for partial reversal of lipid accumulation has been demonstrated in chronic injury ovine models following delayed repair at 30 weeks, or after 40 weeks of detachment without repair (6, 8). Interestingly, a rabbit study found that total fat accumulation was significantly higher in the reattached group compared to the detached tendon, although it was predominantly extramuscular rather than intramuscular fat (7).

Reversal of FI suggested by some animal studies has not been consistently translated to clinical studies, although case series have reported a combination of progression and reversal of fatty changes. A nonsignificant reversal of FI of the infraspinatus and subscapularis muscles was reported by Gerber et al from a series of patients with both intact and failed RC repairs (5). From a series of 57 patients, 6 of 14 patients with moderate supraspinatus FI demonstrated regression, unlike the infraspinatus tendon (15). Minimal to no progression of FI was noted from a prospective case series of 38 patients in patients who maintained intact repairs, as opposed to progression seen in failed repairs (24). In a case series of 57 patients evaluated using CT, Goutallier et al reported a nonsignificant regression of moderate supraspinatus FI in 43% of their patients, even if the repair remained intact (27). However, FI increased across both tendons, and at a faster rate if healing of the tear failed. Therefore, reversibility may be partially dictated by whether or not the tear remains intact and which tendon is involved, as some differences in natural history appear to exist between supraspinatus and infraspinatus tears, possibly due to different loading forces.

In view of the suggested association of suprascapular nerve compression with RC FI, decompression of the suprascapular nerve may play a role in preventing progression of FI.

There is likely a “point of no return” after which the elasticity of the muscle–tendon unit can no longer be regained. Some studies propose that time elapsed before surgery is a key determinant of surgical outcomes following repairs. A small study looking at 14 rabbits found that early repair of detached supraspinatus tendons at 6 weeks prevented an increase in fat accumulation compared to later attachment at 12 weeks (32). However, even after early repair at 6 weeks, a reversal or prevention of fat accumulation was not seen. Yamaguchi et al noted that patients whose FI progressed usually noted pain, so this may be a nonspecific discriminator in management decisions (1). Clinicians should consider early repair to best preserve and restore tendon/muscle integrity.

Discussion

  1. Top of page
  2. Introduction
  3. Pathophysiology of FI
  4. Imaging of fatty changes
  5. Clinical relevance of FI
  6. Reversibility of changes
  7. Discussion
  8. AUTHOR CONTRIBUTIONS
  9. REFERENCES

The physiology and quality of the RC muscles clearly play key roles in surgical and clinical outcomes following RC repairs. Further knowledge is required of the natural history of fatty changes of the RC and to understand whether it is preventable, as well as its implications with regard to healing or rerupture rates. Ideally, a randomized control trial would address whether RC repair can prevent progression, or even cause reversal, of FI and atrophy. Preoperative assessment should include investigation of fatty changes and atrophy of any of the RC muscles, in addition to tear size and degree of retraction. This information can be used to counsel patients regarding their expected outcomes and to guide surgical planning.

Prolonged conservative management of RC tears with early onset of FI may risk worsening of FI, which may make the tear irreparable. Some surgeons advocate early repair of symptomatic RC tears before the onset of severe fatty changes, given the proposed irreversibility, functional consequences, and risk of progression to marked muscle–tendon unit retraction that is likely to place increased tension on the repair. As Goutallier stage 2 is associated with poorer muscle function and increased failure of RC repairs, it may be ideal to repair RC tears prior to the development of severe FI. Time since the onset of tears may also be a critical factor, as there may be a finite window of opportunity within which to achieve reversal of fatty changes within the muscle (33–35).

AUTHOR CONTRIBUTIONS

  1. Top of page
  2. Introduction
  3. Pathophysiology of FI
  4. Imaging of fatty changes
  5. Clinical relevance of FI
  6. Reversibility of changes
  7. Discussion
  8. AUTHOR CONTRIBUTIONS
  9. REFERENCES

All authors were involved in drafting the article or revising it critically for important intellectual content, and all authors approved the final version to be published.

REFERENCES

  1. Top of page
  2. Introduction
  3. Pathophysiology of FI
  4. Imaging of fatty changes
  5. Clinical relevance of FI
  6. Reversibility of changes
  7. Discussion
  8. AUTHOR CONTRIBUTIONS
  9. REFERENCES
  • 1
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