Histologic Differences in Human Rotator Cuff Muscle Based on Tear Characteristics

Abstract

Background: Fatty accumulation in the rotator cuff is associated with shoulder dysfunction and a risk of failure of rotator cuff repair. The aims of this study were to (1) describe cellular findings in rotator cuff muscles in patients presenting with varying degrees of rotator cuff tendon pathology by examining fat content and myofiber cross-sectional area of rotator cuff muscles and (2) correlate histologic features to magnetic resonance imaging (MRI) grades derived with the Goutallier classification.Methods: Rotator cuff muscle biopsies were performed in a consecutive series of patients undergoing arthroscopic shoulder surgery. Rotator cuffs were graded according to the Goutallier classification and labeled as either partial-thickness or fullthickness. Patients without a rotator cuff tear undergoing arthroscopic surgery served as controls. The biopsy specimens were examined using LipidTOX to visualize lipid accumulation. Laminin was used to quantify myofiber cross-sectional area.Results: Twenty-seven patients with a rotator cuff tear and 12 without a tear (controls) were included. There were 24 males (62%). The mean age was 55 years. Patients in the control cohort were younger (mean, 46 years) than those in the treatment group (mean, 60 years, p < 0.01). Within the treatment group, 12 and 15 patients were recorded as having partial and full-thickness rotator cuff tears, respectively. Lipid accumulation visualized at the cellular level was fairly-tomoderately correlated with the Goutallier classification on MRI (R s = 0.705, 95% confidence interval [CI] = 0.513, 0.829). Muscle biopsy specimens with a Goutallier grade of 21 had significantly more lipid accumulation than those with grade-0 (p < 0.01) or grade-1 (p < 0.01) fatty accumulation. Muscle biopsies at the sites of full-thickness tears showed significantly greater lipid accumulation than those associated with either partial (p < 0.01) or no (p < 0.01) tears. Partialthickness rotator cuff tears had no difference in lipid accumulation in comparison to the control group. Muscle biopsy specimens from full-thickness tears had significantly smaller myofiber cross-sectional area when compared with partialthickness tears (p = 0.02) and controls (p < 0.01).Conclusions: Cellular lipid accumulation correlates with the MRI Goutallier grade of fatty accumulation, thus verifying the Goutallier classification at the cellular level. Muscle biopsy specimens from partial-thickness tears are more similar to controls than to those from full-thickness tears, whereas full-thickness tears of all sizes showed significantly greater lipid content and smaller myofiber cross-sectional area compared with partial-thickness tears and controls.Clinical Relevance: Our research confirms the utility of using the Goutallier classification to predict rotator cuff muscle quality and shows that tendon attachment, even if partially torn, protects the muscle from fatty accumulation. Rotator cuff repairs are among the most commonly performed orthopaedic procedures in the United States 1 . Intact r...

Association Between Supraspinatus Tendon Retraction, Histologic Myofiber Size, and Supraspinatus Muscle Atrophy on MRI

“…All patients underwent en bloc supraspinatus muscle biopsy according to the same methodology published previously. 16 To standardize the location of arthroscopic muscle biopsy across patients, the biopsy specimens were collected after rotator cuff repair. The lateral border of the scapular spine was arthroscopically skeletonized with bipolar radiofrequency ablation to differentiate supraspinatus (anterior to scapular spine) from infraspinatus (posterior to scapular spine), and care was taken to ensure that muscle was clearly visualized medial to the musculotendinous junction.…”

“…Detailed methodology on our laminin staining process is available in a previously published study. 16 Once stained, muscle fiber CSAs were quantified using the BioVoxxel toolbox plug-in for ImageJ (National Institutes of Health). 17 Laminin immunofluorescent staining was analyzed and depicted as heat maps, allowing for quantification of myofiber size.…”

“…Although MRI is a clinically useful noninvasive method of assessing muscle atrophy, muscle biopsy has been performed to directly measure myofiber cross-sectional area (CSA) histologically. 5,13,16 Previous histopathologic studies on human rotator cuff muscle have demonstrated that full-thickness supraspinatus tears are associated with corresponding decreased myofiber size as compared with partial-thickness tears. 5,13,16 Despite the growing knowledge of the risk factors and pathogenesis of muscle atrophy after rotator cuff tear,…”

“…5,13,16 Previous histopathologic studies on human rotator cuff muscle have demonstrated that full-thickness supraspinatus tears are associated with corresponding decreased myofiber size as compared with partial-thickness tears. 5,13,16 Despite the growing knowledge of the risk factors and pathogenesis of muscle atrophy after rotator cuff tear,…”

Shoulder & Elbow

“…In this investigation, researchers from Durham (North Carolina, USA) sought to describe the histology of rotator cuff muscles in patients with varying degrees of pathology, to correlate these histological findings to MRI appearances, and hence to correlate these findings to the Goutallier classification which was originally a CT-derived grading system. 7 To accomplish this, during a consecutive series of arthroscopic shoulder surgeries, muscle biopsies were taken intraoperatively from the rotator cuff. Rotator cuff tears were graded using the Goutallier classification, and subsequently labelled as partial- or full-thickness tears.…”