ARTICLE IN PRESS J Shoulder Elbow Surg (2018) ■■, ■■–■■
www.elsevier.com/locate/ymse
ORIGINAL ARTICLE
Superior glenoid inclination and rotator cuff tears Peter N. Chalmers, MD*, Lindsay Beck, BA, Erin Granger, MPH, Heath Henninger, PhD, Robert Z. Tashjian, MD Department of Orthopaedic Surgery, University of Utah, Salt Lake City, UT, USA Background: The objectives of this study were to determine whether glenoid inclination (1) could be measured accurately on magnetic resonance imaging (MRI) using computed tomography (CT) as a gold standard, (2) could be measured reliably on MRI, and (3) whether it differed between patients with rotator cuff tears and age-matched controls without evidence of rotator cuff tears or glenohumeral osteoarthritis. Methods: In this comparative retrospective radiographic study, we measured glenoid inclination on T1 coronal MRI corrected into the plane of the scapula. We determined accuracy by comparison with CT and inter-rater reliability. We compared glenoid inclination between patients with full-thickness rotator cuff tears and patients aged >50 years without evidence of a rotator cuff tear or glenohumeral arthritis. An a priori power analysis determined adequate power to detect a 2° difference in glenoid inclination. Results: (1) In a validation cohort of 37 patients with MRI and CT, the intraclass correlation coefficient was 0.877, with a mean difference of 0° (95% confidence interval, −1° to 1°). (2) For MRI inclination, the inter-rater intraclass correlation coefficient was 0.911. (3) Superior glenoid inclination was 2° higher (range, 1°-4°, P < .001) in the rotator cuff tear group of 192 patients than in the control cohort of 107 patients. Conclusions: Glenoid inclination can be accurately and reliably measured on MRI. Although superior glenoid inclination is statistically greater in those with rotator cuff tears than in patients of similar age without rotator cuff tears or glenohumeral arthritis, the difference is likely below clinical significance. Level of evidence: Level III; Diagnostic Study © 2018 Journal of Shoulder and Elbow Surgery Board of Trustees. All rights reserved. Keywords: Rotator cuff tear; glenoid inclination; rotator cuff; etiology; critical shoulder angle; scapular morphology
The etiology of rotator cuff tears remains controversial.4,27,29,39 Some have argued that rotator cuff tearing is a degenerative, age-related process27,29 driven by hypoxia42-45 and overuse.26 Others have argued that scapular morphology plays a role.1,4,8,15,22,28,39 Recently, multiple authors have
This study was performed under University of Utah Institutional Review Board approval (Protocol # 71740). *Reprint requests: Peter N. Chalmers, MD, Department of Orthopaedic Surgery, University of Utah, 590 Wakara Way, Salt Lake City, UT 84105, USA. E-mail address:
[email protected] (P.N. Chalmers).
shown the critical shoulder angle (CSA) to associate with rotator cuff tears.3,13,18,23,34,37 The CSA is a combination measurement of the acromial index, which has been independently associated with rotator cuff tears,3,37 and glenoid inclination, which has also been independently associated with rotator cuff tears.13,23 Which of these factors is dominant remains unknown. Superior glenoid inclination may alter the muscular vector of the deltoid and rotator cuff with respect to the articular surface. Superior glenoid inclination increases the shear component and decreases the compressive component of the rotator cuff and thus increases the mechanical load on the articular
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ARTICLE IN PRESS 2 margin of the supraspinatus.18,30,46 This increased load may contribute to rotator cuff tears.6,13,23,36,40 However, other studies have not been able to demonstrate a clinically relevant relationship between CSA5,11 or glenoid inclination24 and rotator cuff tears. Heterogeneity in the findings of the prior literature may have resulted from measurement bias and selection bias. Most of the prior studies were performed with 2-dimensional radiographs.3,5,11,13,18,23,34,37 The CSA can only be reliably measured on a high-quality true anteroposterior radiograph,41 and retrospective application of the strict criteria necessary to achieve reliable measurements can result in a substantial selection bias.11 In addition, glenoid inclination cannot be reliably measured on plain radiographs or even on computed tomography (CT) images unless these images are reoriented into the plane of the scapula.9,20 However, inclination measurements have been demonstrated to be reliable on CT images reoriented into the plant of the scapula.9 These measurements on CT have also been shown to be equivalent to gold standard automated 3-dimensional methods on CT.9 However, no prior studies have determined whether magnetic resonance imaging (MRI) inclination measurements are equivalent to CT measurements or whether MRI inclination measurements are reliable. Furthermore, many prior studies did not have agematched controls or had controls in whom the absence of rotator cuff tears and glenohumeral osteoarthritis was not confirmed radiographically.3,5,11,13,18,23,34,37 Thus, the objectives of this study were to determine whether we could (1) accurately measure glenoid inclination on MRI using CT as a gold standard and (2) reliably measure glenoid inclination on MRI, and (3) to determine whether glenoid inclination differs between patients with rotator cuff tears and age-matched controls without evidence of rotator cuff tears or glenohumeral osteoarthritis. We hypothesized that (1) we could accurately measure glenoid inclination on MRI using CT as a gold standard with an intrarater intraclass correlation coefficient (ICC) of >0.75 and an insignificant mean difference between measurements, (2) we could reliably measure glenoid inclination on MRI with an interrater ICC of >0.75, and (3) patients with rotator cuff tears would demonstrate greater superior glenoid inclination than agematched controls that did not exhibit evidence of rotator cuff tears or glenohumeral osteoarthritis.
Materials and methods To address our 3 objectives, we studied 3 patient groups. Informed consent was not required by our institutional review board for this retrospective radiographic study. The first group of patients had an MRI and a CT scan and served as a validation population for inclination measurement accuracy. We conducted a review within our hospital system of all patients who had undergone an arthroscopic labral repair. We reviewed this list and only included patients who had undergone a CT scan and an MRI preoperatively within 6 months of each
P.N. Chalmers et al. other. We excluded patients with evidence of osseous pathology or glenoid bone loss. The second group of patients had rotator cuff tears and relevant medical imaging. We selected these patients from the clinical practice of the senior author (R.Z.T.) and included patients treated operatively and nonoperatively. Inclusion criteria included patients with full-thickness tears of the supraspinatus or infraspinatus on MRI aged between 30 and 80 years. Exclusion criteria included partial-thickness rotator cuff tears, significant glenohumeral arthritis, and prior surgery on the affected shoulder.45 We screened each patient for inclusion by review of the MRI radiology report. An attending surgeon, fellowship trained in shoulder and elbow surgery (P.N.C.), then reviewed the images identified by this search. Only patients confirmed by the radiology report and the attending surgeon’s review to have a full-thickness rotator cuff tear were included within the rotator cuff tear group. The final patient group was a control cohort, aged older than 50, with relevant medical image data and no evidence of a rotator cuff tear or glenohumeral osteoarthritis. We searched our hospital system and created a list of all patients aged older than 50 who had undergone an MRI. A research associate (L.B.) then reviewed the radiology report for each MRI. An attending surgeon, fellowship trained in shoulder and elbow surgery (P.N.C.), then reviewed the images identified by this search. We only included patients confirmed by the radiology report and the attending surgeon’s review to have no evidence of a partial-thickness or full-thickness rotator cuff tear or glenohumeral osteoarthritis within the control group. We excluded patients with glenohumeral osteoarthritis from the rotator cuff tear and control groups because glenohumeral osteoarthritis has also been demonstrated to associate with glenoid inclination.5,36,40
Data collection and radiographic measurement protocol For each patient in the control and rotator cuff tear groups, we collected patient age at the time of the scan. For each patient in the rotator cuff tear group, we collected the following data: the tendons (subscapularis, supraspinatus, infraspinatus, teres minor) that were involved in the tear, the number of tendons involved in the tear, maximal tear width as measured on the sagittal T2 images, maximal tear retraction as measured on the coronal T2 images, and the Goutallier classification for each muscle19 as measured on the most lateral T1 coronal image where the scapular spine and body remain confluent. Glenoid inclination and glenoid version were measured for each patient in the control and rotator cuff tear groups as described previously.9 All measurements were performed in an OsiriX viewer (Pixmeo Sarl, Bern, Switzerland). Inclination measurements were made on T1 coronal images to provide the best osseous detail. First, these coronal images were reoriented into the plane of the scapula. The plane of the scapula is defined by (1) the inferior pole, (2) the medial border on an axial slice at the middle of the glenoid, and (3) the center of the glenoid.7 On the reoriented coronal image at the center of the glenoid, we measured the distance from the medial aspect of the image to the lateral aspect of the glenoid. We only included individuals with a minimum of 8 cm of scapular width imaged because lesser widths have been shown to be associated with significant measurement alterations.10 We considered individuals without a T1 coronal image or without 8 cm of scapular width imaged to have inadequate quality scans.
ARTICLE IN PRESS Glenoid inclination and rotator cuff tears
3 for measurement of accuracy. Measurement of version on MRI has also been shown to be reliable.33 Within this study, we specifically measured the retroversion (ie, the degree to which the glenoid faces posteriorly), with a glenoid orthogonal to the plane of the scapula being defined as having 0° retroversion and with retroversion being defined as positive (+) and anteversion being defined as negative (−). We measured glenoid version as a negative control for objective 3 because there is no current evidence that glenoid version associates with rotator cuff tears.
Objective 1: assessment of accuracy To assess inclination measurement accuracy on MRI, we compared them with CT measurements, which are the current gold standard. First, we performed an a priori power analysis to ensure an adequate sample size for the accuracy determination group. In a previous study, the ICC for CT inclination measurements was 0.9.9 We determined that an ICC of 0.75 was the minimum acceptable.12 Given these expected and minimum ICCs and 2 observations per patient, we determined 36 individuals would be necessary to achieve 90% power using 0.05 as the threshold for significance. Coronal CT and MRI images from the arthroscopic labral repair cohort were then deidentified and randomized and reviewed in blinded fashion. The previously described inclination measurements were performed on these scapular plane–corrected coronal CT and MRI slices, and these inclination measurements were compared using ICCs. In addition, we determined the mean difference and 95% confidence intervals of the mean difference between the CT and MRI inclination measurements.
Objective 2: assessment of reliability Figure 1 Measurement of superior inclination (the angle between the top 2 lines, labeled SI for superior inclination) on (A) magnetic resonance imaging (MRI) and (B) computed tomography (CT). In this patient, 10 cm of scapular width was available on the MRI and 15 cm was available on the CT. Superior inclination in this patient was 15° on MRI and was 17° on CT. Inclination measurements were then taken on these corrected images (Fig. 1). Inclination has been defined previously as the angle between the glenoid and the scapular spine.14,35 We specifically measured the superior inclination (ie, the degree to which the glenoid faces superiorly), with a glenoid orthogonal to the plane of the scapula being defined as having 0° inclination and with superior inclination being defined as positive (+) and inferior inclination being defined as negative (−). We used axial images, similarly reoriented into the plane of the scapula, for the measurement of glenoid version. Version has been previously defined by the line between the anterior and posterior glenoid rim and a line from the medial visible aspect of the scapula and the middle of the glenoid on the axial slice midway between the most proximal slice containing the glenoid and the most distal slice containing the glenoid.16 This measurement on MRI has previously been shown to be equivalent to the same measurement on CT.33 On CT, these measurements have been shown to be reliable and to be equivalent to 3-dimensional measurements.32 We thus considered MRI measurements of glenoid version to be accurate. We used these CT measurements as a gold standard within this study
To assess inclination measurement reliability, inclination in a 36patient subgroup of the control group was measured by 2 authors (P.N.C. and L.B.) blinded to each other’s measurements. We selected this sample size using the same power analyses as described previously. We then compared the MRI inclination measurements from each observer using ICCs. Again, we determined a priori that 0.75 was the minimum acceptable ICC.
Objective 3: comparison of control and rotator cuff tear cohorts We conducted an a priori power analysis using inclination as the primary outcome variable. We performed a pilot study of 50 patients within the rotator cuff tear group who demonstrated a mean ± standard deviation inclination of 11° ± 6°. We assumed a nonnormal distribution and thus used a Mann-Whitney U test to compare groups. We assumed that a 2° difference in inclination could exist based on prior studies13,17,36,37,40,41 and a 1.5:1 ratio of study to control patients based on the expected difficulty of locating control individuals and the expected size of the rotator cuff tear group. With α set at 0.05, our power analysis demonstrated that 105 patients in the control group and 157 patients in the study group would be necessary to achieve a power of 80%. We first calculated descriptive statistics for both groups. We then determined whether age, inclination, and version were normally distributed using the KolmogorovSmirnov test. Mann-Whitney U tests and independent samples Student t test were then conducted as appropriate. P values of .05 were
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P.N. Chalmers et al. Table I
Characteristics of the control and rotator cuff tear groups
Group
Age, yr
Superior inclination, °
Retroversion, °
Control Rotator cuff tear P value
63 ± 8 (50-83) 61 ± 9 (31-81) .621
9 ± 5 (−4 to 23) 11 ± 6 (−1 to 31) <.001
8 ± 5 (−4 to 23) 9 ± 6 (−7 to 23) .141
The results are reported as mean ± standard deviation (range).
Table II
Characteristics of the rotator cuff tear group
Variable
Tear characteristic Tear width, cm Tear retraction, cm
Value 3 ± 1 (1-6) 2 ± 1 (1-6)
Tendons involved
Supraspinatus Infraspinatus Subscapularis Teres minor 1 2 3
86 38 13 4 55 37 8
Tendons, No.
Continuous data are displayed as mean ± standard deviation (range) and categoric data as percentage.
Table III Percentage of patients with each stage of Goutallier fatty infiltration for each muscle within the rotator cuff tear group Tendon
Supraspinatus Infraspinatus Subscapularis Teres minor
Fatty atrophy 0 (%)
1 (%)
2 (%)
3 (%)
4 (%)
25 68 83 94
42 11 7 5
14 8 4 0
11 9 4 1
7 4 2 1
considered significant. All analyses were conducted in Excel X (Microsoft, Redmond, WA, USA) and SPSS 23 software (IBM, Armonk, NY, USA).
Results The initial search of the medical record retrieved 1159 patients with a shoulder MRI within our system. Of these, we excluded 813 due to the presence of a rotator cuff tear or glenohumeral osteoarthritis, 229 for age younger than 50, and 10 for inadequate quality scans or less than 8 cm of scapular width available. Thus, the control cohort consisted of 107 patients (Table I) . The rotator cuff tear cohort initially consisted of 330 patients. Of these, we excluded 138 patients due to inadequate quality scans, less than 8 cm of scapular width available, or the concomitant presence of glenohumeral osteoarthritis. Thus, the rotator cuff tear cohort consisted of 192 patients. Tear characteristics are listed in Table II. Fatty infiltration characteristics of the tendons are listed in Table III.
Figure 2 Box-and-whisker plot displays the glenoid superior inclination for both groups. The top and bottom borders of the boxes represent the interquartile range, with the center line representing the median. The whiskers represent the furthest nonoutlier, nonextreme value. The outliers, those values between 1.5 and 3 box lengths from either end of the box, are denoted with circles. Extreme values, those values more than 3 lengths from either end of the box, are denoted with asterisks.
With regards to objective 1, accuracy of inclination measures in MRI, inclination was measured on the MRIs and CT scans of 37 patients in the arthroscopic labral repair group. The ICC was 0.877 (95% confidence interval, 0.775-0.935). The mean difference between measurements was 0° (range, −1° to 1°). With regards to objective 2, reliability of inclination measures in MRI, 2 authors measured inclination in 44 patients in the control group. The inter-rater ICC was 0.911 (95% confidence interval, 0.842-0.950). With regards to objective 3, superior inclination was 2° higher in the rotator cuff tear group than in the control group (range, 1°-4°, P < .001; Fig. 2). Visual inspection of the box plot demonstrates substantial overlap between groups. Differences between the groups were not significant for glenoid retroversion (P = .141; Table I , Fig. 3) or age (P = .621).
Discussion We confirmed that glenoid inclination can be accurately and reliably measured on MRI using CT as a gold standard. Although rotator cuff tears do demonstrate 2° statistically greater superior glenoid inclination than in age-matched controls, this difference may be below clinical significance. The latter finding suggests that superior glenoid inclination may only play a limited role in the etiology of rotator cuff tears.
ARTICLE IN PRESS Glenoid inclination and rotator cuff tears
Figure 3 Box-and-whisker plots display the glenoid retroversion for both groups. The top and bottom borders of the boxes represent the interquartile range, with the center line representing the median. The whiskers represent the furthest nonoutlier, nonextreme value. The outliers, those values between 1.5 and 3 box lengths from either end of the box, are denoted with circles. Extreme values, those values more than 3 lengths from either end of the box, are denoted with asterisks.
With regards to objectives 1 and 2, we demonstrated that glenoid inclination can be accurately measured using MRI with CT as a gold standard and can be reliably measured using MRI. On CT, inclination measurements corrected into the plane of the scapula have been shown to reliable and equivalent to gold standard automated 3-dimensional methods.9 However, measurements of glenoid inclination on CT images that are not corrected into the plane of the scapula9 and measurements of glenoid inclination on plain radiographs are not accurate.28 Based on our results, we suggest that future studies regarding the connection between glenoid inclination and rotator cuff tears use scapular plane–corrected MRI measurements. With regards to objective 3, patients with rotator cuff tears do demonstrate greater superior glenoid inclination than agematched controls without evidence of rotator cuff tears or glenohumeral osteoarthritis. In our study, the difference between groups was 2°. Although statistically significant, this difference is likely below clinical significance, and inspection of our box plot demonstrates substantial overlap between groups. Our study thus suggests that superior glenoid inclination plays a limited role in the etiology of rotator cuff tears. This result is somewhat in conflict with previous literature. Hughes et al23 found a mean difference in glenoid inclination of 8° between control and full-thickness rotator cuff tears, although they did not use age-matched controls and had a small patient cohort. The remainder of prior studies have examined CSA instead of glenoid inclination.11,23,36,38,40 CSA is a combined measure of glenoid inclination and acromial angle and inclination, and because of the method for CSA measurement, inclination and CSA are not directly numerically comparable. Furthermore, the CSA can only be reliably measured on a high-quality true anteroposterior radiograph because it is altered by scapular position.41 In this study, glenoid inclination was measured on
5 MRI images corrected into the plane of the scapula. Thus our inclination measurements are independent of scapular position, scapular tilt, or scapulothoracic positioning. Only 1 study to date has used strict radiographic inclusion criteria while measuring CSA: Chalmers et al11 found a CSA difference between control patients and rotator cuff tears of 2°. The similarity in findings between our study of glenoid inclination and this prior study of CSA with a completely different patient cohort suggests that scapular morphology may only play a very limited role in rotator cuff tears. Prior studies demonstrating no association between acromial index and rotator cuff tears21 provide further confirmation. These findings call into question interventions that seek to alter the scapular morphology in the treatment of rotator cuff tears.2,25,31 Finally, a difference of 2° is likely below measurement error in a clinical setting and is thus not useful clinically. Our study has several limitations. The use of CT as a gold standard could be considered a limitation; ideally, determination of accuracy would involve the direct comparison of MRI inclination measurements of 3-dimensional measurements. However, the CT measurements used have also been shown to be equivalent to gold standard automated 3-dimensional methods on CT.9 The control cohort was collected retrospectively based on MRI review. These patients could certainly have later sustained a rotator cuff tear, and this difference could reduce the magnitude of the difference between groups. In addition, each of these patients underwent a shoulder MRI. Although the indications for these MRIs varied, most of these patients had shoulder pain of unclear etiology, and abnormalities of scapular morphology may have contributed to the detected differences. However, the purpose of this study was to determine whether glenoid inclination associates with rotator cuff tears, and thus, this control cohort, which was confirmed on MRI to be free of rotator cuff tears, allows us to answer this question even if this cohort could not be considered as a “normal” cohort. In addition, although a matched case-control design could be ideal, we were not able to use this design because an insufficient number of shoulders free of rotator cuff tears or osteoarthritis were available to adequately power our study with this design. However, this limitation is mitigated because there were no differences in age between groups. Finally, the use of labral repair patients to determine the accuracy of MRI for inclination measurement could be considered a limitation because these patients may have anteroinferior osseous changes that could influence inclination measurements. However, if there are associated osseous changes, these changes would affect CT measurements more than MRI measurements and would thus reduce the accuracy of MRI instead of enhancing it. So this limitation is conservative. This limitation is further obviated by our finding that MRI and CT measurements were not significantly different in this population, and thus, this population can be used to determine the accuracy of MRI inclination measurement.
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P.N. Chalmers et al.
Conclusion 7.
Glenoid inclination can be accurately and reliably measured on MRI. Although superior glenoid inclination is statistically greater in those with rotator cuff tears than in patients of similar age without cuff tears or osteoarthritis, the difference is likely below clinical significance, and thus, superior glenoid inclination likely only plays limited role in the etiology of rotator cuff tears.
Acknowledgments
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10.
The authors thank Angela Presson, PhD, for her assistance with power analyses. 11.
Disclaimer Robert Tashjian is a paid consultant for Zimmer and Mitek; has stock in Conextions, INTRAFUSE, Genesis, and KATOR; receives intellectual property royalties from Imascap, Shoulder Innovations, and Zimmer; receives publishing royalties from Springer; and serves on the editorial board for the Journal of Orthopaedic Trauma, the American Journal of Orthopedics, the Journal of Shoulder and Elbow Arthroplasty and the Journal of the American Academy of Orthopaedic Surgeons. The other authors, their immediate families, and any research foundations with which they are affiliated have not received any financial payments or other benefits from any commercial entity related to the subject of this article.
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