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Radiographic findings associated with symptomatic rotator cuff tears
Radiographic findings associated with symptomatic rotator cuff tears Albert W. Pearsall, IV, MD,a Shawn Bonsell, MD,b R. J. Heitman, PhD,a Clyde A. Helms, MD,c Daryl Osbahr, BS,d and Kevin P. Speer, MD,d Mobile, AL, Dallas, TX, and Durham, NC
This study compared shoulder radiographs of patients with a documented rotator cuff tear with those of asymptomatic age-matched controls. Radiographs of 40 subjects with documented rotator cuff tears were evaluated along with similar films of 84 asymptomatic age-matched controls. Three radiographs were taken of each shoulder: (1) acromioclavicular joint view, (2) anterior-posterior view with 30° of external rotation, and (3) supraspinatus outlet view. Two fellowshiptrained radiologists interpreted 14 radiographic areas in a blinded fashion. Inspection of the greater tuberosity showed large positive abnormal ratings for sclerosis, osteophytes, subchondral cysts, and osteolysis. No association was noted between acromial morphology and rotator cuff tears. These results indicate that shoulder radiographs of subjects with a documented rotator cuff tear have greater tuberosity radiographic abnormalities that are not noted in asymptomatic subjects without a rotator cuff tear. No relationship was found between tear length and any of the degenerative conditions. (J Shoulder Elbow Surg 2003;12:122-7.)
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s our understanding of shoulder pathology has evolved, various studies have implied an association between radiographic changes and documented shoulder abnormalities.* In 1983, Neer24 described bony changes in stage III subacromial impingement in patients over 40 years of age. Bigliani and Rockwood3,22,23 documented similar findings with their descriptions of acromial morphology, as well as radiographic changes noted in patients with From the Department of Orthopaedics, University of South Alabama Medical Center, Mobile, AL,a Department of Orthopaedics and Sports Medicine, Baylor University Center of Dallas, Dallas, TX,b and Department of Radiology,c and Division of Orthopaedics,d Duke University Medical Center, Durham, NC. Reprint requests: Albert W. Pearsall, IV, MD, Department of Orthopaedic Surgery, Section of Sports Medicine and Shoulder Service, University of South Alabama Medical Center, 2451 Fillingim St, Mobile, AL 36617-2293. Copyright © 2003 by Journal of Shoulder and Elbow Surgery Board of Trustees. 1058-2746/2003/$35.00 ⫹ 0 doi:10.1067/mse.2003.19 *References 2, 3, 5, 7, 13, 14, 16, 18, 23, 24, 27, 33, 37, 38.
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rotator cuff tears. However, in several studies, the significance of observed radiographic abnormalities in the presence of shoulder conditions such as subacromial impingement, acromioclavicular joint degeneration, and rotator cuff pathology has been less clear.2,3,9,14,18,23,27,32,37 Several authors have described shoulder abnormalities specifically associated with rotator cuff pathology. In 1935, Keyes19 documented that 17% of 98 post-mortem subjects demonstrated a partial rupture of the supraspinatus tendon. He noted surface irregularities of the greater tuberosity and included a radiograph showing calcification of the supraspinatus tendon.19 In 1986, Morrison and Bigliani23 reported an increased incidence of hooked acromions in cadavers with rotator cuff tears. In 1988, Ozaki et al29 described radiographic abnormalities of the anterior acromion in cadavers with full-thickness rotator cuff tears. In a clinical study of patients with documented rotator cuff tears, Norwood et al27 reported incidences of 60% and 61% for subacromial spurring and acromioclavicular degeneration. Numerous studies have also reported a decreased acromiohumeral interval and degenerative greater tuberosity changes in patients with large rotator cuff tears.10,14,16,2729,38
Although various reports have associated acromial morphology with rotator cuff pathology, several cadaveric studies have disputed acromial morphology as being etiologic.28,29 Nicholson et al25 reported that acromial spurring was age-related. They further noted that acromial spurring was not related to acromial morphology and that spur formation was an independent factor contributing to impingement. Recently, Bonsell et al4 evaluated radiographically 84 asymptomatic individuals between the ages of 40 and 83 years who had never sought medical care for their shoulders. They found that acromial osteophytes, acromioclavicular degeneration, and lateral clavicular and acromial sclerosis were correlated with age. To date, no study has compared the radiographic findings of patients with a documented rotator cuff tear with age-matched asymptomatic controls. The purpose of this study was to compare 23 radiographic areas on three shoulder radiographs in 40
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Figure 1 A, Dedicated acromioclavicular (A-C) joint view radiograph. The 12 areas marked were assessed for abnormalities. B, Anteroposterior shoulder radiograph with 30° of humeral external rotation. The 6 areas labeled were assessed for abnormalities. C, Supraspinatus outlet view radiograph. The 5 radiographic criteria indicated were analyzed for differences between the rotator cuff tear and control groups.
patients with documented rotator cuff tears with those in 84 asymptomatic age-matched control subjects. MATERIALS AND METHODS Shoulder radiographs of 40 subjects with surgically proven rotator cuff tears between 1 and 6 cm in length were compared with similar shoulder radiographs of 84 asymptomatic age-matched controls. Individuals for the control group were solicited through a local advertisement requesting persons between the ages of 40 and 85 years to participate as paid volunteers in a research project for the Division of Orthopaedics. The Institutional Review Board approved the project before implementation. Study inclusion requirements stipulated that all control group subjects be asymptomatic in both shoulders with no history of an injury to either shoulder requiring physical therapy, a shoul-
der injection, or surgery. Screening included a detailed questionnaire regarding medical history, handedness, shoulder injury, shoulder pain, and functional limitations. Pregnancy and unwillingness to have radiographs taken were exclusions. Three similar radiographs of each shoulder were taken: a dedicated acromioclavicular joint view, an anterior-posterior view of the glenohumeral joint with 30° of humeral external rotation, and a supraspinatus outlet view. The entry criteria for the control group were met by 84 subjects, 32 men and 52 women, aged 40 to 83 years (mean age, 58 years). Two fellowship-trained bone radiologists interpreted the 504 radiographs. A standardized shoulder radiographic form listed 23 areas to be examined among the 3 radiographic views of each shoulder. These areas included 12 for the acromion and acromioclavicular joint, 5 for the clavicle, and 6 for the greater tuberosity of
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the humerus (Figure 1). Each area was graded on a point scale ranging from 0 to II: no changes (grade 0), mild changes (grade I), or advanced changes (grade II). Acromial shape was described by the classification of Bigliani et al3: type I (flat), type II (curved), and type III (hooked). Each radiologist read all sets of radiographs in a blinded fashion. Similar shoulder radiographs from over 100 patients diagnosed with subacromial impingement, acromioclavicular joint arthritis, or rotator cuff tear were intermixed with the subjects’ films as controls. Forty patients comprised the surgical group. Approximately 80 patients with surgically documented rotator cuff tears, equally divided among 4 age groups (40-49 years, 50-59 years, 60-69 years, and 70-79 years), were selected from the records of one surgeon. For each of these age groups, 10 patients were blindly selected to comprise the 40 patients in the surgical group. All patients had a fullthickness rotator cuff tear documented by magnetic resonance imaging and later confirmed at surgery. Conservative treatment, consisting of at least 6 weeks of rotator cuff rehabilitation and anti-inflammatory medications, failed in all patients. Thirty-four patients underwent an arthroscopic evaluation and an open procedure consisting of a subacromial decompression and rotator cuff repair. Six patients underwent an arthroscopic shoulder evaluation and an open subacromial decompression and debridement of the rotator cuff for a massive, irreparable tear. Rotator cuff tears ranged in size from 1 to 6 cm, with a mean of 3 cm (Table I). Of the 40 patients, ten were aged 40 to 49 years, ten were aged 50 to 59 years, ten were aged 60 to 69 years, and ten were aged 70 to 79 years. Preoperatively, each of the 40 patients with a rotator cuff tear had 3 radiographic views of the involved shoulder taken. These included a dedicated acromioclavicular joint view, an anterior-posterior view of the glenohumeral joint with 30° of humeral external rotation, and a supraspinatus outlet view. These views were similar to those used in the control group with regard to both size and orientation of each film (Figure 1). The same 2 radiologists interpreted all 120 surgical group radiographs. Each of the three shoulder views was examined for 23 areas with the use of the same standardized shoulder form developed for evaluation of the control group radiographs. Each radiologist read all sets of radiographs in a blinded fashion. Identical shoulder radiographs from over 100 patients diagnosed with subacromial impingement, acromioclavicular joint arthritis, or rotator cuff tear were intermixed with the subjects’ films as controls. On the basis of a previous study, 9 of the 23 areas examined were determined to have no abnormal ratings and were not included in the analysis.4 The remaining 14 radiologic areas were classified into 2 groups: normal (grade 0) or abnormal (grade I or II). All radiographs were graded with this classification scheme. Patients were designated as either having a rotator cuff tear (surgical group) or not (control group). In order to increase statistical power through increased sample size, gender was not considered as a separate variable, as a previous study demonstrated no significant difference between sexes.4 Significance testing with the Statistical Package for the Social Sciences (SPSS, Inc, Chicago, Ill) for the injury variable (tear vs no tear) across ratings was undertaken with use of the 2 test.
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Table I Patient age, rotator cuff size, and surgical procedure performed Patient No. Aged 1 2 3 4 5 6 7 8 9 10 Aged 11 12 13 14 15 16 17 18 19 20 Aged 21 22 23 24 25 26 27 28 29 30 Aged 31 32 33 34 35 36 37 38 39 40
Rotator cuff tear size (cm)
Procedure
40-49 y 3 2 4 2 1 1 1 3 1 2
Open Open Open Open Open Open Open Open Open Open
repair repair repair repair repair repair repair repair repair repair
2 3 1.5 2 1 6 2 1 3 2
Open Open Open Open Open Open Open Open Open Open
repair repair repair repair repair debridement repair repair repair repair
2 1.5 1 1 3 3 2 5 6 6
Open repair Open repair Open repair Open repair Open repair Open repair Open repair Arthroscopic debridement Open debridement Open repair
3 6 3 3 6 6 6 6 4 1
Open repair Open debridement Open repair Open repair Open debridement Arthroscopic debridement Open repair Open repair Open repair Open repair
50-59 y
60-69 y
70-79
A separate 2 ⫻ 2 contingency table was established for ratings of each of the 14 degenerative conditions by the injury variable to test the hypothesis of independence. Standardized residuals were used when significant 2 values were found to determine which cells of the contingency table caused departure from independence.26 The 2 values were considered significant at the .05 level.
RESULTS The injury-by-ratings contingency table for sclerosis, osteophytes, and cysts of the acromion and clavicle regions, as well as osteolysis of the greater tuber-
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osity region, showed no significant 2 values (P ⬎ .05; range, P ⫽ .610 to P ⫽ .230). For the greater tuberosity, significant Pearson 2 values were found for sclerosis [2 (1, N ⫽ 124) ⫽ 11.04, P ⫽ .001], osteophytes [2 (1, N ⫽ 124) ⫽ 10.57, P ⫽ .001], and subchondral cysts [2 (1, N ⫽ 124) ⫽ 10.40, P ⫽ .001]. Inspection of the standardized residuals showed large positive standardized residuals in the abnormal rating by injured cells for sclerosis (2.0), osteophytes (2.4), and subchondral cysts (2.2), causing rejection of the hypothesis of independence. These results indicate that shoulder radiographs of subjects with a documented rotator cuff tear have greater tuberosity sclerosis, osteophytes, and subchondral cysts that are not noted on shoulder radiographs of asymptomatic subjects without a documented rotator cuff tear. When acromial shape was analyzed in relation to a tear of the rotator cuff tear, no statistical relationship was noted (P ⬎ .05). In order to determine whether there was a significant difference associated with the size of the rotator cuff tear when normal ratings were compared with abnormal ratings, independent t tests were run for the 14 conditions with tear length used as the dependent variable and the rating (normal vs abnormal) used as the independent variable. No significant difference (P ⬎ .05; range, P ⫽ .904 to P ⫽ .201) for tear length was found between the normal and abnormal ratings for any of the 14 degenerative conditions rated in the dominant shoulder. DISCUSSION Radiographic findings reported in patients with a documented rotator cuff tear include a decreased acromiohumeral interval, a hooked acromion, and degenerative changes of the greater tuberosity and acromioclavicular joint.† Despite the presence of radiographic abnormalities in these patients, in many cases it is unclear whether such changes are related to a deficient rotator cuff or simply to age. Ahovuo et al1 evaluated the diagnostic accuracy of arthrography and plain radiographs in patients with surgically verified rotator cuff tears. They stated that plain radiographs were of no value in the diagnosis of rotator cuff pathology. Patients were not stratified by age or rotator cuff size in the study, which may have contributed to the lack of findings. Recently, in a blinded radiographic evaluation of asymptomatic individuals who had never injured or sought medical attention for their shoulders, Bonsell et al4 noted that acromial and clavicular sclerosis, inferior acromial and clavicular osteophytes, and acromioclavicular joint narrowing were associated with †References 2, 14, 16, 18, 23, 24, 27-29, 31, 37, 38.
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age. They cautioned that radiographic abnormalities associated with full-thickness rotator cuff disease must be differentiated from normal age-related changes. The 4 radiographic findings observed in conjunction with rotator cuff tears in the current study† greater tuberosity sclerosis, osteophytes, cysts, and osteolysis, are not surprising. Because most rotator cuff tears involve the supraspinatus tendon insertion into the greater tuberosity, this area would be suspicious for radiographic abnormalities. Other authors have also noted greater tuberosity changes associated with rotator cuff pathology.2,9,14,16,27,39 Wohlwend et al39 found that when the greater tuberosity was interpreted as irregular, 75% of shoulders had rotator cuff tears on sonographic examination. When the greater tuberosity was read as normal, only 4% of shoulders had evidence of a rotator cuff tear. Although our study is in agreement with the findings of Wohlwend et al, it is the first one to document radiographic changes in comparison to a control group of asymptomatic subjects. Other authors have noted no correlation between greater tuberosity changes and rotator cuff pathology. Huang et al17 evaluated 108 shoulders with radiography and magnetic resonance imaging. They found that cortical thickening and subcortical sclerosis were not seen more frequently in shoulders with rotator cuff disease than in normal shoulders. There were several weaknesses to the study. First, not all patients underwent confirmatory arthroscopic evaluation. For the subset of patients who did, magnetic resonance imaging was only 88% sensitive for identifying a full-thickness tear. They also grouped patients with partial-thickness and full-thickness tears together. In the current study, we found radiographic changes only for those patients with a documented full-thickness tear. Finally, interobserver agreement in the study of Huang et al was poor (0.06 to 0.41). Although, overall, no statistically significant association with greater tuberosity changes was noted in patients with rotator cuff disease, an association between cystlike lesions and shoulders with rotator cuff disease was noted by one observer (P ⬍ .05). Among the various studies that have evaluated radiographic abnormalities in patients with a fullthickness tear, only one used a control group for comparison. Norwood et al27 compared radiographs of patients with a documented rotator cuff tear with those in a group of patients with other pathologic conditions of the shoulder. Although they documented several radiographic abnormalities in the rotator cuff tear group, inconsistencies were present in the study. First, the patients in the control group had shoulder symptoms. Indeed, each patient sought medical attention for his shoulder and required an arthrogram to rule out a rotator cuff tear. Moreover, although no patient in the control group had a tear, each had
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some type of shoulder pathology. It is unclear whether patients in the control group represented a subgroup of the rotator cuff tear group that had not progressed to a complete tear. In contrast, the control group in the current study consisted of patients aged 40 to 83 years who had never had a symptom or sought medical attention for their shoulder.4 Second, Norwood et al27 did not document the size of their study subjects’ rotator cuff tears. Although the tear group was divided into single (group II) and multiple tendon tears (group III), no measurements were recorded. Several studies have shown radiographic abnormalities in patients with massive rotator cuff tears. Such findings include a decreased acromiohumeral interval and acromiohumeral abutment.11,12,14,16,38 It is difficult to know whether group III patients in the study of Norwood et al represented large repairable tears or massive irreparable injuries. The latter group would likely have more rapid and dramatic radiographic abnormalities.27 Third, the radiographic interpretation in the study of Norwood et al27 did not control for side-to-side differences within the same patient. Because right and left radiographic differences may have existed within the control subjects, comparisons between the tear and control groups are difficult to interpret. Finally, it is unclear from their study whether all patients had identical shoulder radiographs and whether the radiographs were interpreted by the same individual and in a blinded fashion. Each of these study inconsistencies undermines the validity of the authors’ conclusions.27 In designing this study, we attempted to eliminate many shortcomings that were present in the study by Norwood et al.27 First, control subjects were asymptomatic in both shoulders, had never injured either shoulder, and had never been treated for a shoulder problem. We believed that this group of asymptomatic individuals most closely represented patients with a low incidence of rotator cuff pathology. Although other authors have documented full-thickness rotator cuff tears in asymptomatic individuals, the reported incidence is low, ranging from 4% to 28% depending on the patient’s age.36 Although various authors have reported an association between acromial shape and tears of the rotator cuff, in the current study, no such relationship was noted.3,9,15,16,18,24,27-29,38 Our results are similar to those of others who have reported no association between acromial spurring and rotator cuff tears.5,6,15,20,21 In a cadaveric study of 306 rotator cuffs, Loehr and Uhthoff20 concluded that degenerative tears originate from intrinsic tendinopathy and are not due to anatomic variations of the acromion. Uhtoff and others confirmed their findings, noting that the hypovascular zone proximal to the insertion of the supraspinatus may have a more significant bearing
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on rotator cuff pathology than extrinsic acromial impingement.5-8,21,35 On the basis of these studies, we believe that intrinsic rotator cuff tendinopathy, rather than secondary acromial impingement, is the primary cause of a full-thickness rotator cuff tear in many patients. This explanation supports our findings that subacromial spurring was not associated with a fullthickness rotator cuff tear. It should be emphasized that the findings in this study pertain to moderate- to large-sized rotator cuff tears. Indeed, rotator cuff tears in our study averaged only 3 cm. More dramatic radiographic abnormalities such as a decreased acromiohumeral distance have been predominantly described in association with massive rotator cuff tears often greater than 5 to 6 cm.11,12,14,16,38 On the basis of the mean size of rotator cuff tears reported in our study, the radiographic abnormalities noted should not be interpreted as representing those associated with massive tears reported by other authors. In this study, radiographic acromioclavicular degeneration was not associated with a full-thickness rotator cuff tear. Previous authors have described clavicular osteophytes and acromioclavicular degeneration in association with rotator cuff pathology.31 However, it is unclear whether acromioclavicular abnormalities were causative or were an age-related incidental finding in the context of primary rotator cuff tendinopathy. Bonsell et al4 and others30,32 have noted acromioclavicular joint degeneration to be agerelated in an asymptomatic population. On the basis of our findings and the observations of others, we believe that radiographic acromioclavicular joint degeneration is not necessarily an indicator of a fullthickness rotator cuff tear. Before implementing this study, we documented radiographic shoulder changes that occur in an asymptomatic population stratified by age.4 We believed that it was essential to determine radiographic changes that occur with age in individuals without a history of shoulder injury. These radiographic findings served as the controls against which the findings in the rotator cuff group were compared. All study radiographs were taken in a uniform fashion by the same radiology technician to eliminate possible inconsistencies in their interpretation. In addition, all radiographs were read in a blinded fashion by two fellowship-trained bone radiologists. We believed that the consensus opinion of two radiologists would eliminate the potential bias of a single viewer. One shortfall of this study is that magnetic resonance imaging was not performed to rule out an asymptomatic rotator cuff tear in the control group. Sher et al36 demonstrated on magnetic resonance imaging that the incidence of full-thickness rotator cuff tears ranged from 4% to 28% in asymptomatic patients between the ages of 40 and 88 years. It should
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be noted that Quinn et al34 have reported magnetic resonance imaging accuracy of 85% for full-thickness rotator cuff tears confirmed at arthroscopy. Therefore, it is possible that Sher et al over-reported the actual number of patients with full-thickness tears. In addition, although any recent neck or shoulder symptoms or a past history of surgery comprised exclusion criteria in the study of Sher et al, they did not specify whether any patient had had a shoulder injury in the past. It is unclear whether patients in their study represented the natural history of rotator cuff pathogenesis or whether a previous rotator cuff injury precipitated the findings noted on magnetic resonance imaging. In the current study, however, it is possible that patients under-reported shoulder symptoms for financial remuneration, which may have led to an underestimation of rotator cuff pathology in our control group. In conclusion, in patients with a small- to moderatesized rotator cuff tear, acromial shape is not predictive of a full-thickness rotator cuff tear. Standard shoulder radiographs in these patients demonstrate greater tuberosity sclerosis, osteophytes, subchondral cysts, and osteolysis that are not noted in patients without shoulder symptoms. REFERENCES
1. Ahovuo J, Paavolainen P, Slatis P. The diagnostic value of arthrography and plain radiography in rotator cuff tears. Acta Orthop Scand 1984;55:220-3. 2. Bernageau J. Roentgenographic assessment of the rotator cuff. Clin Orthop 1990;254:87-91. 3. Bigliani L, Morrison D, April E. The morphology of the acromion and its relationship to rotator cuff tears. Orthop Trans 1986;10: 228. 4. Bonsell S, Pearsall A IV, Heitman R, et al. The relationship of age, gender, and degenerative changes observed on radiographs of the shoulder in asymptomatic individuals. J Bone Joint Surg Br 2000;82:1135-9. 5. Budoff J, Nirschl R, Guidi E. Debridement of partial-thickness tears of the rotator cuff without acromioplasty. Long-term follow-up and review of the literature. J Bone Joint Surg Am 1998;80:733-48. 6. Burkhart S. Arthroscopic debridement and decompression for selected rotator cuff tears. Clinical results, pathomechanics, and patient selection based on biomechanical parameters. Orthop Clin North Am 1993;24:111-23. 7. Burkhead W, Burkhart S, Gerber C, et al. Symposium: the rotator cuff: debridement versus repair-part I. Contemp Orthop 1995; 31:262-71. 8. Codman E. The shoulder. Rupture of the supraspinatus tendon and other lesions in or about the subacromial bursa. Boston: Privately printed; 1934. 9. Cohen R, Williams G Jr. Impingement syndrome and rotator cuff disease as repetitive motion disorders. Clin Orthop 1998;351: 95-101. 10. Cone R, Resnick D, Danzig L. Shoulder impingement syndrome: radiographic evaluation. Radiology 1984;150:29-33. 11. Cotton R, Rideout D. Tears of the humeral rotator cuff: a radiological and pathological necropsy survey. J Bone Joint Surg Br 1964;46:318-28. 12. DeSmet A, Ting Y. Diagnosis of rotator cuff tears on routine radiographs. J Can Assoc Radiol 1962;35:149. 13. Deutsch A, Altchek D, Schwartz E, Otis J, Warren R. Radiologic
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measurement of superior displacement of the humeral head in the impingement syndrome. J Shoulder Elbow Surg 1996;5:186-93. Ellman H, Hanker G, Bayer M. Repair of the rotator cuff. Endresult study of factors influencing reconstruction. J Bone Joint Surg Am 1986;68:1137-44. Getz J, Recht M, Piraino D, et al. Acromial morphology: relation to sex, age, symmetry, and subacromial enthesophytes. Radiology 1996;199:737-42. Hamada K, Fukuda H, Mikasa M, Kobayashi Y. Roentgenographic findings in massive rotator cuff tears. Clin Orthop 1990; 254:92-6. Huang L, Rubin D, Britton C. Greater tuberosity changes as revealed by radiography: lack of clinical usefulness in patients with rotator cuff disease. AJR Am J Roentgenol 1999;172:1381-8. Iannotti J. Full-thickness rotator cuff tears: factors affecting surgical outcome. J Am Acad Orthop Surg 1994;2:87-95. Keyes E. Anatomical observation on senile changes in the shoulder. J Bone Joint Surg Am 1935;17:953-60. Loehr J, Uhthoff H. The pathogenesis of degenerative rotator cuff tears. Orthop Trans 1987;11:237. Loehr J, Uhthoff H. The microvascular pattern of the supraspinatus tendon. Clin Orthop 1990;254:35-8. Matsen F, Arntz C. In: Rockwood C, Matsen F, editors. Rotator cuff tendon failure, 2. Philadelphia: Saunders; 1990. p. 656. Morrison D, Bigliani L. The clinical significance in acromion morphology. Orthop Trans 1986;10:234. Neer C II. Impingement lesions. Clin Orthop 1983;173:70-7. Nicholson G, Goodman D, Flatow E, Bigliani L. The acromion: morphologic condition and age-related changes. A study of 420 scapulas. J Shoulder Elbow Surg 1996;5:1-11. Norusis M editor. SPSS 7.5 guide to data analysis. Upper Saddle River (NJ): Prentice Hall; 1997. Norwood L, Barrack R, Jacobson K. Clinical presentation of complete tears of the rotator cuff. J Bone Joint Surg Am 1989;71:500-5. Ogata S, Uhthoff H. Acromial enthesopathy and rotator cuff tear: a radiologic and histologic postmortem investigation of the coracoacromial arch. Clin Orthop 1990;254:39-48. Ozaki J, Fujimoto S, Nakagawa S, Masuhara K, Tamai S. Tears of the rotator cuff of the shoulder associated with pathological changes in the acromion: a study in cadavera. J Bone Joint Surg Am 1988;70:1224-30. Petersson C. Degeneration of the acromioclavicular joint. Acta Orthop Scand 1983;54:434-8. Petersson C, Gentz C. Ruptures of the supraspinatus tendon: the significance of distally pointing acromioclavicular osteophytes. Clin Orthop 1983;174:143-8. Petersson C, Redlund-Johnell I. Radiographic joint space in normal acromioclavicular joints. Acta Orthop Scand 1983;54: 431-3. Post M, Silver R, Singh M. Rotator cuff tear: diagnosis and treatment. Clin Orthop 1983;173:78-91. Quinn S, Sheley R, Demlow T, Szumowski J. Rotator cuff tendon tears: evaluation with fat-suppressed MR imaging with arthroscopic correlation in 100 patients. Radiology 1995;195:497500. Rothman R, Parke W. The vascular anatomy of the rotator cuff. Clin Orthop 1965;41:176-86. Sher J, Uribe J, Posada A, Murphy B, Zlatkin M. Abnormal findings on magnetic resonance images of asymptomatic shoulders. J Bone Joint Surg Am 1995;77:10-4. Tuite M, Toivonen D, Orwin J, Wright D. Acromion angle on radiographs of the shoulder: correlation with the impingement syndrome and rotator cuff tears. Am J Radiol 1995;165:609-13. Weiner D, McNab I. Superior migration of the humeral head. A radiological aid in the diagnosis of tears of the rotator cuff. J Bone Joint Surg Br 1970;52:524-7. Wohlwend J, van Holsbeeck M, Craig J, et al. The association between irregular greater tuberosities and rotator cuff tears: a sonographic study. AJR Am J Roentgenol 1998;171:229-33.
This study compared shoulder radiographs of patients with a documented rotator cuff tear with those of asymptomatic age-matched controls. Radiographs of 40 subjects with documented rotator cuff tears were evaluated along with similar films of 84 asymptomatic age-matched controls. Three radiographs were taken of each shoulder: (1) acromioclavicular joint view, (2) anterior-posterior view with 30° of external rotation, and (3) supraspinatus outlet view. Two fellowshiptrained radiologists interpreted 14 radiographic areas in a blinded fashion. Inspection of the greater tuberosity showed large positive abnormal ratings for sclerosis, osteophytes, subchondral cysts, and osteolysis. No association was noted between acromial morphology and rotator cuff tears. These results indicate that shoulder radiographs of subjects with a documented rotator cuff tear have greater tuberosity radiographic abnormalities that are not noted in asymptomatic subjects without a rotator cuff tear. No relationship was found between tear length and any of the degenerative conditions. (J Shoulder Elbow Surg 2003;12:122-7.)
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s our understanding of shoulder pathology has evolved, various studies have implied an association between radiographic changes and documented shoulder abnormalities.* In 1983, Neer24 described bony changes in stage III subacromial impingement in patients over 40 years of age. Bigliani and Rockwood3,22,23 documented similar findings with their descriptions of acromial morphology, as well as radiographic changes noted in patients with From the Department of Orthopaedics, University of South Alabama Medical Center, Mobile, AL,a Department of Orthopaedics and Sports Medicine, Baylor University Center of Dallas, Dallas, TX,b and Department of Radiology,c and Division of Orthopaedics,d Duke University Medical Center, Durham, NC. Reprint requests: Albert W. Pearsall, IV, MD, Department of Orthopaedic Surgery, Section of Sports Medicine and Shoulder Service, University of South Alabama Medical Center, 2451 Fillingim St, Mobile, AL 36617-2293. Copyright © 2003 by Journal of Shoulder and Elbow Surgery Board of Trustees. 1058-2746/2003/$35.00 ⫹ 0 doi:10.1067/mse.2003.19 *References 2, 3, 5, 7, 13, 14, 16, 18, 23, 24, 27, 33, 37, 38.
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rotator cuff tears. However, in several studies, the significance of observed radiographic abnormalities in the presence of shoulder conditions such as subacromial impingement, acromioclavicular joint degeneration, and rotator cuff pathology has been less clear.2,3,9,14,18,23,27,32,37 Several authors have described shoulder abnormalities specifically associated with rotator cuff pathology. In 1935, Keyes19 documented that 17% of 98 post-mortem subjects demonstrated a partial rupture of the supraspinatus tendon. He noted surface irregularities of the greater tuberosity and included a radiograph showing calcification of the supraspinatus tendon.19 In 1986, Morrison and Bigliani23 reported an increased incidence of hooked acromions in cadavers with rotator cuff tears. In 1988, Ozaki et al29 described radiographic abnormalities of the anterior acromion in cadavers with full-thickness rotator cuff tears. In a clinical study of patients with documented rotator cuff tears, Norwood et al27 reported incidences of 60% and 61% for subacromial spurring and acromioclavicular degeneration. Numerous studies have also reported a decreased acromiohumeral interval and degenerative greater tuberosity changes in patients with large rotator cuff tears.10,14,16,2729,38
Although various reports have associated acromial morphology with rotator cuff pathology, several cadaveric studies have disputed acromial morphology as being etiologic.28,29 Nicholson et al25 reported that acromial spurring was age-related. They further noted that acromial spurring was not related to acromial morphology and that spur formation was an independent factor contributing to impingement. Recently, Bonsell et al4 evaluated radiographically 84 asymptomatic individuals between the ages of 40 and 83 years who had never sought medical care for their shoulders. They found that acromial osteophytes, acromioclavicular degeneration, and lateral clavicular and acromial sclerosis were correlated with age. To date, no study has compared the radiographic findings of patients with a documented rotator cuff tear with age-matched asymptomatic controls. The purpose of this study was to compare 23 radiographic areas on three shoulder radiographs in 40
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Figure 1 A, Dedicated acromioclavicular (A-C) joint view radiograph. The 12 areas marked were assessed for abnormalities. B, Anteroposterior shoulder radiograph with 30° of humeral external rotation. The 6 areas labeled were assessed for abnormalities. C, Supraspinatus outlet view radiograph. The 5 radiographic criteria indicated were analyzed for differences between the rotator cuff tear and control groups.
patients with documented rotator cuff tears with those in 84 asymptomatic age-matched control subjects. MATERIALS AND METHODS Shoulder radiographs of 40 subjects with surgically proven rotator cuff tears between 1 and 6 cm in length were compared with similar shoulder radiographs of 84 asymptomatic age-matched controls. Individuals for the control group were solicited through a local advertisement requesting persons between the ages of 40 and 85 years to participate as paid volunteers in a research project for the Division of Orthopaedics. The Institutional Review Board approved the project before implementation. Study inclusion requirements stipulated that all control group subjects be asymptomatic in both shoulders with no history of an injury to either shoulder requiring physical therapy, a shoul-
der injection, or surgery. Screening included a detailed questionnaire regarding medical history, handedness, shoulder injury, shoulder pain, and functional limitations. Pregnancy and unwillingness to have radiographs taken were exclusions. Three similar radiographs of each shoulder were taken: a dedicated acromioclavicular joint view, an anterior-posterior view of the glenohumeral joint with 30° of humeral external rotation, and a supraspinatus outlet view. The entry criteria for the control group were met by 84 subjects, 32 men and 52 women, aged 40 to 83 years (mean age, 58 years). Two fellowship-trained bone radiologists interpreted the 504 radiographs. A standardized shoulder radiographic form listed 23 areas to be examined among the 3 radiographic views of each shoulder. These areas included 12 for the acromion and acromioclavicular joint, 5 for the clavicle, and 6 for the greater tuberosity of
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the humerus (Figure 1). Each area was graded on a point scale ranging from 0 to II: no changes (grade 0), mild changes (grade I), or advanced changes (grade II). Acromial shape was described by the classification of Bigliani et al3: type I (flat), type II (curved), and type III (hooked). Each radiologist read all sets of radiographs in a blinded fashion. Similar shoulder radiographs from over 100 patients diagnosed with subacromial impingement, acromioclavicular joint arthritis, or rotator cuff tear were intermixed with the subjects’ films as controls. Forty patients comprised the surgical group. Approximately 80 patients with surgically documented rotator cuff tears, equally divided among 4 age groups (40-49 years, 50-59 years, 60-69 years, and 70-79 years), were selected from the records of one surgeon. For each of these age groups, 10 patients were blindly selected to comprise the 40 patients in the surgical group. All patients had a fullthickness rotator cuff tear documented by magnetic resonance imaging and later confirmed at surgery. Conservative treatment, consisting of at least 6 weeks of rotator cuff rehabilitation and anti-inflammatory medications, failed in all patients. Thirty-four patients underwent an arthroscopic evaluation and an open procedure consisting of a subacromial decompression and rotator cuff repair. Six patients underwent an arthroscopic shoulder evaluation and an open subacromial decompression and debridement of the rotator cuff for a massive, irreparable tear. Rotator cuff tears ranged in size from 1 to 6 cm, with a mean of 3 cm (Table I). Of the 40 patients, ten were aged 40 to 49 years, ten were aged 50 to 59 years, ten were aged 60 to 69 years, and ten were aged 70 to 79 years. Preoperatively, each of the 40 patients with a rotator cuff tear had 3 radiographic views of the involved shoulder taken. These included a dedicated acromioclavicular joint view, an anterior-posterior view of the glenohumeral joint with 30° of humeral external rotation, and a supraspinatus outlet view. These views were similar to those used in the control group with regard to both size and orientation of each film (Figure 1). The same 2 radiologists interpreted all 120 surgical group radiographs. Each of the three shoulder views was examined for 23 areas with the use of the same standardized shoulder form developed for evaluation of the control group radiographs. Each radiologist read all sets of radiographs in a blinded fashion. Identical shoulder radiographs from over 100 patients diagnosed with subacromial impingement, acromioclavicular joint arthritis, or rotator cuff tear were intermixed with the subjects’ films as controls. On the basis of a previous study, 9 of the 23 areas examined were determined to have no abnormal ratings and were not included in the analysis.4 The remaining 14 radiologic areas were classified into 2 groups: normal (grade 0) or abnormal (grade I or II). All radiographs were graded with this classification scheme. Patients were designated as either having a rotator cuff tear (surgical group) or not (control group). In order to increase statistical power through increased sample size, gender was not considered as a separate variable, as a previous study demonstrated no significant difference between sexes.4 Significance testing with the Statistical Package for the Social Sciences (SPSS, Inc, Chicago, Ill) for the injury variable (tear vs no tear) across ratings was undertaken with use of the 2 test.
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Table I Patient age, rotator cuff size, and surgical procedure performed Patient No. Aged 1 2 3 4 5 6 7 8 9 10 Aged 11 12 13 14 15 16 17 18 19 20 Aged 21 22 23 24 25 26 27 28 29 30 Aged 31 32 33 34 35 36 37 38 39 40
Rotator cuff tear size (cm)
Procedure
40-49 y 3 2 4 2 1 1 1 3 1 2
Open Open Open Open Open Open Open Open Open Open
repair repair repair repair repair repair repair repair repair repair
2 3 1.5 2 1 6 2 1 3 2
Open Open Open Open Open Open Open Open Open Open
repair repair repair repair repair debridement repair repair repair repair
2 1.5 1 1 3 3 2 5 6 6
Open repair Open repair Open repair Open repair Open repair Open repair Open repair Arthroscopic debridement Open debridement Open repair
3 6 3 3 6 6 6 6 4 1
Open repair Open debridement Open repair Open repair Open debridement Arthroscopic debridement Open repair Open repair Open repair Open repair
50-59 y
60-69 y
70-79
A separate 2 ⫻ 2 contingency table was established for ratings of each of the 14 degenerative conditions by the injury variable to test the hypothesis of independence. Standardized residuals were used when significant 2 values were found to determine which cells of the contingency table caused departure from independence.26 The 2 values were considered significant at the .05 level.
RESULTS The injury-by-ratings contingency table for sclerosis, osteophytes, and cysts of the acromion and clavicle regions, as well as osteolysis of the greater tuber-
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osity region, showed no significant 2 values (P ⬎ .05; range, P ⫽ .610 to P ⫽ .230). For the greater tuberosity, significant Pearson 2 values were found for sclerosis [2 (1, N ⫽ 124) ⫽ 11.04, P ⫽ .001], osteophytes [2 (1, N ⫽ 124) ⫽ 10.57, P ⫽ .001], and subchondral cysts [2 (1, N ⫽ 124) ⫽ 10.40, P ⫽ .001]. Inspection of the standardized residuals showed large positive standardized residuals in the abnormal rating by injured cells for sclerosis (2.0), osteophytes (2.4), and subchondral cysts (2.2), causing rejection of the hypothesis of independence. These results indicate that shoulder radiographs of subjects with a documented rotator cuff tear have greater tuberosity sclerosis, osteophytes, and subchondral cysts that are not noted on shoulder radiographs of asymptomatic subjects without a documented rotator cuff tear. When acromial shape was analyzed in relation to a tear of the rotator cuff tear, no statistical relationship was noted (P ⬎ .05). In order to determine whether there was a significant difference associated with the size of the rotator cuff tear when normal ratings were compared with abnormal ratings, independent t tests were run for the 14 conditions with tear length used as the dependent variable and the rating (normal vs abnormal) used as the independent variable. No significant difference (P ⬎ .05; range, P ⫽ .904 to P ⫽ .201) for tear length was found between the normal and abnormal ratings for any of the 14 degenerative conditions rated in the dominant shoulder. DISCUSSION Radiographic findings reported in patients with a documented rotator cuff tear include a decreased acromiohumeral interval, a hooked acromion, and degenerative changes of the greater tuberosity and acromioclavicular joint.† Despite the presence of radiographic abnormalities in these patients, in many cases it is unclear whether such changes are related to a deficient rotator cuff or simply to age. Ahovuo et al1 evaluated the diagnostic accuracy of arthrography and plain radiographs in patients with surgically verified rotator cuff tears. They stated that plain radiographs were of no value in the diagnosis of rotator cuff pathology. Patients were not stratified by age or rotator cuff size in the study, which may have contributed to the lack of findings. Recently, in a blinded radiographic evaluation of asymptomatic individuals who had never injured or sought medical attention for their shoulders, Bonsell et al4 noted that acromial and clavicular sclerosis, inferior acromial and clavicular osteophytes, and acromioclavicular joint narrowing were associated with †References 2, 14, 16, 18, 23, 24, 27-29, 31, 37, 38.
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age. They cautioned that radiographic abnormalities associated with full-thickness rotator cuff disease must be differentiated from normal age-related changes. The 4 radiographic findings observed in conjunction with rotator cuff tears in the current study† greater tuberosity sclerosis, osteophytes, cysts, and osteolysis, are not surprising. Because most rotator cuff tears involve the supraspinatus tendon insertion into the greater tuberosity, this area would be suspicious for radiographic abnormalities. Other authors have also noted greater tuberosity changes associated with rotator cuff pathology.2,9,14,16,27,39 Wohlwend et al39 found that when the greater tuberosity was interpreted as irregular, 75% of shoulders had rotator cuff tears on sonographic examination. When the greater tuberosity was read as normal, only 4% of shoulders had evidence of a rotator cuff tear. Although our study is in agreement with the findings of Wohlwend et al, it is the first one to document radiographic changes in comparison to a control group of asymptomatic subjects. Other authors have noted no correlation between greater tuberosity changes and rotator cuff pathology. Huang et al17 evaluated 108 shoulders with radiography and magnetic resonance imaging. They found that cortical thickening and subcortical sclerosis were not seen more frequently in shoulders with rotator cuff disease than in normal shoulders. There were several weaknesses to the study. First, not all patients underwent confirmatory arthroscopic evaluation. For the subset of patients who did, magnetic resonance imaging was only 88% sensitive for identifying a full-thickness tear. They also grouped patients with partial-thickness and full-thickness tears together. In the current study, we found radiographic changes only for those patients with a documented full-thickness tear. Finally, interobserver agreement in the study of Huang et al was poor (0.06 to 0.41). Although, overall, no statistically significant association with greater tuberosity changes was noted in patients with rotator cuff disease, an association between cystlike lesions and shoulders with rotator cuff disease was noted by one observer (P ⬍ .05). Among the various studies that have evaluated radiographic abnormalities in patients with a fullthickness tear, only one used a control group for comparison. Norwood et al27 compared radiographs of patients with a documented rotator cuff tear with those in a group of patients with other pathologic conditions of the shoulder. Although they documented several radiographic abnormalities in the rotator cuff tear group, inconsistencies were present in the study. First, the patients in the control group had shoulder symptoms. Indeed, each patient sought medical attention for his shoulder and required an arthrogram to rule out a rotator cuff tear. Moreover, although no patient in the control group had a tear, each had
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some type of shoulder pathology. It is unclear whether patients in the control group represented a subgroup of the rotator cuff tear group that had not progressed to a complete tear. In contrast, the control group in the current study consisted of patients aged 40 to 83 years who had never had a symptom or sought medical attention for their shoulder.4 Second, Norwood et al27 did not document the size of their study subjects’ rotator cuff tears. Although the tear group was divided into single (group II) and multiple tendon tears (group III), no measurements were recorded. Several studies have shown radiographic abnormalities in patients with massive rotator cuff tears. Such findings include a decreased acromiohumeral interval and acromiohumeral abutment.11,12,14,16,38 It is difficult to know whether group III patients in the study of Norwood et al represented large repairable tears or massive irreparable injuries. The latter group would likely have more rapid and dramatic radiographic abnormalities.27 Third, the radiographic interpretation in the study of Norwood et al27 did not control for side-to-side differences within the same patient. Because right and left radiographic differences may have existed within the control subjects, comparisons between the tear and control groups are difficult to interpret. Finally, it is unclear from their study whether all patients had identical shoulder radiographs and whether the radiographs were interpreted by the same individual and in a blinded fashion. Each of these study inconsistencies undermines the validity of the authors’ conclusions.27 In designing this study, we attempted to eliminate many shortcomings that were present in the study by Norwood et al.27 First, control subjects were asymptomatic in both shoulders, had never injured either shoulder, and had never been treated for a shoulder problem. We believed that this group of asymptomatic individuals most closely represented patients with a low incidence of rotator cuff pathology. Although other authors have documented full-thickness rotator cuff tears in asymptomatic individuals, the reported incidence is low, ranging from 4% to 28% depending on the patient’s age.36 Although various authors have reported an association between acromial shape and tears of the rotator cuff, in the current study, no such relationship was noted.3,9,15,16,18,24,27-29,38 Our results are similar to those of others who have reported no association between acromial spurring and rotator cuff tears.5,6,15,20,21 In a cadaveric study of 306 rotator cuffs, Loehr and Uhthoff20 concluded that degenerative tears originate from intrinsic tendinopathy and are not due to anatomic variations of the acromion. Uhtoff and others confirmed their findings, noting that the hypovascular zone proximal to the insertion of the supraspinatus may have a more significant bearing
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on rotator cuff pathology than extrinsic acromial impingement.5-8,21,35 On the basis of these studies, we believe that intrinsic rotator cuff tendinopathy, rather than secondary acromial impingement, is the primary cause of a full-thickness rotator cuff tear in many patients. This explanation supports our findings that subacromial spurring was not associated with a fullthickness rotator cuff tear. It should be emphasized that the findings in this study pertain to moderate- to large-sized rotator cuff tears. Indeed, rotator cuff tears in our study averaged only 3 cm. More dramatic radiographic abnormalities such as a decreased acromiohumeral distance have been predominantly described in association with massive rotator cuff tears often greater than 5 to 6 cm.11,12,14,16,38 On the basis of the mean size of rotator cuff tears reported in our study, the radiographic abnormalities noted should not be interpreted as representing those associated with massive tears reported by other authors. In this study, radiographic acromioclavicular degeneration was not associated with a full-thickness rotator cuff tear. Previous authors have described clavicular osteophytes and acromioclavicular degeneration in association with rotator cuff pathology.31 However, it is unclear whether acromioclavicular abnormalities were causative or were an age-related incidental finding in the context of primary rotator cuff tendinopathy. Bonsell et al4 and others30,32 have noted acromioclavicular joint degeneration to be agerelated in an asymptomatic population. On the basis of our findings and the observations of others, we believe that radiographic acromioclavicular joint degeneration is not necessarily an indicator of a fullthickness rotator cuff tear. Before implementing this study, we documented radiographic shoulder changes that occur in an asymptomatic population stratified by age.4 We believed that it was essential to determine radiographic changes that occur with age in individuals without a history of shoulder injury. These radiographic findings served as the controls against which the findings in the rotator cuff group were compared. All study radiographs were taken in a uniform fashion by the same radiology technician to eliminate possible inconsistencies in their interpretation. In addition, all radiographs were read in a blinded fashion by two fellowship-trained bone radiologists. We believed that the consensus opinion of two radiologists would eliminate the potential bias of a single viewer. One shortfall of this study is that magnetic resonance imaging was not performed to rule out an asymptomatic rotator cuff tear in the control group. Sher et al36 demonstrated on magnetic resonance imaging that the incidence of full-thickness rotator cuff tears ranged from 4% to 28% in asymptomatic patients between the ages of 40 and 88 years. It should
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be noted that Quinn et al34 have reported magnetic resonance imaging accuracy of 85% for full-thickness rotator cuff tears confirmed at arthroscopy. Therefore, it is possible that Sher et al over-reported the actual number of patients with full-thickness tears. In addition, although any recent neck or shoulder symptoms or a past history of surgery comprised exclusion criteria in the study of Sher et al, they did not specify whether any patient had had a shoulder injury in the past. It is unclear whether patients in their study represented the natural history of rotator cuff pathogenesis or whether a previous rotator cuff injury precipitated the findings noted on magnetic resonance imaging. In the current study, however, it is possible that patients under-reported shoulder symptoms for financial remuneration, which may have led to an underestimation of rotator cuff pathology in our control group. In conclusion, in patients with a small- to moderatesized rotator cuff tear, acromial shape is not predictive of a full-thickness rotator cuff tear. Standard shoulder radiographs in these patients demonstrate greater tuberosity sclerosis, osteophytes, subchondral cysts, and osteolysis that are not noted in patients without shoulder symptoms. REFERENCES
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