Original Article Acta Radiologica 2019, Vol. 60(5) 608–614 ! The Foundation Acta Radiologica The relationship between rotator cuff tear 2018 Article reuse guidelines: and four acromion types: cross-sectional sagepub.com/journals-permissions DOI: 10.1177/0284185118791211 study based on shoulder magnetic journals.sagepub.com/home/acr resonance imaging in 227 patients

Jong Moon Kim1,2, Yong Wook Kim1, Hyoung Seop Kim3 , Sang Chul Lee1, Yong Min Chun4, Seung Ho Joo5 and Hyun Sun Lim6

Abstract Background: Rotator cuff tear (RCT) has been believed to be related to specific types of the acromion. However, most of the studies were performed on a small number of patients with surgical findings not considering the severity of RCT. Purpose: To analyze the relationship between age, gender, the side of the shoulder, the acromion type, and the severity of RCT using shoulder magnetic resonance arthrography (MRA). Material and Methods: A total of 277 shoulder MRA findings were analyzed by a radiologist specializing in the musculoskeletal system. The relationship between variables (age, gender, side of the shoulder, and acromion type) and the injury of the supraspinatus (no rupture, partial rupture, full rupture, complete rupture) was confirmed. The partial tear of the supraspinatus tendon was divided into bursal and articular side tear in order to investigate the damage caused by the anatomical difference of the acromion. We also confirmed the differences between single supraspinatus injury and multiple RCTs. Results: The severity of supraspinatus tear and multiple RCTs were statistically significant with the old age and the right side of the shoulder, but not with a specific acromion type. In supraspinatus partial tear, there was no statistical difference between bursal and articular side tears. Conclusion: Our study revealed that the age at which degeneration could occur also was associated with multiple RCTs and is considered to be the most important factor in RCT, not anatomical structures such as acromion type.

Keywords Acromion, rotator cuff, supraspinatus, shoulder impingement syndrome

Date received: 10 July 2017; accepted: 17 June 2018

1Department and Research Institute of Rehabilitation Medicine, Yonsei University College of Medicine, Seoul, Republic of Korea Introduction 2Department of Rehabilitation Medicine, CHA Bundang Medical Center, CHA University, Seoul, Republic of Korea Rotator cuff tear (RCT) is one of the most common 3Department of Physical Medicine and Rehabilitation, National Health causes of shoulder pain found in the middle-aged popu- Insurance Service Ilsan Hospital, Seoul, Republic of Korea lation (1). However, the etiology and pathogenesis of 4Department of Orthopedic Surgery, Yonsei University College of RCT have not been clearly elucidated and are fre- Medicine, Seoul, Republic of Korea 5Department of Radiology, National Health Insurance Service Ilsan quently debated topics (2). Neer first mentioned the Hospital, Seoul, Republic of Korea term ‘‘shoulder impingement syndrome’’ in 1972, sug- 6Department of Policy Research Affairs, National Health Insurance gesting enthesophytes protruding into the subacromial Service Ilsan Hospital, Seoul, Republic of Korea space is the cause of subacromial impingement and RCT (3). Bigliani et al. classified the shape of the acro- Corresponding author: Hyoung Seop Kim, Department of Physical Medicine and Rehabilitation, mion into three types: type I (flat), type II (curved), and National Health Insurance Ilsan Hospital, 100 Ilsan-roilsan-donggu, type III (hooked). In addition, they popularized the Goyang 10444, Republic of Korea. theory of extrinsic subacromial impingement and Email: [email protected] Kim et al. 609 suggested that type III is relatively rare in asymptom- classified into four types previously described by atic individuals. Lastly, they noted that the occurrence Bigliani and Gagey (4,5). A type I acromion had an of RCT is associated with type III acromion and con- acromial angle of 0–12; a type II, 13–27; a type siderable subsequent studies have confirmed this correl- Ill, > 27; and a type IV, < 0 (Fig. 2) (8,9). The acro- ation (4). Later, Gagey et al. added type IV, a convex mial angle is the sharp bend of acromion where the inferior surface, to the acromial type classification (5). lateral border becomes continuous with the spine of These studies have been the theoretical background for the scapula. acromioplasty. The degree of supraspinatus injury was categorized According to the data of the American Board of into no tear, partial tear, full thickness tear, and com- Orthopedic Surgeons and the ambulatory surgical data- plete rupture (Fig. 3). In T2-weighted (T2W) coronal base of the New York statewide planning and research scan with fat suppression, the radiologist graded cooperative system, acromioplasty has been rapidly normal if there was no abnormality, partial tear if a increasing since the early 2000s (6). high signal line was seen at the articular or bursal However, recently it has been reported that releasing side, full thickness tear if there was a high signal cleft the coracoacromial ligament and removing the suba- through the entire thickness of the tendon with contrast cromial bursa without acromioplasty have shown no media being present in the subacromial bursa and the difference in prognosis with acromioplasty (7). shoulder joint while the continuity of tendon still was Although there have been many studies on the RCTs maintained, and complete rupture if the continuity of according to acromion type, there have been no large- tendon was disrupted. Multiple RCTs were defined as scale studies using magnetic resonance imaging (MRI) subscapularis or infraspinatus tear combined with to confirm the tears. Most studies confirmed only the supraspinatus injury over the partial tear. existence of complete tear using arthroscopy. If the acromion type indeed determines the occur- We aimed to suggest a possible pathophysiology of rence of supraspinatus tendon injury, partial tears RCT by analyzing the relationship of age, gender, the should be dominant on the articular side. To verify side of the shoulder, and the four types of acromion this hypothesis, we subdivided partial tears into the compared with the severity of supraspinatus tear and articular side and bursa side. Articular-sided partial multiple RCTs in MRI findings. tear was defined as a disruption of the smooth under- surface of the tendon, with the accumulation of the Material and Methods contrast medium within a part of the tendon. Bursal sided partial tear was defined as a disruption of the The study was conducted in accordance with the smooth upper surface of the tendon on T2W images Helsinki Declaration and was approved by the institu- obtained at MRA. tional review board (NHIMC 2014-10-008-001). The One-way ANOVA was used to compare age to the Institutional Review Board approved this study severity of supraspinatus tear, bursal/articular partial before its implementation. Between January 2013 and tear, and multiple RCTs. Pearson’s Chi-squared test December 2013, 233 individuals with shoulder pain or a was used to determine the significance between the painful arc which implied shoulder impingement syn- severity of supraspinatus tear and gender, the side of drome underwent a magnetic resonance arthography the shoulder, and acromion type. Ordinal and binary (MRA) scan. All MR images were interpreted by one logistic regression was used to correct confounding fac- resident of radiology and one radiologist who was tors and to compare supraspinatus tear and multiple experienced in musculoskeletal radiology for five RCTs with related factors (age, gender, the side of years and blinded to patients’ clinical information the shoulder, and acromion type). Statistical analyses To verify Neer’s theory that supraspinatus tear occurs were performed with SPSS for Windows (Korean due to repetitive impingement, the inclusion criteria were version 21.0) statistical package (SPSS Inc, Chicago, as follows: (i) clinical diagnosis of impingement syn- IL, USA). drome; and (ii) patients who had undergone MRA. Exclusion criteria included: (i) shoulder pain due to Results trauma; (ii) previous shoulder surgery; (iii) shoulder joint arthritis; (iv) inflammatory arthritis; and (v) con- Variables of the patients, which include age, gender, genital acromion deformity. Two patients with shoulder side of the shoulder, and acromion type in correlation pain due to trauma, one patient with previous surgery, with the severity of supraspinatus tear, are shown in and three patients with rheumatoid arthritis were Table 1. The results demonstrate that severity of excluded and a total of 227 patients were studied (Fig. 1). supraspinatus tears is statistically correlated with The acromial shape was evaluated from the oblique older age and female gender (P < 0.05) but not with sagittal plane lateral to the glenohumeral joint and acromion type. After adjusting for confounding 610 Acta Radiologica 60(5)

Fig. 1. Flow chart of the patient selection.

Fig. 2. Four types of acromion on MRI findings: (a) type I (flat undersurface) acromion in a 61-year-old man, an acromial angle of 0–12; (b) type II (curved convex inferior surface) acromion in a 44-year-old woman, an acromial angle of 13–27; (c) type III (inferiorly beak or hook) acromion in a 68-year-old woman, an acromial angle > 27; and (d) type IV (upward convexity of the inferior border) acromion in a 46-year-old man, an acromial angle < 0. The acromial angle is the sharp bend of acromion where the lateral border becomes continuous with the spine of the scapula. Kim et al. 611

Fig. 3. The pattern of supraspinatus tendon status on T2W coronal scan with fat suppression. Arrowheads show lesion. (a) Normal findings in a 52-year-old woman. (b) Bursa-side partial thickness tear in a 53-year-old woman. (c) Articular side partial thickness tear in a 67-year-old man. (d) Full thickness tear in a 63-year-old man. (e) Complete rupture in a 60-year-old woman.

Table 1. The relationship between variables and the severity of supraspinatus tear.

Complete rupture Variables No tear Partial tear* Full thickness tear with retraction All P value

Age (years) (mean Æ SD) 50.4 Æ 15.7 58.9 Æ 11.7 65.1 Æ 9.6 65.3 Æ 6.6 57.5 Æ 14.0 <0.001 Gender (n (%)) Male 48 (55.2) 32 (43.2) 14 (37.8) 6 (20.7) 100 (44.1) 0.01 Female 39 (44.8) 42 (56.8) 23 (62.2) 23 (79.3) 127 (55.9) Side of the shoulder (n (%)) Right 45 (51.7) 42 (56.8) 26 (70.3) 23 (79.3) 136 (59.9) 0.30 Left 42 (48.3) 32 (43.2) 11 (29.7) 6 (20.7) 91 (40.1) Acromion type (n (%)) Type I 39 (44.8) 29 (39.2) 13 (35.1) 10 (34.5) 91 (40.1) 0.965 Type II 22 (25.3) 23 (31.1) 10 (27.0) 9 (31.0) 64 (28. 2) Type III 18 (20.7) 17 (23.0) 11 (29.7) 8 (27.6) 54 (23.8) Type IV 8 (9.2) 5 (6.8) 3 (8.1) 2 (6.9) 18 (7.9) Total (n (%)) 87 (38.3) 74 (32.6) 37 (16.3) 29 (12.8) 227 (100)

*This categorization includes bursal side tear and articular side tear. factors, old age and the right side of the shoulder was statistically significant difference between bursal and statistically significant (Table 2). articular side partial tears, as shown in Table 3. The lesions for 74 partial tears were categorized into Multiple RCTs were also analyzed and showed that bursal and articular tears. However, there was no age and the side of the shoulder were correlated with 612 Acta Radiologica 60(5)

Table 2. Ordinal logistic regression model on the severity of Table 4. Association between variables and multiple rotator supraspinatus tear. cuff tears.

Ordinal logistic regression Supraspinatus Multiple rotator Variables injury cuff injury* Total P value Variables Coefficient Odds ratio 95% CI P value Age (years) 58.2 Æ 11.6 65.7 Æ 8.1 61.9 Æ 10.7 <0.001 Age 0.06 1.07 1.04–1.09 <0.001 (mean Æ SD) Gender Gender (n (%)) Male 1 0.16 Male 31 (43.1) 21 (30.9) 52 (37.1) 0.136 Female 0.39 1.47 0.86–2.52 Female 41 (56.9) 47 (69.1) 88 (62.9) Side of the shoulder (n (%)) Side of the shoulder Right 41 (56.9) 50 (73.5) 91 (65.0) 0.040 Left 0.003 Left 31 (43.1) 18 (26.5) 49 (35.0) Right 0.77 2.16 1.28–3.66 Acromion type (n (%)) Acromion type Type I 26 (36.1) 26 (38.2) 52 (37.1) 0.217 Type I 0.20 Type II 26 (36.1) 16 (23.5) 42 (30.0) Type II 0.57 1.76 0.95–3.29 Type III 14 (19.4) 22 (32.4) 36 (25.7) Type III 0.41 1.51 0.80–2.86 Type IV 6 (8.3) 4 (5.9) 10 (7.1) Type IV À0.21 0.81 0.30–2.15 Total (n (%)) 72 (51.4) 68 (48.6) 140 (100)

CI, confidence interval. *Multiple rotator cuff injury means supraspinatus injury plus infraspinatus injury and/or subscapularis injury.

Table 3. Association between variables and the bursal/articular side of supraspinatus partial tear. Table 5. Analysis of multiple rotator cuff tears with correction for variables. Variables Bursal side Articular side Total P value Binary logistic regression Age (years) 56.0 Æ 9.49 59.2 Æ 12.3 57.5 Æ 14.0 0.53 Gender (n (%)) Variables Odds ratio 95% CI P value Male 7 (41.2) 26 (45.6) 33 (44.6) 0.75 Female 10 (58.8) 31 (54.4) 41 (55.4) Age 1.08 1.03–1.13 <0.001 Side of the shoulder (n (%)) Gender Right 12 (70.6) 30 (52.6) 42 (56.8) 0.19 Male 1 0.78 Left 5 (29.4) 27 (47.4) 32 (43.2) Female 0.90 0.42–1.94 Acromion type (n (%)) Side of the shoulder Type I 10 (58.8) 20 (35.1) 28 (37.8) 0.28 Left 1 0.11 Type II 4 (23.5) 19 (33.3) 22 (29.7) Right 1.88 0.88–4.04 Type III 3 (17.6) 13 (22.8) 15 (20.3) Acromion type Type IV 0 (0.0) 5 (8.8) 5 (6.8) Type I 1 0.31 Total (n (%)) 17 (23.0) 57 (77.0) 74 (100) Type II 0.76 0.32–1.96 Type III 1.55 0.61–3.91 statistical significance (Table 4). Multiple RCTs were Type IV 0.69 0.16–2.99 more frequent in older age and the right side. Even CI, confidence interval. with multivariate analysis using logistic regression model, age showed a statistically significant odds ratio > 1 in reference to the occurrence of multiple supraspinatus tear would be related to acromion type RCTs, while other factors did not show any correl- and a bursal side tear would be more frequent than an ations (Table 5). articular side tear. However, there were no statistically significant differences between the severity of the Discussion supraspinatus tears and acromion type, and bursal and articular side tears. i.e. a specific type of the acro- Unlike other studies, the severity of supraspinatus tears mion (type III) did not cause more severe attrition to was further subdivided to hopefully discern a more supraspinatus than the other types. accurate relationship between supraspinatus tear and On the other hand, supraspinatus tears are statistic- acromion type (8,10–12). If repetitive impingement ally related to the older age and the right side of the occurs according to acromion type, the severity of a shoulder after adjusting for confounding factors. Kim et al. 613

Increasing age causes degenerative change, i.e. the pro- If the main cause of RCT is not the acromion type, gression of hypovascularity in tendon causes supraspi- acromioplasty in surgical management would not be natus injury and multiple tendon tears (13). Most the optimum choice of treatment. Shin et al. proposed people are right-handed, which implies the overuse that arthroscopic repair of small- to medium-sized and degenerative change of the right shoulder, although RCTs provided pain relief and functional outcome we do not know the exact number of right-handed with or without acromioplasty (18). As clinical out- patients in this study due to it being a retrospective comes were not significantly different, it was suggested one. Only age was statistically significant when the that acromioplasty may not be a necessary method of compounding factor was considered in cases with surgical management in patients with small- to supraspinatus tear and multiple RCTs. Degenerative medium-sized RCTs. MacDonald et al. also com- change by age and overuse make the tendons vulner- menced a study on the viability of acromioplasty in able to tearing. the treatment of full-thickness RCTs with similar Neer and Bigliani reported that the type III acromion results (7). As acromioplasty does not provide any dif- type is closely related to RCT (3,14,15). However, both ference in the moderation of pain or function based on studies were based on only small cases of cadavers, not these studies, conservative management could be opti- live human beings. In contrast to Neer and Bigliani’s mal treatment of RCTs. Kijima et al. also highlighted reports, there have been conflicting results in other cada- the importance of conservative treatment in RCTs, as ver studies. Ozaki et al. studied the relationship of RCT about 90% of patients had none or only slight pain and and pathologic change of acromion in 200 shoulders about 70% had no disturbance in activities of daily life from cadavers and found that the undersurface of acro- 13 years after diagnosis and conservative treatment mion was almost intact in partial RCT; therefore, they (19). These reports contradict the belief that the specific concluded that the pathogenesis of tears is a degenera- type of acromion causes RCT, suggesting that acromio- tive process (16). Panni et al. studied age-related changes plasty may be an inadequate treatment for RCT. Their in the coracoacromial arch and the correlation of these results also suggest an idea similar to ours, that degen- degenerative changes with RCTs of 80 shoulders from 40 eration due to various factors such as age is more cadavers (17). The study revealed that age is related to important than acromion type. degenerative changes in the coracoacromial ligament, The strong points of our study compared to previous degeneration of the acromial bone-ligament junction, studies are that we included the recently classified acro- and acromial spur formation. When comparing the mion type IV and that we also considered the severity bursal and articular side partial tears, the bursal side of supraspinatus tears using MRA. tear was often associated with changes in the coracoa- There are some limitations of this study. First, the cromial ligament and the articular side tear was irre- study was a retrospective analysis and a cross-sectional spective of the undersurface of the acromion, study; thus, it has limited clinical information and does respectively. In other words, bursal side tear is more not have a comparison with normal control group. likely to be caused by coracoacromial ligament due to Second, dominant hand prevalence was not verified, degeneration than acromion type (16,17). which may have an impact on the factor regarding Nonetheless, many clinicians who have accepted the side of the tear either at the right or left side. Neer’s theory still perform acromioplasty, aiming to Finally, the analyses of teres minor lesions were not increase the space beneath the coracoacromial arch included because it is very difficult to confirm teres and reducing the wear on the supraspinatus tendon. minor tears with MRA. They suggest that supraspinatus tears are more In conclusion, we have proved that age is the most common in type III acromion, but since most of the powerful predicting factor whereas acromion type had studies were only on those who underwent surgery, selec- no significant relationship with supraspinatus tear and tion bias may have resulted in erroneous results. Also, multiple RCTs. Putting previous studies and our study because the supraspinatus tears were not divided by into consideration, we can presume that the main mech- severity, it is possible that the results were not accurate anism of multiple RCTs including supraspinatus tear is (8,10–12). Farley et al. also performed a similar study to a degenerative change due to overuse rather than ours on the relationship of MRI findings of acromial related to a specific type of acromion. Further prospect- type and supraspinatus tear at a surgical operation in ive researches are warranted for evaluation of other patients with impingement syndrome (10). Only eight factors that may be involved. patients out of 44 patients had type III acromion. However, thickened coracoacromial ligament and acro- Declaration of Conflicting Interests mioclavicular enthesophyte, related to age, were statis- The author(s) declared no potential conflicts of interest with tically significant with supraspinatus tear. The study respect to the research, authorship, and/or publication of this commented that age is a compounding factor. article. 614 Acta Radiologica 60(5)

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