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Knee Surg Sports Traumatol Arthrosc (2008) 16:408414 DOI 10.

1007/s00167-007-0443-4

SHOULDER

Ultrasound measurement of rotator cuff thickness and acromio-humeral distance in the diagnosis of subacromial impingement syndrome of the shoulder
Jerzy J. Cholewinski Damian J. Kusz Piotr Wojciechowski Lukasz S. Cielinski Miroslaw P. Zoladz

Received: 17 June 2007 / Accepted: 22 October 2007 / Published online: 22 December 2007 Springer-Verlag 2007

Abstract The usefulness of ultrasound measurements in the diagnosis of the subacromial impingement syndrome of the shoulder was evaluated. Fifty-seven patients with unilateral symptoms of the impingement syndrome underwent ultrasound examination of both shoulder joints, which included assessment of rotator cuff integrity, measurement of rotator cuff thickness and the distance between the infero-lateral edge of acromion and the apex of the greater tuberosity of humerus (AGT distance) in the standard ultrasonographic positions. As a control group, 36 volunteers (72 shoulders) with no history of shoulder pain were examined sonographically. Ultrasonographic assessment of humeral head elevation, measured as the AGT distance, proved to be useful in establishing the diagnosis of the subacromial impingement syndrome of the shoulder. A difference in rotator cuff thickness of more than 1.1 mm and a difference in the AGT distance of more than 2.1 mm between both shoulder joints may reect dysfunction of rotator cuff muscles. Keywords Rotator cuff Ultrasonography Measurement Shoulder impingement syndrome

Introduction The subacromial impingement syndrome of the shoulder (SIS) is one of the most common causes of shoulder pain.

J. J. Cholewinski D. J. Kusz P. Wojciechowski L. S. Cielinski (&) M. P. Zoladz Department of Orthopaedics and Traumatolgy, Medical University of Silesia, Zioowa 45/47, 40-635 Katowice, Poland e-mail: lukasc@mp.pl; ortopedia@gcm.pl

It leads to impaired function of the affected upper limb and decreased quality of life of the patients. Although the pathogenesis and natural history of the SIS are well elucidated, the proper diagnosis and treatment of this condition is still associated with many problems and difculties. The main pathogenic factor in the development of the SIS is a rotator cuff disease, particularly a tear, which might be attributed to degenerative changes within the cuff tendons or to extrinsic factors such as shoulder trauma or a mechanical impingement of humeral head and acromion [2, 11, 14]. The rotator cuff pathology leads to a disturbed balance of forces between the cuff muscles (especially the supraspinatus) and the deltoid muscle. The deltoid gains advantage and its pull leads to elevation of the humeral head with respect to the glenoid, which decreases the size of subacromial space and further aggravates the impingement of the rotator cuff and the acromion [6, 7, 11]. The aim of both conservative and operative treatments is to restore the disturbed muscle strength balance and, in that way, to increase the size of subacromial space. Changes in the size of subacromial space can be a sensitive marker of the rotator cuff dysfunction, especially in cases with mild (Neer type I) lesions. It may also serve as a tool for monitoring patients progress and the outcome of treatment. Up to the present, the methods used for measurement of the size of subacromial space are based mainly on plain AP shoulder radiographs, which are not very reliable, and on CT/MRI images or the subacromial space is estimated intraoperatively [6, 7, 22, 26]. There are very few studies that describe the usefulness of ultrasound testing in measuring the acromio-humeral distance in the course of SIS [1, 4]. Our previous experience with diagnostic studies suggested that shoulder ultrasound performed in patients with

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symptoms of SIS usually showed decreased size of subacromial space and decreased rotator cuff thickness (when compared to persons not affected by this condition). Therefore, we hypothesised that shoulder ultrasound might be a sensitive and useful tool for establishing the diagnosis of SIS. The aim of this study was to evaluate the possible usefulness of the ultrasound measurements of the acromiohumeral distance and rotator cuff thickness in the diagnosis and treatment of the SIS.

Materials and methods The study group consisted of 57 patients with symptoms of unilateral SIS, who were treated at the orthopaedic outpatients clinic at our institution and fullled the following inclusion criteria: 1. Typical complaints suggestive of the SIS: shoulder pain and restricted movements of the shoulder joint. Other complaints such as decreased muscle strength, pain in other parts of the extremity, or functional impairment of the affected limb were not taken into consideration. Positive ndings on clinical examination: positive Neer impingement sign, positive Hawkins and Kennedy sign, Positive Neer impingement test with an injection of 10 cc of 1% lidocaine into the subacromial space [2, 8, 14]. Prolonged of symptoms for more than 6 months.

2.

3.

Exclusion criteria included: patient age of less than 30 years, bilateral manifestation of symptoms or concomitant symptoms suggestive of other shoulder disorders, such as: cervical radiculopathy brachialgia caused by peripheral neuropathy or the thoracic outlet syndrome capsulitis adhaesiva (frozen shoulder) arthritis multidirectional instability secondary impingement steroid injections (in order to eliminate cases of possible cuff atrophy secondary to administration of steroids, we excluded patients who were given steroid injection into the subacromial space within two months before study or who were given more than two injections).

between the onset of symptoms and the ultrasound examination was 7 (range 648) months. Prior to the ultrasound examination, some of the patients received conservative treatment with physical therapy, NSAIDs and, on a few occasions, steroid injections. The control group comprised 72 shoulders of 36 volunteers (14 males and 22 females) with no symptoms and negative history of shoulder disorders or trauma. These volunteers were patients and staff of the Department of internal medicine at our medical centre. Subjects affected by systemic diseases of the musculoskeletal system or with history suggestive of excessive use of shoulder joints (e.g. due to occupational activities), were not included. The mean age in the control group was 57 (range 3879) years. The study was conducted between April 2001 and September 2007. All the patients had bilateral shoulder ultrasound examination performed by the senior author in a standardized manner according to the protocol described by Hedtmann and Fett [9]. All ultrasonograms were made in real time with the use of a Toshiba Corevision Pro ultrasound scanner. An 8-MHz linear transducer was routinely used; however, patients with thick layer of subcutaneous fat were scanned with 6-MHz linear transducer. The protocol included sonographic evaluation of both shoulders in the standard I and II views (i.e. transverse and longitudinal views), and in standard auxiliary I, II, and III views. Apart from ultrasound examination, all of the subjects in the study group underwent additional imaging of the affected shoulders with magnetic resonance studies and plain X-rays (standard antero-posterior, antero-posterior with 30 caudal tilt, and Y views). On the basis of radiological ndings, we classied morphology of the acromion according to the system proposed by Bigliani [2].

Ultrasonographic assessment Ultrasonographic assessment included: 1. Evaluation of the rotator cuff integrity in the standard I and II view according to the modied 5-grade Wiener and Seitz classication (Fig. 1) [27]. The status of the rotator cuff was recorded on the basis of the following sonographic criteria: (a) Type I: normal cuff contour and echogenicity, slightly hyperechoic to the deltoid muscle; no cuff discontinuity. (b) Type II abnormal, non-homogenous cuff echogenicity; hypo- or hyperechoic foci within the cuff tendons, with no discontinuities of the internal or external surfaces of the cuff

Ultimately, the study group comprised 23 men and 34 women. The mean age of the patients in this group was 56 (range 3483) years.The right shoulder was affected in 32 cases and the left in 25. The dominant limb was involved in 36 patients (32 right and 4 left shoulders). The mean time

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the deltoid muscle may be found pushed into the cuff defectto the degree where it is in contact with the humeral head visualisation of the hyaline cartilage underlying the cuff tendons naked cartilage sign (e) Type V: non-visualization of the rotator cuff tendons. Subdeltoid fascia and the deltoid muscle apposed to the contour of humeral head.

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3.

Measurement of the rotator cuff thickness in the standard I view. The measurement was usually taken 15 mm lateral to the long biceps tendon, but in cases of partial cuff tear it was measured at the narrowest part of the tendon; in cases with irregular tendon thickness, the measurement was taken 10, 20 and 30 mm lateral to the long biceps tendon an the average result was recorded (Fig. 2). The mean value calculated on the basis of the three measurements allowed for estimation of overall (average) cuff thickness (within the supraspinatus and infraspinatus tendons) with one numerical value. The above described method of measurement was similar to the one described by Wallny et al. [24]. The measurement of distance between the inferolateral edge of acromion and the apex of the greater tubercle was done in the standard II view with the arm in neutral rotation (Fig. 3a, b).

Fig. 1 Classication of rotator cuff tears. a Normal cuff (Type I), b degenerative changes within cuff (Type II), c partial tear (Type III), d full-thickness tear (Type IV), e massive full-thickness tear (nonvisualisation of the cuff) (Type V)

Statistical analysis Categorised data and continuous variables were subjected to statistical analysis. With the KolmogorovSmirnov test

diffuse cuff hypoechogenicity with cuff thickening, especially when accompanied by thickening of subacromial bursa. Type II may be associated with diffuse cuff inammation or degenerative changes with disturbances in the tendon structure. (c) Type III area of cuff discontinuity at the inner or outer side of the cuff tendons local loss of anterior arc of the cuff shape or major hypechoic area within the cuff. This type corresponds to partial full-thickness tear.
Fig. 2 Measurement of the rotator cuff thickness. Standard I view (transverse plane), neutral rotation of humerus. Long biceps tendon (arrow). Supraspinatus tendon is located to the right, subscapularis to the left

(d)

Type IV hypoechoic linear zone extending through the entire thickness of the cuff segmental loss of convex cuff contour

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411 Table 1 The results of sonographical measurements of the rotator cuff thickness and the AGT distance in the control group Results of measurements in the control group Median Range Rotator cuff thickness (mm) AGT distance (mm) Difference in rotator cuff thickness between limbs (mm) Difference in AGT distance between limbs (mm) 6.0 22.7 0.35 0.6 4.06.9 0.01.3 0.03.6 Normal 4.16.7 \1.1 \2.1

18.329.4 19.128.4

The normal values were calculated as an interval between the 5th and the 95th percentile Table 2 Correlation between rotator cuff thickness or AGT distance and age, body mass, height and BMI of the subjects in the control group Rotator cuff thickness R Spearman Age Body mass Body height BMI 0.09 0.21 0.18 0.2 P 0.47 0.08 0.12 0.09 AGT distance R Spearman -0.04 0.15 0.26 0.09 P 0.77 0.21 0.03 0.45

R values of the Spearman test and P values given

Fig. 3 Measurement of the AGT distance. a Overview, b example sonogram: A acromion, TM greater tuberosity

it was found that distributions of most variables differed from the normal distribution (P \ 0.05). Therefore, for describing continuous variables, median and range were considered and non-parametric statistics were applied to verify hypotheses. Wilcoxon test was used to compare continuous variables relating to the same patients in the study group. Continuous variables in the study group, were compared with the control group using the MannWhitney U test. Correlation between two continuous variables were veried with the Spearman rank correlation test. For categorized variables, frequencies were compared with the v2 test. Differences were considered to be statically signicant when the P \ 0.05.

the 95th percentile. The differences in rotator cuff thickness and in AGT distance between both shoulders were calculated and are also given in the Table 1. There was no statistically signicant difference in rotator cuff thickness and AGT distance between the dominant and non-dominant limb. Further statistical analysis was performed in order to nd a possible correlation between rotator cuff thickness and age, body mass, height and BMI of the subjects. However, we noted only a tendency for correlation between rotator cuff thickness and body mass and BMI, which were not statistically signicant (P value respectively 0.08 and 0.09). Similar analysis was performed for AGT distance and a statistically signicant correlation was found between the AGT distance and the body height (Table 2). Study group A sonographic evaluation of rotator cuff integrity was performed and the results were recorded according to the
Table 3 Outcomes of rotator cuff integrity assessment I II 35 61 III 9 16 IV 4 7 V 2 4 Total 57 100

Results Control group The rotator cuff thickness and distance between the inferolateral edge of acromion and the AGT distance were measured and are given in Table 1. The range of normal values was calculated as an interval between the 5th and

N %

7 12

Distribution of cuff tears in the study group

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Knee Surg Sports Traumatol Arthrosc (2008) 16:408414 Table 5 Comparison of rotator cuff thickness and AGT values between contralateral limbs Study group Difference in rotator cuff thickness (mm) Difference in median values Range Difference in AGT distance (mm) Difference in median values Range 2.7 -3.98.6 0.6 0.03.6 0.7 -0.9 to +4.9 0.35 0.01.3 Control group

modied Wiener and Seitz classication (Table 3). Subsequently, rotator cuff thickness and the AGT distance were measured and were recorded in Table 4. The difference in rotator cuff thickness between affected and non-affected shoulders ranged from -0.9 to +4.9 mm (difference in median values of cuff thickness was 0.7 mm). The difference in AGT distance between both shoulders ranged from -3.9 to +8.6 mm (with difference between median values calculated at 2.7 mm). The differences between the affected and the non-affected shoulders were found to be statistically signicant in terms of both rotator cuff thickness and the AGT distance (P = 0.000001). In the course of statistical analysis, the study and the control groups were compared (Table 4). A statistically signicant difference in the AGT distance was found between the affected joints in the study group and the control group (P \ 0.000001), whereas the difference in the AGT distance between the non-affected joints in the study group and the control group was not found to be statistically signicant. A difference in the rotator cuff thickness between affected joints in the study group and the control group was not found to be statistically signicant. Further analysis included comparison of the rotator cuff thickness and the AGT distance between both shoulders of the same subject (Table 5). The mean difference in rotator cuff thickness between both shoulders in the study group was signicantly greater than in the control group (P = 0.001). The same was true for the AGT distance (P = 0.00001). Analysis of data revealed a statistically signicant correlation between type of cuff tear and the value of difference in the rotator cuff thickness and the AGT distance between affected and non-affected joints (P = 0.00003 and P = 0.001, respectively, and R Spearman value R = 0.52 and R = 0.33, respectively). The shape of acromion was classied, according to the Bigliani system [2], as type I in 27 patients, type II in 22 patients and type III in 8 patients. There were no statistically signicant correlations between the morphological type of the acromion and rotator cuff thickness or the AGT distance (P = 0.59 and 0.16, respectively).
Table 4 Comparison of rotator cuff thickness and AGT distance values between the study and the control groups

Discussion With the advent of high-frequency high-resolution transducers, the ultrasound test of the shoulder has become one of the main tools in the evaluation of rotator cuff lesions [12, 1921]. In this study, Hedtmann and Fett shoulder ultrasound protocol was used [9]. This technique is strongly recommended, especially in Europe, and its principles do not differ signicantly from those of the methods described by Mack [12] and Middleton [13], which are more popular in the United States. Rotator cuff tears have been classied according to the modied Wiener-Seitz scale [27] which includes all the possible variants of disturbances of rotator cuff integrity in the course of SIS described by other authors [1921, 23, 24]. The applied classication of lesions corresponds with SIS development stages as proposed by Neer [14]. In our study, signicantly more inammatory or degenerative changes within the rotator cuff (61%) than partial (16%) or total (11%) tears were diagnosed. Such distribution is different from those found in groups studied by Jacobson [10], Mack [12] and Teefey [20, 21] who, however, evaluated patients undergoing operative treatment thus with potentially more severe lesions. According to a number of authors [9, 10, 24], the measurement of rotator cuff thickness, applied in the methodology of this study, can be one of the indicators of morphological status of studied tendons, especially in case of partial lesions, where it might be difcult to conduct a detailed evaluation of the tendons structure. These authors,

Study group, affected

Study group, non-affected

Control group

Affected versus non-affected

Affected versus control

Non-affected versus control

Rotator cuff thickness (mm) Median Range Median Range 5.6 1.29.5 19.4 11.231.2 6.2 4.49.2 22.2 16.434.2 6.0 4.06.9 22.7 18.329.4 P \ 0.000001 P \ 0.000001 P = 0.13 P \ 0.000001 P = 0.07 P = 0.006

AGT distance (mm)

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however, point out the fact that it is necessary to make a comparative analysis of the contralateral joint [3, 9]. The mean rotator cuff thickness in the control group was similar to values given in references as normal [3, 9, 24]. Statistically signicant difference in rotator cuff thickness between the affected and unaffected joints found within the study group results from the decrease in thickness of the rotator cuff during the development of SIS, which was observed by some authors [19, 27]. These observations can also be conrmed by the relationship noticed between rotator cuff thickness and type of tear. According to Hedtman and Fett the decrease in cuff thickness by one third, measured in the transverse plane, as compared to the unaffected joint reects cuff tear [9]. In order to evaluate rotator cuff lesions Wallny et al. proposed to use measurement of the transverse diameter of rotator cuff and of the long-bicep tendon and justied usefulness of an index comprising both values [24]. Some authors, however, do not apply measurement of rotator cuff tendons thickness in their study protocol [20, 21]. One of the principal pathogenic elements of SIS is the elevation of humeral head resulting from disturbed balance of forces between deltoid muscle and rotator cuff [6, 7, 11]. Many studies analyse changes in size of subacromial space on the basis of model studies or on evaluation of X-Ray, CT, MRI or arthroscopic images [6, 7, 11, 18, 22, 25, 26]. There are only few studies that include ultrasound testing in evaluation of subacromial space [1, 4]. On the basis of anatomical studies concluding that the morphology of acromion is constant in a given person, independent of pathogenic factors, [5, 16, 17] a hypothesis can be assumed that under the conditions of standard alignment of the upper limb the distance between inferolateral edge of acromion and apex of greater tuberosity (tuberculum major) of humerus (AGT distance) would be similar for both shoulder joints in subjects with unaffected shoulders. Due to their supercial location these anatomical elements are well visualised in the ultrasound study, which enables measurement of the aforementioned distance. Analysis of the control group conrmed the above-mentioned hypothesisno statistically signicant difference in AGT distance between the same persons limbs were found. The statistically calculated norm for the AGT distance has turned out to have a wide range (19.1 28.4 mm). A calculated norm for the difference in the AGT distance between same persons shoulders (2.1 mm) seems to be of much higher relevance because of the limited inuence of constitutional factors on the studied variable. The statistical analysis which showed statistically signicant difference in the AGT distance between affected shoulders in the study group and in the control group may also point to usefulness of the proposed measurement in diagnosis of SIS. The relationship between AGT difference

between affected and unaffected joints and the morphological type of the rotator cuff tears, though statistically conrmed, requires studies on a greater group of patients, due to weak representation of some lesion types. Nyffeler et al. [15] pointed out the correlation between lateral extension of the acromion and development of the subacromial impingement syndrome and a cuff tear. According to these authors, such lateral extension alters the pattern of forces acting across shoulder joint, so that the deltoid muscle pull results in increased elevation of humerus. However, evaluation of possible correlation between lateral extension of the acromion and rotator cuff thickness or AGT distance, measured with ultrasound studies, would require additional analysis and were beyond the scope of our study. On the other hand, the AGT distance may be reduced due to proliferative changes within the greater tubercle or acromion. However, these radiographically found changes, especially when located within the greater tubercle, are believed to be secondary to the underlying rotator cuff lesion [2, 16, 17]. Our study revealed no statistically signicant correlation between the morphological type of the acromion, classied according to Bigliani, and the AGT distance in the affected joints. This might be explained by the fact that we had measured the distance between the inferolateral edge of the acromion and the greater tubercle, whereas Bigliani type II and III are characterised by elongated anterior portion of the acromion, which is relatively distant from a sonographic plane used for measurements. We did not assess the morphological features of the acromion in the control group. This might be viewed as a methodological weakness of our study. However, due to ethical considerations regarding unnecessary exposure to radiation we could not obtain plain X-rays and MRI evaluation of every patient in the control group was not feasible because of funding problems. Conclusions Ultrasound measurement of the distance between the infero-lateral edge of acromion and the apex of the greater tuberosity (tuberculum maius) of humerus (AGT) enables evaluation of the humeral head elevation. In an ultrasound examination of shoulder, the difference of rotator cuff thickness of more than 1.1 mm and AGT distance of more than 2.1 mm in comparison to the contralateral unaffected joint may point to the dysfunction of rotator cuff muscles.
Acknowledgments The study was conducted in compliance with the current laws of the country in which it was performed and the appropriate approval from institutional review board was granted.

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