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Page 1: 4 B Shoulder Cholewinski Ultrasound Measurem of Rotator Cuff Thickness KSSTA 2007

SHOULDER

Ultrasound measurement of rotator cuff thicknessand acromio-humeral distance in the diagnosisof subacromial impingement syndrome of the shoulder

Jerzy J. Cholewinski Æ Damian J. Kusz ÆPiotr Wojciechowski Æ Lukasz S. Cielinski ÆMiroslaw 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 uni-

lateral 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 volun-

teers (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 reflect 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.

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

difficulties.

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 impinge-

ment 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 sug-

gested that shoulder ultrasound performed in patients with

J. J. Cholewinski � D. J. Kusz � P. Wojciechowski �L. S. Cielinski (&) � M. P. Zoladz

Department of Orthopaedics and Traumatolgy,

Medical University of Silesia,

Ziołowa 45/47, 40-635 Katowice, Poland

e-mail: [email protected]; [email protected]

123

Knee Surg Sports Traumatol Arthrosc (2008) 16:408–414

DOI 10.1007/s00167-007-0443-4

Page 2: 4 B Shoulder Cholewinski Ultrasound Measurem of Rotator Cuff Thickness KSSTA 2007

symptoms of SIS usually showed decreased size of sub-

acromial space and decreased rotator cuff thickness (when

compared to persons not affected by this condition). There-

fore, 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 use-

fulness of the ultrasound measurements of the acromio-

humeral 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 out-

patients clinic at our institution and fulfilled 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.

2. Positive findings on clinical examination: positive

Neer impingement sign, positive Hawkins and Ken-

nedy sign, Positive Neer impingement test with an

injection of 10 cc of 1% lidocaine into the subacromial

space [2, 8, 14].

3. Prolonged of symptoms for more than 6 months.

Exclusion criteria included: patient age of less than

30 years, bilateral manifestation of symptoms or concom-

itant 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).

Ultimately, the study group comprised 23 men and 34

women. The mean age of the patients in this group was 56

(range 34–83) 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

between the onset of symptoms and the ultrasound

examination was 7 (range 6–48) 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 vol-

unteers (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 38–79) 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 ultra-

sound 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 findings, we classified 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 modified 5-grade Wiener

and Seitz classification (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 echogenici-

ty; hypo- or hyperechoic foci within the cuff

tendons, with no discontinuities of the inter-

nal or external surfaces of the cuff

Knee Surg Sports Traumatol Arthrosc (2008) 16:408–414 409

123

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• diffuse cuff hypoechogenicity with cuff

thickening, especially when accompanied by

thickening of subacromial bursa. Type II may

be associated with diffuse cuff inflammation

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.

(d) Type IV

• hypoechoic linear zone extending through the

entire thickness of the cuff

• segmental loss of convex cuff contour

• the deltoid muscle may be found pushed into

the cuff defect—to the degree where it is in

contact with the humeral head

• visualisation of the hyaline cartilage under-

lying 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.

2. 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 supra-

spinatus and infraspinatus tendons) with one numerical

value. The above described method of measurement

was similar to the one described by Wallny et al. [24].

3. The measurement of distance between the infero-

lateral 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).

Statistical analysis

Categorised data and continuous variables were subjected

to statistical analysis. With the Kolmogorov–Smirnov test

Fig. 1 Classification 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)

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

410 Knee Surg Sports Traumatol Arthrosc (2008) 16:408–414

123

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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 Mann–Whitney

U test. Correlation between two continuous variables were

verified with the Spearman rank correlation test. For cat-

egorized variables, frequencies were compared with the v2

test. Differences were considered to be statically significant

when the P \ 0.05.

Results

Control group

The rotator cuff thickness and distance between the infero-

lateral 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

the 95th percentile. The differences in rotator cuff thick-

ness and in AGT distance between both shoulders were

calculated and are also given in the Table 1. There was no

statistically significant difference in rotator cuff thickness

and AGT distance between the dominant and non-domi-

nant limb.

Further statistical analysis was performed in order to find

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 significant (P value respectively 0.08 and 0.09).

Similar analysis was performed for AGT distance and a

statistically significant 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

Fig. 3 Measurement of the AGT distance. a Overview, b example

sonogram: A acromion, TM greater tuberosity

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 Normal

Rotator cuff thickness (mm) 6.0 4.0–6.9 4.1–6.7

AGT distance (mm) 22.7 18.3–29.4 19.1–28.4

Difference in rotator cuff thickness

between limbs (mm)

0.35 0.0–1.3 \1.1

Difference in AGT distance between

limbs (mm)

0.6 0.0–3.6 \2.1

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 AGT distance

R Spearman P R Spearman P

Age 0.09 0.47 -0.04 0.77

Body mass 0.21 0.08 0.15 0.21

Body height 0.18 0.12 0.26 0.03

BMI 0.2 0.09 0.09 0.45

R values of the Spearman test and P values given

Table 3 Outcomes of rotator cuff integrity assessment

I� II� III� IV� V� Total

N 7 35 9 4 2 57

% 12 61 16 7 4 100

Distribution of cuff tears in the study group

Knee Surg Sports Traumatol Arthrosc (2008) 16:408–414 411

123

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modified Wiener and Seitz classification (Table 3). Sub-

sequently, 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 dif-

ferences between the affected and the non-affected

shoulders were found to be statistically significant 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

significant 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 significant. A difference in the rotator cuff

thickness between affected joints in the study group and the

control group was not found to be statistically significant.

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 significantly 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 significant

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 classified, 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 statisti-

cally significant correlations between the morphological

type of the acromion and rotator cuff thickness or the AGT

distance (P = 0.59 and 0.16, respectively).

Discussion

With the advent of high-frequency high-resolution trans-

ducers, the ultrasound test of the shoulder has become one

of the main tools in the evaluation of rotator cuff lesions

[12, 19–21].

In this study, Hedtmann and Fett shoulder ultrasound

protocol was used [9]. This technique is strongly recom-

mended, especially in Europe, and its principles do not

differ significantly 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 classified according to the

modified 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 [19–21, 23,

24]. The applied classification of lesions corresponds with

SIS development stages as proposed by Neer [14].

In our study, significantly more inflammatory 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 treat-

ment 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 difficult to conduct a

detailed evaluation of the tendons structure. These authors,

Table 4 Comparison of rotator

cuff thickness and AGT

distance values between the

study and the control groups

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 5.6 6.2 6.0 P \ 0.000001 P = 0.07 P = 0.006

Range 1.2–9.5 4.4–9.2 4.0–6.9

AGT distance (mm)

Median 19.4 22.2 22.7 P \ 0.000001 P \ 0.000001 P = 0.13

Range 11.2–31.2 16.4–34.2 18.3–29.4

Table 5 Comparison of rotator cuff thickness and AGT values

between contralateral limbs

Study group Control group

Difference in rotator cuff thickness (mm)

Difference in median values 0.7 0.35

Range -0.9 to +4.9 0.0–1.3

Difference in AGT distance (mm)

Difference in median values 2.7 0.6

Range -3.9–8.6 0.0–3.6

412 Knee Surg Sports Traumatol Arthrosc (2008) 16:408–414

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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 significant 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 confirmed 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 reflects cuff tear [9]. In order to evaluate

rotator cuff lesions Wallny et al. proposed to use mea-

surement of the transverse diameter of rotator cuff and of

the long-bicep tendon and justified 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 infero-

lateral 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 superficial location these anatomi-

cal elements are well visualised in the ultrasound study,

which enables measurement of the aforementioned

distance. Analysis of the control group confirmed the

above-mentioned hypothesis—no statistically significant

difference in AGT distance between the same person’s

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 person’s shoulders (2.1 mm) seems

to be of much higher relevance because of the limited

influence of constitutional factors on the studied variable.

The statistical analysis which showed statistically signifi-

cant 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 morpho-

logical type of the rotator cuff tears, though statistically

confirmed, 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 significant correlation

between the morphological type of the acromion, classified

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 sono-

graphic 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 eval-

uation of every patient in the control group was not feasible

because of funding problems.

Conclusions

Ultrasound measurement of the distance between the in-

fero-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 con-

tralateral 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.

Knee Surg Sports Traumatol Arthrosc (2008) 16:408–414 413

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