Original Research

Correlation of Ultrasound Findings

With Clinical Stages and Impairment
in Adhesive Capsulitis of the Shoulder
Jong Geol Do,* MD, PhD, Jin Tae Hwang,† MD, Kyung Jae Yoon,† MD, PhD,
and Yong-Taek Lee,†‡ MD, PhD
Investigation performed at Kangbuk Samsung Hospital, Seoul, Republic of Korea

Background: Ultrasound is an essential tool for diagnosing shoulder disorders. However, the role of ultrasound in assessing and
diagnosing adhesive capsulitis has not been fully studied.
Purpose: To evaluate the ultrasound features of adhesive capsulitis and estimate the correlations between clinical impairment and
ultrasound parameters.
Study Design: Case series; Level of evidence, 4.
Methods: A total of 61 patients with clinically diagnosed unilateral adhesive capsulitis were retrospectively reviewed using high-
resolution ultrasound. To compare ultrasound parameters, we performed ultrasound examinations on both affected and unaf-
fected shoulders. Ultrasound parameters, including thickness of the coracohumeral ligament (CHL), rotator interval (RI), axillary
recess (AR), hypervascularity of the RI, and effusion of the long head of the biceps tendon sheath, were measured. Passive range of
motion (PROM), visual analog scale for pain, and the Shoulder Pain and Disability Index were used for clinical assessment.
Results: The CHL, the RI, and the AR in affected shoulders were significantly thicker than in unaffected shoulders (P < .05). CHL
thickness in affected shoulders was significantly correlated with PROM limitation, which included forward elevation, abduction,
external rotation (ER), and internal rotation (IR) (P < .05). AR thickness correlated with passive forward elevation limitation and
passive IR limitation (P < .05). The CHL was significantly thicker in stage 2 compared with stage 1, and the RI was thicker in stage 2
compared with stage 3. The diagnostic cutoff values for adhesive capsulitis were 2.2 mm for CHL thickness (77% sensitivity,
91.8% specificity) and 4 mm for AR thickness (68.9% sensitivity, 90.2% specificity).
Conclusion: The ultrasound parameters associated with structural changes were correlated with clinical characteristics of
adhesive capsulitis. Thickened CHL, RI, and AR were observed in affected shoulders. The cutoff values of 2.2 mm for CHL
thickness and 4 mm for AR thickness can be used as cutoff diagnostic values for adhesive capsulitis.
Keywords: adhesive capsulitis; frozen shoulder; ultrasonography; shoulder joint; coracohumeral ligament

Adhesive capsulitis is a common condition characterized by compatible hardware, needs relatively long examination time,
progressive pain and limited range of motion in the glenohum- and has other limitations, including high cost. Arthroscopy
eral joint. The pathogenesis of adhesive capsulitis remains provides an accurate assessment of the joint capsule, but
poorly understood but is thought to be the result of synovial because of its invasive nature, its use is limited for diagnostic
inflammation and subsequent capsular fibrosis.3,22 Adhesive purposes. High-resolution ultrasound has been widely used as
capsulitis has been diagnosed as a clinical entity that has a suitable imaging option for musculoskeletal problems, as it
progressive shoulder pain with accompanying decreases in is noninvasive, inexpensive, and easy to perform bilaterally in
both active and passive range of motion in the glenohumeral specific positions.
joint. Arthroscopy, magnetic resonance imaging (MRI), and Previous shoulder MRI studies of adhesive capsulitis
ultrasound allow for visualization of confirmed findings to aid have reported several important radiologic features, such
in proper diagnosis and rule out concurrent pathology.8,23,32 as enhancement and fat obliteration of the rotator interval
MRI is a standard imaging approach for shoulder disorders, (RI), hyperintensity of the inferior glenohumeral ligament,
and reliable signs of adhesive capsulitis on MRI correlate with and thickening of the coracohumeral ligament (CHL) and
clinical impairment.1,31 However, MRI requires MR- the axillary recess (AR).3,8,16,32 However, the role of ultra-
sound in assessing and diagnosing adhesive capsulitis has
The Orthopaedic Journal of Sports Medicine, 9(5), 23259671211003675
not been fully studied. A few studies have evaluated specific
DOI: 10.1177/23259671211003675 ultrasound parameters, including CHL, RI, and AR thick-
ª The Author(s) 2021 ening. Effusion in the long head of the biceps tendon

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1
2 Do et al The Orthopaedic Journal of Sports Medicine

(LHBT) sheath and hypervascularity in the RI have TABLE 1

been reported as useful diagnostic features of adhesive Clinical Stages of Adhesive Capsulitis
capsulitis.6,14,17,20,36-38 However, previous studies included
relatively few participants and their results were Symptom
Stage Duration Symptoms
inconsistent.
Many conditions can cause symptoms similar to those of 1. Prefreezing 0-3 months Pain and limited range of motion
adhesive capsulitis, including full- and partial-thickness 2. Freezing 3-9 months Severely restricted range of motion
rotator cuff tears, calcific tendinitis, glenohumeral or acro- and pain
mioclavicular arthritis, and cervical radiculopathy.16 An 3. Frozen 9-15 months Severe stiffness and minimal pain
accurate diagnosis of adhesive capsulitis can reduce patient 4. Thawing 15-24 months Improvement in range of motion
morbidity by shortening pain duration through physical and minimal pain
therapy and intra-articular steroid injections. Radiologic
findings could play an important role in adhesive capsulitis
diagnosis during the early stages or when clinical features active range of motion in a capsular pattern. The exclusion
are atypical.8,33 In this regard, characteristic ultrasound criteria were as follows: rotator cuff tear or bursitis con-
findings and cutoff values for adhesive capsulitis para- firmed by ultrasound; calcification in the rotator cuff or
meters could be useful for creating a differential diagnosis arthritis in the shoulder region confirmed by routine radio-
between adhesive capsulitis and other diseases that mimic graphic examination; presence of cervical radiculopathy or
adhesive capsulitis. The natural course of adhesive capsu- peripheral nerve disorder of the upper limb; and history of
litis can be divided into 4 stages based on clinical presen- trauma or surgery. Patients who were clinically diagnosed
tation and arthroscopic appearance: prefreezing, freezing, with adhesive capsulitis underwent bilateral shoulder
frozen, and thawing.3,23,24 Identifying the clinical stages is ultrasound examination.
of high importance, as treatment varies according to dis- Hannafin and Chiaia12 described the clinical stages of
ease stage.7,11,16 No studies have comprehensively assessed adhesive capsulitis. In stage 1 (prefreezing), there is usually
the correlations between ultrasound findings and clinical pain with limited range of motion. In stage 2 (freezing), there
features of adhesive capsulitis. Estimating the correlations is chronic pain with severely restricted active and passive
between ultrasound characteristics and clinical features range of motion. In stage 3 (frozen), there is minimal pain
would be useful for individualizing and appropriately treat- with significant limitation of range of motion with a rigid “end
ing patients with adhesive capsulitis. feel.” In stage 4 (thawing), there is minimal pain with progres-
The purpose of this study was to evaluate the ultrasound sive improvement in range of motion. In our study, clinical
features of patients with shoulder adhesive capsulitis and to staging was determined according to symptom duration (stage
determine whether there are any correlations between clin- 1: 0-3 months; stage 2: 3-9 months; stage 3: 9-15 months; and
ical impairment and ultrasound parameters. We hypothe- stage 4: 15-24 months) (Table 1).
sized that the ultrasound features would be related with
adhesive capsulitis and that there is a close relationship Clinical Assessment
between ultrasound features and clinical impairment.
Passive range of motion (PROM), visual analog scale (VAS)
for pain, and the Shoulder Pain and Disability Index
METHODS (SPADI) were used for clinical assessment of adhesive cap-
sulitis. With the patient sitting on a stool and measure-
This was a retrospective cohort study of 61 patients with ments performed, shoulder PROM was assessed using a
unilateral adhesive capsulitis performed at a musculoskel- universal goniometer to record forward elevation (FE),
etal clinic in a tertiary hospital from November 2017 to abduction, external rotation (ER), and internal rotation
November 2019. This study protocol was approved by our (IR) at the back. FE was measured as the maximal arm-
institutional review board, and informed consent was trunk degree when the examiner elevated the upper arm in
waived by the board because of the retrospective study the sagittal plane of the trunk. Abduction was measured in
design. Adhesive capsulitis diagnosis was based on the fol- degrees between the arm and the thorax when the exam-
lowing criteria: unilateral shoulder pain for at least 1 iner elevated the upper arm in the coronal plane. The ER
month; shoulder stiffness; and limitation of passive and was measured in degrees in the sagittal plane, with the arm

‡
Address correspondence to Yong-Taek Lee, MD, PhD, Department of Physical and Rehabilitation Medicine, Kangbuk Samsung Hospital, Sung-
kyunkwan University School of Medicine, 29 Saemunan-ro, Jongno-gu, Seoul 03181, Republic of Korea (email: [email protected]).
*Department of Physical and Rehabilitation Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea.
†
Department of Physical and Rehabilitation Medicine, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul, Republic of
Korea.
Final revision submitted November 3, 2020; accepted December 15, 2020.
J.G.D. and J.T.H. contributed equally to this study.
The authors declared that there are no conflicts of interest in the authorship and publication of this contribution. AOSSM checks author disclosures
against the Open Payments Database (OPD). AOSSM has not conducted an independent investigation on the OPD and disclaims any liability or responsibility
relating thereto.
Ethical approval for this study was obtained from the Ethics Committee of Kangbuk Samsung Hospital (approval No. 2020-01-005).
The Orthopaedic Journal of Sports Medicine Ultrasound the Diagnosis of Adhesive Capsulitis 3

Figure 1. Ultrasound measurement. The B-mode ultrasound scan shows measurement of (A) CHL thickness (dotted line), (B)
oblique axial view of the RI (dotted line), (C) AR at the humeral surgical neck (dotted line), and (D) effusion of the LHBT (asterisks).
AR, axillary recess; CHL, coracohumeral ligament; LHBT, long head of biceps tendon; RI, rotator interval.

in adduction and with 90o elbow flexion.18 The IR was mea- CHL. The axial oblique plane was obtained over the CHL by
sured by noting the highest vertebral level reached with the positioning the transducer on the lateral border of the cor-
thumb at the back. For statistical analysis, we converted acoid process. The CHL was observed as a linear hypere-
values into consecutively numbered groups: the 1st tho- choic band arising from the coracoid process and reaching
racic vertebra to the 12th thoracic vertebra ¼ 1-12; the up to the RI.2 Identification of the CHL from the surround-
1st lumbar vertebra to the 5th lumbar vertebra ¼ 13-17; ing structures was achieved by tilting the probe to reduce
and below the sacrum ¼ 18. When PROM was evaluated, anisotropy and by dynamic examination under internal and
we attempted to diminish the compensatory movement of external rotation.37 Longitudinal images of the CHL were
the spine and stabilize the scapula by pressing firmly on the captured, and the CHL thickness just lateral to the coracoid
scapula.18,25 The PROM of both shoulders was measured in process was measured and recorded (Figure 1A).
a sitting position, which is sufficient to minimize the motion RI Thickness and Hypervascularity. The RI is a free space
of the scapula and easy to perform in the clinic. bounded above by the anterior aspect of the supraspinatus
tendon and below by the superior aspect of the subscapularis
tendon, and the medial border is formed by the lateral margin
Ultrasound Parameters
of the coracoid process.34 The RI is the anterior aspect of the
We performed ultrasound examinations on both affected glenohumeral joint capsule that contains the CHL, the supe-
and unaffected shoulders to compare ultrasound para- rior glenohumeral ligament, and the intra-articular portion of
meters. High-resolution ultrasound examinations of the the biceps tendon. The RI was evaluated in the oblique axial
shoulder were performed using Ultrasound System RS80A plane with the patient’s fist held at the side in a sitting posi-
with Prestige (Samsung Medison), equipped with a tion, as in a previously published study.13,17 For RI assess-
3-12 MHz linear transducer. The standard protocol for ment, a B-mode ultrasound and power Doppler were
scanning shoulder structures to exclude the rotator cuff performed. RI thickness was measured as the shortest dis-
and bursa lesions was performed. Then, CHL, RI, and AR tance between the biceps long head tendon and peribursal fat,
thickness, RI hypervascularity, and LHBT sheath effusion including the CHL, the superior glenohumeral ligament, and
were measured in bilateral shoulders. The ratios among the other RI tissues (Figure 1B). The presence of a power Doppler
CHL, the RI, and the AR were calculated by dividing the signal within the RI was scored dichotomously as either
thickness of the affected shoulder by that of the unaffected absent or present.
shoulder. Examinations were performed by a single expe- AR Thickness. For AR thickness, the patient lay supine,
rienced musculoskeletal physiatrist (J.G.D.). with the elbow flexed at 90o and the forearm neutral. The
CHL Thickness. Patients were scanned in a sitting posi- ultrasound probe was placed longitudinally on the midax-
tion, with ER of the shoulder to stretch and visualize the illary line along the long axis of the humeral shaft.15,28 AR
4 Do et al The Orthopaedic Journal of Sports Medicine

TABLE 2
Epidemiologic and Clinical Characteristics of the Patientsa

Characteristic Total (N ¼ 61) Stage 1 (n ¼ 20) Stage 2 (n ¼ 31) Stage 3 (n ¼ 10) p Value

Age, y 56.2 ± 8.9 56.8 ± 11.0 56.3 ± 8.0 54.8 ± 7.5 .849
Male, n (%) 31 (50.8) 12 (60.0) 16 (51.6) 3 (30.0) .334
Right shoulder affected 28 (45.9) 10 (50.0) 12 (38.7) 6 (60.0) .451
Symptom duration, wk 19.6 ± 14.5 7.2 ± 3.2 18.4 ± 5.1b,c 47.9 ± 8.3 <.001
Hypertension 17 (27.9) 6 (30.0) 8 (25.8) 3 (30.0) .930
Diabetes 15 (24.6) 4 (20.0) 9 (29.0) 2 (20.0) .723
Thyroid disease 4 (6.6) 1 (5.0) 3 (9.6) 0 (0.0) .540
Heart disease 4 (6.6) 0 (0.0) 4 (12.9) 0 (0.0) .160
ROM
FE, deg 129.7 ± 30.0 145.7 ± 27.7 117.5 ± 27.7b 135.5 ± 26.9 .003
Abduction, deg 100.5 ± 44.1 124.7 ± 39.6 82.2 ± 41.0b 109.0 ± 39.0 .002
ER, deg 39.7 ± 23.6 56.2 ± 21.9 30.4 ± 21.3b 35.5 ± 16.9 <.001
IR level 13.3 ± 3.7 11.2 ± 4.0 14.8 ± 3.0b 12.8 ± 3.2 .003
Clinical scores
VAS, pain 5.6 ± 2.1 5.6 ± 2.0 5.6 ± 2.3 5.8 ± 1.7 .958
SPADI, pain (%) 49.4 ± 22.7 52.4 ± 21.0 48.1 ± 23.5 47.2 ± 25.0 .772
SPADI, disability (%) 43.3 ± 22.9 46.7 ± 18.0 42.0 ± 25.6 40.6 ± 24.4 .715
SPADI, total (%) 45.3 ± 21.9 48.4 ± 18.6 44.1 ± 23.6 43.1 ± 24.1 .754
a
Values are expressed as mean ± SD or n (%). Bolded P values indicate statistically significant differences between groups (P < .05). ER,
external elevation; FE, forward elevation; IR, internal rotation; ROM, range of motion; SPADI, Shoulder Pain and Disability Index; VAS,
visual analog scale.
b
Significantly different from stage 1.
c
Significantly different from stage 3.

thickness was determined as the distance from the bony parameters to differentiate an adhesive capsulitis shoulder
cortex to the outer margin of the glenohumeral joint cap- from an unaffected shoulder, we estimated sensitivity and
sule at the humeral surgical neck. The thickest portion of specificity and calculated the area under the curve (AUC)
the AR was measured (Figure 1C). using the receiver operating characteristic (ROC) curve of
Effusion of the LHBT Sheath. Effusion of the LHBT sheath the Youden index.9 Data were analyzed using SPSS Statis-
was evaluated at the proximal humeral metaphysis level, tics Version 24.0 (IBM). All statistical tests were 2-sided, and
which is the most dependent portion of the tendon sheath. significance was set at 5%.
The biceps tendon sheath derives from the extension of the
glenohumeral joint capsule; biceps tendon effusion is attrib-
uted to intra-articular pathology.4 Prominent effusion of the RESULTS
glenohumeral joint increases the biceps tendon sheath effu-
sion.29 In a short-axis scan, effusion surrounding the biceps
Patient Characteristics
tendon was considered abnormal (Figure 1D). We enrolled 61 patients who met the clinical diagnosis of
adhesive capsulitis. The mean age was 56.2 ± 8.9 years, and
Statistical Analysis 31 (50.8%) patients were men. Twenty (32.8%) patients had
stage 1, 31 (50.8%) stage 2, and 10 (16.4%) stage 3 adhesive
Descriptive statistics were used to characterize demographic capsulitis; however, none of the patients had stage 4 of the
and clinical variables. Continuous variables are presented as disease. Patient and clinical characteristics are presented
means and standard deviations for normally distributed data in Table 2. There was a statistically significant difference in
and median and interquartile range for non-normally distrib- symptom duration between stage 2 versus stage 1 and stage
uted data. Distributions were evaluated by visual inspection 3 (P < .001 for both). In addition, significant limitations in
of the variable distribution and with the Shapiro-Wilk test. FE, abduction, ER, and IR were seen in the group with
Frequency count and percentage are presented for categori- stage 2 versus the group with stage 1 adhesive capsulitis
cal variables. The paired t test or the McNemar test were (P  .003 for all). However, there were no significant differ-
used to compare ultrasound parameters between affected ences among the groups for VAS or SPADI.
and unaffected shoulders. One-way analysis of variance and
the Fisher exact test with post hoc adjustment (Bonferroni Comparison of Ultrasound Parameters Between
correction) were used to compare ultrasound parameters and Affected and Unaffected Shoulders
clinical characteristics according to clinical stage. Pearson
and Spearman rank correlations were used to investigate the CHL, RI, and AR thickness in the affected shoulder were
relationships between ultrasound parameters and clinical significantly greater than in the unaffected shoulder. Effu-
variables. To determine the best cutoff points for ultrasound sion of the LHBT sheath and RI hypervascularity were also
The Orthopaedic Journal of Sports Medicine Ultrasound the Diagnosis of Adhesive Capsulitis 5

significantly greater in the affected shoulders (P < .001 for SPADI. However, hypervascularity at the RI was not sig-
both) (Table 3). nificantly correlated with any clinical variables (Appendix
Table A1).
Diagnostic Cutoff Values for Ultrasound
Parameters for Adhesive Capsulitis Comparison of Ultrasound Parameters According
to Clinical Stage
The ROC analysis was performed to estimate diagnostic
cutoff values for ultrasound parameters of adhesive capsu- Ultrasound parameters according to clinical stage are
litis. Using 2.2 mm as an optimal cutoff value for CHL shown in Table 4. The CHL thickness and ratio were sig-
thickness, we achieved 77% sensitivity, 91.8% specificity, nificantly thicker in stage 2 than in stage 1 (P ¼ .013 and
and 0.91 AUC. For AR thickness, a cutoff value of 4 mm .034, respectively), and RI thickness was significantly
yielded 68.9% sensitivity, 90.2% specificity, and 0.85 AUC. thicker in stage 2 than in stage 3 (P ¼ .036). In addition,
LHBT effusion was significantly different in stage 2 com-
pared with stage 3 (71% vs 20%, respectively; P ¼ .016).
Correlations Between Ultrasound Parameters and There were no significant differences between clinical
Clinical Variables stages regarding the remaining ultrasound parameters
(Table 4).
CHL thickness in the affected shoulders was significantly
correlated with PROM limitation, including FE (r ¼ -0.340;
P < .05), abduction (r ¼ -0.439; P < .001), ER (r ¼ -0.600; P DISCUSSION
< .001), and IR (r ¼ 0.314; P < .05). AR thickness was
correlated with passive limitation in FE (r ¼ -0.280; P < This study evaluated ultrasound findings in 61 patients
.05) and IR (r ¼ 0.456; P < .001). LHBT sheath effusion was with unilateral adhesive capsulitis by measuring correla-
significantly correlated with limitations in FE, IR, and total tions between ultrasound parameters and clinical features
of adhesive capsulitis. CHL, RI, and AR in affected
TABLE 3 shoulders were significantly thicker than in unaffected
Ultrasound Parameters Between Affected and Unaffected shoulders. CHL thickness correlated with a decreased
Shoulders (N ¼ 61)a range of motion of the glenohumeral joint. Cutoff values
of 2.2 mm for CHL thickness and 4 mm for AR thickness
Affected Unaffected P yielded optimal diagnostic values for adhesive capsulitis.
Ultrasound Parameter Shoulder Shoulder Value
Furthermore, we found significant differences in ultra-
CHL thickness, mm 2.7 ± 0.6 1.5 ± 0.4 <.001 sound findings according to the clinical stage of adhesive
RI thickness, mm 2.2 ± 0.8 1.9 ± 0.7 .004 capsulitis.
AR thickness, mm 4.5 ± 1.4 2.6 ± 1.1 <.001 Adhesive capsulitis can be divided into different stages
Effusion of the LHBT sheath 34 (55.7) 3 (4.9) <.001 depending on pain, duration of symptoms, and arthroscopic
Hypervascularity of the RI 11 (18) 1 (1.6) <.001 findings. Neviaser and Neviaser24 described the arthro-
scopic stages of adhesive capsulitis, and Hannafin and
a
Values are expressed as mean ± SD or n (%). Bolded P values
Chiaia12 reported 4 stages of adhesive capsulitis based on
indicate statistically significant differences between groups (P <
clinical presentation and arthroscopic appearance. The
.05). AR, axillary recess; CHL, coracohumeral ligament; LHBT,
long head of biceps tendon; RI, rotator interval. stages of adhesive capsulitis are sometimes difficult to
define in clinical conditions because they do not fit well with

TABLE 4
Ultrasound Parameters of Affected Shoulders According to Clinical Stagea

Ultrasound Parameterb Stage 1 (n ¼ 20) Stage 2 (n ¼ 31) Stage 3 (n ¼ 10) P Value

CHL thickness, mm 2.3 ± 0.6 2.9 ± 0.6c

2.7 ± 0.6 .013
CHL ratio, % 151.3 ± 38.3 206.5 ± 91.5c 196.4 ± 56.9 .034
RI thickness, mm 2.1 ± 0.8 2.4 ± 0.8d 1.7 ± 0.6 .036
RI ratio, % 116.7 ± 44.2 119.8 ± 32.8 108.1 ± 36.8 .690
AR thickness, mm 4.5 ± 1.6 4.8 ± 1.4 4.1 ± 0.9 .426
AR ratio, % 172.4 ± 51.7 212.4 ± 125.9 222.0 ± 92.3 .310
Effusion of the LHBT sheath 10 (50) 22 (71)d 2 (20) .016
Hypervascularity of the RI 3 (15) 6 (19.4) 2 (20) >.999
a
Values are expressed as mean ± SD or n (%). Bolded P values indicate statistically significant differences between groups (P < .05). AR,
axillary recess; CHL, coracohumeral ligament; LHBT, long head of biceps tendon; RI, rotator interval.
b
Ratio ¼ percentage of affected/unaffected shoulders.
c
Significantly different from stage 1.
d
Significantly different from stage 3.
6 Do et al The Orthopaedic Journal of Sports Medicine

clinical findings, and arthroscopic examination is not per- related to adhesive capsulitis pathophysiology because they
formed solely for the diagnosis of adhesive capsulitis are highly correlated with functional restriction of the gle-
because of its invasive nature. In our study, the 4 clinical nohumeral joint.
stages were based on the duration of symptoms. This might Previous studies have shown that AR thickening is a
be the reason for the lack of significant differences among key diagnostic finding of adhesive capsulitis.20,30 In an
the stage groups in VAS or SPADI scores. Prospective ultrasound study of 20 patients with adhesive capsulitis,
cohort studies are needed for changes of pathology accord- the mean thickness was 4 mm in affected shoulders and
ing to clinical stage to better understand the pathogenesis 1.3 mm in asymptomatic shoulders (P < .001).20 A retro-
of adhesive capsulitis. In the early adhesive capsulitis spective study of 29 patients with adhesive capsulitis
stages, especially in the prefreezing stage, many symptoms reported that the mean AR thickness in the adhesive cap-
of early-stage adhesive capsulitis are similar to those in sulitis group was higher than that in the control group on
other conditions. In this regard, we routinely performed MRI (4.61 ± 1.53 mm vs 2.55 ± 1.03 mm; P < .001). Addi-
shoulder ultrasound and radiography to exclude rotator tionally, a cutoff value of 4 mm for AR thickness yielded an
cuff tears, calcific tendinitis, and glenohumeral arthritis. excellent diagnostic accuracy, with 58.62% sensitivity and
The primary pathophysiology underlying painful 100% specificity.30 These studies showed that AR thicken-
restriction of the glenohumeral joint in adhesive capsulitis ing represents an important structural change associated
is inflammatory contracture of the shoulder joint capsule. with adhesive capsulitis.19 In our study, AR thickness was
CHL thickening and inferior glenohumeral ligament significantly different between affected and unaffected
abnormalities have previously been reported as important shoulders, corresponding to the results of previous stud-
findings of adhesive capsulitis in imaging studies.20,30,31 ies. The mean AR thickness was 4.5 ± 1.4 mm in affected
Several studies have shown that the CHL is thickened and shoulders and 2.6 ± 1.1 mm in unaffected shoulders. Also,
stiffened in adhesive capsulitis on ultrasound. 6,13,37 the optimal AR cutoff value for adhesive capsulitis diag-
Homsi et al13 found that the mean thickness of the CHL nosis was 4 mm, with 68.9% sensitivity and 90.2% speci-
was significantly greater in adhesive capsulitis (3 mm) ficity. Assessment of AR using ultrasound has several
than in asymptomatic (1.34 mm) and painful (1.39 mm) advantages. It can be used to measure bilateral and com-
shoulders. Cheng et al6 reported that patients with adhe- parative images. AR measurement using ultrasound is
sive capsulitis had significantly thickened CHL (mean, regarded as a practical and reliable tool for adhesive cap-
3.1 mm) on ultrasound. A shear-wave elastography study sulitis diagnosis.
also showed that the CHL elastic modulus was greater in Fibrovascular scar tissue within the RI is a reliable sign
symptomatic adhesive capsulitis shoulders than in unaf- of adhesive capsulitis, and the RI can be thickened in adhe-
fected shoulders.37 A histological study observed fibroblas- sive capsulitis. 17,34 Previously, a study reported that
tic proliferation in the CHL in adhesive capsulitis cases.26 increased vascularity of the RI might be related to adhesive
In clinical practice, surgical release of the CHL can capsulitis.17 However, controversy remains about hyper-
improve shoulder function and range of motion. Contrac- vascularity of the RI in adhesive capsulitis. Cheng et al6
ture of the CHL and RI during surgery was observed in a reported hypervascularity in the RI in 71.1% of adhesive
study of 17 patients with adhesive capsulitis.27 Based on capsulitis shoulders, while Tandon et al35 and Walmsley
these results, the CHL is a major morphologic abnormality et al36 found that only 10% and 29% of patients with adhe-
in adhesive capsulitis, and the CHL measurement is sive capsulitis showed increased RI vascularity. In our
important in adhesive capsulitis. We estimated the cutoff study, increased RI vascularity was observed in 18% of
values for the CHL to diagnose adhesive capsulitis. The patients with adhesive capsulitis. It is difficult to find a
sensitivity, specificity, and AUC values of 77%, 91.8%, and usefulness for RI hypervascularity in assessing adhesive
0.91, respectively, were observed when using CHL thick- capsulitis.
ness of 2.2 mm as the best cutoff value for adhesive capsu- Few studies have evaluated the association between clin-
litis diagnosis. As CHL thickening could be indicative of ical stages and ultrasound findings. An MRI study 5
adhesive capsulitis, the optimal CHL cutoff value that we reported that effusion of the LHBT was more frequently
estimated here might be useful for adhesive capsulitis observed in early stages (1 or 2) than in later stages (3 or
diagnosis. 4), and CHL thickness was not associated with clinical
In our study, thickened CHL was associated with limited stages. In our study, the RI was thicker in stage 2 than in
ROM in all orientations, especially ER, and AR thickness stage 3, and the CHL was significantly thicker in stage 2
was inversely correlated with IR. These results are consis- than in stage 1. Thickened synovium and synovial prolifer-
tent with previous findings. The CHL stabilizes the ation with adhesion in the RI were revealed in stage 2 in
humeral head in ER: It is stretched in maximal ER and is arthrography.8,23 The synovial inflammation with prolifer-
lax in the IR.2 Previous researchers suggested that the ation could affect thickened RI and CHL in stage 2.
CHL plays a role in limiting the range of ER of the gleno- This study had several limitations. First, this was a
humeral joint and that a tightened CHL restricts ER in study with a retrospective design, and although we
patients with adhesive capsulitis.21 Gagey and Boisre- reviewed the data thoroughly, we had insufficient informa-
noult10 reported that IR, ER, and abduction diminished tion about some adhesive capsulitis risk factors, such as
after shrinkage of the inferior glenohumeral ligament, cardiovascular disease and obesity. Despite our retrospec-
which is a component of the AR. It is thought that AR and tive study design, we were able to collect precise clinical
CHL thickening are important anatomic abnormalities features and ultrasound measurements using the
The Orthopaedic Journal of Sports Medicine Ultrasound the Diagnosis of Adhesive Capsulitis 7

standardized shoulder registry program of our institute. 13. Homsi C, Bordalo-Rodrigues M, da Silva JJ, Stump XM. Ultrasound in
Second, none of our patients underwent arthroscopic shoul- adhesive capsulitis of the shoulder: is assessment of the coracohum-
der examination. Third, it is difficult to measure the CHL eral ligament a valuable diagnostic tool? Skeletal Radiol. 2006;35(9):
673-678.
because of its anatomic variability and restricted scanning
14. Kim DH, Cho CH, Sung DH. Ultrasound measurements of axillary
position. Also, ultrasound is an experience-dependent recess capsule thickness in unilateral frozen shoulder: study of cor-
method; thus, it is performed at our institute only by an relation with magnetic resonance imaging measurements. Skeletal
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APPENDIX

TABLE A1
Correlation Between Ultrasound Parameters and Clinical Variablesa

SPADI Score

Forward Elevation Abduction External Rotation Internal Rotation VAS Score Pain Disability Total

CHL thickness
r -0.34 -0.439 -0.6 0.314 0.003 -0.24 -0.16 -0.18
P .008 <.001 <.001 .014 .203 .097 .17 .132
CHL ratio
r -0.31 -0.241 -0.46 0.327 0.072 0.07 0.091 0.021
P .016 .061 <.001 .010 .581 .594 .487 .874
RI thickness
r 0.033 -0.021 0.003 0.038 -0.01 -0.27 -0.17 -0.23
P .803 .873 .984 .77 .93 .038 .199 .081
RI ratio
r 0.072 0.046 0.126 -0.01 -0.06 -0.01 -0.02 -0.04
P .579 .722 .332 .971 .651 .955 .907 .759
AR thickness
r -0.28 -0.152 -0.22 0.456 -0.05 -0.05 0.004 -0.03
P .028 .243 .088 <.001 .704 .708 .976 .848
AR ratio
r -0.03 -0.016 -0.2 0.057 0.29 0.045 0.122 0.099
P .809 .904 .13 .66 .024 .728 .348 .446
Effusion of LHBT sheath
r -0.341 -0.249 -0.18 0.382 0.031 -0.22 -0.25 -0.25
P .007 .053 .165 .002 .811 .089 .057 .049
Hypervascularity in the RI
r 0.039 -0.006 -0.041 0.163 0.004 0.095 0.195 0.161
P .766 .963 .752 .209 .978 .468 .132 .215
a
Bolded P values indicate statistically significant differences between groups (P < .05). AR, axillary recess; CHL, coracohumeral ligament;
LHBT, long head of biceps tendon; RI, rotator interval; SPADI, Shoulder Pain and Disability Index; VAS, visual analog scale.