Functional improvement of bilateral frozen shoulder by unilateral intra-articular corticosteroid injection: a retrospective study

Abstract

Objective

Bilateral frozen shoulder (FS) is often treated with intra-articular corticosteroid injection (IACI). No studies have been performed to establish whether IACI must be administered in both shoulders or in only one shoulder to improve function. This study was therefore performed to determine whether unilateral IACI improves shoulder pain and passive range of motion (pROM) in bilateral FS.

Methods

The medical records of 165 patients with bilateral primary FS who underwent ultrasonography-guided IACI (2 mL of 10-mg/mL triamcinolone acetonide mixed with 5 mL of 1% lidocaine) in one shoulder were retrospectively reviewed. The outcome measures, namely the numeric rating scale (NRS) scores and pROM values (abduction, external rotation, flexion, hyperextension, and internal rotation), were evaluated pre- and post-injection.

Results

The patients’ mean age was 54.0 ± 8.0 years. The mean symptom duration was 6.5 ± 2.8 months. The mean follow-up period after injection was 6.7 ± 0.8 weeks. The NRS scores and pROM values significantly improved in both the injected and non-injected shoulders.

Conclusions

This study showed that unilateral IACI in patients with bilateral FS improves the clinical outcome of the non-injected shoulder. We suggest that physicians observe the non-injected shoulder after unilateral injection rather than performing bilateral injections.

Keywords

Frozen shoulder adhesive capsulitis range of motion shoulder pain intra-articular injection ultrasonography corticosteroid

Introduction

Frozen shoulder (FS), also known as adhesive capsulitis or painful stiff shoulder, is a common shoulder disease. FS begins with inflammation in the capsule of the glenohumeral joint and soft tissues proximal to the synovium and glenohumeral joint, resulting in global fibrosis and contracture in the glenohumeral joint.^1,2 The treatments for FS include application of heat, flexibility exercises, nonsteroidal anti-inflammatory drugs (NSAIDs), oral corticosteroids, intra-articular corticosteroid injection (IACI), hydrodilatation, manipulation, and arthroscopic capsular release.^1–5

IACI is a conservative treatment for FS. It is effective for rapid reduction of inflammatory pain in the freezing and early frozen stages of FS.^6,7 However, excessive doses of corticosteroids cause local and systemic complications such as tendon rupture, cartilage degeneration, disturbance of the menstrual pattern, hot flash-like symptoms, and hyperglycemia in patients with diabetes mellitus;⁸ therefore, a minimum dose of corticosteroid should be administered.¹

Although FS occurs unilaterally in most patients, it may also occur bilaterally. The prevalence of bilateral FS reportedly ranges from 20% to 50% of the total incidence of FS,^9,10 and its risk in patients with diabetes is higher at 42% to 59%.^11–14 Although basic treatments for bilateral FS do not differ from those of unilateral FS, close attention is needed when IACI is considered as a treatment option. In principle, IACI should be performed bilaterally in symptomatic shoulders; however, a simultaneous bilateral injection at twice the usual dose may increase the risk of systemic complications due to corticosteroid overdose. In contrast, if half the usual dose for unilateral FS is administered in each shoulder, the anti-inflammatory effect of the corticosteroid may be insufficient. Alternatively, it is possible to inject another dose into the other shoulder after a unilateral injection. If the unilateral injection sufficiently mitigates the pain in both shoulders, the second injection is unnecessary, which can alleviate the cost and inconvenience to the patient as well as the risk of complications after the injection. This study was therefore performed to investigate whether a unilateral injection for bilateral FS improves pain and passive range of motion (pROM) in both shoulders.

Materials and methods

Ethics approval and consent to participate

The study was conducted in accordance with the Declaration of Helsinki. The Institutional Review Board of Ajou University Hospital reviewed the medical ethics and approved this study (IRB approval number: AJIRB-MED-MDB-19-251). The requirement for informed consent was waived because of the retrospective study design. All patients’ details have been de-identified. The reporting of this study conforms to the STROBE guidelines.¹⁵

Study design and patients

This retrospective study was conducted in a university-affiliated tertiary care hospital and involved outpatients from the rehabilitation clinics. All patients underwent a standardized history taking, physical examination, and ultrasonographic evaluation by the lead author as well as active and passive range of motion testing, a painful arc and impingement test, a resistance test, muscle strength testing, and checking for tenderness and swelling of the lesion in both shoulders. Among the patients who visited the outpatient clinic with symptoms of FS from March 2011 to February 2019, patients who met the following three criteria were included in this study: (1) presence of bilateral symptomatic primary FS with normal radiographic findings in both shoulders and >30-degree restriction in pROM in two or more planes of movement;¹⁶ (2) lack of response to at least 1 month of conservative treatment, including oral NSAIDs and/or flexibility exercise; and (3) treatment by ultrasonography-guided IACI in the more painful side. The exclusion criteria were (1) secondary FS caused by inflammatory or infectious arthritis, cerebrovascular accident, tumor, or fracture; (2) partial- or full-thickness rotator cuff tear on both physical and ultrasonographic examinations; (3) referred pain from the posterior neck suggestive of cervical radiculopathy; (4) prior surgery involving either the cervical or shoulder region; and (5) diabetes with an uncontrolled blood glucose level (fasting blood glucose level of >150 mg/dL or postprandial 2-hour blood glucose level of >200 mg/dL).

Ultrasonography-guided IACI and exercise education

The patients were allowed to choose the preferred shoulder for the injection considering the degree of pain. The lead author administered the ultrasonography-guided IACIs. The patients were instructed to maintain a sitting position with their palms on their belly. After aseptic preparation, the lead author inserted a 23-gauge, 6-cm-long needle parallel to the transducer, beginning from the posterior side of the shoulder. The needle was advanced under real-time ultrasonography (Logiq P6; GE Healthcare, Buckinghamshire, UK) using 10-MHz linear transducers until the needle tip entered the glenohumeral joint. The lead author then injected 2 mL of 10-mg/mL triamcinolone acetonide mixed with 5 mL of 1% lidocaine.

After the injection, the patients were instructed on a home exercise program to increase their pROM, including stretching forward and bending down to a desk as well as performing a wall-climbing exercise, internal and external rotation with a bar, and posterior shoulder stretching.¹⁷ We explained to the patients that no oral medications were needed because their symptoms might adequately improve with IACI. No oral medications (NSAIDs, analgesics, or opioids) were prescribed after the injection except when the patient specifically requested medications. Patients prescribed oral medications were excluded from the study.

Outcome measures

The numeric rating scale (NRS) score and pROM were compared pre- and post-injection. All outcome measures were evaluated by the lead author. The NRS score, which was the primary outcome measure, was used to assess shoulder pain. The NRS is a self-reporting scale ranging from 0 to 10 that assesses the intensity of global shoulder pain. pROM was measured in degrees using a goniometer for abduction, forward flexion, and external rotation. External rotation was measured at 90 degrees of shoulder abduction and 90 degrees of elbow flexion. Hyperextension and internal rotation were measured as the length (cm) from the spinous process of the seventh cervical vertebra to the tip of the thumb in the standing position.¹⁸ This method has high intrarater reliability¹⁹ and is relevant to activities of daily living, such as dressing, bathing, and toileting.²⁰

Subgroup analysis

A subgroup analysis was performed by dividing the patients into those with and without diabetes.

Statistical analysis

All statistical analyses were performed with R version 3.5.3 (www.r-project.org). The paired t-test was used to compare the pre- and post-injection changes in the NRS score and pROM in the injected and non-injected shoulders. The Wilcoxon signed-rank test rather than the paired t-test was conducted if the Shapiro–Wilk test result was significant. The independent t-test was used to compare the changes in outcome measures between the injected and non-injected shoulders. Statistical significance was set at P < 0.05.

Results

The electronic medical records of 226 patients with bilateral shoulder pain were reviewed. Six patients were excluded because of insufficient data. Another 55 patients were excluded because at least one shoulder was diagnosed with a disease other than FS (rotator cuff disorder in 24 patients, osteoarthritis in 12, myofascial pain syndrome in 9, labrum injury in 6, and rheumatic arthritis in 4). Therefore, 165 patients (69 men, 96 women) with bilateral FS were included in this study. Table 1 shows the patients’ general characteristics. Their mean age was 54.0 ± 8.0 years (range, 38–77 years). The mean symptom duration was 6.5 ± 2.8 months (range, 3–12 months). Twenty patients had diabetes and 145 did not. In our clinic’s outpatient protocol, patients are asked to visit the clinic again for follow-up after 6 weeks. Only patients who returned to the clinic within 6 to 8 weeks were enrolled in the study. Therefore, mean follow-up duration after injection was 6.7 ± 0.8 weeks. No patients developed serious complications such as infection or bleeding.

Table 1.

Baseline characteristics of patients (all, N = 165; non-diabetic, n = 145; diabetic, n = 20).

Characteristic	Value
Age, years
All	54.0 ± 8.0 (38–77)
Non-diabetic	54.2 ± 8.1 (38–77)
Diabetic	52.5 ± 6.5 (40–64)
Sex, men : women
All	69 (41.8) : 96 (58.2)
Non-diabetic	63 (43.4) : 82 (56.6)
Diabetic	6 (30.0) : 14 (70.0)
Duration of symptom, months
All	6.5 ± 2.8 (3–12)
Non-diabetic	6.5 ± 2.3 (3–12)
Diabetic	6.4 ± 1.8 (3–9)
Follow-up after injection, weeks
All	6.7 ± 0.8 (6–8)
Non-diabetic	6.7 ± 0.8 (6–8)
Diabetic	6.7 ± 0.7 (6–8)

Data are presented as mean ± standard deviation (range) or n (%).

Table 2 shows the changes in the outcome measures after IACI. There was a statistically significant improvement in the NRS score and pROM values, including abduction, external rotation, flexion, hyperextension, and internal rotation after IACI in the injected shoulder (P < 0.001 for all). Interestingly, there was also a statistically significant improvement in the NRS score and pROM values of the non-injected shoulder (flexion, P = 0.013; all other parameters, P < 0.001). The independent t-test also showed a significant improvement in the outcome measures of the injected shoulder (P < 0.001 for all). These results indicate that the improvement of all outcome measures was greater in the injected than non-injected shoulder.

Table 2.

Changes in outcome measures after intra-articular corticosteroid injection.

	Before injection	After injection	P*	△	P ^†
Numeric rating scale score
Injected shoulder	6.3 ± 1.3	2.3 ± 1.3	<0.001	−4.0	<0.001
Non-injected shoulder	4.4 ± 0.6	2.4 ± 1.2	<0.001	−2.0	<0.001
Abduction, degrees
Injected shoulder	78.0 ± 26.4	106.6 ± 35.0	<0.001	28.8	<0.001
Non-injected shoulder	103.1 ± 28.7	118.7 ± 30.9	<0.001	15.6	<0.001
External rotation, degrees
Injected shoulder	27.4 ± 12.8	40.5 ± 15.2	<0.001	13.1	<0.001
Non-injected shoulder	39.8 ± 14.7	48.0 ± 16.0	<0.001	8.2	<0.001
Flexion, degrees
Injected shoulder	129.3 ± 20.5	139.1 ± 21.7	<0.001	9.8	<0.001
Non-injected shoulder	141.0 ± 19.0	144.3 ± 21.2	0.013	3.3	<0.001
Hyperextension and internal rotation, cm
Injected shoulder	45.3 ± 11.4	36.6 ± 11.5	<0.001	−8.7	<0.001
Non-injected shoulder	33.1 ± 9.1	30.6 ± 9.3	<0.001	−2.5	<0.001

Data are presented as mean ± standard deviation.

*Comparison of outcome measures before and after injection within the same-side shoulder.

△Change in outcome measures between before and after injection.

^†Comparison of changes in outcome measures between the injected and non-injected shoulders.

A subgroup analysis was performed by dividing the patients into those without diabetes (n = 145) and those with diabetes (n = 20). According to the paired t-test, patients without diabetes showed improvement in all outcome measures of both the injected and non-injected shoulders after IACI (P < 0.05). However, in patients with diabetes, all outcome measures of the injected shoulder improved, whereas in the non-injected shoulder, improvement was seen only in the NRS score and abduction (Table 3). According to the independent t-test for comparison of changes in outcome measures between the injected and non-injected shoulder, there was a statistically significant difference between the injected and non-injected shoulder in all outcome measures in patients without diabetes (P < 0.05), meaning that the improvement of all outcome measures was greater in the injected than non-injected shoulder. However, in patients with diabetes, there was a significant improvement in the injected shoulder only in the NRS score, hyperextension, and internal rotation.

Table 3.

Subgroup analysis (non-diabetic, n =145; diabetic, n = 20) of outcome measures after intra-articular corticosteroid injection in patients with and without diabetes.

	Before injection		After injection		P*		△		P ^†
	Injected shoulder	Non-injected shoulder	Injected shoulder	Non-injected shoulder	Injected shoulder	Non-injected shoulder	Injected shoulder	Non-injected shoulder	P ^†
Numeric rating scale score
Non-diabetic	6.3 ± 1.3	4.4 ± 0.6	2.4 ± 1.4	2.5 ± 1.2	<0.001	<0.001	−4.0	−2.0	<0.001
Diabetic	6.4 ± 1.2	4.3 ± 0.5	1.9 ± 1.0	2.0 ± 0.7	<0.001	<0.001	−4.6	−2.3	<0.001
Abduction, degrees
Non-diabetic	78.2 ± 25.5	104.2 ± 23.4	107.9 ± 34.8	120.4 ± 30.2	<0.001	<0.001	29.8	16.2	<0.001
Diabetic	75.3 ± 25.3	95.0 ± 23.0	97.0 ± 17.8	106.3 ± 19.5	<0.001	0.004	21.8	11.3	0.070
External rotation, degrees
Non-diabetic	27.7 ± 13.4	39.8 ± 15.5	41.2 ± 15.3	48.6 ± 16.4	<0.001	<0.001	13.6	8.8	0.001
Diabetic	25.6 ± 11.1	39.8 ± 12.7	35.3 ± 10.9	44.0 ± 11.9	<0.001	0.062	9.7	4.2	0.054
Flexion, degrees
Non-diabetic	130.0 ± 19.7	141.2 ± 18.6	139.9 ± 20.6	144.4 ± 20.0	<0.001	0.012	10.0	3.2	<0.001
Diabetic	124.5 ± 23.9	139.7 ± 20.9	132.9 ± 26.3	143.5 ± 21.0	0.038	0.126	8.4	3.8	0.308
Hyperextension and internal rotation, cm
Non-diabetic	44.6 ± 11.1	32.8 ± 9.3	36.1 ± 11.3	30.1 ± 9.5	<0.001	<0.001	−8.5	−2.7	<0.001
Diabetic	50.6 ± 10.6	35.4 ± 7.5	40.0 ± 8.6	34.3 ± 7.7	<0.001	0.333	−10.6	−1.0	<0.001

Data are presented as mean ± standard deviation.

^*Comparison of outcome measures before and after injection within the same-side shoulder.

△Changes in outcome measures between before and after injection.

^†Comparison of changes in outcome measures between the injected and non-injected shoulders.

Discussion

To the best of our knowledge, this is the first study to monitor the prognosis of bilateral FS after a unilateral injection. In this retrospective study, we administered ultrasonography-guided IACI to the shoulder with more severe pain in 165 patients with bilateral symptomatic primary FS who complained of pain and pROM limitation in both shoulders. We then investigated the changes in the NRS score and pROM values throughout an average 6.7-week follow-up. After the injection, the NRS scores and all pROM values significantly improved not only in the injected shoulder but also in the non-injected shoulder.

In one study involving 30 patients with rheumatoid arthritis and bilateral synovitis of the knees, IACI of 20 mg triamcinolone hexacetonide administered to the unilateral knee also resulted in improvement in the non-injected knee.²¹ In another study of 20 patients with rheumatoid arthritis, IACI of 4 mg dexamethasone tert-butylacetate (9 patients) or 80 mg methylprednisolone acetate (11 patients) injected into the knee joint resulted in improved hand grip in 7 patients.²² IACI has local effects in the injected joint as well as systemic effects in remote joints.²³ These studies show the possibility of a systemic effect of IACI. We speculate that the significant improvement in the NRS score and pROM in the non-injected shoulder in the present study could be attributed to the systemic action of the corticosteroid injected in one shoulder after absorption into the synovium of the glenohumeral joint, leading to inflammation reduction in the non-injected shoulder. In shoulder pathologies such as FS or rotator cuff disease, intra-articular or periarticular corticosteroid injection is a method of choice among physicians because it rapidly reduces inflammation around the lesion in comparison with oral administration of corticosteroids and particularly acts locally, resulting in less severe systemic adverse effects.^24,25 In contrast to the expectation that a corticosteroid injection is locally acting, the corticosteroid is rapidly absorbed into the synovium after injection and thereafter induces systemic effects.^26,27 Moreover, several studies showed no significant difference in the improvement of shoulder pain between systemic corticosteroid injection and local corticosteroid injection; this occurred because the corticosteroid exerts its effect systemically rather than locally. Valtonen²⁸ reported that single gluteal and subacromial corticosteroid (betamethasone) injections significantly and equally improved supraspinatus tendonitis compared with placebo. In a randomized double-blind study that compared subacromial injection of corticosteroids (local group) and gluteal injection of corticosteroids (systemic group) in patients with rotator cuff disease after 6 weeks, there was no significant difference in the primary outcome measures (the Shoulder Pain and Disability Index score) between the groups.²⁹ In other words, the two studies suggested that the effect of corticosteroids on the reduction of shoulder pain should be attributed to a systemic effect rather than a local effect based on the results in the two groups. However, the findings of our study differ from those of previous studies. Specifically, we observed greater improvement in all outcome measures in the injected than non-injected shoulder. This means that the improvement of outcomes by local corticosteroid injection is greater than that produced by the systemic effect of the corticosteroid.

When IACI is considered for bilateral FS, administration of the injection in both shoulders would result in a high dose of corticosteroid, thus increasing the risk of adverse events due to the systemic effects of corticosteroid. Alternatively, a lower dose of a unilateral injection can be administered to each shoulder; however, this may result in a weaker inflammation reduction effect or a higher total injection dose compared with unilateral injection. Additionally, multiple injections may be inconvenient for patients. As mentioned earlier, simultaneous bilateral injections at twice the usual dose may increase the risk of systemic complications. In contrast, if half the usual dose for unilateral FS is administered in each shoulder, the anti-inflammatory effect of the corticosteroid may be insufficient. The dose of triamcinolone for FS treatment is diverse, ranging from 10 to 80 mg;^30–35 however, a dose of 20 to 40 mg is most common.³¹ We considered an injected dose of 20 mg to be the “usual dose” and one that is sufficient to produce a favorable response to FS treatment.³¹

Although a previous study showed no difference between 20 and 40 mg of triamcinolone in the treatment of unilateral FS,³¹ there is a likely increase in the systemic effect (via an increase in absorption by the synovium) of a larger unilateral corticosteroid dose on pain reduction in the non-injected shoulder of patients with bilateral FS. Thus, further studies should focus on the difference in the effect of corticosteroid injections using a series of doses with consideration of the degree of pain in both shoulders, body weight, and presence of diabetes.

The natural history of FS can generally be divided into three stages^4,36: the freezing, frozen, and thawing stages. The first (freezing) stage is characterized by gradual pain and loss of motion lasting up to 9 months. During the second (frozen) stage, which lasts from 4 to 12 months, pain decreases but stiffness persists and continues to affect patients’ ability to perform activities of daily living. The thawing stage is a period of recovery characterized by progressive improvement in pROM that can take 12 to 42 months. Because the purpose of IACI is to reduce pain caused by capsular inflammation, many authors assert that IACI is effective in the freezing or early frozen stages with moderate to severe pain.^1,6 We included patients with a pain duration of up to 12 months, which is considered long enough to include patients in the freezing to frozen stages.

The result of the subgroup analysis indicated that the effect of IACI was weaker in the patients with than without diabetes. It is widely accepted that the treatment of FS is more difficult in patients with than without diabetes, and patients with diabetes show a more diminished response to treatment.^37–40 Diabetic patients commonly have more limitations of pROM than non-diabetic patients.⁴¹ High blood glucose levels cause excessive glycosylation.⁴² In diabetic FS, a structural change in the joint capsule as a result of more rapid collagen glycosylation and cross-linking of collagen might be related to the worse prognosis, resulting in more severe shoulder pain, reduced mobility, and a poorer functional outcome.^11,43–45 When applying our study results to diabetic patients, it should be noted that the effect of IACI on both the injected and non-injected shoulder may be less pronounced than that in non-diabetic patients.

Our study had several limitations. First, it was a retrospective study conducted in a single institution. Second, the average follow-up interval was 6.7 weeks from the application of IACI. We assumed that a follow-up of 6.7 weeks would be sufficient because the purpose of our study was to investigate the effect of IACI based on systematic reviews suggesting that corticosteroid injection has a short-term benefit for shoulder pain.^7,46 However, previous studies, in which the prognosis of FS was monitored after one session of IACI, revealed that the improvement in pain and pROM lasted for 6 to 12 weeks and that 26 weeks of follow-up showed an extra effect of the injection.^3,31,47 Therefore, follow-up of more than 6 weeks is required to determine the full effect of IACI. Third, although all the patients were instructed to carry out flexibility exercise programs at home, we did not check the patients’ compliance individually, and exercise could cause a significant confounding effect. Fourth, shoulder-specific functional scales that reflect the gains in activities of daily living should have been investigated; however, we did not include these assessments. Fifth, we diagnosed FS in 226 patients with bilateral shoulder pain through physical examination, shoulder X-rays, and ultrasonography. However, because laboratory examinations, electromyography, and cervical and shoulder magnetic resonance imaging were not performed, potential comorbidities of autoimmune diseases (e.g., rheumatoid arthritis, polymyalgia rheumatica), myopathy, and cervical radiculopathy could not be excluded. Moreover, in practice, it is not easy to differentiate idiopathic FS and rotator cuff stiffness without a cuff tear on ultrasonography. Although we tried to exclude patients with pain due to rotator cuff stiffness through physical examination and ultrasonographic evaluation, they may have been included in the study. Furthermore, although FS may occur in the bilateral shoulders, simultaneous onset on both sides is not common, and the duration of symptoms often differs between the two sides. We should have checked the duration of symptoms separately for each shoulder to exclude systemic diseases.

In conclusion, this retrospective study demonstrated that unilateral IACI for bilateral FS improved the outcome of the non-injected shoulder as well as the injected shoulder. Therefore, we suggest that for patients with bilateral FS, physicians should monitor the prognosis of the non-injected shoulder after a unilateral injection rather than perform simultaneous bilateral IACI to both shoulders. In future, a prospective study will be required to monitor the difference in the dosage duration effects of IACI.

Footnotes

Acknowledgements

The authors thank Editage for English language editing and Hyun Young Lee, PhD for providing statistical support.

Authors’ contributions

MK and SHY contributed to the design of the study. MK, KYK, YGH, and SHM performed the experiments and analyzed the data. MK drafted the manuscript and was the principal author of the paper. MK, KYK, SHM, and KYJ interpreted the results and wrote the manuscript. All authors contributed to manuscript revision and approved the final version. SHY was responsible for the conceptualization and supervision of the study.

Data availability statement

Data are available upon reasonable request.

Declaration of conflicting interest

The authors declare that there is no conflict of interest.

Funding

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

ORCID iD

Seung-Hyun Yoon

References

Hannafin

and Chiaia

TA.

Adhesive capsulitis. a treatment approach. Clin Orthop Relat Res 2000; 372: 95–109.

Neviaser

and Neviaser

RJ.

Adhesive capsulitis of the shoulder. J Am Acad Orthop Surg 2011; 19: 536–542.

Lee

Yoon

Lee

, et al. Capsule-preserving hydrodilatation with corticosteroid versus corticosteroid injection alone in refractory adhesive capsulitis of shoulder: a randomized controlled trial. Arch Phys Med Rehabil 2017; 98: 815–821.

Chambler

and Carr

AJ.

The role of surgery in frozen shoulder. J Bone Joint Surg Br 2003; 85: 789–795.

Buchbinder

Green

Youd

, et al. Oral steroids for adhesive capsulitis. Cochrane Database Syst Rev 2006: CD006189.

Ahn

Lee

Kang

, et al. Early intra-articular corticosteroid injection improves pain and function in adhesive capsulitis of the shoulder: 1-year retrospective longitudinal study. PM R 2018; 10: 19–27.

Buchbinder

Green

and Youd

JM.

Corticosteroid injections for shoulder pain.

Cochrane Database Syst Rev 2003; 2003: CD004016.

Jacobs

JW.

How to perform local soft-tissue glucocorticoid injections.

Best Pract Res Clin Rheumatol 2009; 23: 193–219.

Endres

ElHassan

Higgins

, et al. The stiff shoulder. In: Rockwood

Matsen

Wirth

, et al. (eds) The shoulder. 4th ed. Philadelphia: Saunders, 2009, pp.1405–1435.

10.

Pillai

and Cuomo

Classification, evaluation and nonoperative treatment of frozen shoulder. In: Iannotti

and Williams

(eds) Disorders of the shoulder: reconstruction. 3rd ed. Philadelphia: Lippincott Williams & Willkins, 2013, pp.203–210.

11.

Thomas

McDougall

Brown

, et al. Prevalence of symptoms and signs of shoulder problems in people with diabetes mellitus. J Shoulder Elbow Surg 2007; 16: 748–751.

12.

Bridgman

JF.

Periarthritis of the shoulder and diabetes mellitus.

Ann Rheum Dis 1972; 31: 69–71.

13.

Lundberg

BJ.

The Frozen shoulder: clinical and radiographical observations the effect of manipulation under general anesthesia structure and glycosaminoglycan content of the joint capsule local bone metabolism. Acta Orthop Scand 1969; 40: 1–59.

14.

Guyver

Bruce

and Rees

JL.

Frozen shoulder–a stiff problem that requires a flexible approach.

Maturitas 2014; 78: 11–16.

15.

Von Elm

Altman

Egger

, et al. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. Ann Intern Med 2007; 147: 573–577.

16.

Buchbinder

Green

Forbes

, et al. Arthrographic joint distension with saline and steroid improves function and reduces pain in patients with painful stiff shoulder: results of a randomised, double blind, placebo controlled trial. Ann Rheum Dis 2004; 63: 302–309.

17.

Lento

Ihm

Kennedy

, et al. Peripheral joint and soft tissue injection techniques. In: Braddom

(ed) Physical Medicine and Rehabilitation. 4th ed. Philadelphia: Elsevier, 2011, pp.517–540.

18.

Edwards

Bostick

Greene

, et al. Interobserver and intraobserver reliability of the measurement of shoulder internal rotation by vertebral level. J Shoulder Elbow Surg 2002; 11: 40–42.

19.

Hovinga

CA.

Novel anticonvulsant medications in development.

Expert Opin Investig Drugs 2002; 11: 1387–1406.

20.

Rah

Yoon

Moon

, et al. Subacromial corticosteroid injection on poststroke hemiplegic shoulder pain: a randomized, triple-blind, placebo-controlled trial. Arch Phys Med Rehabil 2012; 93: 949–956.

21.

Bird

Ring

and Bacon

PA.

A thermographic and clinical comparison of three intra-articular steroid preparations in rheumatoid arthritis.

Ann Rheum Dis 1979; 38: 36–39.

22.

Koehler

Urowitz

and Killinger

DW.

The systemic effects of intra-articular corticosteroid. J Rheumatol 1974; 1: 117–125.

23.

Ward

and Mason

Systemic effects from hydrocortisone acetate administered intra-articularly to rheumatoid patients. J Lab Clin Med 1953; 42: 961–962.

24.

Snibbe

and Gambardella

RA.

Use of injections for osteoarthritis in joints and sports activity.

Clin Sports Med 2005; 24: 83–91.

25.

Kitridis

Tsikopoulos

Bisbinas

, et al. Efficacy of pharmacological therapies for adhesive capsulitis of the shoulder: a systematic review and network meta-analysis. Am J Sports Med 2019; 47: 3552–3560.

26.

Armstrong

English

Gibson

, et al. Serum methylprednisolone levels following intra-articular injection of methylprednisolone acetate. Ann Rheum Dis 1981; 40: 571–574.

27.

Habib

GS.

Systemic effects of intra-articular corticosteroids.

Clin Rheumatol 2009; 28: 749–756.

28.

Valtonen

EJ.

Double acting betamethasone (Celestone Chronodose®) in the treatment of supraspinatus tendinitis: a comparison of subacromial and gluteal single injections with placebo.

J Int Med Res 1978; 6: 463–467.

29.

Ekeberg

Bautz-Holter

Tveita

, et al. Subacromial ultrasound guided or systemic steroid injection for rotator cuff disease: randomised double blind study. BMJ 2009; 338: a3112.

30.

Gam

Schydlowsky

Rossel

, et al. Treatment of “frozen shoulder” with distension and glucorticoid compared with glucorticoid alone. a randomised controlled trial. Scand J Rheumatol 1998; 27: 425–430.

31.

Yoon

Lee

, et al. Optimal dose of intra-articular corticosteroids for adhesive capsulitis: a randomized, triple-blind, placebo-controlled trial. Am J Sports Med 2013; 41: 1133–1139.

32.

Carette

Moffet

Tardif

, et al. Intraarticular corticosteroids, supervised physiotherapy, or a combination of the two in the treatment of adhesive capsulitis of the shoulder: a placebo-controlled trial. Arthritis Rheum 2003; 48: 829–838.

33.

Moore

Arthrocentesis technique and intraarticular therapy. In: Koopman

(ed) Arthritis and allied conditions: a textbook of rheumatology. Philadelphia: Lippincott Williams & Wilkins, 2001, pp.848–859.

34.

Kesson

Atkins

and Davies

Musculoskeletal injection skills. London: Butterworth-Heinemann, 2002. ISBN 0-750-64372-2.

35.

De Jong

Dahmen

Hogeweg

, et al. Intra-articular triamcinolone acetonide injection in patients with capsulitis of the shoulder: a comparative study of two dose regimens. Clin Rehabil 1998; 12: 211–215.

36.

Dias

Cutts

and Massoud

Frozen shoulder.

BMJ 2005; 331: 1453–1456.

37.

Barbosa

Swamy

Salem

, et al. Chronic adhesive capsulitis (frozen shoulder): comparative outcomes of treatment in patients with diabetes and obesity. J Clin Orthop Trauma 2019; 10: 265–268.

38.

Alsubheen

Nazari

Bobos

, et al. Effectiveness of nonsurgical interventions for managing adhesive capsulitis in patients with diabetes: a systematic review. Arch Phys Med Rehabil 2019; 100: 350–365.

39.

Alhashimi

RAH.

Analytical observational study of frozen shoulder among patients with diabetes mellitus.

Joints 2018; 6: 141–144.

40.

Cho

Jin

and Kim

DH.

Comparison of clinical outcomes between idiopathic frozen shoulder and diabetic frozen shoulder after a single ultrasound-guided intra-articular corticosteroid injection. Diagnostics (Basel) 2020; 10: 370.

41.

Cinar

Akpinar

Derincek

, et al. Comparison of arthroscopic capsular release in diabetic and idiopathic frozen shoulder patients. Arch Orthop Trauma Surg 2010; 130: 401–406.

42.

Gundtoft

Kristensen

Gulaksen

, et al . Prevalence of diabetes mellitus in patients with shoulder symptoms is low. Dan Med J 2013; 60: A4705.

43.

Vishwanath

Frank

Elmets

, et al. Glycation of skin collagen in type I diabetes mellitus. Correlation with long-term complications. Diabetes 1986; 35: 916–921.

44.

Hsu

and Sheu

WH.

Diabetes and shoulder disorders.

J Diabetes Investig 2016; 7: 649–651.

45.

Monnier

Sell

Abdul-Karim

, et al. Collagen browning and cross-linking are increased in chronic experimental hyperglycemia. Relevance to diabetes and aging. Diabetes 1988; 37: 867–872.

46.

Coombes

Bisset

and Vicenzino

Efficacy and safety of corticosteroid injections and other injections for management of tendinopathy: a systematic review of randomised controlled trials. Lancet 2010; 376: 1751–1767.

47.

Prestgaard

Wormgoor

MEA

Haugen

, et al. Ultrasound-guided intra-articular and rotator interval corticosteroid injections in adhesive capsulitis of the shoulder: a double-blind, sham-controlled randomized study. Pain 2015; 156: 1683–1691.