Does the intervention for adhesive capsulitis in patients with diabetes differ from that for patients without diabetes?: A systematic review

Abstract

Background:

Adhesive capsulitis (AC) is often accompanied by pain and restriction in range of movement, which long lasting symptoms often have negative impact on patients’ work and lives. Since diabetes mellitus (DM) is an independent risk factor for developing AC, and AC with DM have more limitations of joint motion than general people.

Aims:

The aim of the present study is to evaluate the difference of clinical efficacy between diabetes and non-diabetes, and to explore whether AC with diabetes need special intervention compared to non-diabetes.

Methods:

Pubmed NCBI and Embase were searched for studies published in the last 30 years. We conducted a literature search for terms regarding AC and DM on Pubmed NCBI and Embase.

Results:

A total of 9 studies eligible for inclusion. The affected shoulders in these studies ranged from 26 to 135, 460 shoulders (551 participants) in total, including 166 shoulders in diabetic group and 394 shoulders in non-diabetic/idiopathic group. Interventions included shock wave therapy, hydrodilatation, arthroscopic capsular release, manipulation under cervical nerve root block. Evaluation indicators included pain, certain shoulder questionnaires, range of motion. Positive clinical efficacy were emerged after interventions between the 2 groups. The studies that better improvement of pain in non-diabetic/idiopathic group were 2 of 6, that of certain shoulder questionnaires were 4 of 8, that of range of motion were 3 of 6.

Conclusions:

Whether AC combined with DM or not, the current treatment could achieve positive clinical effectiveness and there is some statistical evidence show that the curative effect of AC combined with DM is worse than non-diabetic. In other words, the available evidence suggests that patients with DM might require additional rehabilitation measures with routine glycemic control.

1. Introduction

Adhesive capsulitis (AC) was first recognized by Duplay in 1896. In 1934, Codman described the diagnostic criterion, which comprises idiopathic onset, painful restriction of shoulder movements with limitation of flexion and external rotation with a normal radiograph.^[1,2] Although this condition is self-limiting, chronic symptoms often have a negative impact on patients’ work and lives.^[3,4]

The exact pathogenesis of AC remains unclear, but several characteristics have been considered to be adhesive capsulitis risk factors, including diabetes mellitus (DM), age, female sex, dyslipidemia, hyperthyroidism, autoimmune diseases and stroke etc.^[5–7] In particular, the overall prevalence of AC in people with DM was estimated to be approximately 10% to 76% in type 1 diabetes and 7% to 30% in type 2 diabetes compared to 2% to 5% in the general population, and the prevalence of DM in people with AC was estimated to be approximately 30%.^[8–10]

Management of AC includes nonsurgical therapies and surgical therapies. In terms of nonsurgical treatments, several randomized controlled trials have demonstrated the effectiveness of oral medication, physical therapy, acupuncture, steroid injection, and capsular distension.^[11–14] In terms of operative treatments, the main intervention is arthroscopic capsular release, which has been proven to be effective.^[15] Since DM is an independent risk factor for developing AC, AC patients with DM generally have more limitations of joint motion than healthy people.^[16] We are deeply concerned about knowing whether AC patients with diabetes need special intervention compared to patients without diabetes.

2. Search strategy

The literature was searched for articles published in English. The authors searched until May 2023 for articles published in MEDLINE through PubMed in addition to clinical trials published in Embase using the Ovid interface. The search terms included “frozen shoulder” or “adhesive capsulitis” or “scapulohumeral periarthritis” or “shoulder periarthritis” or “shoulder stiffness” and “diabetes.” The search strategy is illustrated in Flowchart (Fig. 1).

Figure 1.

Flowchart.

3. Data extraction and management

The main purpose of this review was to assess the treatment of adhesive capsulitis in patients with diabetes, so all studies on the treatment of adhesive capsulitis in patients with diabetes were aggregated for review. Participants were enrolled in the study if they exhibited global restriction of active and passive shoulder movements, particularly external rotation (<50% of the contralateral normal shoulder), experienced pain at rest and during movement, and radiographs confirmed the absence of any other pathology. We excluded studies showing adhesive capsulitis secondary to other pathologies, such as trauma, rotator cuff lesions, tumors, and rheumatological disorders. Studies in which the main content included epidemiological investigation and etiology discussion were also excluded. Some studies only included AC in patients with diabetes but did not show the subgroup analysis of diabetes, which also met the exclusion criteria. The studies in which participants were not allocated according to a protocol established before the beginning of the study met the exclusion criteria; in other words, retrospective studies did not meet the inclusion criteria. Only primary research published in the English language was considered for review.

The authors independently applied the search strategy to the selected references and extracted the data from these databases. The titles and abstracts were also independently reviewed, and duplicate articles or those not related to the research purpose were removed. Regardless of doubt, the full text was retrieved for further scrutiny.

The included studies were evaluated for level of evidence and risk of bias by 2 independent reviewers using the validated Methodological Index for Non-Randomized Studies (MINORS)^[17] (Table 1).

Table 1.

Assessment of methodological quality and risk of bias according to MINORs criteria

Criteria	Ahmed 2019	Bell 2003	Ragab 2011	Tawfeek 2022	Mehta 2014	Cinar 2010	Takahashi 2020	Cho 2016	Sofia 2023
A clearly stated aim	2	2	2	2	2	2	2	2	2
Inclusion of consecutive patients	1	0	0	2	1	0	1	0	2
Prospective collection of data	1	0	0	2	1	0	2	0	2
Endpoints appropriate to the aim of the study	2	2	2	2	2	2	2	2	2
Unbiased assessment of the study endpoint	2	0	0	2	0	0	0	0	2
Follow-up period appropriate to the aim of the study	1	2	1	2	2	1	2	2	2
Loss to follow up less than 5%	0	0	0	0	0	0	0	0	0
Prospective calculation of the study size	0	0	0	0	0	0	0	0	2
An adequate control group	2	2	2	2	2	2	2	2	2
Contemporary groups	2	2	2	2	2	2	2	2	2
Baseline equivalence of groups	2	0	1	2	0	1	1	2	2
Adequate statistical analyses	0	0	0	0	0	0	0	0	2
Total	14	10	10	18	12	10	14	12	22

4. Results

The search strategy and a flowchart are provided in Figure 1. A total of 9 studies were eligible for inclusion from 1981 to 2023 and were comparative case series (MINORS scale: 10–22).^[18–26] In all the studies, participants were divided into diabetic and nondiabetic/idiopathic groups (Table 2). AC secondary to other pathologies, as mentioned above, was not included in these included studies. The number of affected shoulders in these studies ranged from 26 to 135, 460 (551 participants), including 166 shoulders in the diabetic group and 394 shoulders in the nondiabetic/idiopathic group. Interventions included shock wave therapy (SWT), hydrodilatation, arthroscopic capsular release (ACR), and manipulation under cervical nerve root block (MUC), with 1 involving SWT, 1 involving hydrodilatation, 5 involving ACR, and 1 involving MUC. All participants performed the therapeutic exercise as a routine treatment after interventions, however in the study performed by Takahashi, MUC was used. The outcomes assessed included pain, functional scores of the shoulder, and inflammatory indicators. The visual analog scale (VAS) was used to assess pain intensity. Assessment for shoulder function included range of motion (ROM), Shoulder Pain and Disability Index (SPADI), Constant-Murley Score (CMS), Japanese Orthopedic Association scores, American shoulder and elbow score (ASES score), Disabilities of the Arm, Shoulder and Hand questionnaire score (DASH score) and University of California, Los Angeles score (UCLA score) in included studies. Questionnaires about shoulder, such as ASES, DASH, and SPADI, are widely used in the clinic and have been proven acceptable to measure shoulder function.^[27] Ahmed also evaluated inflammatory indicators pre- and posttreatment, including C-reactive protein (CRP) and interleukin-6 (IL-6).

Table 2.

A summary of the included studies

Auther	Design	Patients’ characteristics	Intervention	Outcome measures	Follow-up periods
Ahmed et al 2019	Comparative case series	- group diabetic: n = 25, age = 57.9 ± 7.7, BMI = 27.8 ± 2.8, DOS = 6.3 ± 2.58, FBS = 178.34 ± 11.6 - group non-diabetic: n = 25, age = 59.3 ± 7.0, BMI = 28.3 ± 2.97, DOS = 6.1 ± 2.32, FBS = 86.75 ± 7.2	- 4-week Shock wave therapy, 2000 impulses in one session, the density of energy was 0.22 mJ/mm2, the pulse rate was 10/s, and the frequency was 1–15 Hz. - 4-week therapeutic exercise program: passive stretching exercise, strengthening exercise, and mobilization for the shoulder.	- VAS - SPADI - ROM (FF, Ab, IR) - CRP - IL-6	- 4 wk
Bell et al 2003	Comparative case series	- group diabetic: n = 15, - group non-diabetic: n = 94	- Hydrodilatation: injected 2 mL of 2% Lignocaine and 1 mL of Betamethasone, injected normal saline (10–55 mL). - Took daily self-assisted passive range of motion exercise programme.	- Degree of pain (Severe, Moderate, Mild, Nil) - ROM (FF, Gleno-humeral Ab, ER)	- 2 mo
Ragab et al 2003	Comparative case series	- group diabetic: n = 13, n of shoulder = 14, age = 50 (41–67), DOS = 11 (9–18) - group idiopathic: n = 11, n of shoulder = 12, age = 49 (42–67), DOS = 10 (9–17)	- Arthroscopic capsular release - Passive range of motion exercises	- UCLA score - CMS	- group diabetic: 28.4 mo - group idiopathic: 31.6 mo
Tawfeek et al 2022	Comparative case series	- group diabetic: n = 19, 17 F + 2 M, age = 47.47 ± 6.16, affected side: 8 right/11 left - group non-diabetic: n = 13, 9 F + 4 M, age = 50.15 ± 5.74, affected side: 4 right/9 left	- Arthroscopic rotator interval release - Passive movement and capsular stretching exercises	- VAS - UCLA score	- 4 wk
Mehta et al 2014	Comparative case series	- group diabetic: n = 21, 12 F + 9 M, age = 54 (49–64), DOS = 8.2 (6–12) - group non-diabetic: n = 21, 12 F + 9 M, age = 55 (48–65), DOS = 8.5 (6–13) - All in phase II	- Arthroscopic capsular release - Passive range of motion exercises	- CMS - Degree of pain (None, Mild, Moderate, Severe)	- 6 wk - 6 mo - 2 yr
Cinar et al 2010	Comparative case series	- group diabetic: n = 14, 13 F + 1 M, n of shoulder = 15, age = 51 (40–65), affected side: 12 right/3 left, DOS = 10.0 ± 6.4 - group idiopathic: n = 12, 11 F + 1 M, n of shoulder = 13, age = 48 (41–58), affected side: 4 right/9 left, DOS = 7.7 ± 4.2	- Arthroscopic capsular release - Active and passive joint motions	- ROM (FF, Ab, ER, IR) -UCLA scores -CMS	- group diabetic: 48.5 ± 35.5 mo - group idiopathic: 60.2 ± 28.8 mo
Takahashi et al 2020	Comparative case series	- group diabetic: n = 15, 5 F + 15 M, n of shoulder = 15, age = 52.1 (42–61), affected side: 12 right/3 left - group non-diabetic: n = 81, 55 F + 26 M, n of shoulder = 86, age = 51.3 (38–70), affected side: 45 right/41 left	- MUC	- ROM (FF, ER, IR) - JOA score - CMS - UCLA score	- 3 mo - 6 mo - 1 yr
Cho et al 2016	Comparative case series	- group diabetic: n = 17, 10 F + 7 M, age = 55.7 ± 7.0, DOS = 9.6 ± 7.3, - group idiopathic: n = 20, 15 F + 5 M, age = 55.6 ± 9.1, DOS = 12.8 ± 8.5	- Arthroscopic capsular release - Continuous passive-motion exercises	- VAS - UCLA score - ASES score - ROM (FF, ER, IR) IR: values into contiguously numbered groups: T1 through T12 to 1 through 12; L1 through L5 to 13 through 17; sacrum to 18; and buttock to 19.	- 3 mo - 6 mo - 12 mo - Final (N/A)
Sofia et al 2023	Comparative case series	- group diabetic: n = 25, - group idiopathic: n = 110	- Hydrodilatation: 0.9% NS, 1% lidocaine, 0.25% bupivacaine, 40 mg triamcinolone (90% NS, 2.5% lidocaine, 5% bupivacaine, 2.5% triamcinolone, 10–55 mL). - Cryotherapy, physiotherapy	- VAS - DASH score - ASES score - ROM (FF, ER, IR, AD&IR)	- 1 mo - 3 mo - 6 mo

Ab = abduction, AD&IR = adduction and internal rotation, ASES score = American shoulder and elbow score, BMI = body mass index (kg/m²), CMS = Constant-Murley Score, CRP = C-reactive protein (mg/L), DASH score = Disabilities of the Arm, Shoulder and Hand questionnaire score, DOS = duration of symptom (mo), ER = external rotation, F = female, FBS = fasting blood sugar (mg/dL), FF = forward flexion, IL-6 = interleukin-6 (ng/mL), IR = internal rotation, JOA score = Japanese Orthopaedic Association scores, M = male, MUC = manipulation under ultrasound-guided fifth and sixth cervical nerve root block, ROM = range of motion, SPADI = Shoulder Pain and Disability Index, UCLA score = University of California, Los Angeles score, VAS = visual analog scale.

4.1. Pain

Pain was analyzed in 6 studies; among them, VAS was used in 4 studies, and the degree of pain (severe, moderate, mild, and nil) was used in 2 studies (Table 3). Ahmed, Tawfeek and Cho reported that VAS scores were significantly improved in both the diabetic group and the idiopathic/nondiabetic group after intervention (SWT, ACR, respectively), and there was no statistically significant difference between the 2 groups. Bell described that the improvement was not as good in the diabetic group; however, no systematic statistical analysis was performed. Mehta indicated that improvement in the nondiabetic patients was better at both 6 weeks and 6 months (P < .01) but was not statistically significant (P = .09) at 24 months. Sofia employed a line chart to illustrate that pain relief was less pronounced in the diabetic group during the initial stages of treatment (1 month, 3 months), with no significant disparity observed at the conclusion of the follow-up period (6 months).

Table 3.

Summary of the improvement in pain in included studies

Study	Diabetic	Idiopathic/non-diabetic	Statistically significant difference
Ahmed et al 2019 n = 50	VAS 7.9 ± 1.2 to 2.8 ± 0.92	VAS 7.6 ± 1.34 to 1.9 ± 0.73	Nil
Bell et al 2003 n = 109	Severe 2 Moderate 3 Mild 5 Nil 5	Severe 0 Moderate 7 Mild 25 Nil 62	Improvement pain in most patients, not good in the diabetic patients.
Tawfeek et al 2022 n = 32	VAS 7.84 ± 0.96 to 1.63 ± 1.42	VAS 8.23 ± 1.09 to 2.31 ± 1.32	Nil
Mehta et al 2014 n = 21	Severe 0 Moderate 2 Mild 5 Nil 14	Severe 0 Moderate 0 Mild 2 Nil 19	Improvement in the non-diabetics was better at both 6 weeks and 6 mo (P < .01), not statistically significant (P = .09) at 24 mo.
Cho et al 2016 n = 37	VAS 7.0 ± 1.8 to 0.5 ± 1.3	VAS 7.4 ± 1.5 to 0.5 ± 1.0	Nil
Sofia et al 2023 n = 135	VAS 9.3 ± 2.1 (before) After: no specifics	VAS 7.3 ± 1.8 (before) After: no specifics	Improvement in the non-diabetics was better at both 1 mo and 3 mo, no statistical significance at 6 mo (Not P < .01).

VAS = visual analog scale.

4.2. Range of motion

Forward flexion, abduction, external rotation, internal rotation, adduction and internal rotation were reported in most studies (Table 4). In all the studies, a statistically significant improvement in ROM was recorded in both groups from pre- to postintervention. Three studies reported that the improvement in ROM was not significantly different between the diabetic group and the idiopathic/nondiabetic group. Forward flexion, abduction and internal rotation after SWT; forward flexion, external rotation, abduction, adduction and internal rotation after hydrodilatation; forward flexion, external rotation and internal rotation after MUC. Cinar indicated that improvement in internal rotation and abduction was significantly greater in the diabetic group (P < .05). In Cho’s study, forward flexion was better in the idiopathic group at 3 (P = .011) and 6 (P = .045) months; internal rotation was better in the idiopathic group at 6 (P = .006) and 12 (P = .041) months; and external rotation was better in the idiopathic group at 6 months (P = .021).

Table 4.

Summary of the improvement in ROM in included studies

Study	Diabetic	Idiopathic/non-diabetic	Statistically significant difference
Ahmed et al 2019 n = 50	FF 94.35 ± 6.38 to 138.52 ± 12.3 Ab 103.53 ± 7.98 to 154.66 ± 20.32 IR 23.33 ± 4.57 to 38.2 ± 6.21	FF 96.79 ± 6.87 to 145.2 ± 11.15 Ab 102.1 ± 7.63 to 159.5 ± 10.97 IR 24.6 ± 4.26 to 42.33 ± 2.44	Nil
Bell et al 2003 n = 109	FF 124–154 Gleno-humeral Ab 60–80 ER 28–62	FF 113–152 Gleno-humeral Ab 55–81 ER 25–56	N/A
Cinar et al 2010 n = 28	FF 75.3 ± 23.9 to 141.0 ± 19.8 Ab 56.3 ± 24.0 to 128.3 ± 28.0 ER 11.7 ± 10.6 to 56.7 ± 20.1 IR 15.3 ± 5.2 to 34.7 ± 24.7	FF 69.2 ± 31.5 to 153.1 ± 19.3 Ab 66.5 ± 27.5) to 153.0 ± 22.1 ER 6.2 ± 12.4 to 72.3 ± 14.9 IR 14.6 ± 11.3 to 67.7 ± 4.4	Improvement in the IR and Ab was significantly greater in idiopathic group compared with diabetic group (P < .05).
Takahashi et al 2020 n = 101	FF 95 (3th mo) to 160.8 (12th mo) ER 22.6 (3th mo) to 41.6 (12th mo) IR L3 (3th mo) to L2 (12th mo)	FF 105 (3th mo) to 163.5 (12th mo) ER 19.6 (3th mo) to 53.7 (12th mo) IR L3 (3th mo) to L1 (12th mo)	Nil
Cho et al 2016 n = 37	FF 90.0 ± 23.2 to 168.8 ± 4.9 ER 15.0 ± 11.9 to 65.9 ± 6.2 IR 17.2 ± 1.9 to 9.8 ± 3.1	FF 90.0 ± 20.6 to 169.5 ± 2.2 ER 15.3 ± 10.3 to 65.8 ± 9.1 IR 16.4 ± 1.7 to 9.0 ± 2.2	FF was better in idiopathic group at 3 (P = .011) and 6 (P = .045) mo. IR was better in idiopathic group at 6 (P = .006) and 12 (P = .041) mo. ER was better in the idiopathic group at 6 mo (P = .021).
Sofia et al 2023 n = 135	No specifics	No specifics	Ab, IR, ER and AD&IR was better in idiopathic group at 6 mo (Not P < .01).

Ab = abduction, AD&IR = adduction and internal rotation, ER = external rotation, FF = forward flexion, IR = Internal rotation, ROM = range of motion.

4.3. Shoulder functional scores

Eight studies used the shoulder questionnaire (Table 5), and UCLA was used in 5 studies. There was a statistically significant improvement in UCLA in both groups from pre- to postintervention, and the difference between the 2 groups was not statistically significant.

Table 5.

Summary of the improvement in functional measures in included studies

Study	Diabetic	Idiopathic/non-diabetic	Statistically significant difference
Ahmed et al 2019 n = 50	SPADI 7.4 ± 1.2 to 1.9 ± 0.85	SPADI 6.92 ± 1.3 to 1.5 ± 0.68	Nil
Ragab et al 2003 n = 26	UCLA score 10.3 ± 2.5 to 29.1 ± 5.5 CMS 31.1 ± 6.1 to 83.1 ± 17.8	UCLA score 10.1 ± 2.3 to 31.9 ± 3.5 CMS 30.1 ± 6.2 to 92.1 ± 9.8	CMS was better in idiopathic group (P < .05). Nil in UCLA score (P > .05).
Tawfeek et al 2022 n = 32	UCLA score 13.37 ± 3.73 to 31.74 ± 3.51	UCLA score 12 ± 3.19 to 30.31 ± 3.61	Nil
Mehta et al 2014 n = 42	CMS 36.6–84.4	CMS 38.4–88.6	The mean CMS was better in non-diabetes group at 6 wk (P < .01) and 6 mo (P < .01). Nil at 2 yr (P = .12)
Cinar et al 2010 n = 28	UCLA scores 10.1 ± 2.6 to 29.0 ± 5.7 CMS 30.4 ± 6.2 to 82.0 ± 18.2	UCLA scores 10.0 ± 2.1 to32.7 ± 3.6 CMS 29.6 ± 5.8 to 93.6 ± 10.	CMS was better in idiopathic group (P < .05). Nil in UCLA score (P > .05).
Takahashi et al 2020 n = 101	CMS 57.1 (3 mo) to 94 (12 mo) JOA score 57.3 (3 mo) to 94 (12 mo) UCLA score 17.8 (3 mo) to 32.6 (12 mo)	CMS 61.2 (3 mo) to 94.2 (12 mo) JOA score 60.6 (3 mo) to 94.1 (12 mo) UCLA score 19 (3 mo) to 32.7 (12 mo)	Nil
Cho et al 2016 =37	UCLA score 11.7 ± 5.3 to 34.4 ± 1.5 ASES score 28.1 ± 14.9 to 95.0 ± 8.2	UCLA score 12.8 ± 3.9 to 34.2 ± 1.9 ASES score 30.0 ± 15.4 to 96.7 ± 6.1	Nil
Sofia et al 2023 n = 135	DASH score 72.15 ± 13.39 (before) After: no specifics	DASH score 40.63 ± 16.34 (before) After: no specifics	Better in the idiopathic group (Not P < .01).

ASES score = American shoulder and elbow score, CMS = Constant-Murley Score, DASH score = Disabilities of the Arm, Shoulder and Hand questionnaire score, JOA score = Japanese Orthopaedic Association scores, SPADI = Shoulder Pain and Disability Index, UCLA score = University of California, Los Angeles score.

The CMS included in 4 studies was improved in both groups after intervention, but there were some different results between the 2 groups. Ragab, Mehta and Cinar reported that the improvement was better in the idiopathic/nondiabetic group, and the interventions were SWT, ACR and ACR. Ragab’s result based on a long follow-up period (idiopathic group: 28.4 months, idiopathic group: 31.6 months) showed that the idiopathic group was better (P < .05). Mehta found that CMS was better at 6 weeks (P < .01) and 6 months (P < .01) but was not statistically significant at 2 years (P = .12). Cinar stated that CMS was better in the idiopathic group (P < .05) after a long follow-up period (idiopathic group: 48.5 ± 35.5 months, idiopathic group: 60.2 ± 28.8 months). Sofia was the sole individual to utilize the DASH score, which indicated that the nondiabetic cohort exhibited superior outcomes compared to the diabetic cohort.

4.4. Inflammatory indicators

Only Ahmed described the changes in inflammatory factors before and after the intervention (Table 6). CRP and IL-6 showed a statistically significant decline in both groups (P < .05), and the difference between the 2 groups was not statistically significant (P > .05). However, for CRP and IL-6, compared to the diabetic group (57.89% and 34.6%), there were greater percentages of improvement in the nondiabetic group (67.28.6% and 43.4%).

Table 6.

Summary of the improvement in inflammatory markers levels in included studies

Study	Diabetic	Idiopathic/non-diabetic	Statistically significant difference
Ahmed et al 2019 n = 50	CRP 12.54 ± 1.3 to 5.28 ± 1.15 IL-6 13.3 ± 3.8 to 8.7 ± 2.56	CRP 10.24 ± 1.24 to 3.35 ± 0.48 IL-6 11.33 ± 1.6 to 6.41 ± 0.95	Nil

CRP = C-reactive protein (mg/L), IL-6 = Interleukin-6 (ng/mL).

5. Discussion

In this study, we found that whether AC was combined with or without DM, SWT, ACR, and MUC had positive clinical efficacy, which showed statistically significant improvements in pain relief, ROM, and shoulder questionnaires among the included studies. For pain relief, 3 of 6 studies showed no statistically significant difference; one showed better improvement in the nondiabetic group, and 2 indicated better improvement in the nondiabetic group at early stages after treatment (respectively 6 weeks, 6 months, and 1 month, 3 months), but the difference was not statistically significant at the end of the follow-up (respectively 24 months, and 6 months). Regarding ROM, 3 studies reported better improvement in ROM in the idiopathic/nondiabetic group, 2 studies reported no significant difference between the 2 groups, and one study did not discuss the differences. For the shoulder questionnaires, 4 studies showed no significant difference, and 4 studies reported that the shoulder questionnaires (3 CMS, 1 DASH) improved slightly more in the idiopathic/nondiabetic group. The results of the analysis showed that the better shoulder questionnaires in the nondiabetic group were in the studies that used ACR (n = 3) and hydrodistension (n = 1) as intervention. In these studies, we found different surgical positions, including the lateral decubitus (LD) position or beach-chair (BC) position. However, Houck reported that ACR in either the LD position or BC position can result in positive clinical efficacy and found no significant difference between the 2 positions, showing only that manipulation under anesthesia is performed more frequently in the BC position than in the LD position.^[28] The rotator interval region and coracohumeral ligament release, the anterior and posterior capsulotomy, were conducted in the operation by 3 researchers, and physiotherapy program started within 3 days after ACR. Therefore, the reason for the better shoulder questionnaires in the idiopathic/nondiabetic group could not be confirmed.

The duration of symptoms before intervention in the studies in which CMS was better in the diabetic group was 11 (9–18) months in the diabetic group and 10 (9–17) months in the idiopathic group in Ragab’s study, 8.2 (6–12) months in the diabetic group and 8.5 (6–13) months in the idiopathic group Mehta’s study, 10.0 ± 6.4 months in the diabetic group and 7.7 ± 4.2 months in the idiopathic group in Cinar’s study. There was no statistically significant difference in outcomes between the 2 groups in Ahmed’s study, in which the durations of symptoms were 6.3 ± 2.58 months and 6.1 ± 2.32 months, which seem to be shorter than those in the 3 studies mentioned above. The better improvement of ROM in the idiopathic group was in Cinar’s and Cho’s studies, and the durations of symptoms were 10.0 ± 6.4/7.7 ± 4.2 months and 9.6 ± 7.3/12.8 ± 8.5 months, respectively (diabetic group/idiopathic group). However, Bell and Tawfeek did not show the duration of symptoms at baseline, and only Ahmed described the symptoms as mentioned above. It also appears to be like the better results were in the shorter duration of symptom cohorts. In both Bell’s and Mehta’s research, the idiopathic group showed greater pain relief (duration of symptoms was not available), and the duration of symptoms was longer than in Ahmed’s and shorter than in Cho’s. There seems to be no clear correlation between the degree of pain improvement and the duration of symptoms. However, Sofia’s study showed that the more procedures required in diabetic patients at the end of the follow-up. Among the factors examined, diabetes, the number of years after diagnosis of diabetes, and the number of procedures until month 6 were the factors significantly positively correlated with pain at the end of the follow-up. Multivariate analysis showed that the number of procedures was the only factor independently correlated with the outcome.

As in Ahmed’s study, maybe CRP and IL-6 could be included as a part of the outcomes. CRP and IL-6 were decreased significantly in both groups, and there was no statistically significant difference between the 2 groups after SWT intervention. Meanwhile, the VAS, ROM and shoulder questionnaires also decreased, and there was no statistically significant difference between them. However, compared with the other 7 studies, the follow-up period was short, just 4 weeks. Most researchers accepted that adhesive capsulitis was accompanied by inflammatory and fibrotic processes. Lho^[29] demonstrated elevated inflammatory cytokines, including interleukin (IL)-1α, IL-1β, tumor necrosis factor (TNF)-α, cyclooxygenase (COX)-1, and COX-2, in capsular and bursal tissues in AC. Increased adipocytes in diabetic patients secrete proteins and cytokines, such as TNF-α, IL-6, and IL-13, which result in overproduction of proinflammatory factors, destruction of normal tissue architecture and fibrosis.^[30] Therefore, it might be a way to predict outcomes by monitoring inflammatory factors and then adjusting the therapeutic schedule according to the level of inflammatory factors.

As an important indicator to evaluate blood glucose control, HbA1c was not evaluated in the included studies, but the HbA1c level has not been proven to be significantly associated with DM.^[31] Salek reported that DM type II patients who presented with AC had higher serum triglyceride levels than DM type II patients without frozen shoulder.^[32] Other common biochemical indicators, such as serum values of urea, uric acid, creatinine, calcium, or phosphorus, were not found to be associated with morbidity.^[33]

6. Conclusions

The key pathophysiology and natural history of adhesive capsulitis have not been completely revealed. The ideal treatment for adhesive capsulitis is not known. In conclusion, Whether AC combined with DM or not, the current treatment could achieve positive clinical effectiveness and there is some no statistical evidence show that the curative effect of AC combined with DM is worse than non-diabetic. In other words, the available evidence suggests that patients with DM do not might require additional rehabilitation measures with routine glycemic control. There are some limitations to the present review that warrant discussion. First, the sample size was still small. Second, there 3 types of intervention, so the sample size for a single intervention was even smaller. Third, there were some differences in the follow-up period among studies, which may lead to bias in this study. More multi-center and large-sample studies are needed to analyze whether AC patients with diabetes need special intervention compared to patients without diabetes.

Acknowledgments

Thanks to Shixiong Yi for communicating with American Journal Experts, making the right grammar, sentence structure, word usage, spelling, capitalization, punctuation, format in the manuscript.

Author contributions

Data curation: Shuquan Tang, Xiaoya Tan.

Methodology: Xiaoya Tan.

Visualization: Shuquan Tang.

Writing – original draft: Shuquan Tang.

Writing – review & editing: Xiaoya Tan.