|Year : 2019 | Volume
| Issue : 9 | Page : 2927-2932
Is it necessary to screen patient with adhesive capsulitis of shoulder for diabetes mellitus?
SK Rai1, Manoj Kashid2, Barun Chakrabarty3, Vimal Upreti4, Omna Shaki5
1 Department of Orthopaedics, 151 Base Hospital, Guwahati, Assam, India
2 Department of Orthopaedics, SMBT Medical Colleges, Igatpuri, Nasik, Maharashtra, India
3 Department of Pathology, 151 Base Hospital, Guwahati, Assam, India
4 Department of Medicine, 151 Base Hospital, Guwahati, Assam, India
5 Department of Trauma & Emergency, 151 Base Hospital, Guwahati, Assam, India
|Date of Submission||23-Mar-2019|
|Date of Decision||25-Mar-2019|
|Date of Acceptance||06-Apr-2019|
|Date of Web Publication||30-Sep-2019|
Dr. Manoj Kashid
Associate Professor, Department of Orthopaedics, SMBT Medical Collages, Igatpuri, Nasik - 422 403, Maharashtra
Source of Support: None, Conflict of Interest: None
Background: Idiopathic adhesive capsulitis of shoulder is common cause of pain and restriction of shoulder motion between the ages of 30 and 65. The prevalence of adhesive capsulitis is as high as 10% to 22% in diabetes mellitus as compared normal population which is 02% and 04%. Therefore, the doubt arises whether patients developed adhesive capsulitis are at greater risk to develop diabetes mellitus and should be screen for diabetes so that it can be detected early. Purpose: To compare the prevalence of prediabeties and diabetes mellitus among patients with features of idiopathic adhesive capsulitis of shoulder who are otherwise healthy. Methods: Patients between 30-65 years of age who attended Orthopaedics OPD with features of idiopathic adhesive capsulitis of shoulder were included. Participated underwent a 2 hour long oral glucose tolerance test and based on fasting and 2-hour plasma glucose levels, patients were diagnosed as normal glucose tolerance, prediabetic, or diabetic and the results were matched with previous published data. Results: 135 patients as participated and completed the test. 21 (15.5%) patients with idiopathic adhesive capsulitis of shoulder were found to be prediabetic, and 37 (27.4%) patients were found to be diabetic. However, 31 patients had family history of diabetes. Conclusion: Based on our study, we can recommend that patients with features of idiopathic adhesive capsulitis of shoulder should be screened at least for fasting and post prandial blood sugar so that diabetes can be detected early.
Keywords: Adhesive capsulitis, blood glucose level, diabetes mellitus, frozen shoulder, screening
|How to cite this article:|
Rai S K, Kashid M, Chakrabarty B, Upreti V, Shaki O. Is it necessary to screen patient with adhesive capsulitis of shoulder for diabetes mellitus?. J Family Med Prim Care 2019;8:2927-32
|How to cite this URL:|
Rai S K, Kashid M, Chakrabarty B, Upreti V, Shaki O. Is it necessary to screen patient with adhesive capsulitis of shoulder for diabetes mellitus?. J Family Med Prim Care [serial online] 2019 [cited 2021 May 12];8:2927-32. Available from: https://www.jfmpc.com/text.asp?2019/8/9/2927/268013
| Introduction|| |
Adhesive capsulitis or 'Frozen shoulder' is a common orthopaedic condition characterized by painful and restricted active and passive range of motion of the shoulder, especially abduction and internal rotation, which incapacitates the patient to comb hair or touch their back with hand.
Idiopathic adhesive capsulitis of shoulder is common cause of pain and restriction of range of shoulder motion between the ages of 30 and 65 years in general orthopaedic practice. However the prevalence of adhesive capsulitis of shoulder among the general population is between 2% and 4%,, and a significantly higher prevalence of 10-22% has been observed in patients with diabetes mellitus.,,
Idiopathic adhesive capsulitis of shoulder (IAFS) occurs spontaneously without an organic cause, or it may be associated with local pathology or systemic disorders like connective tissue disorders, autoimmune disease and spondyloarthropathy etc., The diagnosis of IAFS is usually made on clinical basis with features of pain and limitation in passive range of motion, especially abduction and internal rotation of the shoulder, in the absence of local shoulder pathology such as rotator cuff pathology, glenohumeral arthritis, supraspinatus tendinitis or tear.,,,
In the literature, although the prevalence of IAFS among the general population is between 2-4%,, a significantly higher prevalence between 10-22% has been noted in patients with diabetes mellitus. Since diabetic patients are more prone to develop adhesive capsulitis than non-diabetics, the question arises whether patients developing features of adhesive capsulitis or confirmed as adhesive capsulitis are at greater risk to develop diabetes. Not much study has done to address this issue.
Diabetic mellitus can be detected by the oral glucose tolerance test, which involves taking of 75 gm of glucose orally that can detect abnormal glucose metabolism in otherwise normal individual. This is also known as 'Glucose stress test' and is considered the most appropriate laboratory test to detect prediabetic states in otherwise normal healthy individuals. Patients with deranged glucose intolerance test (because of abnormal glucose metabolism) are labeled as prediabetics, however, there is a significant probability that they become frank diabetics in the future.,,
It is always advisable and prudent to early detection of prediabetes (impaired glucose intolerance) and diagnosis of diabetes. Early detection and timely treatment has been shown to reduce the risks of target organ damage such as cardiovascular, renal, optic and neurological disease related complications, hence the significance of early detection of diabetes is clear so that complication can be minimized.,, Therefore, if we suspect that the development of adhesive capsulitis may be associated with future emergence of diabetes, routine evaluation for prediabetes should be performed for these patients when seen by primary care physician or by orthopaedic surgeon.
There should be high index of suspicion that the otherwise healthy patient of adhesive capsulitis may be diabetic. And if not, he may turn into a future diabetic and should be screened in same visit by primary care physician.
In this study, we aim to find out whether the diagnosis of adhesive capsulitis is an indication to screen for diabetes. This will help in early detection of prediabetics and diabetics when patients consulted a primary care physician for frozen shoulder/adhesive capsulitis.
| Methods|| |
This study consisted of patients from a hospital who attended Orthopaedic OPD and has features of Idiopathic adhesive capsulitis of shoulder. A hospital ethical committee duly approved this study. The study was conducted in 151 Base Hospital, Guwahati, India, between August 2017 and May 2018.
- Age 30 to 65 years
- No detectable shoulder pathology in radiograph
- Absence of a full-thickness rotator cuff tear in an ultrasound examination or in MRI
- No history of diabetes mellitus or taking antidiabetics
- Age less than 30 and more than 65
- Detectable shoulder pathology in radiograph
- Presence of a full-thickness rotator cuff tear in an ultrasound examination or in MRI
- History of diabetes mellitus or taking antidiabetic medication.
All included patients has similar complaints such as painful shoulder motion, especially abduction, inability to comb hair and difficulty in touching back. All were subjected to routine heamogram, Rheumatological workup and radiological workup, and finally diagnosed as Idiopathic adhesive capsulitis of shoulder in the absence of any organic cause. Once patient has been diagnosed as Idiopathic adhesive capsulitis of shoulder, he or she was asked to participate in the study and written consent was taken. They were asked to come the next day on fasting state for glucose tolerance test.
Patients were advised to fast overnight. In the morning, venous blood was withdrawn, for fasting sugar and then 75 g of glucose mixed with water was given to drink. Patient was allowed to move around and after 2 hours later, venous blood (anticubital vein) sample was withdrawn. Blood samples immediately taken to laboratory where these samples are kept at appropriate temperature, and glucose-level analysis was done. Fasting and post-glucose loading results were noted for each patient. 135 patients participated as well as completed the test. Based on the plasma glucose levels, patients were diagnosed as normal glucose tolerance, prediabetic (impaired fasting glucose and abnormal 2-hour glucose tolerance), or as frank diabetic as shown in [Table 1] and [Table 2].,,
|Table 1: Classification of glucose intolerance according to plasma glucose level|
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|Table 2: Summary of WHO diagnostic criteria (1999) for diabetes and intermediate hyperglycaemia|
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The percentage of prediabetic patients in our study was compared with other published reports regarding prevalence of prediabetes in the general, age-matched population using a one-sided Chi-square test. Univariate analysis was also conducted, and differences were noted and considered significant at P ≤ 0.05.
| Results|| |
In the present study, there were 47 female and 88 male participants. The mean age was 47.5 years (range, 30-65 years; SD ± 10.5). The right side shoulder was involved in 38 patients (28.1%) and left side was in 76 (56.2%) and remaining 21 (15.5%) has bilateral involvement of shoulder. 11 patients (8.1%) has a family history of diabetes. The mean body mass index (BMI) was 26.5 kg/m 2 (range, 17.4-36.8 kg/m 2; SD ± 5.9).
Mean glucose fasting level was 4.5 mmol/L (range, 2.6-6.3 mmol/L; SD, ±0.8), and mean 2-hour glucose level was 5.4 mmol/L (range, 3.6-10.6 mmol/L; SD, ±1.4). 21 (15.5%) patients were diagnosed as prediabetes during this study and 37 (27.4%) were diagnosed as diabetic. There were 3 (2.2%) patients with an impaired fasting glucose of 5 mmol/L. 4 (2.9%) patients had abnormal 2-hour plasma glucose levels of 8.6, 10.3, 11.4 and 11.9 mmol/L, and were therefore diagnosed as impaired glucose tolerance. BMI of above 4 patients were found to be similar to those of the entire group (range, 20.2-32.2 kg/m 2, mean ± SD, 25.1 ± 5.7 kg/m 2). These 4 patients had a family history of diabetes in parents. In our study, 37 (27.4%) were diagnosed as diabetic.
The prevalence of prediabetes (included 3 patients with an impaired fasting glucose and 4 patients of abnormal 2-hour plasma glucose levels) in patients with adhesive capsulitis was 28 (20.7%) (28 of 135). The prevalence of diabetes was 37 (27.4%) (37 of 135). In our study, the total prevalence of a diabetic condition in patients with adhesive capsulitis was 71.5% (58 of 135).
The P values was found to be significant when the percentage of prediabetics and diabetics in our study was compared with previously published data of the prevalence of prediabetes in a general age-matched based population. We found statistically significant differences while comparison as shown in [Table 3].
|Table 3: Demographic and clinical factors of adhesive capsulitis shoulder patients in normal, diabetics|
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Demographic and clinical factors of adhesive capsulitis shoulder patients in non-diabetics and pre-diabetics as shown in [Table 4].
|Table 4: Demographic and clinical factors of adhesive capsulitis shoulder patients in normal, pre-diabetics|
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Demographic and clinical factors of adhesive capsulitis shoulder patients in non-diabetics and diabetics as shown in [Table 5].
|Table 5: Prevalence of glucose intolerance/diabetes in different populations with similar ethnicities and age group to the present study|
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| Discussion|| |
This study aimed to prospectively evaluate the prevalence of prediabetes and diabetes in patients presented with adhesive capsulitis with no prior diagnosis of prediabetes and diabetes. Our results showed 15.5% pre-diabetics and 27.4% diabetic. However, low prevalence was noted by Safran, O  where he reported only 4 (8%) of 50 patients were prediabetic.
To compare our results of prevalence of prediabetes and diabetics in our study with the general age-matched based prevalence, we used previously published data.,,,,, We compared our data with groups of similar population and similar age categories, as shown in [Table 3] and [Table 6]. The prevalence of prediabetes and diabetics in our study group 15.5% and 27.4%, respectively, which was within the comparable range found in similar age-matched based populations study. Therefore, the prevalence of diabetes and prediabetes in patients with adhesive capsulitis who are not known prediabetics or diabetics was similar to that of an age-matched studied population.
|Table 6: Summary of studies identifying diabetes in populations of adhesive capsulitis|
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Our results are similar from a previously published study that involved the same screening. In that study by Zreik, N. H et al., a meta-analysis demonstrates an overall mean prevalence of adhesive capsulitis in diabetics as high as of 13.4% and concluded that the routine screening should be done for diabetes. Another study by Tighe and Oakley  studied 52 patients who had adhesive capsulitis without a prior history of prediabetes or diabetes. He used a 2-hour plasma glucose test, and found a prevalence of 48% for prediabetes and 3.8% for diabetes, and concluded that patients with frozen shoulder should be routinely screened for diabetes. Patient presented with adhesive capsulitis in more severe form and it is difficult in treatment in the diabetic population because due to chronic inflammation lead to excessive accumulation of collagen and other extracellular matrix, which may result in fibrosis, necrosis, and finally destruction of normal tissue architecture.
Etiopathophysiology of adhesive capsulitis in diabetics
Adhesive capsulitis in diabetics is a consequence of visceral adiposity and inflammation that occurs via several inflammatory mediators. Exacerbate inflammation caused by proteins and cytokines such as tumor necrosis factor alpha (TNF-α) and interleukin-6 secreted by Adipocytes and results in synovial and connective tissue fibrosis. Long term inflammation lead to excessive accumulation of collagen and other extracellular components, which destroy normal tissue architecture. The effects of above factors results in persistence of inflammation and limited disease resolution. Thus, adhesive capsulitis characterized by an inflammatory and fibrotic condition.
It has been advocated by many authors that patients diagnosed with adhesive capsulitis should undergo diabetic checkup to screen them for prediabetes if they are not known to be diabetics., Inayat F, in 2017, conducted study on 80 diabetes patient to find out prevalence of frozen shoulder and it was 41.3%. Another similar study done by Easmin in 2017 which was a crosscut survey that include 125 prediabetic patients and he found that the prevalence of frozen shoulder among diabetic patients was 14.40%. Moazma in 2018 conducted a study on 315 diabetic patient and noted that 31.7% patients were having Adhesive Capsulitis.
Our findings show important implications for management of adhesive capsulitis and early detection of diabetics. This confirms the high prevalence and increased relative risk of adhesive capsulitis in diabetics. This should alert the primary health care providers and Orthopedician to screen for diabetes in patients presented with features of adhesive capsulitis in otherwise health individual.
| Limitation|| |
A limitation of this study is the lack of control group, which may have led to inaccurate estimation of prediabetes in the general as well as, aged-matched population. However, the rate of prediabetes and diabetics in present study was relatively small as compared with a relevant similar population.
| Conclusions|| |
Based on our study and in view of above findings, the healthcare giver should routinely screen the patients presenting with adhesive capsulitis of the shoulder for prediabeties and diabetes.
I would like show my gratitude to all laboratory and OPD staff for their active assistance and especial thanks to the patients who gave their consents to participate in this study.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Hsu JE, Anakwenze OA, Warrender WJ, Abboud JA. Current review of adhesive capsulitis. J Shoulder Elbow Surg 2011; 20:502-14.
Sheridan MA, Hannafin JA. Upper extremity: Emphasis on frozen shoulder. Orthop Clin North Am 2006; 37:531-9.
Brue S, Valentin A, Forssblad M, Werner S, Mikkelsen C, Cerulli G. Idiopathic adhesive capsulitis of the shoulder: A review. Knee Surg Sports Traumatol Arthrosc 2007; 15:1048-54.
Smith LL, Burnet SP, McNeil JD. Musculoskeletal manifestations of diabetes mellitus. Br J Sports Med 2003; 37:30-5.
Robinson CM, Seah KT, Chee YH, Hindle P, Murray IR. Frozen shoulder. J Bone Joint Surg Br 2012; 94:1-9.
Arkkila PE, Kantola IM, Viikari JS, Ronnemaa T. Shoulder capsulitis in type I and II diabetic patients: Association with diabetic complications and related diseases. Ann Rheum Dis 1996; 55:907-14.
Page P, Labbe A. Adhesive capsulitis: Use of evidence to integrate your intervention. N Am J Sports Phys Ther 2010; 5:266-73.
Laslett LL, Burnet SP, Jones JA. Musculoskeletal morbidity: The growing burden of shoulder pain and disability and poor quality of life in diabetic outpatients. Clin Exp Rheumatol 2007; 25:422-9.
Tighe CB, Oakley WS Jr. The prevalence of a diabetic condition and adhesive capsulitis of the shoulder. South Med J 2008; 101:591-5.
Nathan DM, Davidson MB, DeFronzo RA, Heine RJ, Henry RR, Pratley R, et al
. Impaired fasting glucose and impaired glucose tolerance: Implications for care. Diabetes Care. 2007; 30:753-9.
Lequesne M, Dang N, Bensasson M, Mery C. Increased association of diabetes mellitus with capsulitis of the shoulder and shoulder-hand syndrome. Scand J Rheumatol 1977; 6:53-6.
Harris MI, Hadden WC, Knowler WC, Bennett PH. Prevalence of diabetes and impaired glucose tolerance and plasma glucose levels in U.S. population aged 20-74 yr. Diabetes 1987; 36:523-34.
Chawla A, Chawla R, Jaggi S. Microvasular and macrovascular complications in diabetes mellitus: Distinct or continuum? Indian J Endocrinol Metab 2016; 20:546-51.
Fong DS, Aiello LP, Ferris FL 3rd
, Klein R. Diabetic retinopathy. Diabetes Care 2004; 27:2540-53.
Rema M, Premkumar S, Anitha B, Deepa R, Pradeepa R, Mohan V. Prevalence of diabetic retinopathy in urban India: The Chennai Urban rural epidemiology study (CURES) eye study, I. Invest Ophthalmol Vis Sci 2005; 46:2328-33.
Lorenzo C, Hartnett S, Hanley AJ, Rewers MJ, Wagenknecht LE, Karter AJ, et al
. Impaired fasting glucose and impaired glucose tolerance have distinct lipoprotein and apolipoprotein changes: The insulin resistance atherosclerosis study. J Clin Endocrinol Metab 2013; 98:1622-30.
Rao SS, Disraeli P, McGregor T. Impaired glucose tolerance and impaired fasting glucose. American Family Physician 2004;69:1961-8.
World Health Organization. Department of Non-Communicable Disease Surveillance. WHO; Geneva: 1999. Definition, Diagnosis and Classification of Diabetes Mellitus and its Complications; Part 1. Diagnosis and Classification of Diabetes Mellitus.
Yudkin JS, Alberti KG, McLarty DG, Swai AB. Impaired glucose tolerance. BMJ 1990; 301:397-402.
Modan M, Halkin H, Karasik A, Lusky A. Effectiveness of glycosylated hemoglobin, fasting plasma glucose, and a single post load plasma glucose level in population screening for glucose intolerance. Am J Epidemiol 1984; 119:431-44.
Kidwai SS, Wahid L, Siddiqi SA, Khan RM, Ghauri I, Sheikh I. Upper limb musculoskeletal abnormalities in type 2 diabetic patients in low socioeconomic strata in Pakistan. BMC Res Notes 2013; 17:16.
Mathew AJ, Nair JB, Pillai SS. Rheumatic-musculoskeletal manifestations in type 2 diabetes mellitus patients in south India. Int J Rheum Dis 2011; 14:55-60.
Dehghan A, Salami MA, Yasaii M. The prevalence of adhesive shoulder capsulitis in Diabetes mellitus and prediabetes. Int J Rheum Dis 2010; 13:1756-841.
Cagliero E, Apruzzese W, Perlmutter GS, Nathan DM. Musculoskeletal disorders of the hand and shoulder in patients with diabetes mellitus. Am J Med 2002; 112:487-90.
Milgrom C, Novack V, Weil Y, Jaber S, Radeva-Petrova DR, Finestone A. Risk factors for idiopathic frozen shoulder. Isr Med Assoc J 2008; 10:361-4.
Wang K, Ho V, Hunter-Smith DJ, Beh PS, Smith KM, Weber AB. Risk factors in idiopathic adhesive capsulitis: A case control study. J Shoulder Elbow Surg 2013; 22:e24-9.
Rauoof MA, Lone NA, Bhat BA, Habib S. Etiological factors and clinical profile of adhesive capsulitis in patients seen at the rheumatology clinic of a tertiary care hospital in India. Saudi Med J 2004; 25:359-82.
Safran O, El-Haj M, Leibowitz G, Beyth S, Furman Z, Milgrom C, et al
. Should Patients With Frozen Shoulder Be Screened for Diabetes Mellitus?. Orthopaedic Journal of Sports Medicine 2017;5:2325967117716450.
Zreik NH, Malik RA, Charalambous CP. Adhesive capsulitis of the shoulder and diabetes: A meta-analysis of prevalence. Muscles Ligaments Tendons J 2016; 6:26-34.
Griggs SM, Ahn A, Green A. Idiopathic adhesive capsulitis. A prospective functional outcome study of nonoperative treatment. J Bone Joint Surg Am 2000; 82A: 1398-407.
Welty FK, Alfaddagh A, Elajami TK. Targeting inflammation in metabolic syndrome. Transl Res 2015; 3:1-23.
Kaviratne M, Hesse M, Leusink M, Cheever AW, Davies SJ, McKerrow JH, et al
. IL-13 activates a mechanism of tissue fibrosis that is completely TGF- independent. J Immunol 2004; 173:4020-9.
Salek AK, Mamun MA, Haque MA, Mannan M, Ali E, Islam S, et al
. Serum triglyceride level in type 2 diabetes mellitus patients with or without frozen shoulder. Bangladesh Med Res Counc Bull 2010; 36:64-7.
Sung CM, Jung TS, Park HB. Are serum lipids involved in primary frozen shoulder? A case-control study. JBJS Am 2014; 96:1828-33.
Inayat F, Ali NS, Shahid H, Younus F. Prevalence and determinants of frozen shoulder in patients with diabetes: A single center experience from Pakistan. Cureus 2017; 9:e1544.
Easmin AD. Prevalence of frozen shoulder among diabetes mellitus patients: A cross cut survey. Ortho Rheum Open Access 2017; 9:555759.
Moazma A, Bhutta AH. Prevalance of frozen shoulder in diabetic patients (40-60 year). Phys Med Rehabil Int 2018; 5:1152.
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]
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