International Journal of Physical Medicine & Rehabilitation
Open Access

Incidence of Diabetes Mellitus Type II and Pre-Diabetes among Shoulder Impingement Syndrome Patients and Related Modifying Factors: Epidemiological Study

Author info »

Introduction

A variety of musculoskeletal diseases have been found to have high incidence among diabetic patients compared to healthy control subjects [1-7].

These conditions including several disorders affecting the hands such as limited joint mobility, stenosing flexor tenosynovitis, dupuytren’s contractures and diabetic sclerodactly. The shoulders such as frozen shoulder (adhesive capsulitis) and rotator cuff tendinopathy, disorder with major neurologic component including Carpal Tunnel Syndrome (CTS) and neuropathic arthropathy and several other conditions [1,2].

These musculoskeletal conditions lead to pain and disability. Recognition and treatment of such conditions is very important for quality of life improvement of such patients [1,2].

The etiology of occurrence of musculoskeletal disorders in long standing diabetes mellitus may be due to various modification of connective tissue ranging from glycosylation of protein with accumulation of advanced Glycation End Products (AGEs) to microvascular damage of blood vessels and nerves and deposition of extracellular matrix protein in the skin and periarticular tissue. This could potentially affect tendon strength and repair and play a role in microvascular complication and inflammation [1,2,8,9].

Shoulder pain among diabetic are very common. Two types of shoulder problems usually complicate diabetes mellitus, adhesive capsulitis (frozen shoulder) and shoulder impingement syndrome (rotator cuff tendinopathy) [1,2].

Shoulder impingement syndrome i.e. Rotator cuff tendinopathy occurs three times more often in those patients with diabetes Mellitus compared to non- diabetics. Most commonly affecting supra-spinatous tendon [10-15]. These typically result in pain with overhead activities [16,17].

The suggested mechanism involving periarticular calcium hydroxyapatite deposition predominantly in the area of rotator cuff tendons [10].

The exact incidence of diabetes among patients with shoulder impingement which diabetic stage as well as modifying factors need further in-depth study.

Objective

Measure the incidence of Diabetes Mellitus (DM) among patients with shoulder impingement syndrome and the factors that can modify that disease.

Materials and Methods

Design

Prospective cross -sectional study.

Participants

412 patients presented with unilateral or bilateral shoulder pain suspecting shoulder impingement syndrome.

Exclusion criteria

Those having manifestations suggesting of cervical radiculopathy, neuromuscular diseases, or shoulder trauma history.

Interventions

Each patient was subjected to the following; demographic data including occupation, body mass index, detailed medical history including DM history. Shoulder exam including impingement provocative tests; Hawkins test, Neer’s sign. Neck exam including Spurling test. Full neurological exam.

Main outcome measures

Laboratory testing including glycosylated hemoglobin (HgA1c), liver and kidney functions. Shoulder MRI if possible.

Statistical analysis

Data were fed to the computer using IBM SPSS software package version 24.0.

Qualitative data were described using number and percent. Comparison between different groups regarding categorical variables was tested using Chi-square test.

Quantitative data were described using mean and standard deviation for normally distributed data.

For normally distributed data, comparison between two independent population were done using independent t-test while more than two population were analyzed F-test (ANOVA) to be used.

Significance test results are quoted as two-tailed probabilities. Significance of the obtained results was judged at the 5% level.

Results

Demonstrates demographic data of the included patients. Mean age 59.4 ± 11.123. All patients were right-handed, Male 37.1%, female 62.9%, Mean body mass index (BMI) 32.2 ± 8.2. majority were manual workers (55.1%). Presents the incidence of shoulder impingement with different sexes. No significant relationship between shoulder impingement and sex (Tables 1 and 2).

Table 1: Demographic and clinical data of the studied group.

Table 2: Relation between incidence of sex and shoulder impingement.

Demonstrates the relationship between shoulder impingement, BMI, age and HgA1c, with positive significant relationship between BMI, age, and HgA1c (Table 3).

Table 3: Relation between age, BMI, HgA1c and shoulder impingement.

Presents the relationship between different categories of HgA1c and shoulder impingement. HgA1c <5.5 has the fewest patients (7.3%), highest number of patients with HgA1c 5.5- 6.0. significant incidence of shoulder impingement with rising category of HgA1c with highest among Hga1c >7 (p=0.0001) with significant bilateral disease (Table 4).

Table 4: Relation between HgA1c category and shoulder impingement.

Demonstrates the incidence of shoulder impingement among diabetics and non-diabetics. Significant incidence of shoulder impingement (unilateral or bilateral among diabetics (HgA1c >6) compared to non- diabetics (p=0.011) (Table 5).

Table 5: Relation between incidence of diabetes mellitus and shoulder impingement.

Discussion

This study was aimed to evaluate the incidence of diabetes mellitus and prediabetes among patients diagnosed with shoulder impingement syndrome. We have used HgA1c as a qualifying measure for the diabetic status and related the incidence of shoulder impingement to different categories of HgA1c. There was significantly high incidence of shoulder impingement with rising levels of HgA1c. Also, the laterality of the disease significantly increased with the rising categories of HgA1c. The categories of HgA1c that represents prediabetes still have shown significant high incidence of shoulder impingement syndrome. Whereas HgA1c below 5.5 showed non- significant occurrence of shoulder impingement, which actually could highly suggest cause effect relationship between diabetes mellitus and shoulder impingement syndrome.

In this study, there was significant relationship between incidence of shoulder impingement and BMI and age but not with sex.

Regarding risk factors of shoulder impingement, Sayamapanathan et al. in their study suggested that male gender, age and hand dominance are among the risk factors of rotator cuff tendinopathy [18].

In this study, there was significant relationship between BMI and different categories of HgA1c and shoulder impingement syndrome.

Wendelboe et al. concluded in his study to evaluate the association between body mass index and surgery for rotator cuff tendinitis, that there is association between obesity and shoulder repair surgery in men and women who are fifty-three to seventy -seven years of age and body mass index represent a risk factor for rotator cuff tendinitis [19].

Sisodia et al. reported significant correlation between body mass index and glycemic control as measured by HgA1c in type 2 DM [20].

Gumina et al. reported significant association between body fat, body mass index and rotator cuff tear, but did not explain the possible underlying etiological factors [21].

Revising literature, there is high prevalence of shoulder disorders among diabetic patients and it is considered the highest musculoskeletal complications [22].

The pathogenic mechanisms of chronic tendinopathy are not fully understood and several major non-mutually exclusive hypotheses including activator of hypoxia-apoptosis- pro-inflammatory cytokines cascade, Neurovascular ingrowth, increased production of neuro-mediators and erroneous stem cell differentiation have been proposed. Diabetes is important risk factors [23].

BMI the suggested mechanism of shoulder impingement or rotator cuff tendinopathy in case of diabetes mellitus due to various modification of connective tissue ranging from glycosylation of protein with accumulation of advanced glycation end products (AGEs) to microvascular damage of blood vessels and nerves and deposition of extracellular matrix protein in the skin and periarticular tissue. This could potentially affect tendon strength and repair and play a role in microvascular complication and inflammation [1,2,8,9].

Leong et al. conducted meta-analysis and concluded that age above 50 years, diabetes and overhead activities were associated with increased risk of rotator cuff tendinopathy [24].

In this study, we have chosen HgA1c as a measure of the diabetic status.Revising literature regarding HgA1c, and how accurate it is as a tool to measure the diabetic status;Hemoglobin A1c is the measurement of glycosylated hemoglobin and can aid in both the diagnosis and continued management of diabetes mellitus. Accurate Hg A1c is an essential part of decision making in the diagnosis and treatment of type 2 diabetes. Although national standards exist to eliminate technical error with HgA1c testing.

Multiple errors whether elevated or decreased HgA1c sometimes happen. Also, some variation with ethnicity and even normal aging have been reported [25].

Another study to assess the accuracy of HgA1c suggested that hgA1c >6.5 demonstrates a moderate agreement with fasting glucose and 2-hour post prandial for diagnosing diabetes among adult Italian Caucasian subjects [26].

Another study comparing between HgA1c and fructosamine which of them is better index of glycemic control in type ii diabetes, serum fructosamine assay can better reflect average blood glucose concentration over the previous 3-6weeks and Hg A1c is better reflective over the previous 8-10 weeks. HgA1c measurement correlate more significantly with home capillary blood glucose levels than the fructosamine assay, even over the previous 2-3 weeks [27].

Another study assessed how A1c reflect glycemic control, it evaluated whether interindividual heterogeneity in the erythrocyte transmembrane glucose gradient might explain discordances between A1c and glycemic control based on measured fractosamine. They concluded that interindividual heterogeneity in glucose gradients across RBC membranes that affect hemoglobin glycation and have implication for diabetes complication risk and risk assessment [28].

Among adults in China, the estimated overall prevalence of Diabetes was 10.9% and that for prediabetes was 35.7% difference from previous estimate for 2010 may be due to an alternate method of measuring HgA1c [29].

Regarding Pre-diabetes (intermediate hyperglycemia) is a high- risk state of diabetes that is defined by glycemic variables that are higher than normal but lower than diabetes thresholds [30].

In this study we had detected significant incidence of shoulder impingement among the categories of patients’ prediabetes status, this suggests that the musculoskeletal complications of diabetes particularly shoulder impingement syndrome could take place prior to the discovery of overt diabetic status.

In conclusion; High incidence of DM/prediabetes among shoulder impingement patients. Level of HgA1c significantly proportionate to incidence and laterality. This suggests that it is part of musculoskeletal complication of DM. that can evidently occur with prediabetes status. Body mass index and age significantly affected the incidence but not the sex.

Conclusion

High incidence of DM/prediabetes among shoulder impingement patients. Level of HgA1c significantly proportionate to incidence and laterality. This suggests that it is part of musculoskeletal complication of DM. that can evidently occur with prediabetes status. Body mass index and age significantly affected the incidence but not the sex.

References

1. Al-Homood IA. Rheumatic conditions in patients with diabetes mellitus. Clin Rheumatol. 2013;32(5):527-533.
2. Lebiedz OD, Kaj J. Rheumatic manifestations of diabetes mellitus. Rheum Dis Clin North Am. 2010;36(4):681-699.
3. Gauri LA, Fatima Q. Musculoskeletal manifestations of diabetes mellitus. J Indian Med Assoc. 2009;107(11):819-821.
4. Arkkila PE, Gautier JF. Musculoskeletal disorders in diabetes mellitus: An update. Best Pract Res Clin Rheumatol. 2003;17(6):945-70.
5. Philipp T, Franekova L, Vnitr Lek. Musculoskeletal manifestations of diabetes mellitus. 2006;52(7-8):742-747.
6. Parada-Turska J, Majdan M. The musculoskeletal system in diabetic patients. Postepy Hig Med Dosw. 2005;59:236-244.
7. Adriaanse Mc, Drewes HW, Van der Heide I, Struys JN, Boan CA. The impact of co- morbid chronic conditions on quality of life in type 2 diabetes patients. Qual life Res. 2016;25(1): 175.
8. Huang Sw, Wang WT, Chou LC, Liou TH, Chen YW, Lin HW. Diabetes Mellitus increases the risk of rotator cuff tear repair surgery. A population-based cohort study. J Diab Compl. 2016;30(8):1473.
9. Broronlee M, Cerami A, Vlassara H. Advanced glycosylation end products in tissue and the biochemical basis of diabetic complications. N Engl J Med. 1988;318(20):1315
10. Mavrikakis ME, Drimis S, Kontoyannis DA, Rasidakis A, Moulopoulou ES, Kontoyannis S. Calcific shoulder periarthritis (tendinitis) in adult onset diabetes mellitus: A controlled study. Ann Rheum Dis. 1989:48(3);211-214.
11. Hioteng L, Chuen FUS, Xin He, Ham Oh J, Nobuyuki Y, Shu H. Risk factors for rotator cuff tendinopathy: A systemic review and meta -analysis. J Rehabil Med. 2019;4;51(9):627-637.
12. 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(6):487.
13. Shen PC, Chang PC, Jou IM, Chen CH, Lee FH, Hsieh JL. Hand tendinopathy risk factors in Taiwan: A population -based cohort study. Medicine (Baltimore). 2019;98(1):e13795.
14. Lannotti JP, Bernot MP, Kullman JR, Kelley MJ, Williams GR. Post-operative assessment of shoulder function: A prospective study of full thickness rotator cuff tears. J shoulder Elbow Surg. 1996;5(6):449.
15. Dela RTL, Wang Aw, Zheng MH. Tendinosis of the rotator cuff a review. J Musculoskel Res. 2001;5:143.
16. Garving C, Jakob S, Bauer I, Nadjar R, Brunner UH. Impingement syndrome of the shoulder. Dtsch Arztebl Int. 2017;114(45):765-776.
17. Billi A, Acatalucci, Barile A, Masciocchi C. Joint impingement syndrome. Clinical features. Eu J Radiol. 1998;27(1):s39-41.
18. Sayamapanathan AA, Andrew THC. Systemic review on risk factors of rotator cuff tears. J Orthop Surg (Hong Kong). 2017;25(1):2309499016684318.
19. Wendelboe AM, Hegmann KT, Gren LH, Alder SC, White Jr GL, Lyon JL. Assocaition between body mass index and surgery for rotator cuff tendinitis. J bone Joint Surg. AM. 2004;86(41):743-747.
20. Sisodia RK, Chouhan M. The study of correlation between Body Mass Index and glycemic control-HbA1c in diabetes type 2 patients. Int J Adv Med. 2019;6(6):1788-1791.
21. Gumina S, Candela V, Passaretti D, Latino G, Venditto T, Mariani L, et al. The association between body fat and rotator cuff teat: The influence on rotator cuff tear sizes. J Shoulder elbow surg. 2014; 23(11):1669-74.
22. Alsubheen SA, Mac Dermid JC, Overend TJ, Faber KJ. The diabetic shoulder- A literature review. J Diabetes Clin Res. 2019;(2):59-70
23. Lui PPY. Tendinopathy in diabetes mellitus patients-Epidemiology, Pathogenesis and management. Scand J Med Sci Sports. 2017;27(8):776-787.
24. Leong HT, Fu SC, He X, Oh JH, Yamamoto N, Hang S.  Risk factors for rotator cuff tendinopathy: A Systemic review and meta-analysis. J Rehabil Med. 2019;51(9):627-637.
25. Shepard JG, Airee A, Dake AW, McFarland M, Vora A. Limitation of A1c Interpretation. South Med J. 2013;108(12):724-9.
26. Marini MA, Succurre E, Arturi F, Ruffo MF, Andreozzi F, Sciacqua A, et al. Comparison of A1c , fasting and 2-h post load plasma glucose criteria to diagnose diabetes in Italian  Caucasians. Nutr Metab Cardiovasc Dis. 2012;22(7):561-6.
27. Chen HS, Chen RL, Chang ZY, Da Li H, et al. A comparison of fructosamine and HgA1c for home self monitoring blood glucose levels in type 2 diabetes. Zhi (Taipei). 2002;65(4):151-155.
28. Khera PK, Joiner CH, Carruthers A, Lindsell CJ, et al.  Evidence for interindividual heterogeneity in the glucose gradient across the human red blood cell membrane and its relationship to hemoglobin glycation. Diabetes. 2008;57(9):2445-52.
29. Wang L, Gao P, Zhang M, Huang Z, Zhang D, Deng Q, Li Y, et al. Prevalence of ethnic pattern of diabetes and prediabetes in  China in 2013. JAMA. 2017;317(24):2515-2523
30. Tabak AG, Herder C, Rathmann W, Brunner EJ, Kivimaki M. Prediabetes: A high -risk state for diabetes development. Lancet. 2012;379(9833):2279-2290.