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Rheumatology Advance Access originally published online on August 18, 2008
Rheumatology 2008 47(10):1583-1586; doi:10.1093/rheumatology/ken333
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© The Author 2008. Published by Oxford University Press on behalf of the British Society for Rheumatology. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Predictors of shoulder pain and shoulder disability after one year in diabetic outpatients

L. L. Laslett1, S. P. Burnet1, C. L. Redmond1 and J. D. McNeil1

1The University of Adelaide Discipline of Medicine, Modbury Hospital, Modbury, Australia.

Correspondence to: L. L. Laslett, The University of Adelaide Discipline of Medicine, Modbury Hospital, Smart Road, Modbury, SA 5092, Australia. E-mail: laura.laslett{at}adelaide.edu.au


   Abstract
Top
 Abstract
Introduction
 Methods
 Results
 Discussion
 Conclusion
 Acknowledgements
 References
 
Objective. To investigate factors associated with changes in shoulder pain and disability in diabetic outpatients over 1 yr.

Methods. Cross-sectional study with 12-month follow-up in diabetic outpatients (n = 179) using the shoulder pain and disability index (SPADI) and SF-36 version 2.

Results. Patients with diabetes and shoulder pain or disability are more likely to be older and female. After 12 months of follow-up, one-quarter of participants without pre-existing symptoms at baseline developed clinically significant pain (28%) or disability (25%). Of the patients with pre-existing shoulder pain or disability, half reported clinically significant worsening (10 percentage points) in shoulder pain (58%) or disability (45%) over 12 months. Few patients demonstrated clinically significant improvement in pain (11%) or disability scores (19%). The remaining one-third of the patients reported no change in symptoms (30% pain; 35% disability). Increasing intensity of pain scores between baseline and 12 months was associated with older age, higher HbA1c and less pain at baseline. Increasing disability score between baseline and 12 months was associated with having had eye laser surgery, greater pain at baseline and less disability at baseline.

Conclusion. Shoulder pain and disability are common, and persistent in adults with diabetes. Having higher HbA1c levels or having had treatment for retinopathy was associated with worsening shoulder pain and disability, confirming that glycaemic control and diabetic complications are associated with worsening shoulder pain or disability over 12 months of observation.

KEY WORDS: Diabetes mellitus, Shoulder pain, Shoulder disability, Musculoskeletal, Diabetic complications, Glycosylated haemoglobin, Diabetic retinopathy


   Introduction
Top
 Abstract
 Introduction
Methods
 Results
 Discussion
 Conclusion
 Acknowledgements
 References
 
Cross-sectional studies show that a number of factors are associated with shoulder pain and shoulder symptoms in patients with diabetes. These include advancing age [1], diabetes duration [1–4] and diabetes complications including retinopathy, albuminuria [2] and autonomic neuropathy [1], but not peripheral neuropathy [4]. Therefore, the relevant question for the treating clinician is which factor(s) determine persistence or worsening of pain and disability over time.

The link between shoulder pain or disability and diabetes is postulated to be excessive glycosylation of connective tissue, particularly collagen [5]. Patients who have had long-term intensive treatment of their diabetes have been shown to have lower levels of skin collagen glycosylation, glycoxidation and cross-linking [6], and slower rates of accumulation of advanced glycosylation end-points (AGEs) [7] than patients treated under conventional regimes. Elevation of AGEs have been associated with early stages of clinically evident nephropathy and retinopathy [8].

We aimed to investigate factors associated with change in shoulder pain and shoulder disability in patients with diabetes over 1 yr of follow-up.


   Methods
Top
 Abstract
 Introduction
 Methods
Results
 Discussion
 Conclusion
 Acknowledgements
 References
 
We conducted a cross-sectional study with follow-up after 6 and 12 months. Study patients were recruited from the diabetic outpatient clinic over 2002–03. Consecutive patients with and without shoulder symptoms were approached. Control patients were also recruited; investigations of factors common to diabetic and control patients have been reported elsewhere [9]. Ethical approval was obtained from Modbury Hospital's Research and Ethics Committee and was obtained according to the Declaration of Helsinki. All participants provided informed consent.

Data collection
Basic demographic information and information on shoulder symptoms were collected at baseline from case notes and interview. Glycaemic control was assessed using HbA1c. Diabetic complications were assessed using serum creatinine results and self-reported eye laser surgery as proxy markers for diabetic nephropathy and retinopathy. Consenters completed the Shoulder Pain and Disability Index (SPADI) questionnaires at baseline. A subset of patients also received the SF-36 version 2 (SF-36v2). Patients with current shoulder symptoms were offered a shoulder assessment by a rheumatologist (S.P.B.) to determine a clinical diagnosis of their shoulder symptoms. The most common clinical findings were rotator cuff pathology (31/40 patients), followed by frozen shoulder, found in 8/40 patients [9].

Instruments used
A shoulder-specific questionnaire (SPADI) [10] and a general quality of life questionnaire (SF-36v2) [11] were used. These questionnaires and their method of use are described elsewhere [9].

Statistical analysis
Microsoft Access (2000, Microsoft Corporation, Redmond, WA, USA), and Intercooled Stata 10.0 for Windows (2008, StataCorp, College Station, TX, USA) were used to collect and analyse data. Variables which had a statistically significant linear relationship with changes in shoulder pain and disability or quality of life over 12 months at the 25% level were included in a step-wise multiple regression [12] with a P-value for entry of 0.1 to obtain an optimum set of predictor variables. Regressions were refitted without a constant when the constant term was not significant.


   Results
Top
 Abstract
 Introduction
 Methods
 Results
Discussion
 Conclusion
 Acknowledgements
 References
 
Baseline cross-sectional data
Persons with shoulder pain or disability were more likely to be older women (P ≤ 0.05) (Table 1).


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  		TABLE 1. Baseline demographic and diabetic dataa at baseline by current shoulder symptoms

 
The average pain intensity increased between baseline and follow-up (P < 0.01). Differences on disability scores between baseline and follow-up were not statistically significant (P = 0.058). There was no difference in baseline pain score (P = 0.92) or baseline disability score (P = 0.77) between participants who did and did not return the questionnaire after 12 months.

Patients in our sample have relatively modest pain and disability at baseline with an average of 35/100 on pain and disability scores in symptomatic patients, compared with 50–65/100 in comparable studies of unselected patients with shoulder pain seeking treatment [13, 14].

One quarter of asymptomatic patients (SPADI pain scale or disability scale <10) developed clinically significant shoulder pain (28%) (95% CI 18.7, 39.6; n = 19) or shoulder disability (25%) (95%CI 16.0, 36.8; n = 16) after 12 months.

The majority of patients with pre-existing shoulder pain or disability (SPADI pain scale or disability scale ≥10) experienced clinically significant worsening after 12 months of follow-up, with 58% experiencing worsening pain (95% CI 43.3, 71.6; n = 25) and 45% experiencing worsening disability (95% CI 31.2, 60.1; n = 19). Eleven percent (95% CI 5.1, 24.5; n = 5) had less intense pain and 19% had lower disability scores (95% CI 10.0, 33.3; n = 8). The remaining one-third had stable pain (30%) (95% CI 18.6, 45.1; n = 13) or disability (35%) (95% CI 23.0, 50.8; n = 15).

Factors associated with change in shoulder pain over 12 months
The following factors were significantly associated with change in shoulder pain between baseline and 12 months of follow-up and were entered into a multiple linear regression: age, HbA1c, diabetes duration, having had eye laser surgery, baseline pain score, baseline mental quality of life and baseline physical quality of life. Few patients completed both the SPADI and the SF-36, and therefore variables obtained using the SF-36 were omitted due to the smaller numbers, even though inclusion of the SF-36 yielded models with better explanatory power. The patients completing the SF-36v2 were recruited early in the cohort, and there was no relationship between completion of the SF-36 and any demographic variables at the 5% level.

The final model for predicting change in pain score over 12 months (n = 110) included: HbA1c, age and baseline pain score (Table 2). The regression equation is: change in pain score over 12 months = (3.123 x HbA1c) + (0.340 x age) – (0.189 pain score at baseline) – 33.224. This accounted for 10% of the variation in the change in pain score.


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  		TABLE 2. Factors predicting change in pain and disability scales between baseline and 12 months of follow-up

 
Therefore, if two patients have the same baseline pain score, the patient with higher HbA1c is likely to see a greater increase in pain score over 12 months.

If two patients have the same HbA1c, the patient with the higher baseline pain score is likely to see a greater reduction in pain score over 12 months, and if two patients have the same HbA1c and pain score at baseline, the patient who is older is more likely to see a greater increase in pain score over 12 months. The extent of the change in pain score can be determined from the regression equation.

Factors associated with change in shoulder disability over 12 months
Variables which had a linear relationship with change in shoulder disability from baseline to 12-month follow-up of P < 0.25 were included in a multiple logistic regression. These were: gender, HbA1c, serum creatinine, having had eye laser surgery, pain score at baseline, disability score at baseline, and mental and physical quality of life (mental and physical component score) at baseline. As per pain score, SF-36 variables were not included in the final model.

The final model for predicting change in disability score over 12 months (n = 107) was: change in disability score over 12 months = 8.632 + [9.317 x eye laser surgery status (1 for yes and 0 for no)] + (0.610 x pain score at baseline) – (0.845 x disability score at baseline). This explained 28% of the variance.

Therefore, if two patients have the same pain and disability score at baseline, the patient who has had laser eye surgery is more likely to experience worsening of shoulder disability over 12 months; similarly, patients with a higher pain score at baseline, and patients with a lower disability score at baseline are more likely to experience worsening shoulder disability at 12 months.

In our cohort, having had laser eye surgery was associated with diabetes duration (r = +0.44, P < 0.001), and diabetes type (r = +0.30, P < 0.001).


   Discussion
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
Conclusion
 Acknowledgements
 References
 
Patients were more likely to experience increasing pain over 12 months if they were older, had worse HbA1c and less intense pain at baseline. They were more likely to experience increasing disability over 12 months if they had had eye laser surgery for retinopathy, more intense pain at baseline and less disability at baseline.

The higher proportion of women amongst patients with shoulder symptoms is consistent with other reports [3], but the underlying reason for this is unclear.

Higher HbA1c at baseline was associated with increases in pain score over 12 months; HbA1c was not associated with current shoulder symptoms at baseline. The fact that we used only one HbA1c result is unlikely to have affected the outcome at baseline as other studies have used average HbA1c over 4 yrs [3] and 5 yrs [1] with the same result. The period of exposure to high blood glucose levels required before the shoulder symptoms are evident may be much longer than period of glucose control that HbA1c measures (3–6 months). Some authors have hypothesized that overall glycaemic control, including in the years before those reflected in the available HbA1c levels is a determinant of the presence or absence of musculoskeletal symptoms (such as shoulder symptoms) in patients with diabetes [3]. Since Australian patients are diagnosed with diabetes an estimated 10 yrs after diabetes onset [15], this is a long period of time during which glycaemic control may be poor. A compatible explanation is that longer term indices of glycaemic control such as AGEs and glycated collagen from skin biopsies might be better predictors of diabetic complications since these have been found to correlate with early manifestations of renal and retinal disease in patients with type 1 diabetes [8], though these measures are more suited to research than regular clinical practice due to the more invasive nature of the test. Therefore, we conclude that control of blood sugar may play some role in evolving shoulder pain and/or disability, but that the relationship is not straightforward.

The association of worsening disability scores with having had laser eye surgery for retinopathy is very interesting. Arkkila et al. [1] found associations between retinopathy and prevalence of adhesive capsulitis in patients with type 1 diabetes (but not type 2). Adhesive capsulitis was strongly associated with duration of diabetes in both types 1 and 2 diabetes, but this disappeared after adjustment for age and diabetes duration [1]. Therefore, having had laser eye surgery might be a marker of disability, perhaps related to poor vision. Alternatively, having had laser eye surgery might be a composite measure of true diabetes duration (since diabetes may have been present for some years prior to diagnosis in patients with type 2 diabetes [15]) and long-term average blood glucose levels. Severe visual impairment (but not moderate visual impairment) has been associated with disability in patients with diabetes [16]. This disability related to activities of daily living in very vision-focused tasks such as housework or cooking meals. The disability items in the SPADI are not vision-focused; therefore, this is unlikely to explain the association between the laser eye surgery for retinopathy and disability score as measured by the SPADI.

The multiple regression models (Table 2) both retained at least one diabetes-specific factor. This validates the concept that having diabetes is an important factor in shoulder pain and disability; and that factors related to diabetes such as glycaemic control and diabetic complications are also important in shoulder function. We conclude that we are not simply looking at a group of people with shoulder problems who also happen to have diabetes.

We were unable to fully assess the role of mental quality of life in change in shoulder pain and disability due to the limited number of patients who completed the SF-36 in addition to the SPADI. We suggest that further research is needed on the role of mental quality of life in shoulder pain and disability. Also, there remain many unmeasured factors associated with changes in shoulder pain and shoulder disability in addition to quality of life that warrant further investigation.


   Conclusion
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusion
Acknowledgements
 References
 
Persons with diabetes and shoulder pain or shoulder disability were more likely to be older and females.

Patients who were older, had higher HbA1c, less intense shoulder pain at baseline and were more likely to experience worsening shoulder pain after 12 months. Patients who had undergone laser eye surgery for retinopathy, had more intense shoulder pain at baseline, less severe shoulder disability at baseline and were more likely to experience worsening disability over 12 months.

Glycaemic control and diabetic complications are associated with worsening shoulder pain and disability in outpatients with diabetes. Existing shoulder pain and disability are also important predictors of change in shoulder pain and disability over 12 months.

Formula


   Acknowledgements
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusion
 Acknowledgements
References
 
We would like to thank Dr T. Glynn, Dr H. Nicolson and Sr N. Price at the Diabetic Outpatient Clinic at Modbury Hospital, and Dr J. Field at the University of Adelaide Faculty of Health Sciences Statistical Support Service for his statistical analyses and comments on earlier drafts of this manuscript.

Funding: This study was supported by a research grant from the Modbury Hospital Foundation.

Disclosure statement: The authors have declared no conflicts of interest.


   References
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusion
 Acknowledgements
 References
 

  1. 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.[Abstract/Free Full Text]
  2. Sattar MA, Luqman WA. Periarthritis: another duration-related complication of diabetes mellitus. Diabetes Care (1985) 8:507–10.[Abstract]
  3. 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.[CrossRef][Web of Science][Medline]
  4. Bridgman JF. Periarthritis of the shoulder and diabetes mellitus. Ann Rheum Dis (1972) 31:69–71.[Free Full Text]
  5. Paul RG, Bailey AJ. Glycation of collagen: the basis of its central role in the late complications of ageing and diabetes. Int J Biochem Cell Biol (1996) 28:1297–310.[CrossRef][Web of Science][Medline]
  6. Monnier VM, Bautista O, Kenny D, et al. Skin collagen glycation, glycoxidation, and crosslinking are lower in subjects with long-term intensive versus conventional therapy of type 1 diabetes: relevance of glycated collagen products versus HbA1c as markers of diabetic complications. DCCT Skin Collagen Ancillary Study Group. Diabetes Control and Complications Trial. Diabetes (1999) 48:870–80.[Abstract]
  7. Salmela PI, Oikarinen AI, Ukkola O, et al. Improved metabolic control in patients with non-insulin-dependent diabetes mellitus is associated with a slower accumulation of glycation products in collagen. Eur J Clin Invest (1995) 25:494–500.[CrossRef][Web of Science][Medline]
  8. Beisswenger PJ, Makita Z, Curphey TJ, et al. Formation of immunochemical advanced glycosylation end products precedes and correlates with early manifestations of renal and retinal disease in diabetes. Diabetes (1995) 44:824–9.[Abstract]
  9. Laslett LL, Burnet SP, Jones JA, Redmond CL, McNeil JD. 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.[Web of Science][Medline]
  10. Roach KE, Budiman-Mak E, Songsiridej N, Lertratanakul Y. Development of a shoulder pain and disability index. Arthritis Care Res (1991) 4:143–9.[Medline]
  11. Ware JE Jr, Gandek B. Overview of the SF-36 health survey and the International Quality of Life Assessment (IQOLA) project. J Clin Epidemiol (1998) 51:903–12.[CrossRef][Web of Science][Medline]
  12. Hosmer DW, Lemeshow S. Applied logistic regression. (1989) New York: John Wiley & Sons, Inc.
  13. Williams JW Jr, Holleman DR Jr, Simel DL. Measuring shoulder function with the shoulder pain and disability index. J Rheumatol (1995) 22:727–32.[Web of Science][Medline]
  14. Shanahan EM, Ahern M, Smith M, Wetherall M, Bresnihan B, FitzGerald O. Suprascapular nerve block (using bupivacaine and methylprednisolone acetate) in chronic shoulder pain. Ann Rheum Dis (2003) 62:400–6.[Abstract/Free Full Text]
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Submitted 14 April 2008; revised version accepted 14 July 2008.
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