|Year : 2016 | Volume
| Issue : 4 | Page : 151-156
Study of musculoskeletal disorders in a cohort of Egyptian diabetic patients and its relation to glycemic control
Amir A Youssef1, Adel A Shabana1, Mohammed K Senna1, Alaa M Wafa2, Manar M Elshewehy3
1 Department of Rheumatology and Rehabilitation, Faculty of Medicine, Mansoura University Student Hospital, Mansoura University, Mansoura, Egypt
2 Department of Internal Medicine, Faculty of Medicine, Mansoura University Student Hospital, Mansoura University, Mansoura, Egypt
3 Department of Rheumatology and Rehabilitation, Mansoura University Student Hospital, Mansoura University, Mansoura, Egypt
|Date of Submission||01-Nov-2016|
|Date of Acceptance||02-Dec-2016|
|Date of Web Publication||8-Mar-2017|
Manar M Elshewehy
Rehabilitation and Rheumatology, Department of Rheumatology and Rehabilitation, Mansoura University Student Hospital, Mansoura University, Suez Canal Street, Mansoura, 35111
Background Diabetes mellitus (DM) affects the musculoskeletal (MSK) system, resulting in significant morbidity. These manifestations are unrecognized, though they are found in daily practice.
Aim To study the effect of DM on the MSK system and the prevalence of these MSK disorders among Egyptians.
Patients and methods In total, 100 patients with type 1 DM, 100 patients with type 2 DM, and 100 normal controls were examined for different types of MSK disorders. Fasting and postprandial blood glucose, glycosylated hemoglobin, and lipid profile testings were done for patients and controls. Plain radiography of the dorsolumbar region and ankle joint and nerve conduction study of the median nerve were done in some selected cases.
Results These MSK manifestations were found in patients with types 1 and 2 DM, and their prevalence rates are as follows: carpal tunnel syndrome (14 and 5%, respectively), sclerodactyly (9 and 3%, respectively), Charcot joint (2 and 4%, respectively), limited joint mobility (2 and 6%, respectively), stenosing tenosynovitis (1 and 5%, respectively), shoulder capsulitis (1 and 10%, respectively), diffuse idiopathic skeletal hyperostosis (0 and 3%, respectively) and Dupuytren’s contracture (0 and 1%, respectively). MSK manifestations were more prevalent in patients with longer disease duration, poor glycemic control, and higher levels of lipid profile.
Conclusion The result of this study emphasizes the importance of glycemic control and its relation to MSK manifestations, in addition to the new finding that elevated levels of low-density lipoprotein are significantly related to MSK manifestations.
Keywords: diabetes mellitus, glycemic control, musculoskeletal manifestations
|How to cite this article:|
Youssef AA, Shabana AA, Senna MK, Wafa AM, Elshewehy MM. Study of musculoskeletal disorders in a cohort of Egyptian diabetic patients and its relation to glycemic control. Tanta Med J 2016;44:151-6
|How to cite this URL:|
Youssef AA, Shabana AA, Senna MK, Wafa AM, Elshewehy MM. Study of musculoskeletal disorders in a cohort of Egyptian diabetic patients and its relation to glycemic control. Tanta Med J [serial online] 2016 [cited 2018 Mar 24];44:151-6. Available from: http://www.tdj.eg.net/text.asp?2016/44/4/151/201725
| Introduction|| |
Diabetes mellitus (DM) is a chronic metabolic disease of high morbidity and mortality, which has become a public health problem . DM is characterized by the presence of hyperglycemia owing to defective insulin secretion, defective insulin action, or both . The commonest endocrinal arthropathies are musculoskeletal (MSK) complications of DM, which have been underestimated and poorly treated when compared with other diabetic complications . Limited joint mobility (LJM), Dupuytren’s contracture (DC), carpal tunnel syndrome (CTS), diabetic muscle infarction (DMI), and diffuse idiopathic skeletal hyperostosis (DISH) syndrome are examples of MSK manifestations occurring in diabetic patients .
| Patients and method|| |
Overall, 100 patients with type 1 diabetes mellitus (T1DM), 100 patients with type 2 diabetes mellitus (T2DM), and 100 age-matched and sex-matched normal controls were examined for the following types of MSK disorders:
- Diabetic sclerodactyly, which is defined as thickening of the skin on the dorsal surface of the hand, associated with LJM in the absence of Raynaud’s phenomenon, calcinosis, and telangiectasia to differentiate from scleroderma.
- Flexor tenosynovitis or stenosing tenosynovitis or trigger finger, which is diagnosed by palpating a nodule or thickened flexor tendon with locking phenomenon during finger flexion or extension.
- DC is diagnosed by the presence of one of the following features: a palmar or digital nodule; tethering of palmar or digital skin; a pretendinous band and a digital flexion contracture; and palpable thickening of the palmar fascia, with a flexor deformity of the second, third, fourth, or fifth finger.
- CTS, which is defined as weakness or pain in the hand, evidence of thenar atrophy, or nocturnal paresthesia of the thumb, index, and long fingers, with or without a positive Tinel’s or Phalen’s sign. CTS was excluded if other causes, such as thyroid disease, acromegaly, or C5/C6 radiculopathy, were suspected. A history of surgery was considered as an evidence of the disease. Confirmatory nerve conduction study was done for 28 patients who had clinical suspension suggestive of CTS.
- Diabetic cheiroarthropathy or LJM, which is diagnosed by the ‘prayer’s sign’ in which the patient was asked to approximate the palmar surfaces of their interphalangeal joints, with the fingers fanned out and the wrist maximally extended. If they were unable to do so, the test was considered positive.
- Frozen shoulder or adhesive capsulitis was considered when patients reported unilateral shoulder pain for at least 1 month, an inability to lie on the affected shoulder, and limited active and passive shoulder joint movement of less than 50% in at least three planes were found.
- Charcot joint or neuropathic arthropathy, which is defined as painless swelling and deformity of the weight-bearing joints with the classical finding of articular surface destruction, dislocation, disorganization, and increased bone density of the involved joint on radiographs. Charcot joint is suspected in long-standing diabetic patients with peripheral neuropathy with repeated trauma to the affected joint. The affected joint at first is hot, red, swollen, and painful. Later on, the affected joint is painless, but there will be deformity, and the most common joint to be affected is the ankle.
- DISH syndrome, which is diagnosed based on the classification criteria set by Resnick and Niwayama , which requires radiographically recognized bridges connecting at least four contiguous vertebrae of the thoracic spine, with preservation of the intervertebral disc space and absence of apophyseal joints or sacroiliac inflammatory changes. Plain radiograph of the dorsolumbar spine was done only for patients complaining of back pain (86 patients). It occurs mostly in long-standing T2DM. It affects male more often than female individuals. It is clinically suspected in obese male patients older than 40 years with long-standing T2DM complaining of back pain.
- Reflex sympathetic dystrophy, which is defined as unilateral, localized, or diffused pain associated with swelling or trophic changes and vasomotor disturbance with impaired mobility of the affected limb.
- Diabetic amyotrophy, which is defined as wasting of the proximal upper or lower extremity muscles or the paraspinal muscles proceeded by severe pain and decreased sensation of the involved part.
- DMI, which is defined as a palpable painful mass with swelling and induration of the surrounding tissue without systemic symptoms, in addition to evidence of edema in the muscle on MRI. A history of surgery for removal of DMI was also considered as evidence of the disease.
All patients and control underwent the following:
- History taking and demographic data collection: age, sex, residence, occupation, onset of the disease, current medication for DM, and other diseases, if any.
- General examination: height, weight, BMI, and waist circumference (WC).
- Fasting plasma glucose (FPG) and postprandial blood glucose.
- Plain radiograph of the dorsolumbar region and ankle joint and nerve conduction study of the median nerve were done for some selected cases.
Glycosylated hemoglobin (HbA1c) and lipid profile [cholesterol, high-density lipoprotein, low-density lipoprotein (LDL), and triglycerides] tests was done for all patients.
| Results|| |
[Table 1] shows the number and percentage of MSK manifestations found in each group of patients and the total number and percentage of all cases and their significant value. It was noticed that CTS was the most frequently found MSK manifestation in patients with T1DM (14%), whereas shoulder capsulitis was the most frequently found MSK manifestation in patients with T2DM (10%).
|Table 1 Musculoskeletal manifestations found in patients with their percentages|
Click here to view
[Table 2] shows the relation between different variables affecting the presence of MSK manifestation of DM in both groups and their significant value. It is noticed that variables like age, BMI, and WC have more effect on the development of MSK manifestations in patients with T2DM than in patients with T1DM, whereas variable like duration of the disease has more effect on patients with T1DM than those with T2DM.
|Table 2 Relation between age, body mass index, waist circumference, fasting plasma glucose, postprandial blood glucose, duration of the disease, glycosylated hemoglobin, and lipid profile and presence or absence of musculoskeletal manifestations in both type 1 diabetes mellitus and type 2 diabetes mellitus|
Click here to view
[Table 3] shows that duration of the disease. HbA1c and LDL are the most important variables that affect the occurrence of MSK manifestations in all diabetics.
[Table 4] shows that duration of the disease. HbA1c and LDL are the most important variables that affect the occurrence of MSK manifestations in patients with T1DM.
|Table 4 Multivariate stepwise regression analysis for type 1 diabetes mellitus|
Click here to view
The duration of the disease and FPG are the most important variables that affect the occurrence of MSK manifestations in patients with T2DM as shown in [Table 5].
|Table 5 Multivariate stepwise regression analysis for type 2 diabetes mellitus|
Click here to view
| Discussion|| |
We have found that the following MSK manifestations are more common to occur in diabetics than in other population: CTS 19% (14% in T1DM and 5% in T2DM), sclerodactyly 12% (9% in T1DM and 3% in T2DM), shoulder capsulitis 11% (1% in T1DM and 10% in T2DM), LJM 8% (2% in T1DM and 6% in T2DM), Charcot joint 6% (2% in T1DM and 4% in T2DM), trigger finger 6% (1% in T1DM and 5% in T2DM), DISH syndrome 3% (0% in T1DM and 3% in T2DM), and DC 1% (0% in T1DM and 1% in T2DM). Most of these MSK manifestations are more commonly found in T2DM which may be because of various factors like age, as T2DM patients were older; BMI and WC, as T2DM patients were more obese than T1DM patients; glycemic control, as T2DM patients had more elevated FPG and postprandial blood sugar levels and also more elevated HbA1c levels; and lastly, hyperlipidemia may plays a role, as T2DM patients had more elevated values of lipid profile. Also a combination of all these factors may be the cause of existence of all of these MSK manifestations. Another hypothesis is that insulin has a protective role against development of all of these MSK manifestations, which is why their occurrence is less in patients with T1DM. On the contrary, sclerodactyly and CTS are more developed in patients with T1DM than in those with T2DM. The only variant that is more elevated in T1DM than in T2DM is the disease duration. So, this may indicate that sclerodactyly and CTS are more affected by disease duration rather than other factors affecting the patients.
Arkkila and Gautier  have stated that the precise etiology of DM-associated periarticular changes remains doubtful; there is evidence that abnormal collagen deposition in the periarticular connective tissues alters the composition of structural matrix and the mechanical characters of these tissues. Diabetic complications (such as dysautonomia in neuropathic arthropathy) seem to be the cause of some MSK manifestations, and some share pathological mechanisms with microvascular disease. Genetic factors would be etiologically associated with MSK disorders in DM patients, but there is not enough data to support this hypothesis.
Attar  has stated that MSK manifestations were diagnosed in 17.9% of the patients. MSK disorders were more common in patients with T2DM (91.1%) than in those with T1DM (8.9%). The manifestations were CTS in 6.7% of the patients, shoulder capsulitis in 6.7%, diabetic amyotrophy in 4.8%, flexor tenosynovitis in 4.4%, diabetic cheiroarthropathy in 3.2%, and diabetic sclerodactyly in 2%. DC, DMI, neuropathic arthropathy, and DISH syndrome were found in 0.4%. None of the patients had reflex sympathetic dystrophy. Agrawal et al.  have found in their study that 57.01% of the total number of patients had rheumatologic manifestations, and these manifestations predominated more often among T1DM patients. DISH syndrome was present in 13% of the patients, and they all had T2DM. Frozen shoulder was present in 20% of the patients, and it was found to occur more frequently in T2DM patients. DC was present in 7.2% of the patients, most of them had T1DM. Neuroarthropathy was present in 2.9% of the patients, and most of them were T2DM patients. In case of chieroarthropathy, it was present in 22.6% of the patients, and it occurs more frequently in T1DM patients. Flexor tenosynovitis was present in 8.1% patients, and most of them had T1DM. Sarkar et al.  have found in their study that adhesive capsulitis was seen in 17.9% of diabetics compared with 7% in control group. Diabetic hand syndrome was seen in 13.1% of diabetics but was not observed in the control group. DC was noted in 46.7% of diabetics compared with 17% of control. DISH syndrome was seen in 28.7% of diabetics compared with only 2.5% of control. Neuroarthropathy was seen in 3.2% diabetic compared with 0.6% in control.
Bhowmik and Upadhyaya  stated that CTS is a type of entrapment neuropathy that occurs owing to compression of the median nerve between the carpal ligament and other surrounding structures as it passes in the carpal tunnel. The classical clinical picture includes pain and numbness and tingling of the thumb, index, and middle finger and along the medial aspect of the ring finger. The physical examination of CTS includes the following: the ‘shaking sign’, in which symptoms disappear after vigorous flapping of the hands; Tinel’s sign, in which percussion on the median nerve aggravates pain resembling an electric sensation along the course of the median nerve; and Phalen’s test (wrist dorsiflexion) in which the patient holds the hands against each other in full palmar flexion, and numbness begins between 30 and 120 s in this fixed position.
Al-Homood  reported that increased prevalence of CTS among diabetics is explained by the presence of intrinsic nerve pathology in addition to mechanical compression. These intrinsic nerve factors include loss of normal regenerative ability in the peripheral nerve because of microangiopathy, macrophage dysfunction, abnormalities in the retrograde cell body reaction, Schwann cell dysfunction, or decreased expression of neurotrophic factors and their receptors. Swelling of the median nerve and increased signal intensity on T2-weighted images will be demonstrated by MRI, which indicates accumulation of the axonal transportation, myelin sheath degeneration, or edema, which are the signs that should be found to diagnose CTS.Smith et al.  reported that adhesive capsulitis can be diagnosed clinically by progressive, agonizing limitation of shoulder movement, especially external rotation and abduction. The joint capsule becomes thick and firmly adherent to the humeral head, which results in marked reduction in the capacity of the glenohumeral joint. The disease progresses into three distinct phases: painful phase, then adhesive phase, and lastly resolution phase.
Garcilazo et al.  have found that there are three theories explaining the pathophysiology of shoulder capsulitis. The first hypothesis states that there is inflammation in the synovium and presence of inflammatory cytokines with subsequent fibrosis. The second one supposes that the disease would be the result of an algoneurodystrophic process. Last hypothesis is based on the histopathologic changes like fibroblast proliferation followed by cellular transformation to myofibroblasts that results in characterizing fibrosing condition rather than an inflammatory disorder like DC.
Gameiro Silva and Skare  stated that diabetic sclerodactyly is characterized by skin changes (thick, rigid, and waxy skin) which are similar to that occurring in scleroderma. Arterial calcification is a frequent radiological finding. Dermal thickening, collection of connective tissue in the reticular dermis with increased collagen cross-linking, and small amounts of mucin are commonly seen on histological examination. These skin changes should be differentiated from those of scleroderma, by absence of the following pathological findings: Raynaud’s phenomenon, dermal atrophy, telangiectasia, and autoantibodies. The longer the duration of DM, the more frequent the development of skin changes, although they have also been reported in children with recent-onset DM.
A multivariate stepwise regression analysis was done for all patients to find out which is the most important factor affecting the development of MSK manifestations of DM, and it was found that glycemic control assessed by HbA1c is the most important factor (odds ratio: 2.23) followed by duration of the disease (odds ratio: 1.24) and lastly LDL (odds ratio: 1.02). Then multivariate stepwise regression analysis was done for T1DM patients only to find out which is the most important factor affecting the development of MSK manifestations in T1DM, and it was found that glycemic control assessed by HbA1c is the most important factor (odds ratio: 2.44) followed by duration of the disease (odds ratio: 1.24) and lastly LDL (odds ratio: 1.02). Lastly, multivariate stepwise regression analysis was done for T2DM patients only to find out which is the most important factor affecting the development of MSK manifestations in T2DM, and it was found that duration of the disease (odds ratio: 1.275) is the most important factor followed by FPG levels (odds ratio: 1.013).
| Conclusion|| |
MSK manifestations of DM are the most common endocrinal-related arthropathies, yet still under recognized and poorly treated. These manifestations are linked to multiple variants like age of the patients, duration of the disease, glycemic control, and the new interesting finding of elevated LDL levels. Further research is needed to emphasize this genuine finding.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Gameiro Silva MB, Skare TL. Musculoskeletal disorders in diabetes mellitus. Rev Bras Reumatol 2012; 52:594–609.
Goldenberg R, Punthakee Z. Definition, classification and diagnosis of diabetes, prediabetes and metabolic syndrome. Can J Diabetes 2013; 37:8–11.
Attar SM. Muscloskeletal manifestations of diabetic patients at a tertiary center. Libyan J Med 2012; 7:19162–19169.
Resnick D, Niwayama G. Diagnosis of bone and joint disorders. 2nd ed. Philadelphia, PA: WB Saunders; 1988. pp. 1563–1615.
Arkkila PET, Gautier J-F. Musculoskeletal disorders in diabetes mellitus: an update. Best Pract Res Clin Rheumatol 2003; 17:945–970.
Agrawal RP, Gothwal S, Tantia P, Agrawal R, Rijhwani P, Sirohi P, Meel JK. Prevalence of rheumatological manifestations in diabetic population from North-West India. J Assoc Physicians India 2014; 62:788–792.
Sarkar RN, Banerjee S, Basu AK, Bandyopadhyay D. Rheumatological manifestations of diabetes mellitus. J Indian Rheumatol Assoc 2003; 11:25–29.
Bhowmik M, Upadhyaya S. Rheumatic manifestations in diabetes mellitus patients. Apollo Med 2013; 10:126–133.
Al-Homood IA. Rheumatic conditions in patients with diabetes mellitus. Clin Rheumatol 2013; 32:527–533.
Smith LL, Burnet SP, McNeil JD. Musculoskeletal manifestations of diabetes mellitus. Br J Sports Med 2003; 37:30–35.
Garcilazo C, Cavallasca JA, Musuruana JL. Shoulder manifestations of diabetes mellitus. Curr Diabetes Rev 2010; 6:334–340.
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]