The Achilles tendon (AT) is the largest, toughest, and strongest tendon in the human body, formed when the aponeurosis of the soleus and gastrocnemius muscles combine(1). It extends from the myotendinous junction distally to its insertion site on the upper half of the posterior surface of the calcaneus. It is approximately 15 cm long and 6 mm thick(1). Tendinopathy is one of the musculoskeletal manifestations of diabetes mellitus. Diabetes mellitus (DM) causes pathological changes in the Achilles tendon, which could lead to structural or functional dysfunction or precipitate diabetic foot syndrome(2). Diabetic tendon damage is a complex, multifactorial process characterized by excessive accumulation of advanced glycation end products (AGEs), inflammatory response dysfunction, neurovascularization, peripheral neuropathy, and vasculopathy(2).
In keeping with the application of musculoskeletal ultrasonography to diverse clinical situations(3,4), the AT has also been assessed in DM patients using ultrasound and magnetic resonance imaging, and the findings included increased AT thickness and structural abnormalities(5–9).
Aside from the thickening of the AT(10), other features, like abnormal morphology (twisted, curved, overlapping, and highly disorganized fibers), and calcific degeneration have been identified as degenerative changes affecting the AT. These alterations may be present in the initial stages of type 2 diabetes (T2DM)(11). Since T2DM diagnosis is often made when some patients already have evidence of chronic complications, it implies that the effects of hyperglycemia would have been exerted for a while on tendon structures(11). Altered AT fibrillary pattern, the presence of hypoechoic areas, and calcific foci within the tendon are common degenerative abnormalities(12).
While the stiffness of the Achilles tendon is not directly measured on B-mode ultrasonography, changes such as thickening and echotexture alterations (which have been shown in kinematics studies to alter the foot loading pattern and pose a considerable risk for plantar ulcer)(13,14) can be readily assessed on ultrasound.
This study aims to determine and analyze the prevalence, pattern, and modifying factors (age, body mass index, coexisting peripheral neuropathy, diabetes duration) of diabetic degenerative Achilles tendinopathy in patients with type 2 diabetes mellitus in our locality.
Eighty (80) subjects with type 2 diabetes mellitus (T2DM) and 80 age/sex-matched controls were enrolled in this descriptive cross-sectional study. The ethics committee of the hospital approved the study protocol. All recruited participants gave written, informed consent.
All participants were ≥40 years old. The subjects were confirmed diabetic patients attending the endocrinology clinic of the hospital, while the controls were healthy volunteers with fasting blood glucose (FBG) of <6.1 mmol/L. Exclusion criteria were renal failure, dyslipidemia, history of peripheral vascular disease, smoking, Charcot neuroarthropathy, congenital ankle deformities, chronic heel pain, lower limb amputation, chronic steroid use, neurological disorders (besides those associated with DM), musculoskeletal diseases, rheumatoid disease, and bodybuilding(10).
The biodata, relevant clinical history, diabetes duration, and history of previous foot ulcers were documented. Weight, height, and body mass index (BMI) of the participants were recorded. A 10 g Semmes-Weinstein monofilament was used to assess for peripheral neuropathy (PN)(10). Fasting blood glucose (FBG; for the entire study population) and glycated hemoglobin (HbA1c; for diabetic subjects only) levels were determined using established standard methods(10). Fasting blood glucose (FBG) was categorized as <5.6 mmol/L, 5.6–6.9 mmol/L, and ≥7.0 mmol/L to represent good FBG, impaired FBG, and poor FBG control, respectively. A MINDRAY® model DC-7 ultrasound scanner (Shenzhen Mindray Bio-medical Electronics, Nanshan, Shenzhen, China) with a 7.5–12.0 MHz high-frequency linear array transducer was used for Achilles tendon sonography. The first author performed all ultrasound scans to reduce interobserver variability.
After adequate exposure of the leg by rolling up clothing up to the knees, Achilles tendon (AT) sonography was performed with the participant lying prone on the examination couch, with their feet projecting beyond the edge of the couch and pointing downward, and the ankle in the neutral position at an angle of 90 degrees (Fig. 1). The Achilles tendons of both legs were scanned in longitudinal and transverse planes from the myotendinous junctions to their insertion site on the calcaneus bones. The presence or absence of disorganization of the tendon fibers, hypoechoic foci, and calcifications was documented.
The study data were analyzed using the IBM SPSS Statistics for Windows version 20 (IBM Corp., Armonk, N.Y., USA). The normality of data was determined using the Kolmogorov-Smirnov test. Descriptive and inferential analyses were applied as appropriate. Chi-square test was used to detect the association between the categorical variables, while the independent samples t-test was used to compare the mean values of continuous quantitative variables. A
There were 80 type 2 diabetics (30 males and 50 females) and 80 non-diabetic controls (34 males and 46 females) matched for age and sex. The mean age of T2DM subjects and healthy controls was 60.9 ± 10.3 years (range 41–79 years) and 61.0 ± 10.3 years (range 40–79 years), respectively (
There was no significant difference between the mean BMI of the subjects (70.0 ± 12.1 kg/m2) and controls (67.0 ± 10.6 kg/m2);
Most (48.8%) of the diabetic subjects had poor FBG control, 31.2% had impaired FBG level, while 20.0% had good FBG control. Glycated hemoglobin (HbA1c) level was categorized as good (<7.0%) and poor (≥7.0%) glycemic control. Most T2DM subjects (51; 63.8%) had HbA1c level ≥7.0% while 29 (36.2%) had HbA1c <7.0%.
More T2DM subjects had right AT disorganized fibers (Fig. 2), which was 43/80 (53.8%) compared with 14 (17.5%) controls (
Variables | Study group, |
|
df |
|
|
---|---|---|---|---|---|
Diabetics ( |
Controls ( |
||||
|
|||||
Present | 4 (5.0) | 0 (0.0) | 0.120* | ||
Absent | 76 (95.0) | 80 (100.0) | |||
|
|||||
Present | 5 (6.3) | 2 (2.5) | 0.443* | ||
Absent | 75 (93.8) | 78 (97.5) | |||
|
|||||
Present | 43 (53.8) | 14 (17.5) | 22.919 | 1 |
|
Absent | 37 (46.3) | 66 (82.5) | |||
|
|||||
Present | 41 (51.3) | 12 (15.0) | 23.728 | 1 |
|
Absent | 39 (48.8) | 68 (85.0) | |||
|
|||||
Present | 16 (20.0) | 4 (5.0) | 8.229 | 1 |
|
Absent | 64 (80.0) | 76 (95.0) | |||
|
|||||
Present | 15 (18.8) | 6 (7.5) | 4.440 | 1 |
|
Absent | 65 (81.2) | 74 (92.5) | |||
|
|||||
Present | 44 (55.0) | 15 (18.8) | 22.581 | 1 |
|
Absent | 36 (45.0) | 65 (81.2) | |||
|
|||||
Present | 42 (52.5) | 15 (18.8) | 19.867 | 1 |
|
Absent | 38 (47.5) | 65 (81.2) |
AT hypoechoic foci (Fig. 3) in both feet were more common in T2DM patients than controls. Twenty percent of T2DM subjects had hypoechoic foci in their right AT, while only 5% of controls had this feature (
The presence of either of calcific foci, disorganized fibers, and/or hypoechoic foci in the right AT was compared between T2DM subjects and controls; the prevalence was significantly higher among T2DM subjects than controls (55.0% vs. 18.8%,
The mean age of those with disorganized AT fibers was significantly higher than the mean age of those without disorganized fibers (
Variables | Degeneration | t |
|
|
---|---|---|---|---|
Present | Absent | |||
AT disorganized fibers | ||||
|
63.8 ± 8.7 | 56.6 ± 11.0 | 3.132 | 0.003 |
|
26.44 ± 4.36 | 25.14 ± 4.67 | 1.272 | 0.207 |
|
8.7 ± 5.4 | 7.4 ± 2.4 | 1.409 | 0.163 |
|
8.7 ± 2.8 | 8.2 ± 2.4 | 0.853 | 0.396 |
|
67.0 (16.0–116.8) | 24.0 (6.0–61.8) | -2.294 | 0.022** |
|
||||
|
65.9 ± 7.2 | 59.7 ± 10.6 | 2.773 | 0.009 |
|
25.86 ± 4.72 | 25.94 ± 4.49 | -0.068 | 0.946 |
|
9.7 ± 7.3 | 7.8 ± 3.4 | 1.004 | 0.330 |
|
9.5 ± 3.0 | 8.3 ± 2.5 | 1.757 | 0.083 |
|
64.5 (28.5–103.0) | 37.5 (8.8–96.8) | -0.848 | 0.396** |
|
||||
|
65.5 ± 7.2 | 60.6 ± 10.5 | 1.134 | 0.260 |
|
27.87 ± 5.52 | 25.77 ± 4.42 | 1.100 | 0.275 |
|
7.9 ± 3.0 | 8.2 ± 4.6 | -0.144 | 0.886 |
|
9.3 ± 3.8 | 8.5 ± 2.5 | 0.508 | 0.632 |
|
65.0 (21.5–206.3) | 38.5 (7.5–96.3) | -1.042 | 0.298** |
|
||||
|
63.8 ± 8.7 | 56.5 ± 11.2 | 3.094 | 0.003 |
|
26.41 ± 4.32 | 25.15 ± 4.74 | 1.219 | 0.227 |
|
8.8 ± 5.4 | 7.3 ± 2.2 | 1.740 | 0.086 |
|
8.8 ± 2.8 | 8.0 ± 2.2 | 1.395 | 0.167 |
|
66.0 (17.0–116.5) | 23.0 (6.0–62.0) | -2.218 | 0.027** |
*
Variables | Diabetics’ |
|
df |
|
||
---|---|---|---|---|---|---|
AT disorganized fibr | ||||||
Present | Absent | Total | ||||
|
||||||
40–49 | 3 (20.0) | 12 (80.0) | 16 (100) | 12.315 | 3 |
|
50–59 | 11 (68.8) | 5 (31.3) | 16 (100) | |||
60–69 | 20 (69.0) | 9 (31.0) | 29 (100) | |||
70–79 | 14 (70.0) | 6 (30.0) | 20 (100) | |||
|
||||||
Male | 24 (80.0) | 6 (20.0) | 30 (100) | 8.000 | 1 |
|
Female | 24 (48.0) | 26 (52.0) | 50 (100) | |||
|
||||||
Normal | 19 (51.4) | 18 (48.6) | 37 (100) | 2.233 | 2 | 0.327 |
Overweight | 18 (69.2) | 8 (30.8) | 26 (100) | |||
Obese | 11 (64.7) | 6 (35.3) | 17 (100) | |||
|
||||||
<5 years | 20 (46.5) | 23 (53.5) | 43 (100) | 7.715 | 2 |
|
5–10 years | 17 (70.8) | 7 (29.2) | 24 (100) | |||
>10 years | 11 (84.6) | 2 (15.4) | 13 (100) | |||
|
||||||
Present | 41 (71.9) | 16 (28.1) | 57 (100) | 11.757 | 1 |
|
Absent | 7 (30.4) | 16 (69.6) | 23 (100) | |||
|
||||||
<5.6 (mmol/L) | 10 (62.5) | 6 (37.5) | 16 (100) | 0.059 | 2 | 0.971 |
5.6–6.9 (mmol/L) | 15 (60.0) | 10 (40.0) | 25 (100) | |||
≥7.0 (mmol/L) | 23 (59.0) | 16 (41.0) | 39 (100) | |||
|
||||||
Poor (HbA1c ≥7.0%) | 32 (62.7) | 19 (37.3) | 51 (100) | 0.442 | 1 | 0.506 |
Good (HbA1c <7.0%) | 16 (55.2) | 13 (44.8) | 29 (100) |
The prevalence rates of disorganized AT fibers among T2DM subjects with time interval since diagnosis of <5 years, 5–10 years, and >10 years were 46.5%, 70.8%, 84.6%, respectively (
The mean FBG level was higher among those with disorganized AT fibers at 8.7 ± 5.4 mmol/L compared with those without disorganized AT fibers at 7.4 ± 2.4 mmol/L (
Variables | Diabetics’ |
|
df |
|
||
---|---|---|---|---|---|---|
AT hypoechoic foci | ||||||
Present | Absent | Total | ||||
|
||||||
40–49 | 0 (0.0) | 15 (100.0) | 15 (100.0) | 0.060* | ||
50–59 | 2 (12.5) | 14 (87.5) | 16 (100.0) | |||
60–69 | 9 (31.0) | 20 (69.0) | 29 (100.0) | |||
70–79 | 5 (25.0) | 15 (75.0) | 20 (100.0) | |||
|
||||||
Male | 9 (30.0) | 21 (70.0) | 30 (100.0) | 3.000 | 1 | 0.083 |
Female | 7 (14.0) | 43 (86.0) | 50 (100.0) | |||
|
||||||
Normal | 7 (18.9) | 30 (81.1) | 37 (100.0) | 1.526 | 2 | 0.466 |
Overweight | 7 (26.9) | 19 (73.1) | 26 (100.0) | |||
Obese | 2 (11.8) | 15 (88.2) | 17 (100.0) | |||
|
||||||
<5 years | 6 (14.0) | 37 (86.0) | 43 (100.0) | 2.320 | 1 | 0.314 |
5–10 years | 7 (29.2) | 17 (70.8) | 24 (100.0) | |||
>10 years | 3 (23.1) | 10 (76.9) | 13 (100.0) | |||
|
||||||
Present | 15 (26.3) | 42 (73.7) | 57 (100.0) |
|
||
Absent | 1 (4.3) | 22 (95.7) | 23 (100.0) | |||
|
||||||
<5.6 (mmol/L) | 4 (25.0) | 12 (75.0) | 16 (100.0) | 0.506 | 2 | 0.776 |
5.6–6.9 (mmol/L) | 4 (16.0) | 21 (84.0) | 25 (100.0) | |||
≥7.0 (mmol/L) | 8 (20.5) | 31 (79.5) | 39 (100.0) | |||
|
||||||
Poor (HbA1c ≥7.0%) | 11 (21.6) | 40 (78.4) | 51 (100.0) | 0.216 | 1 | 0.642 |
Good (HbA1c <7.0%) | 5 (17.2) | 24 (82.8) | 29 (100.0) |
The mean age of those with and without hypoechoic foci in either AT was 65.9 ± 7.2 years and 59.7 ± 10.9 years, respectively (
There was no statistically significant difference in the prevalence of tendoachilles hypoechoic foci between T2DM subjects with DM duration of <5 years (6/43; 14%), 5–10 years (7/24; 29.2%) and >10 years (3/13; 23.1%) (
The mean FBG was higher among those with AT hypoechoic foci (9.7 ± 7.3 mmol/L) than those without (7.8 ± 3.4 mmol/L) (
There was no significant difference in the prevalence of AT calcifications among T2DM subjects based on age, gender, and body mass index (
Variables | Diabetics’ | Total |
|
|
---|---|---|---|---|
AT calcifications | ||||
Present | Absent | |||
|
||||
40–49 | 0 (0.0) | 15 (100.0) | 15 (100.0) | 0.512 |
50–59 | 1 (6.3) | 15 (93.8) | 16 (100.0) | |
60–69 | 4 (13.8) | 25 (86.2) | 29 (100.0) | |
70–79 | 1 (5.0) | 19 (95.0) | 20 (100.0) | |
|
||||
Male | 3 (10.0) | 27 (90.0) | 30 (100.0) | 0.667 |
Female | 3 (6.0) | 47 (94.0) | 50 (100.0) | |
|
||||
Normal | 3 (8.1) | 34 (91.9) | 37 (100.0) | 0.564 |
Overweight | 1 (3.8) | 25 (96.2) | 26 (100.0) | |
Obese | 2 (11.8) | 15 (88.2) | 17 (100.0) | |
|
||||
<5 years | 2 (4.7) | 41 (95.3) | 41 (100.0) | 0.295 |
5–10 years | 2 (8.3) | 22 (91.7) | 24 (100.0) | |
>10 years | 2 (15.4) | 11 (84.6) | 13 (100.0) | |
|
||||
Present | 5 (8.8) | 52 (91.2) | 57 (100.0) | 0.667 |
Absent | 1 (4.3) | 22 (95.7) | 23 (100.0) | |
|
||||
<5.6 (mmol/L) | 2 (12.5) | 14 (87.5) | 16 (100.0) | 0.203 |
5.6–6.9 (mmol/L) | 0 (0.0) | 25 (100.0) | 25 (100.0) | |
≥7.0 (mmol/L) | 4 (10.3) | 35 (89.7) | 39 (100.0) | |
|
||||
Poor (HbA1c ≥7.0%) | 3 (5.9) | 48 (94.1) | 51 (100.0) | 0.662 |
Good (HbA1c <7.0%) | 3 (10.3) | 26 (89.7) | 29 (100.0) |
Among the controls, the prevalence of disorganized AT fibers and AT hypoechoic foci differed significantly across various age groups (both
Variables | Present | Absent | Total |
|
|
---|---|---|---|---|---|
|
|||||
|
|||||
40–49 | 0 (0.0) | 16 (100.0) | 16 (100.0) |
|
|
50–59 | 2 (13.3) | 13 (86.7) | 15 (100.0) | ||
60–69 | 7 (25.0) | 21 (75.0) | 28 (100.0) | ||
70–79 | 7 (33.3) | 14 (66.7) | 21 (100.0) | ||
|
|||||
Male | 8 (23.5) | 26 (76.5) | 34 (100.0) | 0.460 | 0.497 |
Female | 8 (17.4) | 38 (82.6) | 36 (100.0) | ||
|
|||||
Normal | 7 (17.5) | 33 (82.5) | 40 (100.0) | 1.615 | 0.446 |
Overweight | 8 (26.7) | 22 (73.3) | 30 (100.0) | ||
Obese | 1 (10.0) | 9 (90.0) | 10 (100.0) | ||
|
|||||
|
|||||
40–49 | 0 (0.0) | 16 (100.0) | 16 (100.0) |
|
|
50–59 | 0 (0.0) | 15 (100.0) | 15 (100.0) | ||
60–69 | 2 (7.1) | 26 (92.9) | 28 (100.0) | ||
70–79 | 5 (23.8) | 16 (76.2) | 21 (100.0) | ||
|
|||||
Male | 3 (8.8) | 31 (91.2) | 34 (100.0) | 1.000* | |
Female | 4 (8.7) | 42 (91.3) | 46 (100.0) | ||
|
|||||
Normal | 3 (7.5) | 37 (92.5) | 40 (100.0) | 0.327* | |
Overweight | 2 (6.7) | 28 (93.3) | 30 (100.0) | ||
Obese | 2 (20.0) | 8 (80.0) | 10 (100.0) | ||
|
|||||
|
|||||
40–49 | 0 (0.0) | 16 (100.0) | 16 (100.0) | 1.000* | |
50–59 | 0 (0.0) | 15 (100.0) | 15 (100.0) | ||
60–69 | 1 (3.6) | 27 (96.4) | 28 (100.0) | ||
70–79 | 1 (4.8) | 20 (95.2) | 21 (100.0) | ||
|
|||||
Male | 0 (0.0) | 34 (100.0) | 34 (100.0) | 0.505* | |
Female | 2 (4.3) | 44 (95.7) | 46 (100.0) | ||
|
|||||
Normal | 1 (2.5) | 39 (97.5) | 40 (100.0) | 1.000* | |
Overweight | 1 (3.3) | 29 (96.7) | 30 (100.0) | ||
Obese | 0 (0.0) | 10 (100.0) | 10 (100.0) |
The orientation of the collagen fibers in tendons is generally orderly and parallel in pattern. Diabetes mellitus causes increased production of advanced glycosylation end products, which leads to cross-linking within the collagen fibers, which can deteriorate the biomechanical function of tendons and ligaments(15). In this study, the prevalence of degenerative features was significantly higher among T2DM subjects (55.0% in the right AT and 52.5% in the left AT) than controls (18.8% in both ATs) (
There were no significant gender differences among the controls in the prevalence of any of the degenerative changes. However, in the T2DM subjects, a significantly higher rate was recorded among males than females for disorganized AT fibers. Abate
Overweight is a known risk factor for tendon degeneration(5); however, in this study, both T2DM subjects and controls showed no significant influence of BMI on the occurrence of disorganized AT fibers, AT hypoechoic and calcific foci. This observation agrees with the findings of Batista
The duration of DM was associated with disorganized AT fibers in this study. The prevalence of hypoechoic foci and calcifications increased with increasing duration of DM, but it was not statistically significant. Abate
The disorganization of AT fibers was significantly higher (71.9%) among T2DM subjects with peripheral neuropathy (PN) than those without PN (30.4%). Similarly, the presence of hypoechoic foci was also more statistically significant among T2DM subjects with PN (26.3%) than those without PN (4.3%). These observations align with the findings of Abate
Though increased degenerative changes were observed with an increased level of dysglycemia, there was no significant association between any of the AT degenerative changes and the level of glycemic control, as measured by fasting blood glucose and glycated hemoglobin. This agrees with the findings of Batista
This study demonstrated structural changes in Achilles tendons that are highly suggestive of biomechanical alterations. Type 2 diabetic patients have a higher prevalence of degenerative changes than non-diabetic controls. These changes are significantly influenced by PN and the duration of DM diagnosis. Further studies to evaluate progression and/or regression of these degenerative changes with clinical management are necessary.
Regarding study limitations, the duration of diabetes mellitus was estimated from the time of diagnosis in a hospital. This is a conservative estimation as subjects could have had the disease before reporting to the hospital.