Correlation of some predisposing intrinsic conditions with the morphological integrity of the Achilles tendon.

BACKGROUND: Most studies have focused on ill-tendons with a little insight on how intrinsic factors correlate with the Achilles tendon (AT) morphology. AIM: This study aims at establishing how blood pressure (BP), blood glucose (BG), and body mass index (BMI) correlate with the morphology of the AT with emphasis on width changes.
MATERIALS AND METHODS: Participants were volunteers who were recruited during and after an organized health fair by the Medical Students' body of All Saints University, School of Medicine, Commonwealth of Dominica. A total of 336 people, consisting of 135 males and 201 females volunteered for the study. The most dominant age group was between 60 and 65 years. A self-administered questionnaire was used to acquire necessary information, and a preliminary clinical procedure was used to check for BP, BG, and BMI. Ultrasound examination was done in B-mode using a linear array high-frequency probe with a mediolateral approach at the AT.
RESULTS: Among the participants, 42.68%, 69.75%, and 30.38% had normal BP, BG, and BMI readings, respectively. BP, BG, and BMI statistically supported the hypothesis. Individuals with extreme BP, BG, and BMI had their AT width wider when compared with individuals with normal systemic readings. Sonographic examination revealed most participants with normal tendon morphology while some identifiable changes were observed among others.
CONCLUSION: This study suggests that BP, BG, and BMI could affect the morphological integrity of the AT. It indicates that asymptomatic high blood sugar and BP could weaken the AT, leading to pain which may appear unrelated to the physician and patient.

INTRODUCTION

The Achilles tendon (AT), also known as tendon calcaneus and triceps surae tendon, is identified as the strongest and thickest tendon in the body, which functions by attaching the triceps surae (consisting of soleus and the two heads of gastrocnemius muscle) to the calcaneus.[12] Its evolutional tracing presented its absence in the genus, Australopithecus, the ancestral genus of Homo, hence illustrating its contribution to natural selection.[3] The term “Achilles” originated from Achilles, the son of King Peleus, who died by an arrow in the heel, thus “Achilles heel” connoting “principal weakness” as recorded in Greek mythology.[4] Been observed to easily induce pain, the AT is recorded as one of the most injured and surgically repaired tendons in the human body, with a higher incidence among individuals involved in strenuous activities such as athletic performance.[1]

The merging of the gastrocnemius (containing type 2 muscle fibers activated mainly by jumping and running) and soleus muscle (containing type 1 muscle fibers stimulated for stability, mainly when standing) forms the AT which inserts at the calcaneus.[56] The gastrocnemius muscle of 11–26 cm by length is usually identified as been flat and wide at its origin which becomes round and narrow distally; it interacts with the aponeurosis of the soleus muscle by its aponeurosis joining at 12 cm proximal to its calcaneal attachment or by direct insertion. The soleus component with a range of 3–11 cm originates as a band on the posterior aspect of the head of the fibula and crosses the soleal line medially on the tibia.[7] It also forms the anterior surface of the tendon.[8] This makes the triceps surae to have both an eccentric and concentric contraction. The AT is peculiar for possessing paratenon which consists of a deep layer which interacts with epitenon and a superficial layer that relates with the underlying layer through mesotenon.[9] The paratenon which originates from the deep fascia of the leg, covering the posterior of the tendon, is usually associated with the “watershed band” when it thickens.[710] Histological examination of the AT shows dense connective tissue with over 90%–95% of its cellular type as fibroblasts, usually referred to as tenocytes.[9] Chondrocytes, synovial cells, and vascular cells which are located mostly at the point of insertion make up the other 5%–10%.[10] However, other cells such as macrophages could be seen with myofibroblastic observations in a pathologically affected tendon.[5] The structure of the AT involves collagen fibrils which form the fascicles that are wrapped by endotenon, forming the tendon.[11] The tendon is also covered by epitenon which is then surrounded by paratenon. A thin layer of fluid also exists in between these layers, preventing friction.[7]

The tendon although being poorly vascularized receives blood supply from the branches of peroneal and posterior tibial arteries which inserts at the musculotendinous junction, on the tendon body, and at the tendon-bone junction.[10] Blood flow tends to intensify with increased physical activity.[8] Innervation of the AT is primarily mediated by the sural nerve and the cutaneous branches from the saphenous and tibial nerves.[9]

The stretch and recoil property of the AT give them the ability to lengthen 10% their size, thereby conserving and providing elastic energy.[9] This elastic energy reduces the demands placed on the muscles. The normal stretching range is usually 4% maximum, with collagen deformity occurring at 8%, and rupture at above 8% stretching.[1213] Studies revealed that males tend to have a larger cross-sectional area, higher maximum rupture load, and more stiffness than females whereas much younger tendons have lower stiffness but more tensile rupture strength.[9] The tendon possesses the strength to accommodate a load of 10 kN which is roughly 12.5 times the normal body weight. Various activities usually relay different amounts of load on the tendon, for example, squat jump relays 2.3 kN, 3.8 kN for hopping, 1.9 kN for counter jumps, 9 kN for running, 2.6 kN for slow walking, and <1 kN for cycling.[71213] AT tendinopathy are usually linked to tendon degeneration and faulty mechanics;[14] the watershed area of the tendon (2–6 cm from the calcaneal insertion) makes the tendon susceptible to rupture at this location when there is a degenerative condition or concentrated pressure slanted on the tendon.[15] Source of damage on the AT could be intrinsic (systemic) or extrinsic (activities).

Most studies have identified the role of many extrinsic factors such as sports, activity, and injury on the health of the AT; this study thus profiles the influence of some systemic conditions on the width of the Achilles as a means of identifying any correlationship.

MATERIALS AND METHOD

Participants

Participants were recruited by two approaches. This included attendees at the health fair organized By the medical Students’ body of All Saints University, School of Medicine, and volunteers who responded to fliers invited for the study after the health fair. This health fair is an approved program by both the University governing body and the Ministry of Health, Commonwealth of Dominica. The study was approved by the Research and Ethical Committee of the All Saints University, School of Medicine. A consent form detailing the procedure to be performed was given to the volunteers, and the procedure was further duly explained by student assistants at the fair.

Selection criteria

Participants selected for this study were all right-handed individuals only, as this has been shown to correlate with ankle dominance. Studies have shown that right-handed individuals have left ankle dominance[16] and thus our choice of the right ankle (nondominant) over the left ankle (dominant). Moreover, the left ankle in right-handed individuals has been shown to be subjected to more strain and rupture (Maffulli, 1999).[17] Hence, we settled for the nondominant right ankle. Our choice of scanning one ankle rather than both stems from the proven fact that there is no significant difference in the cross-sectional area and mean width of the AT of the dominant and nondominant ankles for frequently or nonfrequently exercising participants.[18] Hence, for consistency, we decided on the nondominant right ankle only for all participants.

Preliminary checks

The variables included in the questionnaire were sex, age, lifestyles categorized as sedentary, active, involvement or noninvolvement in sports, and use of heeled footwears (classified based on the frequency of use or nonuse). Subsequently, some basic clinical procedures were done, such as blood pressure (BP) checks and classified using the hypertension classification,[19] body mass index (BMI)[20] and blood glucose (BG) checks which were categorized into normoglycemia, hypoglycemia, hyperglycemia, and diabetic. The participants categorized as hyperglycemic are those having: (i) impaired fasting glucose and (ii) those with a provisional diagnosis of diabetes.[21] The participants categorized as diabetic are those who gave a history of previously confirmed cases of diabetes and are on treatment.

Ultrasound Examination and measurements

The method used in this study was not the conventional method of examining the AT which is the posterior-anterior with the subject prone on the examination bed;[222324] rather in this study, the AT was examined using the mediolateral approach with the participants lying in the supine position.

The participants were requested to lie on their backs on the examination bed, with a little twist to the right. The right knee slightly flexed and the right ankle slightly dorsiflexed to an angle between 80° and 90° to make the tendon relatively taut and straighten out any loose skin around the tendon for better apposition of the transducer. This approach was used as most of the participants felt more comfortable in the supine position; therefore, for consistency sake, we decided this approach for all participants.

The measurement of the AT width was carried out by an experienced single investigator using a DUS-5000 ultrasound machine (Miami, Florida, USA) with a high frequency of 45-mm linear array transducer set to musculoskeletal (MSK) at a default frequency of 8.5 MHz at B-mode. With the area to be scanned exposed, the transducer was applied longitudinally to the medial side of the tendon posterior to the medial malleolus with the transducer placed to span 2–7 cm proximal to its insertion at the calcaneus to visualize the middle portion of the tendon from its medial paratenon to the lateral paratenon. This part of the tendon has been shown to be most prone to clinical and radiological AT injuries because of its relatively reduced blood supply comparative to the upper and the lower portions.[25] The mediolateral dimensions were taken twice and the mean was used in the analysis.

Statistical analysis

Statistical analysis was performed by STATA/IC 13.0 for windows (Texas, USA). Group comparisons based on the self-administered questionnaire were done by Chi-square test. ANOVA was used to compare groups of means. Multiple regression analysis was also performed to predict the width of the AT from BP, BG, and BMI. Statistical hypothesis tests with P < 0.05 were considered as significant. Values are presented as mean (standard deviation) or % (number).

RESULTS

A total of 336 Dominicans voluntarily participated in the study. They comprised 40.18% (135/336) males and 59.82% (201/336) females. Participants were from 10 to 70 years, with the most dominant age group between 60 and 65 years. Participants were grouped and organized based on self-administered questionnaires [Table 1].

Table 1

Demographic information and their impact on the width of the AT

Baseline characteristics	Frequency % (n)	Mean AT width mm (S.D)	Chi-squared P
Sex
Male	40.18 (135/336)	10.65 (1.89)	0.08
Female	59.82 (201/336)	10 (1.1)
Lifestyle
Sedentary lifestyle	18.24 (60/336)	10.38 (1.6)	0.25
Active lifestyle	81.76 (269/336)	10.28 (1.83)
Sporting activities
Actively involved in low impact sporting activities	50.60 (127/336)	10.2 (1.93)	0.07
No sporting activities	49.40 (124/336)	10.1 (1.55)
Females and foot wear
Females who wear heels frequently	23.88 (48/201)	10.40 (1.9)	0.44
Females who rarely wear heels	40.30 (81/201)	9.89 (1.84)
Females who do not wear heels	31.34 (63/201)	9.81 (1.86)	0.42

Distribution of AT width based on BP, BG, and BMI was organized [Table 2]. About 42.68% (140/328), 3.66% (12/328), 30.49% (100/328), 18.29% (60/328), and 4.88% (16/328) were identified as normal, hypotensive, prehypertensive, stage 1 hypertensive, and stage 2 hypertensive, respectively. Furthermore, 36.18% (106/293) and 29.69% (87/293) were recognized as been overweight and obese, respectively. Evaluation of BG identified 69.75% (196/281) with normal BG levels while 7.83% (22/281), 19.57% (55/281), and 2.85% (8/281) had hypoglycemic, hyperglycemic, and diabetic readings, respectively.

Table 2

Associating predisposing intrinsic factors on the width of the AT

Category by evaluation	Mean AT width mm (S.D)	Chi- Squared P
Normal B.P	10.04 (1.85)	0.04
Prehypertensive B.P	10.46 (1.75)
Stage 1 hypertensive B.P	10.18 (1.72)
Stage 2 hypertensive B.P	10.55 (1.92)
Normal B.G	10.10 (1.79)	0.03
Hypoglycemic	10.22 (1.61)
Hyperglycemic (impaired glucose homeostasis and provisional diagnosis of diabetes)	10.87 (2.01)
Diabetic	10.49 (1.84)
Underweight	9.06 (1.66)	0.04
Normal BMI	10.50 (2.08)
Overweight	10.31 (1.58)
Obese	10.10 (1.88)

Multiple regression analysis to predict the width of the AT from BP, BG, and BMI evaluation indicated that these variables statistically significantly predicted the size of the AT, F (3, 360) = 18.98, P = 0.03, except BMI (with 95% confidence interval from 3% to 30%, and 1% to 15% for BP and BG, respectively). Relating females that enjoy using heels as footwear to their AT width showed no statistical significance (P = 0.436). It also appeared that the diameter of the AT increased with respect to age (P < 0.01). There were no statistically significant differences between the group means of AT width and BP, BG, and BMI as determined by one-way ANOVA, P = 0.29, 0.05, 0.07, respectively.

Aside from measuring the width of the Achilles, sonographic evaluation of AT of each participant was also carried out [Figure 1]. The AT, a dense regular connective tissue, is represented sonographically as neatly arranged, linear, and parallel hyperechoic lines which are properly encased in a dense irregular connective tissue sheath known as the epitenon (can be seen as a hyperechoic boundary around the tendon). However, there were a few cases of connective tissue hypertrophy, fluid accumulation from possible underlying inflammation, cystic degeneration or intrasubstance partial tear, and microcalcifications.

Figure 1

Classical sonographic images (a) normal tendon (b) Thickening of the connective tissue peritendineum in a participant with normal blood glucose and body mass index but previous history of high blood pressure. (c) Mild tenosynovitis in a participant with noncontributory factor (d) cystic degeneration or intrasubstance partial tear in an overweight individual (e) tenosynovitis in a participant with noncontributory factor (f) microcalcifications as represented by acoustic shadows in a participant with noncontributory factor

DISCUSSION

Achilles tendinopathy is a common injury among athlete and nonathlete.[26] AT injury are mainly grouped into intrinsic and extrinsic factors.[27] An injury is usually linked with overuse stress, poor vascularity, poor flexibility, sex, endocrine and metabolic disorder, and genetic makeup.[28] Excessive loading during vigorous activities tends to be the main stimulus for AT injury.[27] However, overuse may not be the case among the general population; thus, this study intends to identify the impact of intrinsic factors on the width of the AT among nonathletic Dominicans. Pathologies associated with an increase in the width of the AT have been linked to fat deposits, inflammatory events, and calcification.[929] As a result, conditions such as hypertension, dyslipidemias, obesity, and insulin resistance could be described as situations that can increase the width of the AT,[293031] thus the aim of the study. Previous studies have linked sedentary lifestyles and obesity to tendinopathy.[32] The long term use of high heels have also been reported to affect the elasticity and length of the tendon to a relative degree. This is mainly due to the reduced workload on the tendon [Table 1].[33]

Correlating body mass index on the width of the Achilles

The current study demonstrated a similar link between BMI and the AT width when compared to previous studies. An increase in BMI has been observed to surge cases of hypertension, MSK illness, and diabetes.[34] The excessive distribution of fat among overweight and obese individuals has been well associated with sonographic abnormalities of the AT such as calcification and increased intratendinous microvessels.[34] Obesity could initiate overload syndrome which is preceded by increased AT thickness and inflammatory series leading to type 3 collagen replacing the ideal type 1 collagen.[35] Studies have identified BMI to be directly proportional with AT pathology.[36]

Correlating diabetes mellitus on the width of the Achilles

The fact that increase in BG causes nonenzymatic glycosylation, which affects collagen cross-linkage, could explain why this study experienced the width of the AT being in close correlate with BG.[35] Previous observations on leptin-deficient mice have linked diabetes with tenocyte degeneration, increased proliferation of vessels, and increased chondrocyte-like tendon cells.[36] Furthermore, earlier studies identified increased thickness of the AT and ligaments among diabetic individuals.[37] Loss of elasticity of the AT leading to increased forefoot pressure has also been observed among diabetics.[38] Similarly to previous studies,[3940] this study correlated an increase in blood glucose to be directly proportional to the width of the AT.

Correlating blood pressure on the width of the Achilles

Increase in BP has been reported to cause vascular damage;[41] since the AT is poorly vascularized from the branches of peroneal and posterior tibial arteries,[10] any ischemic damage could lead to the release of inflammatory chemical mediators,[42] thus increasing the width, as described in this study [Figure 1b and Table 2]. Among various factors leading to increased BP, dyslipidemias are the major cause of Achilles tendinopathy among individuals experiencing high BP.[27]

Sonographic interpretation

Normal tendon exhibits a fine fibrillar architecture with slightly hyperechoic lines bordering the tendon, the paratenon [Figure 1a]. Thickened connective tissue endotenon with corresponding AT hypertrophy is usually demonstrated by increased fibrillary echogenicity within the tendon, and this has been linked to more load on the Achilles,[4344] as in this case of a hypertensive retired cricket player [Figure 1b]. A thin rim of fluid which is homogeneously anechoic at the periphery of the AT which might represent a case of mild tenosynovitis,[9] as seen in Figure 1c. A fibrillary pattern loss with abnormal focal areas which are anechoic as shown in Figure 1d may indicate a probable cystic degeneration or intrasubstance partial tear. Fluid collection is shown as areas of reduced echogenicity with an interrupted fibrillary linear pattern of the tendon [Figure 1e]. The fluid under the paratenon is indicative of a tenosynovitis.[9] Achilles tendinosis can also be represented by the fusiform swelling with slight hypoechogenicity and a mild fibrillary pattern loss [Figure 1e]. Microcalcification is visible as posterior acoustic shadows due to the dense nature of calcified tissue [Figure 1f].

For this study, no clinical standards were set because this is the first time to the best of our knowledge when these three noncommunicable diseases (obesity, diabetes, and hypertension) are being correlated with the integrity and width of the AT using the ultrasound. Findings from this study are a revelation from the point of view that even in developing countries, noncommunicable diseases are on the increase. This will worsen the sedentary lifestyle through reduced mobility following the micropathologies of the AT correlating with high BP, glucose, and BMI. If unchecked, this will constitute a vicious cycle by AT-related pathologies increasing the rate of sedentary lifestyle, thus reinforcing positive feedback. The impact from this study is the application of a noninvasive technology, the ultrasound, to evaluate and monitor the impact of noncommunicable diseases on the process of individual mobility.

CONCLUSION

The AT is the strongest tendon in the body which can be affected by systemic irregularities. This study aimed to identify how some of these intrinsic factors could affect the width of the AT. The study identified BG, BP, and BMI to be directly correlated to the width of the AT. However, among other data assessed such as age, sex, sedentary/active lifestyle, low impact sporting activities, and the use of heals by females, it was observed that they had no link with the width of the AT. It was also deduced from this study that asymptomatically high BP, BG, and BMI can alter the morphology of the AT and possibly its integrity. Thus, physicians should consider assessing for BP, BG, and BMI levels when patients present with AT pathology with noncontributory history.

Financial support and sponsorship

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors. However, materials used were properties of All Saints University, School of Medicine, Commonwealth of Dominica.

Conflicts of interest

There are no conflicts of interest.