Introduction

Accounting for up to one-third of rheumatological consults in the United Kingdom, tendinopathies are among the common causes of musculoskeletal disorders in patients being visited in primary care offices [1]. Achilles tendon has been proven to be involved in numerous rheumatological diseases such as rheumatoid arthritis, gout, crystal pyrophosphate deposition disease, and axial spondyloarthropathies, to name only a few [2,3,4]. Achilles tendinopathy (AT) is a common debilitating tendon disorder in the lower extremity and is mostly prevalent among athletes, especially in professionals in track and field sports [5]. AT is generally thought to have a degenerative nature, mostly attributed to the impaired tendon homeostasis secondary to chronic mechanical loading [6]. About one-third of patients with AT have a sedentary lifestyle [2]. Middle-aged (30–55-year-old) people carry a higher risk of developing AT [7]. The incidence of AT in general population is around 6%, but it is higher in athletes; on average, one of every 20 runners develops AT [8, 9]. Kinematic studies show that repeated stretch–shortening cycles of the gastrosoleus complex in sport activities such as running or jumping, are the main cause of AT [5]. In addition to biomechanical factors and lower limb malalignment, such as foot hyperpronation [10, 11], other etiologies including hyperlipidemia, hypertension [12], hypo- and hyper-thyroidism [13], and long-term use of certain medicines (e.g., fluoroquinolones such as ciprofloxacin [14], and corticosteroids [15]) can predispose individuals to AT. A number of epidemiological studies have revealed that men are more susceptible to develop AT compared with women [16,17,18,19,20]. However, the role of sex, as a risk factor for AT, is controversial. For instance, the results of a research conducted by Maffuli et al., reveal no evidence that male sex is a risk factor for AT [21].

More than half (55–65%) of AT occurs in the middle part of the Achilles tendon, about 2–7 cm proximal to the calcaneus, the so-called “midportion AT,” where the blood flow is low. The next most commonly affected site is the insertion of the tendon to the heel bone observed in 20–25% of patients—termed “insertional AT” [18, 22,23,24].

Clinical presentation of AT might differ from place to place, depending on the prevailing daily activities done in a region, which in turn depend on the culture of people. There is scarce information about clinical presentation of AT in Iran. We therefore conducted this study to determine the clinical picture of AT in a group of clients attending to a referral center outpatient orthopedics clinic in Shiraz, southern Iran.

Materials and methods

In a cross-sectional study, using a convenient sampling technique, 61 patients referring to an outpatient clinic affiliated to Shiraz University of Medical Sciences with a definite diagnosis of AT were selected. The clinic was a referral center with more than 250 patients complaining musculoskeletal disorders coming from various regions of the southern Iran. Those with partial- or full-thickness tear of Achilles tendon, patients with history of radicular pain or lower extremity injury, individuals with previous history of surgery on their lower extremity, and pregnant women were excluded from the study. The criteria used in our study for the diagnosis of AT were based on Maffulli et al. [25], criteria including presence of pain and tenderness, tendon stiffness and functional limitation. A standing plain roentgenogram was also taken from each participant for better assessment of the Achilles tendon. Age, site of pain, body mass index (BMI), and level of physical activity (self-expression) were recorded for each patient.

Ethics

The study was conducted according to the principles of the Declaration of Helsinki. Written informed consent was obtained from all study participants; they were assured that their data will be kept confidential and that their identity will not be revealed. Ethical approval for this study was obtained from Ethics Committee of Shiraz University of Medical Sciences (Protocol No: IR.SUMS.REHAB.REC.1397.012, December 19, 2018).

Statistical analysis

IBM® SPSS® Statistics for Windows ver 26 (IBM Corp, Armonk, NY, USA) was used for data analysis. One-sample Kolmogorov–Smirnov test was used to assess whether or not a continuous variable follows normal distribution. Normally distributed variables were presented as mean and the standard deviation (SD). Student’s t test for independent samples was used for comparing means of two normally distributed variables; Levene’s test was used to evaluate the homogeneity of variance between the two groups. Categorical variables were presented as absolute number and percentages. Either χ2 or Fisher’s exact test (when appropriate) was used to compare the distribution of two categorical variables. Pearson’s correlation coefficient was used to assess the correlation between two normally distributed continuous variables. Linear regression analysis was used to assess the linear association between the BMI (dependent variable) and age (independent variable). All tests were two-tailed. A p value < 0.05 was considered statistically significant.

Results

We studied 61 patients (46 [75%] women and 15 [25%] men). Age and BMI followed a normal distribution (one-sample Kolmogorov–Smirnov test, p = 0.2 for both variables). The mean age of participants was 47.7 (SD 11.1) years. More than half (57%, 26 of 46) of the studied women were aged 48 years or more. The mean BMI was 28.7 (SD 4.2) kg/m2 (Table 1). There was no significant correlation (Pearson’s r = –0.028, p = 0.832) between the age and BMI (Fig. 1).

Table 1 Distribution of studied variables stratified by the site of tendinopathy
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Fig. 1
figure 1

Scatter plot showing the correlation between age and BMI

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Forty-six (75%) of 61 studied participants had no regular sport activity. The most common site of AT was insertional (80%) followed by midportional (15%); AT affected both sites in three (5%). The prevalence of insertional AT among 58 patients with only one site affected, was 84% (95% confidence interval [CI]: 72% to 92%), significantly (p < 0.001) higher than that of midportional AT. Women were also more frequently affected than men (p < 0.001) (Table 1). The distribution of AT did not significantly depend on age, BMI, or sex (Table 1).

Discussion

We found that three-quarters of the participants presenting with AT had no regular sport activity, that the most commonly affected site was insertional, and that women were more frequently affected than men. The mean age of participants, 47.7 years, was consistent with what has been reported in the literature [7].

A national and subnational metaregression analysis on the trend of physical activity among Iranian adults between 2001 and 2016, report that 73% of studied women and 59% of men residing in Fars province, southern Iran, had insufficient physical activity [26]. The higher observed prevalence of AT among women compared with men in our study, might thus be attributed to insufficient regular physical activity, although we cannot be sure about it as the level of activity in our patients was just assessed by asking the participants about their daily physical activities (self-expression).

A systematic review and meta-analysis published in 2018 shows that the mean age of menopause among Iranian women is 48 years [27]. It has been shown that blood estrogen level may have a role in the homeostasis of tendon [28], and that estrogen deficiency can decrease the collagen turn-over rate and tendon elasticity [29]. Because 26 (57%) of 46 studied women were aged 48 years or more, it is very likely that many of them were post-menopausal in whom the trophic effect of estrogen on tendons would be vanished. That might be another reason why the prevalence of AT in women was significantly higher than that in men in our study.

Higher BMI is commonly associated with foot hyperpronation posture leading to whipping phenomenon on the Achilles tendon and consequent insertion of undue tensile stress and strain on the medial aspect of the tendon with ultimate increasing likelihood of AT [30, 31]. No significant correlation was observed between the age and BMI in our patients (Fig. 1).

In contrary to what has been reported in a number of previous studies [18, 22,23,24], where the prevalence of midportional AT was higher in a group of athletes, especially among male runners, insertional AT was more prevalent in our study. This difference could be attributed to the amount of physical activity of the study participants—our study participants were mainly women with a sedentary life (low physical activity). These contradictory observations underline the pivotal role of sex and physical activity in the pathogenesis of AT and the site of involvement. However, the exact mechanisms underlying the pathogenesis of AT is still unknown.

A possible mechanism would be aging. Histopathological studies have revealed that aging process has a detrimental effect on tendon blood supply with resultant switching of tenocytes metabolism from aerobic to anaerobic pathways [32, 33]. Furthermore, it has been shown that aging is associated with increased extracellular concentrations of damage-associated molecular patterns (DAMPs), a group of molecules consisting of intracellular proteins and nucleic acids released following cellular damage, which are among the important effectors of the innate immune system and causes of chronic inflammation [34]. DAMPs also play important roles in the pathophysiology of many rheumatological disorders including tendinopathies [1]. The tendon elasticity decreases by aging so that a compensatory increase in muscle activity should occur [35]. This increased muscle activity, in turn, results in a higher tendon temperature. Chronic accumulative overloading of tendon during lifetime accompanied by the aforementioned age-related pathological continuum ultimately led to tendon degeneration.

The convenient sampling technique used in this study was among the limitations of this study. However, our center was a referral center for patients from southern Iran and our sample would be considered a representative sample of all patients in the region. Another limitation of our study was that we did not collect details of physical activity of the participants. The level of physical activity was self-expressed by the participants. Nor did we record and report the radiography findings of our patients. We did also not record the biomechanical factors that could be involved in development of AT or medications that could potentially cause AT used by our patients. We could not assess the effect of BMI on development of AT for lack of a control group (those without AT), which could be considered another limitation for this study.

Conclusion

It seems that the clinical presentation of AT in our region is somewhat different from those reported in other regions of the world. For better evaluation of patients with AT, it is necessary to study the epidemiology of this condition in each part of the world. Further well-controlled studies conducted on larger groups of patients are needed to elucidate the causes of observed differences among various reports.