Risk Factors

 

Dorsiflexion ROM & AT

Dorsiflexion range of motion (DF ROM) has been cited as a risk factor for the development of AT. Alterations in dorsiflexion range of motion have been associated with higher incidence and risk of AT (Carcia et al, 2010). A prospective study carried out by Mahieu et al (2006) measured DF ROM with knee flexed and extended, in order to isolate the significance of gastrocnemius and soleus individually. Their findings illustrated that increased passive dorsiflexion (<9°) in knee extension tended towards a significant association with the development of AT.

 

A study of similar design justified measuring dorsiflexion with an extended knee as the knee is flexed to approximately 40° in mid stance of running, when the ankle is in greatest dorsiflexion. Conversely to the findings in the previous study (Mahieu et al, 2006) the most significant finding in this group was that in the AT group ankle dorsiflexion with the knee flexed was limited (Rabin et al, 2014). Unit odds ratio indicated that for every 1° increase in DF ROM, the chances of developing AT were reduced by 0.23. It was also demonstrated that non-weight bearing range of dorsiflexion of less than 22° is a cut-off point for increased risk of developing AT (Rabin et al, 2014).

 

Somewhat supporting both studies, the findings of a 2-year prospective study of risk factors indicated that alterations in the DF ROM (increased or decreased) leads to increased susceptibility to AT (Kaufman et al, 1999). With knee extended, decreased DF ROM (<11.5°) makes a person 3.5 times more likely to develop AT. Alternately, increased dorsiflexion ROM (>15°) leads to 2.5 times greater risk of developing AT (Kaufman et al, 1999). These findings were supported by a systematic review which also finds reduced DF predisposes to AT (Manteanu & Barton, 2011).

 

The effect of limited dorsiflexion is theorised to contribute to the development of AT by increasing the pressure of shock absorption by the plantarflexors during running, and increasing the strain on the TA (Rabin et al, 2014). This has an effect of reducing the internal loading capacity of the TA (Manteanu & Barton, 2011). Another proposed mechanism for its effect is traction from the soleus muscle on the TA. As the deep calf muscle attached to the medial aspect of the TA, an area where 91% of US changes are found, it is hypothesised that traction from an inflexible soleus muscle may lead to AT (de Vos et al, 2012).  The inter-rater reliability of ankle dorsiflexion goniometric ROM assessment is reported to be up to 0.69, with excellent intra-rater reliability of 0.90 (Martin & McPoil, 2005).

 

Adiposity and AT

Adiposity is believed to have a strong association with the development of AT. There are 2 proposed mechanisms of action for the influence of adiposity, which are mechanical and systemic processes (Gaida et al, 2009). The mechanical process suggests that higher levels of adiposity leads to increased body weight and higher forces travelling through the tendon. This sustained higher load puts increased strain on the tendon and leads to AT. This systemic effect explores the interference of bioactive peptides released by adipose tissue on the tendon structure. Increased adipose tissue increases the risk of cardiovascular disease, with increased low-level inflammation due to cytokines, and increase resistance to the flow of blood. This increased resistance is proposed to have negative influences on the healing capabilities of the tendon, with reduced oxygen supply and metabolism (Gaida et al, 2009). In an investigation of the effects of adiposity on the presence of ultrasonographic tendon changes Abate et al (2012) found that there was a significant prevalence of tendon changes in overweight runners. There were less sonographically visible changes in runners with lower body mass index (BMI), or sedentary individuals who were overweight (Abate et al, 2012). The authors also proposed an explanation for this, suggesting that fat distribution and adiposity may influence the function of the tendon components such as tenocytes and blood vessels. Their justification was that when the overweight runners caused micro trauma to the tendon, appropriate healing mechanisms were delayed by this influence, and degenerative changes occurred (Abate et al, 2012).

 

Gaida et al (2010) stated that men with a waist circumference of greater than 83cm were at greater risk of developing AT, with 33% of these individuals suffering from the condition. They also found that men had greater central fat distribution, and women predominantly had a peripheral distribution of fat, due to the influence of oestrogen on the prevention of central accumulation of fat (Bagge et al, 2011). Gaida et al (2010) found that 43% of the group with AT had significantly greater adiposity levels than the control group

 

 

Subtalar joint motion & pronation

Subtalar joint motion has been shown to have an association with the presence of AT.  Abnormal subtalar joint range of motion is determined by increased range of motion in the planes of inversion and eversion (Munteanu & Barton, 2011). Both increased inversion and eversion have been shown to be present in sufferers of AT (Rabin et al, 2014; Kaufman et al, 1999). A possible mechanism for the influence of subtalar eversion is that limited dorsiflexion (DF) may lead to compensatory pronation of the foot, which in turn will cause internal rotation of the tibia. This internal rotation will be corrected to tibial external rotation when the knee is extended. This increased rotation of the tibia causes “wringing” of the TA, and forces the gastrocnemius and soleus to produce greater forces to plantarflex the foot during terminal stance of running (McCrory et al, 1999). Munteanu & Barton, 2011) The tightness of the TA & gastrocnemius-soleus complex has also been owed to increased pronation, as the reduced ROM of DF may be due to prolonged contraction of the triceps surae in an attempt to control pronation (O’ Donoghue et al, 2008). Also, as 91% of US detected mid-portion disorders of the TA occur on the medial segment, there is believed to be an association between hyper-pronation of the foot leading to excessive posteromedial strain on the TA (de Vos et al, 2012).

 

In their systematic review Muntaenu & Burton (2011) established that athletes with AT displayed greater subtalar eversion ROM. This was supported by the prospective study carried out by Rabin et al (2014) on military recruits, with similar conclusions being drawn. Kaufman and colleagues (1999) demonstrated that increased ROM of subtalar inversion significantly increased the risk of AT, with those demonstrating more than 32.5° of inversion being 2.8 times more likely to display the condition. Limited ROM of inversion (<26°) was also shown to have a correlation with the condition in the same study (1.8 times more likely) (Kaufman et al, 1999).

 

There were variable results presented for goniometric subtalar joint ROM assessment. Scores of intrarater reliability were consistent for both inversion and eversion, with very good scores of 0.79 and 0.78 respectively (Elveru et al, 1988). Inter-rater reliability of the same sample presented rather poor results (0.32 & 0.17 respectively), which casts doubt upon the reliability of the measure when using different assessors. This result is consistent with other literature in the area, which also finds poor reliability for the interrater measurement of subtalar range of motion (Smith-Oricchio & Harris, 1990).

 

Plantar flexion strength and AT

There has been an association between plantarflexion strength and AT, and this association may be either a consequence of the injury, or a risk factor for its development (Carcia et al, 2010). It has been shown through a cohort study that the plantarflexion strength measures of individuals suffering from AT are significantly lower than those of a healthy population (McCrory et al, 1999). However, in the AT group, strength was similar in both legs, suggesting that strength deficits may have been present before the clinical presentation of symptoms (McCrory et al, 1999).

 

A prospective study carried out by Mahieu et al (2006) found significant plantarflexion strength differences for almost all subjects affected by AT. Pre-training strength measurements on army recruits showed significantly less plantarflexion forces in the group that later developed symptoms of AT. They theorised that greater muscle strength in the triceps surae complex produces stronger tendons that are better able to resist strain and deal with the application of heavy loads (Mahieu et al, 2006). Through a battery of testing, Sibernagel et al (2006) were able to identify functional restrictions in the AT group. They showed impairments in strength through decreased performance of maximum concentric heel raise and maximum concentric-eccentric heel raise. They performed comparisons between the effected side and the non-effected side in the same individual and also demonstrated strength deficits between these, with consistently lower scores for the effected side (Sibernagel et al, 2006).

 

Thus from this we can conclude that decreased plantarflexion strength leads to an increased risk of the development of AT. We can also see that those with AT exhibit decreased -plantarflexion torque and strength on the effected side. 

 

Age as a risk factor for AT                                     

The association between age and AT has been mentioned frequently throughout the literature, with a belief that AT is most common in the fourth decade of life, and between the ages of thirty five and forty five (Wyndow et al, 2010). Kraemer and colleagues found a slight correlation between age and AT with increased average age in the AT group of a matched pair analysis (Kraemer et al, 2012). A low quality prospective study carried out by Gajhede-Knudsen et al (2013) found similar results in a group of elite footballers competing in European club competition, with the average age of those suffering AT 27.2 years, compared to the symptoms free group with a mean age of 25.6 years. Contradicting these, Di Caprio et al (2010) in a prospective risk factor assessment argue that there was no association between AT and age in his cohort of recreational and competitive runners.

 

The proposed method of effect of age on AT has also been investigated, with authors presenting their view on different mechanisms. Decreased arterial blood flow, local hypoxia, decreased nutrition, impaired metabolism and the presence of free radicals were cited by one study as the negative effects of aging on the tendon’s ability to carry load and recover from micro-trauma (Fredburg & Stengaard-Pederson, 2008). Carcia et al (2010) offers other alternative explanations of the effects of aging on the tendon’s susceptibility to injury. It is believed in this review that the tendon undergoes morphological and biomechanical changes similar to other body tissues, associated with aging. It is proposed that aging decreases collagen diameter & density, as well as the glycosaminoglycan and water content of the tendon. The biomechanical effects of aging on the tendon may include decreased tensile strength, reduced linear stiffness and a compromised ultimate load (Carcia et al, 2010). Also associated with aging are a decreased rate of collagen synthesis, and an accumulation of obstructive macromolecules in the tendon matrix. All of these proposed mechanisms are more common in individuals over the age of 35 (Carcia et al, 2010).

 

Genetics & AT

As with many other conditions, there is believed to be a genetic/hereditary component in the development of AT. This is believed to be influenced by the effect of genes on the inflammatory pathway in the pathogenesis of AT. It has been suggested that inflammatory gene expression profiles of tenocytes are modulated in response to mechanical loading, and that cytokines trigger tenocyte apoptosis and pathological extracellular matrix degeneration (September et al, 2011). This becomes pathological when the rate of degeneration exceeds the healing response, and this is believed to be the case with this genetic predisposition. However, only two gene variations have been shown to have an association with AT, therefore the genetic influence on the development of AT is relatively rare (September et al, 2008). The association between genes and AT has been shown to be significant; however there has not been an association between genetics and TA rupture (Magra & Maffuli, 2007).

 

Fluoroquinolones & AT

The development of AT has been associated with a history of treatment with quinolone antibiotics. These are often used in the treatment of community acquired respiratory infections (Khaliq & Zhanel, 2003). Fluoroquinolone induced AT has been reported in approximately 6% of cases after taking the antibiotic (Carcia et al, 2010). The presentation of symptoms may occur within 2 hours of commencing treatment or up to 6 months after discontinuing antibiotic therapy, though up to 85% present within one month of commencement (Lewis & Cook, 2014). Symptoms usually present quickly with sudden onset of pain and morning stiffness in the tendon, and 95% of cases are reported in the TA (Lewis & Cook, 2014). Presentation of fluoroquinolone induced tendinopathy is more common in middle aged men, and can be influenced by comorbidities such as corticosteroid use (32.7% of AT patients), renal transplants (12.2%-15.6%), diabetes mellitus and rheumatic disease. It has also been shown increased prevalence in very physically active patients (Khaliq & Zhanel, 2003). Fluoroquinolone use should be discontinued immediately when symptoms of AT appear (Lewis & Cook, 2014). Treatment of fluoroquinolone induced AT differs slightly from traditional treatment with the first phase of treatment involving supporting the chemically damaged TA with a brace to allow for tendon recovery before later beginning a progressive loading program (Lewis & Cook, 2014).

 

Comorbidities associated with AT

The comorbidities associated with AT include conditions associated with reducing the blood flow to the region. These conditions can affect the blood supply or quality of blood to the region. This causes damage as a mechanism for tendinopathy is a failed healing response in the tendon. If the blood supply to the region is reduced, or the quality of nutrients received from the blood is affected, the tendon may not have the metabolites available to boost the healing process. Medical conditions that have been repeatedly associated with AT include obesity, hypertension, increased cholesterol and diabetes (Carcia et al, 2010). In all of these conditions the quality of blood supply is affected. Kraemer et al (2012) discussed similar comorbidities, with links between familial hypercholesterolemia, arterial hypertension, diabetes (in men under the age of 44) and AT. Interestingly, it was found that there were significantly less people with cardiovascular disease and smokers in the group with AT than in the control group (Kraemer et al, 2012). The possible explanation offered for this was that 70% of people who suffer from AT regularly participate in physical activity, and physical activity is a method of preventing cardiovascular disease. The reduced number of smokers was explained by examining the lifestyle habits of people who regularly exercise, and hypothesising that the culture and lifestyle of those who regularly exercise may suggest that less of the physically active cohort smoke, as well as the association between running and smoking cessation (Oestergaard Neilsen et al, 2012).

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Table 2.1: Additional risk factors discussed in the literature (van Ginkel et al, 2009; Taunton et al, 2002; Carcia et al, 2010).

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Table 2.2: Assessment of risk factors (Carcia et al, 2010)

 

Training Characteristics and AT

Training characteristics and loading of the TA are believed to be a large determinant of the development of tendinopathy. Some of the cited training errors include increase in mileage, increase in intensity and returning from a ‘lay-off’ period of inactivity (Carcia et al, 2010). A systematic review of running related injuries investigated the effects of training volume, distance, time, frequency, intensity and pace on the development of running related injuries in novice, recreational and elite runners (Oestergaard Neilsen et al, 2012). In a review of the aetiology of running injuries, Hreljac (2003) concluded that overuse running related injuries were preventable as the causes of these injuries were training errors.

 

Volume/Distance:

In a systematic review of the above mentioned running related injury factors, volume in the form of distance covered per week was assessed as a risk factor for the development of injuries (Oestergaard Nielsen et al, 2012). 4 prospective cohort studies showed an increased relative risk of running related injury in runners who cover various distances per week. Running greater than 20 miles per week doubled the risk of injury in men, and triple this risk in women. It was shown that running greater than 40 miles per week significantly increased the risk of injury, with men and women up to 3 times more likely to develop running related injuries, including AT, when consistently (for greater than 3 months) covering these distances. Contradicting these findings, 2 other prospective studies mentioned in this systematic review found no significant association between miles run per week and the development of running related injuries.

 

The finding of several retrospective studies in this systematic review supported the assumption that greater miles per week increase the risk of running related injuries. One of these studies found that the proportion of women reporting injury was highest from those covering 40-49 miles per week, and the proportion of men reporting injury was highest among those running 30-39 miles per week. 2 further studies reported that the average weekly mileages of runners sustaining injuries were higher than uninjured runners [26.3km (injured) vs 22.0km (uninjured); 47.5mls (injured) vs 29.6mls (uninjured)]. It was also found that the relative risk of injury in runners who’s longest weekly run exceeds 5 miles was higher than those who do not run this distance (men 2.49, women 1.78).

 

Duration

The duration of running has frequently been reported in the units of minutes per week, and the prevalence of injury is reported as ‘running related injury per thousand hours of running’ (RRI/1000hrs). The prevalence of injuries varies greatly for experienced runners and marathon runners to novice runners.

RRI prevalence per session running length was investigated by one study, concluding that 15 minutes, 30 minutes and 45 minutes duration of running for novice runners lead to differences in the number of injuries (22%, 24% & 54% respectively). Novice runners are reported to have a very high risk of injury, with up to 33 RRI/1000hrs being reported in novice runners who spend 52-59mins/week running in this systematic review. Prevalence of RRI/1000hrs is much lower in experienced marathon runners with reported varying between 6.9-12.1 RRI/1000hrs in athletes running between 162 and 240 minutes per week. This association was acknowledged by the authors of this systematic review, with their reasoning that the risk of injury per mile of training decreases with greater total mileage for experienced and marathon runners. They believe that experienced runners may have a greater knowledge of their own injury thresholds compared to novice runners, and may make efforts not to exceed these thresholds, thereby leading to decreased injury rates per miles and minutes of running every week.

 

Intensity

Running speed/intensity may not have a decisive bearing on the development of AT. In this systematic review, 2 studies found that running intensity may have an influence, with findings that less than 8 minutes per mile may lead to more injuries than more than 8 minutes per mile. The other study found a similar association with greater or less than 15 minutes per mile. No other studies review showed a significant association between the intensity and the development of Achilles injuries.

 

Frequency

There was no significant association between the frequency of running and the prevalence of AT in this systematic review. The only association between RRIs and frequency were found for shin pain and anterior thigh muscular injuries.

 

 

Running Terrain

Running surfaces have been associated in the past with AT, with more compliant surfaces, uneven ground and changing terrains cited as factors that may predispose individuals to the condition (Pierre-Jerome et al, 2010; Cadez-Schmidt et al, 2014). However, much of the evidence for this is anecdotal and low quality studies. A prospective study found no influence of the running surface on the development of injury, but the authors did feel that it was more difficult to assess this due to limitations in quantifying the intensity of running and time spent on each of the different surfaces (Taunton et al, 2002).

 

Changes in training characteristics

It has been proposed that overuse injuries including AT occur more frequently during periods of changing and increasing training intensity, duration, or frequency (Schepsis et al, 2002; Carcia et al, 2010; Pierre-Jerome et al, 2010). However, though this association may be explained biomechanically through the increased loading strain on the tendon through increased mileage/intensity of training, there is a very limited background evidence to support the association. The link is drawn on assumptions and retrospective analysis rather than prospective research (Clement et al, 1981). One randomized control trial found no link between graded increase in training intensity (10% per week) and standard training increase (24% increase per week) over a thirteen week period. The incidence of running related injuries was 20.8% in the graded training group compared to 20.3% in the standard training program group (Buist et al, 2008). Though the large body of retrospective and case study evidence would suggest that rapid increase in training intensity is a direct risk factor for TA injuries, the findings presented in the present RCT encourages scepticism in the interpretation of these studies. It was suggested that more rapid increases in training intensity of up to 40% may be more effective in highlighting the issue, though there are ethical issues to be considered before undertaking such a project (Carcia et al, 2010).

 

The findings of the above RCT should not be interpreted as a justification for increasing training intensity by up to 24% weekly, rather that more high quality research with different populations may need to be carried out before recommendations can be made on the subject.

 

 

 

Clinical Implications

Due to age related physiological changes, the process associated with tendinopathy is most common in the 4th decade of life, with an increased risk of the condition in people over the age of 35. Those with abnormal sub-talar and dorsiflexion ranges are predisposed to the condition, with increases and decreases in the available range of both movements being strongly associated with the condition. Higher levels of fat have been associated with the condition in both men and women, with a central distribution of fat being seen in men, and women presenting with more peripherally distributed fat. There is a tentative link between genetic predisposition and AT development, as well as a correlation between certain comorbidities such as obesity, diabetes and hypercholesterolemia, which it is believed affects the peripheral arterial blood supply. Though little significant research evidence exists for its affect, the link between training characteristics and symptom development in AT in an athletic population cannot be understated. Drawing from clinician experience, the association between an increased intensity of training or sudden change in training characteristics was stressed to us as a crucial factor in the development of this condition, and risk factor assessment should certainly contain an aspect of training characteristic profiling.

 

Key References

• Carcia, C., Martin, R., Houck, J., Wurich, D. (2010). Achilles Pain, Stiffness, and Muscle Power Deficits: Achilles Tendinitis. Journal of Orthopaedic Sports Physical Therapy. 40 (9)