Infrared thermography applied to lower limb muscles in elite soccer players with functional ankle equinus and non-equinus condition

Introduction

Gastrocnemius-soleus equinus (GSE) is a functional limitation of the ankle. GSE is defined as the inability of the ankle to dorsiflex beyond a neutral position with the knee extended (it remains <0°) or with the knee flexed (it remains <0°) (after excluding osseus restriction) (DiGiovanni et al., 2002; Downey & Banks, 1989). Although GSE is clinically asymptomatic, it may cause an alteration in the triceps surae muscles, tibialis anterior muscle (TA), and Achilles tendon (AT). GSE is closely related to asymmetric loading patterns and muscular alteration for contraction (Lamm, Paley & Herzenberg, 2005; Silfverskiöld, 1924; Downey, 1992; Root, Orien & Weed, 1977).

Asymmetric body loading is associated with GSE and may cause a higher activation of low-back and pelvic muscles (e.g., the quadratus lumborum) and lower limb muscles (e.g., the TA). GSE has been much studied using the mean of force pressure platform, Romberg-test analysis, and sway-area development approaches (Blustein & D’Amico, 1985; Mahar, Kirby & McLeod, 1985; Bhave, Paley & Herzemberg, 1999; Blake & Ferguson, 1992). The relationships between muscle contraction condition and posture have been investigated by electromyography (Vink & Huson, 1987; Gurney et al., 2001; Balestra et al., 2001). GSE condition shows a relationship with gait and posture (Bhave, Paley & Herzemberg, 1999; Blake & Ferguson, 1992). Also, several studies have investigated whether activation of skeletal muscles promotes heat transfer and thus increases cutaneous temperature (Merla et al., 2005; Zontak et al., 1998; Kurt & Damiano, 2016; Formenti et al., 2017).

Orthostatic posture is typically assessed by the complex activation of anti-gravitational muscles (e.g., the triceps surae muscles). Modifications in cutaneous temperature are associated with gait and posture alterations, asymmetric loading forces, and an altered range of ankle or knee movement. High thermal infrared (IR) imaging can non-invasively identify cutaneous temperature variations (Merla et al., 2005).

Here we aimed to assess whether high-resolution thermal IR can detect cutaneous temperature variations in GSE and Non-GSE individuals and thus detect association between the extensibility to triceps-surae (with GSE and Non-GSE) and the role of TA in professional sportsmen. The aim of the study was to check thermal differences between GSE and Non GSE-group before running and after running exercise.

Methods

In this case-control study, 21 healthy male participants (professional soccer players) (age 23 ± 2.9 years, body mass index (applying Quetelet’s equation follow BMI = weight (kg) / height(m)²) 20.2 ± 1.2) were included. A consecutive sampling method was used to select participants. Eighteen subjects were right-footed, and three were left-footed, as defined by the self-report on the lower limb predominant used in sports activities. All participants successfully completed the study. The exclusion criteria were the presence of musculoskeletal injuries, low back and pelvic pain, sprains, tendon injuries in lower limbs, use of drugs in the week preceding the test, and scoliosis.

The principal study variable was temperature. An IR ThermaCam was used to register the maximum, minimum and mean temperature values of the TA, AT, and G regions.

Data Analysis

IR-images and data were analyzed using rater (DRS) with the FLIR^® software Termocan Researcher Professional V.2.9 (FLIR, Wilsonville, OR, USA). This software provides to rater the minimum, maximum and mean thermal values for the selected muscles. This body selections-regions were bilaterally selected with landmark position and selected by the blinded clinical operator who ignored hypothesis of study and the experimental conditions. An IR-Imaging example is shown in Fig. 1.

Statistical Analysis

Statistical analyses were performed with SPSS (version 22.0 for Windows, IBM SPSS Statistics for Windows; IBM, Armonk, NY, USA) with an α error of 0.05 (95% confidence interval (CI)), with the desired power of 80% (β error of 0.2).

A Shapiro–Wilks test was used to assess data normality. All data were normally distributed, and parametric statistical tests were selected. The mean and standard deviation of the temperature data were obtained for the selected lower limb muscles (AT, TA,G).

Unpaired sample student’s t test were performed to test for statistically significant differences in height, weight, body mass index, and age between the two groups. A Paired Student’s t-tests were performed to determine differences between the groups (equinus vs. non-equinus), as well as between imaging sessions (before vs. after running).

Results

We found no statistically significant differences between the equinus vs. non-equinus groups for participant height, weight, age or body mass index (Table 1).

We found no significant differences in TA, G or AT temperatures between the GSE and non-GSE participants before running (Table 2).

However, after running, the TA temperature (minimum, maximum, and mean) was significantly warmer in the GSE than the Non GSE participants (P < .05). Also, the minimum G temperatures (both right and left) and left AT mean temperature were significantly warmer in the GSE than the Non-GSE participants (Table 3).

Discussion

Here, we identified an increase in TA temperature after running in professional soccer professionals with GSE condition compared to those without GSE. The minimum G temperatures (right and left lower limb) and mean AT (left lower limb) temperature were also higher in GSE than non-GSE participants.

Ankle torque was higher in GSE participants than non-GSE participants (Wrobel, Connolly & Beach, 2004). The TA requires stronger contraction in GSE condition and, therefore, might be affected early by fatigue, thus explaining our observed increase in TA temperature in GSE participants compared to non-GSE participants. While participants remain without running activity, we didn’t found differences. The running exercise may serve a stimulus to increase temperature in muscles and consequently differences between groups.

Researchers have addressed the necessary degrees of ankle dorsiflexion and basal values (DiGiovanni et al., 2002; Root, Orien & Weed, 1977). Biomechanically, the maximum ankle dorsiflexion during the stance-phase of a normal gait occurs before heel lift with the knee extended (DiGiovanni et al., 2002). The minimum ankle range of motion for normal gait is 10° dorsiflexion and 20° plantarflexion (DiGiovanni et al., 2002; Downey & Banks, 1989; Root, Orien & Weed, 1977). The most deeply known range of movement values for ankle dorsiflexion in the reviewed literature for static evaluation that the minimum dorsiflexion movement for the ankle for normal gait is 10° of motion (Lamm, Paley & Herzenberg, 2005; Mcglamry & Kitting, 1973; Knutzen & Price, 1994; Nuber, 1988; Lavery, Armstrong & Boulton, 2002; Wrobel, Connolly & Beach, 2004; Winter, 1984). GSE produces a higher loading force to the foot and can lead to foot-ankle biomechanical pathologic (e.g., plantar fasciitis, pes planus, hallux abductus valgus, Achilles tendinosis, Charcot’s midfoot collapse, and diabetic ulcerations) (Lamm, Paley & Herzenberg, 2005). DiGiovanni et al. (2002) found GSE in patients with foot and ankle pain. However, GSE is also found in asymptomatic patients (Brodersen, Pedersen & Reimers, 1993).

Further studies will be needed to improve our knowledge of muscle condition and to establish the clinical relevance of the association between temperature and cutaneous muscle projection (Abate et al., 2010). Based on our findings, we propose that IR-imaging can be a reliable tool for clinical therapeutic assessment.

Conclusions

GSE participants had a higher TA muscle temperature after exercise that non-GSE participants. The GSE groups showed a higher TA skin temperature. Therefore infrared thermography, in the way it measures skin temperature, could serve as screening tool for preventing or therapeutic actions. Further research is needed to identify other factors associated with GSE condition, as well as to better understand the factors that contribute to different temperature pattern in the lower limbs.

Supplemental Information