Achilles tendinopathy is the umbrella term used to describe the clinical presentation of activity-related Achilles tendon pain, morning stiffness, focal tendon tenderness, and intratendinous imaging changes (31). It is a prevalent musculoskeletal disorder in today’s society, particularly for those in running-based sports. Specifically, Achilles tendinopathy is accountable for between 8% and 15% of all injuries in recreational runners (4,12,17,22) with a cumulative lifestyle incidence of 24% in athletes (22). Identification of intrinsic factors associated with the condition will assist in the appropriate management and prevention of the condition.
While the activity of the triceps surae and other distal muscles has been the focus of studies investigating factors associated with Achilles tendinopathy, it is possible that activation of proximal muscles may also be important for this condition. One study has investigated proximal neuromotor control during running in Achilles tendinopathy and reported a significant reduction in amplitude of gluteus medius (GMED) activity after heel strike in individuals with Achilles tendinopathy compared to healthy controls (1). GMED and gluteus maximus (GMAX) activation is known to influence joint excursions and torques at the hip (24,33). Interestingly, it has been identified that it is not only the magnitude of activation but also the timing of activation that is associated with hip kinematics (33). Alterations in hip kinematics may be linked with more distal mechanics via two different mechanisms: (i) a mechanical link in the transverse and frontal planes and (ii) a mechanical link in the sagittal plane.
First, recent studies in runners have highlighted that the frontal and transverse plane hip kinematics are closely linked with kinematics at the tibia and ankle. Specifically, moderate to strong correlations exist between hip internal–external rotation and tibial internal–external rotation (30), between hip internal–external rotation and rearfoot eversion–inversion (30), and between hip adduction and rearfoot eversion (2). Willson et al. (33) have previously reported that delayed onset of GMED and GMAX is associated with increased hip adduction and internal rotation excursion during running in females with patellofemoral pain. Thus, it is conceivable that altered activation of the gluteal muscles, which contributes to increased hip adduction and internal rotation (33), may be associated with increased rearfoot eversion. Interestingly, previous studies have reported increased rearfoot eversion during running in individuals with Achilles tendinopathy (8,20,27). Despite this theoretical link in the frontal and transverse planes, timing of gluteal muscle activation has not been investigated in Achilles tendinopathy.
An alternative explanation for the link between gluteal activation and Achilles tendinopathy is the established interaction between the moments acting at the hip and ankle in the sagittal plane during gait. Data from walking studies indicate that the hip and ankle may work in partnership to maintain the required support moment (19,29). For example, modifying gait to increase plantarflexion moment has been shown to result in a reduction in the extension moment acting at the hip (19). Thus, it is conceivable that, with a lower hip extension moment, compensations—such as an increase in the ankle plantarflexion moment—may occur. Such compensations may have negative implications for the Achilles tendon because a higher plantarflexion moment will likely increase the load acting on the tendon. Given that the GMAX is integral to the hip extension moment (24), alterations in GMAX activation may reflect or cause changes in the ankle plantarflexion moment and pathology in the Achilles tendon. Despite the theoretical link between GMAX activation and Achilles tendinopathy, however, differences in the timing of activation with Achilles tendinopathy have not previously been investigated.
As the evidence above has outlined, the timing of gluteal muscle activation may be linked with Achilles tendinopathy; however, this has not previously been investigated. Therefore, the aim of this study was to compare the timing of GMED and GMAX activation in male distance runners with symptomatic Achilles tendinopathy to those of healthy male distance runners. We hypothesize that runners with Achilles tendinopathy will demonstrate altered timing of GMED and GMAX activation during running.
MATERIALS AND METHODS
Fourteen males with symptomatic Achilles tendinopathy and 19 healthy male controls participated in the study. This cohort was a subgroup of participants recruited for previously published studies (5,25,34). The study was approved by the University of Melbourne Human Research Ethics Committee, and all participants provided written informed consent. Participants were recruited from the community of Melbourne, Australia, and were screened over the phone to determine eligibility. For inclusion in either group of the study, participants were to be male, older than 18 yr, and currently partaking in running activities involving ≥20 km·wk−1. Participants were excluded from either group if they had a history of previous lower limb surgery, a history of systemic inflammatory disorders, or had Achilles tendon trauma or rupture.
To be included in the Achilles tendinopathy group, participants were also required to have no other lower limb injury at the time of testing or in the past 12 months aside from symptoms of midportion Achilles tendinopathy (Achilles tendon pain with running, hopping and palpation, morning stiffness, and symptoms affecting exercise activity). Confirmation of eligibility for the symptomatic midportion Achilles tendinopathy group was made using diagnostic ultrasound. The features of tendinopathy required for inclusion in the Achilles tendinopathy group included tendon thickening and/or focal lesion (5). Control group participants were required to be injury-free at the time of testing, not had any lower limb injury that had stopped them running for more than 1 wk for the 12 months before testing, and have no observable features of tendinopathy on diagnostic ultrasound.
Participant characteristics, including age, height, weight, and weekly running volumes, were collected from all participants. In addition, the Achilles tendinopathy group completed questionnaires regarding the affected side, symptom duration, and the Victorian Institute of Sport Assessment–Achilles (VISA-A) questionnaire. The VISA-A questionnaire is a validated and reliable index of clinical severity of Achilles tendinopathy, which consists of eight questions that measure the domains of pain, function in daily living, and sporting activity (26). Results range from 1 to 100, where 100 represents an asymptomatic score. All questionnaires were completed before the commencement of running trials.
Participants were required to run at 4 m·s−1 (±10%) along a 25-m walkway in the human movement laboratory. Timing gates (Jaycar Electronics, Australia) were used to confirm the running velocity. Participants ran repeatedly along the walkway for approximately 3 min to accommodate themselves to footwear (Nike Straprunner IV running sandals; Nike, Beaverton, OR), the required speed and the equipment. A minimum of six successful trials were obtained for analysis. EMG and force plate data were recorded throughout the running trials. No subject reported that running in the prescribed footwear was uncomfortable or difficult. For the Achilles tendinopathy group, the symptomatic or most symptomatic side in the case of bilateral symptoms was tested. For the control group, the dominant leg was tested.
EMG activity was acquired via a telemetered EMG system (Glonner Biotel99; Rackenbrandt Electronik, Munich Germany) from the GMED and GMAX muscles. Recordings were performed using bipolar Ag/AgCl gel-filled self-adhesive electrodes (Kendall Medi-Trace 100; Covidien, Mansfield, MA) with a fixed interelectrode distance of 22 mm. Electrode placement locations and skin preparation procedures were in accordance with recommendations of the SENIAM group (Surface ElectroMyoGraphy for the Non-Invasive Assessment of Muscles) (13). GMED electrode placement was at 50% distance along a line from the iliac crest to the greater trochanter. GMAX electrode placement was at 50% distance along a line between the sacral vertebrae and the greater trochanter. A ground electrode was placed over the midportion of the anterior tibia. Before electrode placement, skin was shaved, lightly abraded with medical abrasion tape, and swabbed with alcohol. Electrodes were secured with a hypoallergenic tape (Fixomull; Beiersdorf Australia, North Ryde, Australia). The raw EMG signal was passed through a differential amplifier at a gain of 1000, high pass filtered at 16 Hz, 16-bit A-D converted, and sampled at 1080 Hz. For each muscle, the EMG signal was checked via visual inspection of raw EMG while the subject selectively activated the muscle. The quality of the recording for each muscle was monitored throughout the testing session. Vertical ground reaction force (Fz) data were acquired using an AMTI force plate (AMTI, Watertown, MA) mounted into the laboratory walkway. Data were captured with a Vicon 16-bit AD convertor (Oxford, UK) at a sampling rate of 1080 Hz.
Force platform data were processed using Vicon Workstation v4.6 (Vicon). Gait events of heel strike and toe-off were identified for each trial from the vertical component of the force plate data using a 10-N threshold. EMG recordings were adjusted for direct current offset, full-wave rectified, filtered to remove low-frequency movement artifact using a fourth-order Butterworth filter with a high-pass cutoff of 10 Hz, and smoothed using the moving average over a 20-ms time window. Three temporal variables were manually identified via visual inspection of EMG data: (i) onset of muscle activity (onset), (ii) offset of muscle activity (offset), and (iii) duration of muscle activity (duration). A muscle was considered active when the amplitude of EMG activity exceeded 15% of the peak amplitude for more than 10% of the stride cycle (10). Onset and offset of muscle activity were then visually confirmed as the time point relative to heel strike that the burst of muscle activity started and finished (ms). Duration was the amount of time (ms) that the muscle was active, calculated as the difference between the onset and offset times. We evaluated the reliability of this method of EMG onset and offset detection before data processing. Intraclass correlation coefficients (type 3.5) all exceeded 0.93, which demonstrate excellent reliability as defined by Landis and Koch (18).
EMG recordings were unsuccessful for two participants for GMED (two control participants) and for two participants for GMAX (one control participant and one Achilles tendinopathy participant) and were therefore excluded from analysis. All data were analyzed using Statistical Packages for Social Sciences (SPSS 19 for Windows; Norusis/SPSS, Inc, Chicago, IL). Skewness and kurtosis values indicated that the data were normally distributed. A multivariate ANCOVA with between-subject factor of group (Achilles tendinopathy, control) and variables of onset, offset, and duration was performed for each muscle. Age, weight, and height were included as covariates. The α level was set at 0.05 for all analyses. Statistically significant main effects were followed up with tests of simple effects to obtain point estimates of effect (95% confidence intervals [CI] for differences between groups). Standardized mean differences (SMD = mean difference / standard deviation) were calculated to provide an estimate of the effect. SMDs were classified as small (0.2–0.6), moderate (0.6–1.2), or large (>1.2) (15).
There were no significant differences in height, weight, or distance run each week between the two groups (P > 0.05; see Table 1). The Achilles tendinopathy group were, on average, significantly older than the control group (control 36.6 yr vs. Achilles tendinopathy 42.6 yr, P = 0.04). The Achilles tendinopathy group scored a mean ± SD of 70 ± 10 on the VISA-A.
Comparison of EMG between groups
The multivariate ANCOVA identified between-group differences for both GMED (P < 0.001) and GMAX (P = 0.004). Figure 1 illustrates the group means and 95% CI for EMG variables. For GMED, there was a delay in the onset of activity by 0.16 s (95% CI = 0.09–0.24 s, P < 0.001, SMD = 2.1) and a shorter duration of activation by 0.18 s (95% CI = 0.10–0.25 s, P < 0.001, SMD = 2.3) when compared to the control group. The magnitude of the difference observed in GMED onset and duration represents 22% and 25% of the gait cycle (stride time = 0.72 s). However, GMED offset was not significantly different (P = 0.063). GMAX followed the trend shown by the GMED with the Achilles tendinopathy group demonstrating a delay in the onset of activity by 0.09 s (95% CI = 0.03–0.16 s, P = 0.008, SMD = 1.4) and a shorter duration of activation by 0.12 s (95% CI = 0.05–0.19 s, P = 0.002, SMD = 1.8) compared to the control group. However, unlike GMED, GMAX exhibited an earlier offset of muscle activity by 0.03 s (95% CI = 0.01–0.04 s, P = 0.001, SMD = 1.5) in the Achilles tendinopathy group compared to the control group. The magnitude of the difference observed in GMAX onset, offset, and duration of activity represents 13%, 17%, and 4% of the gait cycle, respectively.
To our knowledge, this is the first study to demonstrate significant differences in the timing of the GMED and GMAX muscles in runners suffering from Achilles tendinopathy compared with uninjured healthy runners. Our findings indicate that differences in neuromotor control of the gluteal muscles exist in runners with Achilles tendinopathy, suggesting a link between the mechanics at the hip and the ankle. This may have implications for the rehabilitation and/or prevention of this pathology.
During normal running gait, it is understood that GMED typically activates before heel strike, with continued activation through early stance to stabilize the hip and maintain a level pelvis (1,28). Our findings demonstrate that before heel strike, individuals with Achilles tendinopathy had delayed onset of GMED. Conceivably, altered activation of GMED may have implications for mechanics at the knee and importantly at the ankle. Specifically, an altered GMED activation pattern, such as that observed in this study (delayed onset and shorter duration), may result in excessive hip adduction and/or internal rotation. In accordance with the kinetic chain theory (16), this would translate to internal tibial rotation and, subsequently, greater eversion of the rearfoot. This proposition is supported by previous studies. First, Willson et al. (33) have reported that, during running, greater hip adduction was correlated with delayed GMED onset. Second, other studies have reported strong associations between hip adduction and rearfoot eversion during gait, albeit during walking (2). This is consistent with previous works that have reported greater pronation and pronation velocity in participants with Achilles tendinopathy compared with healthy controls (8,20,27). In light of this and the fact that minimal differences have been reported in local muscle activation between Achilles tendinopathy and controls (1,34), it is plausible that different mechanics in runners with Achilles tendinopathy may originate from altered activation of the GMED muscle.
Although we observed differences in the onset and duration of GMED activation, we did not observe a difference in offset of this muscle’s activation. The magnitude of the difference was small (SMD = 0.4) and post hoc power calculation indicates that our sample size sufficiently powered this analysis (9). Based on these findings, the onset of GMED activation seems to be important with this pathology and guides the clinician to address GMED onset timing rather than offset timing.
GMAX is also a potent external rotator of the hip because previous research has reported that the combination of its physiological cross-sectional area and moment arm suggests a large capacity to produce an external rotation moment at the hip joint (7,24). It is plausible that an altered GMAX activation pattern, such as that observed in this study (delayed onset, earlier offset, and shorter duration), could result in GMAX not sufficiently controlling femoral position in preparation for heel strike and during stance phase. This is supported by a study on female runners with and without patellofemoral pain syndrome that reported a moderate correlation (r = −0.52) between GMAX onset time and both hip adduction and internal rotation excursions during running (33). As discussed previously, Barton et al. (2) reported strong associations between greater hip adduction and greater rearfoot eversion ranges of motion during walking. These studies support the hypothesis that altered GMAX activation may influence femoral adduction and/or internal rotation and, in turn, foot pronation. Our finding on differences in GMAX activation in individuals with Achilles tendinopathy may indicate that this link between GMAX activation and distal kinematics also influences distal injuries of the lower limb, in this case, the Achilles tendon.
GMAX is the primary hip extensor during gait, and differences in its activation, as shown in this study, will likely have significant ramifications for lower limb motor control during running. It is possible that a shorter duration of GMAX activation may result in reduced hip extensor power and forward propulsion of the center of mass (23). Previous studies in walking indicate that sagittal plane kinetics at the hip and ankle interact to maintain forward propulsion, i.e., a reduction in the moment acting at one joint will result in an increase in the moment at the other (19,29,32). Therefore, it is conceivable that a shorter duration of GMAX activation may reflect or cause an increased contribution toward forward propulsion from the ankle joint. This increased contribution from the ankle joint may be achieved by increased concentric triceps surae activation and, consequently, greater concentric load on the Achilles tendon. Studies of triceps surae muscle activation in runners with Achilles tendinopathy, however, generally report minimal differences from healthy runners and indicate that ankle moments and Achilles tendon load might not be increased with Achilles tendinopathy (1,34). Further study is therefore required to discern if altered hip and ankle kinetics exist in runners with Achilles tendinopathy.
Alterations in GMED and GMAX activation observed in the current study may occur as a consequence of the pain and dysfunction associated with the condition. Moseley et al. (21) have previously reported the influence of pain on motor control, observing delayed onset of some deep trunk muscles before voluntary arm movement in healthy subjects with anticipation of experimental back pain. In another study, Franettovich et al. (11) reported that the duration of symptoms and pain severity explained 57% of the reduction in GMED activity during walking in individuals with exercise-related leg pain. It is possible that the presence of pain in the Achilles tendon may have altered the activation patterns of the GMED and GMAX during the running task. In the current study, we cannot investigate the temporal relationship between muscle activity patterns and injury because of the cross-sectional nature of the study design. Future prospective studies are needed to discriminate whether the neuromotor control of the gluteal muscles is a consequence of the symptoms associated with Achilles tendinopathy, a predisposing factor for the disorder, or a combination of both.
It is possible that, in this group, concurrent to differences in timing of gluteal muscle activation, there may have been differences in the amplitude of gluteal muscle activation and in kinematics and kinetics. This, however, was not the aim of the current study. Future research is required to investigate amplitude of GMAX activation, hip kinematics, and hip kinetics during running in individuals with Achilles tendinopathy.
Although Achilles tendinopathy is a prominent condition found in runners, it is important to note that approximately 30% to 31% of all patients with Achilles tendinopathy are physically inactive. Moreover, we recruited male participants only because evidence suggests higher rates of Achilles tendinopathy in males than in females (14). Therefore, the results of this study might not be generalized to the entire affected population. Further studies are needed to observe the neuromotor control of the GMED and GMAX in sedentary and female populations.
In summary, this study provides preliminary evidence on altered neuromotor control of the GMED and GMAX muscles in male runners with Achilles tendinopathy. However, it is not clear whether these alterations are a predisposing factor to the condition, a consequence of the condition, or a combination of both. Further prospective studies are required to discern the temporal nature of this relationship. Nevertheless, this study highlights to clinicians the importance of considering proximal factors, such as neuromotor control of the GMED and GMAX muscles, in the assessment and management of individuals with Achilles tendinopathy. Although there are no studies to date that have investigated effective interventions for retraining gluteal muscle timing, several interventions—including biofeedback (3), strengthening (3), and taping (6)—have shown efficacy in altering the timing of other lower limb muscles. It is hoped that these results provide impetus for future studies to evaluate the effectiveness of proximal interventions for the rehabilitation or prevention of Achilles tendinopathy.
The authors thank Sally Childs, Affendi Haris Phuah, and James Pope for assistance with participant recruitment and data collection.
Footwork Podiatric Laboratory (a manufacturer of foot orthoses) provided in-kind funding to support the research program from which this study emanates. The authors have not used foot orthoses in this study and, as such, have not referred to Footwork Podiatric Laboratory within the text of this article.
The authors acknowledge no conflict of interests.
The results of the present study do not constitute endorsement by the American College of Sports Medicine.
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