Abstract
Background:Abnormal lower limb biomechanics is speculated to be a risk factor for Achilles tendinopathy. This study systematically reviewed the existing literature to identify, critique and summarise lower limb biomechanical factors associated with Achilles tendinopathy. Methods:We searched electronic bibliographic databases (Medline, EMBASE, Current contents, CINAHL and SPORTDiscus) in November 2010. All prospective cohort and case-control studies that evaluated biomechanical factors (temporospatial parameters, lower limb kinematics, dynamic plantar pressures, kinetics [ground reaction forces and joint moments] and muscle activity) associated with mid-portion Achilles tendinopathy were included. Quality of included studies was evaluated using the Quality Index. The magnitude of differences (effect sizes) between cases and controls was calculated using Cohen’s d (with 95% CIs). Results:Nine studies were identified; two were prospective and the remaining seven case-control study designs. The quality of 9 identified studies was varied, with Quality Index scores ranging from 4 to 15 out of 17. All studies analysed running biomechanics. Cases displayed increased eversion range of motion of the rearfoot (d = 0.92 and 0.67 in two studies), reduced maximum lower leg abduction (d = -1.16), reduced ankle joint dorsiflexion velocity (d = -0.62) and reduced knee flexion during gait (d = -0.90). Cases also demonstrated a number of differences in dynamic plantar pressures (primarily the distribution of the centre of force), ground reaction forces (large effects for timing variables) and also showed reduced peak tibial external rotation moment (d = -1.29). Cases also displayed differences in the timing and amplitude of a number of lower limb muscles but many differences were equivocal. Conclusions:There are differences in lower limb biomechanics between those with and without Achilles tendinopathy that may have implications for the prevention and management of the condition. However, the findings need to be interpreted with caution due to the limited quality of a number of the included studies. Future well-designed prospective studies are required to confirm these findings. Keywords:Achilles tendon, Tendinopathy, Biomechanics, Risk factor Background Achilles tendinopathy is a common musculoskeletal
and without Achilles tendinopathy that may have implications for the prevention and management of the condition. However, the findings need to be interpreted with caution due to the limited quality of a number of the included studies. Future well-designed prospective studies are required to confirm these findings. Keywords:Achilles tendon, Tendinopathy, Biomechanics, Risk factor Background Achilles tendinopathy is a common musculoskeletal dis- order that can impair physical function in daily living, occupation and sporting environments. The prevalence of Achilles tendinopathy has been reported to be greater in males [1]. The condition accounts for between 8 and 15% of all injuries in recreational runners [2-4] and has a cumulative lifetime incidence of approximately 24% in athletes [5]. Although Achilles tendinopathy is common in athletes, one-third of patients with chronic Achilles tendinopathy are not physically active [6]. In some set- tings, approximately 30% of patients who present with this condition undergo surgical treatment [6,7]. Achilles tendinopathy is considered a multifactorial condition, with both extrinsic and intrinsic factors thought to contribute to its development [8-10]. Pro- posed extrinsic risk factors include altered weightbearing surfaces (excessively hard, slippery or uneven) [8,10], * Correspondence: s.munteanu@latrobe.edu.au 1 Musculoskeletal Research Centre, Faculty of Health Sciences, La Trobe University, Bundoora 3086, Victoria, Australia Full list of author information is available at the end of the article Munteanu and BartonJournal of Foot and Ankle Research2011,4:15 http://www.jfootankleres.com/content/4/1/15 JOURNAL OF FOOT AND ANKLE RESEARCH © 2011 Munteanu and Barton; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
inappropriate footwear [8,10,11], training errors [10], use of specific medications such as fluoroquinolones [12] and the type of exercise activity (e.g., sports involving the stretch-shorten cycle such as running or jumping) [5]. Proposed intrinsic risk factors include previous injury [8], increased age [13], presence of specific genetic variations such as polymorphisms occurring within the COL5A1 and tenascin-C genes [14], male gender [15], increased adiposity and/or metabolic disor- ders [16,17], pre-existing tendon abnormalities [18], tri- ceps surae inflexibility [10,19], hormonal status [20-22] and abnormal lower limb biomechanics [8,10,15,23]. Alterations in lower limb biomechanical characteris- tics including temporospatial parameters, lower limb kinematics, dynamic plantar pressures, kinetics (ground reaction forces and joint moments) and muscle activity are frequently associated with Achilles tendinopathy [8,15,23]. One biomechanical factor commonly consid- ered to be associated with Achilles tendinopathy is the presence of excessive foot pronation [8]. Clement et al. [10] originally proposed that excessive pronation of the foot may lead to Achilles tendinopathy through two mechanisms. First, excessive pronation of the foot is speculated to create greater hindfoot eversion motion, resulting in excessive forces on the medial aspect of the tendon and subsequent microtears. Second, abnor- mal pronation of the foot is thought to lead to asyn- chronous movement between the foot and ankle during the stance phase of gait, resulting in a subse- quent‘wringing’effect within the Achilles tendon. This ‘wringing’effect is theorised to cause vascular impair- ment within the tendon and peritendon [10] and ele- vated tensile stress [24] leading to subsequent degenerative changes in the Achilles tendon. In addi- tion to kinematic theories, altered lower limb muscle function (timing, amplitude or co-ordination of con- tractions of the triceps surae) [23-26] and altered lower limb kinetics [11,24,25,27] have also been specu- lated to be risk factors for Achilles tendinopathy by increasing tendon loading. Several studies have beenperformed to investigate the association between abnormal lower limb biome- chanics and Achilles tendinopathy. Critiquing and summarising results from these studies is now required to assist in the development of; (i) preventative strate- gies, and; (ii) specific and effective management strate- gies for the condition. However, at present, the
factors for Achilles tendinopathy by increasing tendon loading. Several studies have beenperformed to investigate the association between abnormal lower limb biome- chanics and Achilles tendinopathy. Critiquing and summarising results from these studies is now required to assist in the development of; (i) preventative strate- gies, and; (ii) specific and effective management strate- gies for the condition. However, at present, the aetiology of Achilles tendinopathy is not clearly under- stood [8]. Therefore, the aim of the present study was to perform a systematic review of the existing litera- ture (prospective cohort and retrospective case-control studies) to identify, critique and summarise lower limb biomechanical factors associated with Achilles tendinopathy. Methods Inclusion and exclusion criteria Prospective cohort and case-control studies evaluating biomechanical factors associated with mid-portion Achilles tendinopathy (i.e., 2-6 cm proximal to its inser- tion) were considered for inclusion. The inclusion cri- teria required participants to be described as having: midsubstance tendinopathy of the Achilles, Achilles ten- dinitis, tenosynovitis or tendinosis[28]. Additional terms such asAchilles tendinopathy, tenopathy, tendinosis, partial rupture, paratenonitis, tendovaginitis, peritendi- nitis and achillodyniahave also been used to describe the problems of non-insertional pain associated with the Achilles tendon so were also used [29]. Measures of interest were gait characteristics including temporospa- tial parameters, lower limb kinematics, dynamic plantar pressures, kinetics (ground reaction forces and joint moments) and muscle activity. Unpublished studies, case-series studies, non-peer- reviewed publications, intervention studies, studies not involving humans, reviews, letters, opinion articles, non- English articles and abstracts were excluded. Studies which included participants with concomitant injury or pain from structures other than the mid-portion of the Achilles tendon (e.g., insertional Achilles tendon pathol- ogy) or that failed to localise the pathology in the ten- don were excluded. Search Strategy MEDLINE (OVID) (1950-), EMBASE (1988-), CINAHL (1981-), SPORTDiscus and Current Contents (1993 week 27-) electronic databases were searched in November 2010 (week 3). A generic search strategy was formulated [28,30] and the results are reported in Additional Data File 1. Review process All titles and abstracts found were downloaded into Endnote version XI (Thomson Reuters, Philadelphia, PA) giving a set of 2701 citations. The set was
(1981-), SPORTDiscus and Current Contents (1993 week 27-) electronic databases were searched in November 2010 (week 3). A generic search strategy was formulated [28,30] and the results are reported in Additional Data File 1. Review process All titles and abstracts found were downloaded into Endnote version XI (Thomson Reuters, Philadelphia, PA) giving a set of 2701 citations. The set was cross- referenced and any duplicates were deleted, leaving a total of 1575 citations. Each title and abstract was evalu- ated for potential inclusion by two independent reviewers (SEM and CJB) using a checklist developed from the inclusion/exclusion criteria outlined above (see Additional File 2). If insufficient information was con- tained in the title and abstract to make a decision on a study, it was retained until the full text could be obtained for evaluation. Any disagreements regarding studies were resolved by a consensus meeting between the two reviewers. Methodological quality assessment The methodological quality of each included study was assessed using 16 items (maximum score of 17) of the Munteanu and BartonJournal of Foot and Ankle Research2011,4:15 http://www.jfootankleres.com/content/4/1/15 Page 2 of 16
‘Quality Index’considered relevant for assessing pro- spective cohort and case-control study designs (Table 1) [31]. The original Quality Index scale consisting of 26 items was shown to have high internal consistency (KR- 20 = 0.89), test-retest (r = 0.88) and inter-rater (r = 0.75) reliability and high criterion validity (r≥0.85) [31]. Two reviewers (SEM andCJB) applied the quality index to each included study independently, and any scoring discrepancies were resolved through a consensus meeting. Statistical analysis Inter-rater reliability of each item of the Quality Index was evaluated using unweighted kappa and percentage agreement statistics, and the overall score was evaluated using the intra-class correlation coefficient (ICC 3,1) with corresponding 95% confidence intervals (CIs). Means and standard deviations for all continuous data were extracted and effect sizes (Cohen’ s d) (with 95% CIs) calculated to allow comparison between each study’s results. To allow visual comparison, effect sizes were entered into forest plots. Categorical data (e.g. fre- quency of foot type) was compared between groups using odds ratios (with 95% CIs) transformed to effect sizes (with 95% CIs) as described by Chinn et al. [32] Calculated effect sizes were considered statistically sig- nificant if their 95% CI did not cross zero. If inadequate data were available from original studies to complete effect size calculations, attempts were made via email to contact the study’s corresponding author for additional data. Sample sizes (limbs analysed), the presence or absence of symptoms, participant demographics (gender, age, BMI, mass, height, duration of symptoms and sporting experience) and biomechanical analysis details were also extracted to assist in interpretation of findings. Results Following the search, nine studies were deemed appro- priate for inclusion [2,11,19,24,25,27,33-35]. This included two prospective cohort [2,19] and seven case- control study designs [11,24,25,27,33-35]. There were no disagreements amongst reviewers. One study [33] did not contain appropriate data to complete effect size cal- culations, meaning data extraction (effect size calcula- tions) was performed on a total of eight studies [2,11,19,24,25,27,34,35]. Quality assessment of included studies All individual items from the Quality Index scale demonstrated high inter-rater reliability (kappas≥0.57) with percentage agreement≥77.8% (Table 1). The total score
no disagreements amongst reviewers. One study [33] did not contain appropriate data to complete effect size cal- culations, meaning data extraction (effect size calcula- tions) was performed on a total of eight studies [2,11,19,24,25,27,34,35]. Quality assessment of included studies All individual items from the Quality Index scale demonstrated high inter-rater reliability (kappas≥0.57) with percentage agreement≥77.8% (Table 1). The total score obtained from the Quality Index scale demon- strated high inter-rater reliability (ICC 3,1= 0.98). Additional data Additional data required to complete effect size calcula- tions was provided by Baur et al. [11]. Additionally, Van Ginckeletal.[2]providedreviseddataforsome reported variables which were reported erroneously in their manuscript. Methodological data to assist interpretation of results Table 2 shows the samples sizes and population charac- teristics. Table 3 shows thebiomechanical analysis details of each of the included studies. Differences in lower limb biomechanics between those with and without Achilles tendinopathy Temporospatial gait characteristics Four [11,24,33,34] studies controlled gait velocity. Of the remaining five studies [2,19,25,27,35], only one [27] reported temporospatial data, with effect size calcula- tions indicating no differences in velocity, stride length, stride time or stride frequency between cases and con- trols. Additionally, another study [35] reported that no significant differences in gait velocity were evident between groups but did not present supporting data. Lower limb kinematics Three studies investigated frontal plane rearfoot kine- matics (Figure 1) [25,34,35]. Those with Achilles tendi- nopathy displayed greater rearfoot eversion range of motion when shod (d = 0.92) but not unshod [34] and greater eversion range of motion of the ankle/rearfoot (d = 0.67) [35]. Effect size calculations for all other fron- tal plane rearfoot kinematics comparisons were not sta- tistically significant. Four studies investigated tibial segment and ankle joint kinematics (Figure 2) [24,27,34,35]. Donoghue et al.[34]showedreducedmaximumlowerlegabduction (barefoot) in cases (d = -1.16). Ryan et al. [35] showed reduced maximum ankle dorsiflexion velocity in cases (d = -0.62). All other tibial segment and ankle kinematic comparisons were not significantly different between groups [24,27,34,35]. Three studies performed analyses for knee and hip kinematics (Figure 3) [24,27,34]. Azevedo et al. [27] reported that the magnitude of knee flexion between
(barefoot) in cases (d = -1.16). Ryan et al. [35] showed reduced maximum ankle dorsiflexion velocity in cases (d = -0.62). All other tibial segment and ankle kinematic comparisons were not significantly different between groups [24,27,34,35]. Three studies performed analyses for knee and hip kinematics (Figure 3) [24,27,34]. Azevedo et al. [27] reported that the magnitude of knee flexion between heel strike and midstance was significantly reduced in cases (d = -0.90). Effect size calculations for all other knee joint kinematics comparisons were not significantly different between groups [24,27,34]. There were no sta- tistically significant effects for comparisons in sagittal plane hip kinematics [27]. Plantar pressure parameters A large number of plantar pressure parameters were analysed across three studies [2,11,19] (Figures 4A-D and 5). A prospective study by Van Ginckel et al. [2] showed that those who developed Achilles tendinopathy Munteanu and BartonJournal of Foot and Ankle Research2011,4:15 http://www.jfootankleres.com/content/4/1/15 Page 3 of 16
Table 1 Modified Downs and Black Quality Index results, and inter-rater reliability for each item and total score Prospective (P) or retrospective case-control (R) study (1) Clear aim/ hypothesis (2) Outcome measures clearly described (3) Participant characteristics clearly described (5) Confounding variables (age, gender, BMI/height/ weight and participant activity levels) described (6) Main findings clearly described (7) Measures of random variability provided (10) Actual probability values reported (11) Participants asked to participate representative of entire population (12) Participants prepared to participate representative of entire population (15) Blinding of outcome assessor (16) Analyses performed were planned (18) Appropriate statistics (20) Valid and reliable outcome measures (21) Appropriate case-control matching (same population) (22) Participants recruited over the same period of time (25) Adjustment made for confounding factors Total Azevedo et al. [27] R111 2111U U U11UUU111 Baur et al. [11] R110 0000U U U11UUUU4 Donoghue et al. [34] R110 11100 0 U11UUU07 Donoghue et al. [33] R110 11110 0 U11UUU08 Kaufman et al. [19] P111 11111 U 111U11013 McCrory et al. [25] R110 1110U U U11UUU18 Ryan et al. [35] R101 1111U U U11U1U110 Williams et al. [24] R111 2111U U 011UUU111 Van Ginckel et al. [2] P111 21111 U 111U11115 % agreement 100.0 100.0 100.0 77.8 88.9 88.9 88.9 88.9 88.9 77.8 88.9 88.9 100.0 77.8 100.0 88.9 Reliability 1.00 1.00 1.00 0.63 0.61 0.61 0.77 0.82 0.74 0.57 Uc Uc 1.00 0.63 1.00 0.80 0.98 (0.905- 0.995) (For items 1-3, 6, 7, 10-12, 15, 16, 18, 20, 21, 22 and 25)-0: No, 1: Yes, U: Unable to determine (which received a score of 0) (For item 5)-0: No, 1: Partially, 2: Yes Abbreviations: Uc; Results not distributed appropriately for this statistic to be calculated. Munteanu and BartonJournal of Foot and Ankle Research2011,4:15 http://www.jfootankleres.com/content/4/1/15 Page 4 of 16
Table 2 Sample sizes and population characteristics from each included study StudySymptomatic (yes/no) Sample size (limbs) Gender (n) (Male/Female) Mean age ± SD (range) (years) Mass (kg), height (cm), BMI Experience: years of sporting activity AT C AT CATCATCATC Azevedo et al. [27] Yes 21 21 16/5 16/5 41.8 ± 9.7 (NR) 38.9 ± 10.1 (NR) 77.6, 177.8, NR 70.2, 174.3, NR > 3 years* Baur et al. [11]Yes 16 28 NR NR36 ± 9 (NR)*73, 179, NR*NR‘experienced’* Donoghue et al. [33] No 12 12 11/1 11/1 38.7 ± 8.1 (NR) 44.3 ± 8.4 (NR) 73.3, 175, NR 79.3, 178, NR NRNR Donoghue et al. [34] No 11 11 10/1 10/1 39.6 ± 7.7 (NR) 45.2 ± 8.1 (NR) 71.9, 174, NR 77.9, 177, NR NRNR Kaufman et al. [19] No 17 299 17/0 299/022.5 ± 2.5 (NR)*78.0, 177.0, NR*2-7 times/week fitness preparation, 73% reported having run or jogged on a regular basis for a period of 3 or more months before reporting to training* McCrory et al. [25] Yes 31 58 NR NR 38.4 ± 1.8 (NR) 34.5 ± 1.2 (NR) 71.4, 174.5, NR 70.0, 174.5, NR 11.9 ± 1.4 9.6 ± 0.8 Ryan et al. [35]Yes 27 21 NR NR 40 ± 7 (NR) 40 ± 9 (NR) 78, 181, NR 71, 177, NR NRNR Van Ginckel et al. [2] No 10 53 2/8 8/45 38.0 ± 11.35 (NR) 40.0 ± 9.00 (NR) 69.8, 167.1, 24.95 70.0, 168.3, 24.69 00 Williams et al. [24] No8 8 6/2 5/3 36.0 ± 8.2 (NR) 31.8 ± 9.3 (NR) 67.3, 176, NR 65.6, 170, NR 19.1 ± 7.7 11.0 ± 9.1 Abbreviations: AT, Achilles tendinopathy group; C, control group; NR, not reported; *, Specified total group characteristics only Munteanu and BartonJournal of Foot and Ankle Research2011,4:15 http://www.jfootankleres.com/content/4/1/15 Page 5 of 16
demonstrated significantly reduced displacement of the posterior-anterior component of the centre of force at last foot contact (d = -0.95), posterior-anterior displace- ment of the centre of force during forefoot push-off phase (d = -0.75), total posterior-anterior displacement of the centre of force (d = -0.95) and medio-lateral force distribution under the metatarsal heads at forefoot flat (d = -0.93) (Figure 4A). Further those who developed Achilles tendinopathy displayed reduced timing of initial contact at the second metatarsal head region (d = -1.00) (Figure 4B), relative peak force at the medial heel (d = -0.73), time to peak force at the lateral heel (d = -1.08) and at the medial heel (d = -0.72) regions (Figure 4C). Additionally, increases were found for peak force at the fifth metatarsal head region (d = 0.84) (Figure 4C) and force-time integral at the fifth metatarsal head region (d = 0.81) (Figure 4D) in those who developed Achilles tendinopathy [2]. Figure 5 shows that lateral deviation of the centre of pressure in the rear-and mid-foot (Alat [barefoot]) was significantly reduced in cases (d = -0.98) [11]. The fre- quency of dynamic pes planus or pes cavus (assessed using dynamic arch index in both barefoot and shod conditions) was not significantly different between those who did and did not develop Achilles tendinopathy [19]. Lower limb external kinetics One study analysed lower limb joint moments (Figure 6). Peak tibial external rotation moment was signifi- cantly reduced in cases (d = -1.29) [24]. Three studies analysed ground reaction forces [11,25,27] (Figure 7A-C). The normalised time to first vertical peak (d = 19.54) [25] and normalised time to Table 3 Lower limb biomechanical analyses, gait characteristics and footwear conditions of included studies Study Biomechanical variable(s) Gait characteristics Footwear condition(s) Azevedo et al. [27] Muscle activity (integrated EMG: normalised EMG amplitude as a percentage of root mean square amplitude): tibialis anterior, peroneus longus, lateral gastrocnemius, rectus femoris, biceps femoris and gluteus medius; Kinematics (3D using Vicon ® System 370 Version 2.5): sagittal plane hip, knee and ankle joints; Kinetics: anterior-posterior and vertical ground reaction force; Temporospatial parameters (speed, stride