Evaluating eccentric hip torque and trunk endurance as mediators of changes in lower limb and trunk kinematics in response to functional stabilization training in women with patellofemoral pain.

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Evaluating Eccentric Hip Torque and Trunk Endurance as Mediators of Changes in Lower Limb and Trunk Kinematics in Response to Functional Stabilization Training in Women With Patellofemoral Pain Rodrigo de Marche Baldon, Sara Regina Piva, Rodrigo Scattone Silva and Fábio Viadanna Serrão Am J Sports Med published online March 19, 2015 DOI: 10.1177/0363546515574690 The online version of this article can be found at: http://ajs.sagepub.com/content/early/2015/03/18/0363546515574690

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Evaluating Eccentric Hip Torque and Trunk Endurance as Mediators of Changes in Lower Limb and Trunk Kinematics in Response to Functional Stabilization Training in Women With Patellofemoral Pain Rodrigo de Marche Baldon,* PT, PhD, Sara Regina Piva,y PT, PhD, Rodrigo Scattone Silva,y PT, MSc, and Fa´bio Viadanna Serraõ,yz PT, PhD Investigation performed at Federal University of Saõ Carlos, Saõ Carlos, Brazil Background: Altered movement patterns of the trunk and lower limbs have been associated with patellofemoral pain (PFP). It has been assumed that increasing the strength of the hip and trunk muscles would improve lower limb and trunk kinematics in these patients. However, evidence in support of that assumption is limited. Purpose: To determine whether increases in the strength of hip muscles and endurance of trunk muscles in response to functional stabilization training will mediate changes in frontal plane lower limb kinematics in patients with PFP. Study Design: Controlled laboratory study. Methods: Thirty-one female athletes were randomized to either a functional stabilization training group that emphasized strengthening of the trunk and hip muscles or a standard training group that emphasized stretching and quadriceps strengthening. Patients attended a baseline assessment session, followed by 8 weeks of intervention, and were then reassessed at the end of the intervention period. The potential mediators that were evaluated included eccentric torque of hip muscles and endurance of the trunk muscles. The outcome variables were the lower limb and trunk kinematics in the frontal plane assessed during a single-legged squat task. Results: The eccentric strength of the gluteus muscles showed a mediation effect ranging from 18% to 32% on changes to frontal plane kinematics (decreased ipsilateral trunk inclination, pelvis contralateral depression, and hip adduction excursions) observed in the functional stabilization training group after intervention. Conclusion: Although the mediation effects were small, the results suggest that improvements in the strength of the gluteus muscles can influence the frontal plane movement patterns of the lower limb and trunk in women with PFP. Clinical Relevance: Patients with PFP might benefit from strengthening of the hip muscles to improve frontal plane lower limb and trunk kinematics during functional tasks. Keywords: knee; patella; biomechanics; clinical assessment; rehabilitation; injury prevention

Patellofemoral pain (PFP) is one of the most common overuse disorders of the knee treated in general practice.39 Patients with a history of PFP have an increased risk for developing patellofemoral osteoarthritis.41 Additionally, up to 91% of patients with a diagnosis of PFP will complain of knee pain and limited physical function several years after initial presentation.38 Studies have shown that patients with PFP have poor trunk and hip movement

control, and these alterations to kinematics have been associated with increased patellofemoral joint stress and pain.19,29,30,32 Specifically, in the frontal plane, patients with PFP exhibit increased hip adduction, contralateral pelvis depression, and ipsilateral trunk inclination during weightbearing activities when compared with healthy subjects.29,42,43 Excessive hip adduction is thought to increase the quadriceps angle and the lateral pressure on the patellofemoral joint.19 Excessive trunk ipsilateral inclination is thought to be a compensatory movement, performed to prevent contralateral pelvis depression. However, during single-legged activities, excessive ipsilateral trunk inclination moves the ground-reaction force laterally to the knee

The American Journal of Sports Medicine, Vol. XX, No. X DOI: 10.1177/0363546515574690 Ó 2015 The Author(s)

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joint and increases the external knee abduction moment and the quadriceps angle, contributing to PFP.6,35 Given that the hip abductor, lateral rotator, and extensor muscles, along with the trunk muscles, control the movements of the hip joint and the trunk in closed kinetic chain activities, it has been commonly assumed that improving the strength of these muscles is associated with improvements in lower limb and trunk kinematics.10,11,21,31 However, previous research has reported that improvements in hip and trunk strength do not necessarily affect lower extremity kinematics,8,13 suggesting that factors other than muscle strength might play a relevant role in frontal plane kinematics. We recently reported results of a randomized clinical trial comparing 2 exercise approaches for treating patients with PFP.2 The training program that primarily focused on hip and trunk strengthening—named functional stabilization training (FST)—successfully improved lower limb kinematics in the frontal plane in comparison to a more traditional training program—named standard training (ST)—focused on quadriceps strengthening. Although we hypothesized that the strengthening of the hip muscles might have been associated with these changes to kinematics, a mediator analysis was necessary to confirm or reject this hypothesis. Treatment mediators identify possible mechanisms through which a treatment might achieve its effects and that could be considered causal links between treatment and outcome.22 Understanding the mechanisms through which a treatment operates facilitates the development of interventions where efficient components might be reinforced and refined and where redundant components could be discarded. Thus, this study aimed to examine the mechanisms by which a training program focusing on hip and trunk strengthening (in this case, the previously reported FST) leads to changes in kinematics. Specifically, we tested if the increases in hip strength and trunk endurance as a result of the participation in FST were mediators of changes in hip adduction, pelvis depression, and trunk ipsilateral inclination observed in patients with PFP.

analog scale for a minimum of 8 weeks; (2) anterior or retropatellar knee pain during at least 3 of the following activities—ascending/descending stairs, squatting, running, kneeling, jumping and prolonged sitting; and (3) insidious onset of symptoms unrelated to trauma. The exclusion criteria adopted in the study were the following: previous surgery in the lower limbs, presence of intra-articular pathologic abnormalities, involvement of the collateral or cruciate ligaments, patellar instability, Sinding-LarsenJohansson or Osgood-Schlatter syndrome, knee joint effusion, hip pain, or palpation of the iliotibial band, patellar tendon, or pes anserinus tendons that reproduced the patient’s pain.4,30

Randomization Randomization was done in blocks of 4. Consecutively numbered opaque envelopes were prepared ahead of time with the randomization scheme using a computer-generated table of random numbers. A person unaware of any information about the patients performed the randomization and provided the assignment to the treating physical therapist. Randomization was performed after the baseline assessment, and the patients were blinded to group allocation.

Procedures All patients read and signed an informed consent form. This study was approved by the Ethics Committee for Research on Human Subjects of the Federal University of Saõ Carlos. Patients attended a baseline assessment, followed by 2 months of intervention, and were then reassessed. The assessments consisted of an evaluation of trunk, pelvis, and lower extremity kinematics during a single-legged squat task. They also involved trunk muscle endurance tests and eccentric hip isokinetic torque evaluations. All assessments were performed on the most painful limb according to the patient’s perception.

Outcome Measures METHODS Patients This study used data from a previous randomized controlled single-blind study (for details, see Baldon Rde et al2). Thirty-one female recreational athletes between 18 and 30 years of age with PFP were randomly assigned to the FST (n = 15) or ST (n = 16) group. Patients were recruited between March and November of 2012. Eligibility criteria included (1) anterior knee pain of at least 3 cm on a visual

Kinematics Evaluation. Trunk, pelvis, and lower extremity kinematics in the frontal plane were assessed during a single-legged squat task using the Flock of Birds electromagnetic tracking system (Ascension Technology Corp) integrated with the MotionMonitor software (Innovative Sports Training Inc). The single-legged squat was chosen because it is a task frequently used in research to assess lower limb biomechanics in people with PFP.12,30 Also, altered movement patterns during the single-legged squat task have been shown to reflect poor movement

z Address correspondence to Fa´bio Viadanna Serraõ, PT, PhD, Department of Physiotherapy, Federal University of Saõ Carlos, Rodovia Washington Luis, km 235, CEP: 13565-905, Saõ Carlos, SP, Brasil (e-mail: [email protected]). *Department of Physiotherapy, Federal University of Saõ Carlos, Saõ Carlos, Brazil. y Department of Physical Therapy University of Pittsburgh, Pittsburgh, Pennsylvania, USA. One or more of the authors has declared the following potential conflict of interest or source of funding: This project was financially supported by the Coordenacxaõ de Aperfeicxoamento de Pessoal de Nı´vel Superior (CAPES).


Vol. XX, No. X, XXXX

Gluteal Strength as Mediator of Improvement in Kinematics

Figure 1. (A) Patient performing the single-legged squat task. (B) Real-time visualization during the kinematic evaluation and definitions of the kinematic variables of interest.

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Kinematics data were filtered using a fourth-order, zero-lag, low-pass Butterworth filter at 6 Hz. The Euler angles were calculated using the joint coordinate system definitions recommended by the International Society of Biomechanics per the MotionMonitor software.45 The kinematic variables studied were trunk ipsilateral/contralateral inclination, pelvis contralateral elevation/depression, and hip adduction/abduction (Figure 1B). Trunk ipsilateral inclination, pelvis contralateral depression, and hip adduction were considered positive values. The pelvis movement angles were calculated using the laboratory frame, while the other angles were calculated using the patient frame. The variables represented the movement excursions, which were calculated by subtraction of the values acquired when the knee was at 60° of flexion from that recorded in the single-legged static position. Reliability of this movement analysis protocol is adequate, with intraclass correlation coefficients (ICCs) ranging from 0.92 to 0.95 and standard errors of measurement ranging from 0.07° to 1.83°.30 The kinematics data were processed using custom MATLAB software (MathWorks Inc).

Potential Mediators 42

control in other functional activities, such as running and jump landings.40,42 Before testing, 5 electromagnetic tracking sensors were attached to the sternum, sacrum (S2), and midlateral thighs and medial to the tibial tuberosity using double-sided adhesive tape. The kinematics data were collected at a sampling rate of 90 Hz.30 Before dynamic testing, the medial and lateral malleoli and femoral epicondyles were digitized to determine the ankle and knee joint centers, respectively. The hip joint center was estimated using the functional approach described elsewhere.23 The C7-T1, T12-L1, and L5-S1 joint spaces were also digitized, and the trunk and pelvis angles were designated by the sternal and sacral sensors. A static frame was taken with the patient standing on both legs to determine the neutral alignment angles of the joints. Then, the patients were asked to stand on the affected lower limb, with the knee of the contralateral limb at 90° of flexion, hip in neutral position, and the arms crossed in front of the thorax (single-legged static position) (Figure 1A) for the anatomic frame. Kinematics variables were calculated using the data collected in this position as reference. Patients were then asked to squat from the static position to at least 60° of knee flexion and then return to the starting position. To ensure that the desired knee flexion had been reached, the task was visually inspected in real time using the MotionMonitor software (Innovative Sports Training Inc). The execution time of the single-legged squat was standardized at 2.0 6 0.3 seconds. Each patient completed 3 attempts for familiarization and 5 acceptable trials for data analysis, with a 1-minute rest interval between trials. If any of the evaluation requirements were violated or if the patients lost balance during the task, the attempt was invalidated and repeated. The average kinematics data obtained from 5 acceptable trials were used for the statistical analysis.

Trunk Muscle Endurance Evaluation. Trunk muscle endurance was defined as the time that a patient could hold a predefined static position. The endurance of the posterior trunk muscles was assessed with the patients lying prone with the lower body fixed to the test bench at the knees and hips. Before testing, the upper body of the patient was held out of the test bench with the arms resting on the ground. At the beginning of the test, each patient was instructed to extend her upper body and hold it horizontal to the floor with upper limbs across the chest.26 Endurance of the anterior trunk muscles was assessed with the patient holding the body in a straight line while supported only by both forearms and feet.7 Endurance of the lateral muscles of the trunk was quantified with the patients in a side-lying position on the affected side. Each patient was instructed to support herself only on 1 forearm and her feet and to lift her hips off the test bench and sustain the full body straight. The arm of the uninvolved side was held beside the trunk. The tests were conducted in a random order, and all tests were interrupted when the patients were not able to sustain the position. A single trial of each position was performed with a 2-minute rest interval between positions. The duration of time in seconds that the patients could hold the positions was used for the statistical analysis. Reliability of these tests has been reported to be excellent, with ICCs ranging from 0.95 to 0.99 and standard errors of measurement ranging from 3.40 to 9.93 seconds.7,26 Eccentric Hip Torque Evaluation. The eccentric hip torque variables were quantified in a random order using an isokinetic dynamometer Biodex Multi-Joint System 2 (Biodex Medical System Inc) at an angular speed of 30 deg/s. Data were recorded using the Biodex Advantage Software 4.0 at a sampling rate of 100 Hz. Eccentric torque evaluations were chosen because they better represent the muscle


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action necessary during functional weightbearing activities. This assessment was performed 48 to 96 hours after the trunk endurance evaluation. Eccentric hip abductor and adductor torques were tested with the patients in a side-lying position. The evaluated hip was positioned superiorly and in neutral alignment in all 3 planes. The contralateral hip and knee were flexed and fixed with straps, and the trunk was stabilized using a single belt proximal to the iliac crest. The rotational axis of the dynamometer was aligned with the hip joint center in the frontal plane, and the lever arm was laterally attached to the thigh under test, 5 cm proximal to the base of the patella. The test was from 0° (neutral) to 30° of hip abduction.1 The main muscles that generate eccentric hip abductor torque at this position are all fibers of the gluteus medius, gluteus minimus, and tensor fasciae latae. The main muscles generating eccentric hip adductor torque are the pectineus, adductor longus, gracilis, adductor brevis, and adductor magnus (both anterior and posterior heads).33 For the eccentric test of the hip medial and lateral rotator muscles, patients were placed in sitting position with their knees and hips flexed at 90°. The rotational axis of the dynamometer was aligned with the center of the patella and the lever arm attached 5 cm proximal to the lateral malleolus. The distal thigh of the lower limb under test and the trunk were stabilized with straps. The range of motion of this test was from 10° of hip medial rotation to 20° of hip lateral rotation.1 The main muscles responsible for producing eccentric hip medial rotator torque with the hip positioned in 90° of flexion are all fibers of the gluteus medius, gluteus minimus, tensor fasciae latae, piriformis, and most portions of the gluteus maximus. The muscles producing eccentric hip lateral rotator torque in this position are the deep hip muscles, which include the obturator externus, obturator internus, and quadratus femoris.5,33 Before testing, the patients performed 5 submaximal and 2 maximal reciprocal eccentric contractions of each test for familiarization. After 3 minutes of rest, the patients performed 2 series of 5 maximal repetitions with a 3-minute rest period between them. Verbal encouragement was provided to stimulate the patients to produce maximum torque. To correct for the influence of gravity on the torque data, the limb was weighed before each test according to the instructions manual of the dynamometer. For statistical analysis, the peak torque from either the first or second series normalized by body mass (Nm/kg) was used. Reliability of these tests are adequate, with ICC3,1 ranging from 0.78 to 0.97.1

Interventions Treatment started 3 to 5 days after baseline isokinetic assessment. Patients from both groups performed the training protocol 3 times per week for 8 weeks with at least 24 hours between intervention sessions. All sessions were supervised by a physical therapist. For both groups, the initial loads for most strengthening exercises were based on the 1-repetition maximum performed at the beginning of week 1 and repeated at the beginning of the weeks 3

Figure 2. The 3-variable framework showing the direct (c) and indirect (a ! b) paths. and 6. During the exercises, the knee pain could not be higher than 3 on a scale of 0 to 10. The loads were progressed when the patients were able to perform the set of exercises without exacerbation of knee pain or excessive fatigue and if they had no more local muscle pain 48 hours after the previous training session. The FST consisted of weightbearing and nonweightbearing exercises to enhance the strength of the trunk and hip muscles. The main objective of the first 2 weeks (phase 1) was to improve motor control of the trunk and hip muscles mainly using nonweightbearing exercises. For the next 3 weeks (phase 2), the main objective was to increase strength of the trunk and hip muscles using weightbearing activities. In the final 3 weeks of treatment (phase 3), patients were continually educated to perform the functional exercises with the lower extremities in neutral frontal alignment and to avoid quadriceps dominance by leaning the trunk forward, with hinging at the hips. The ST consisted of stretching exercises of the hamstrings, ankle plantar flexors, quadriceps, lateral retinaculum, and iliotibial band, as well as traditional weightbearing and nonweightbearing exercises for quadriceps strengthening. For a detailed description of the exercises with their progression for both groups, see Baldon Rde et al.2

Statistical Analysis Data were analyzed with respect to their distribution and homogeneity of variance using the Shapiro-Wilk and Levene tests, respectively. To assess mediation effects, we followed the 3-variable framework described by MacKinnon et al25 (Figure 2). In this model, the intervention condition FST versus ST (predictor) is assumed to have both direct and indirect paths to the changes in frontal plane kinematics (outcomes). As shown in Figure 2, c is considered the direct path, whereas a ! b is the indirect path passing through the isokinetic hip torque and endurance trunk variables (potential mediators). According to Baron and Kenny,3 4 conditions must be present for a variable to be considered a mediator: (1) the predictor must be significantly associated with the outcome, (2) the predictor must be significantly associated with the hypothesized mediator, (3) the mediator must be significantly associated with the outcome after controlling for the predictor, and (4) the effect of the predictor on the outcome must be small after controlling for the mediator.




TABLE 1 Demographic Characteristics of Randomized Patients at Baselinea Variable

ST Group

Age, y Height, m Mass, kg Body mass index, kg/m2

22.78 1.66 57.37 20.73

6 6 6 6

3.31 0.08 8.41 2.09

FST Group 21.31 1.62 58.31 22.27

6 6 6 6

2.65 0.06 7.29 2.52

a

Data are presented as mean 6 SD. FST, functional stabilization training; ST, standard training.

The assumptions above were tested with 3 multiple regression analysis as suggested by Holmbeck.18 The first regression tested the association between the predictor and the outcomes (first assumption), and the second regression tested the association between the predictor and the potential mediators (second assumption). The third regression tested the association between the potential mediators and the outcomes after controlling for the predictor (third assumption). Then, it was observed whether the association of the predictor with the outcome after controlling for the potential mediators was smaller than that observed in the first regression (fourth assumption). Specifically, the greater the reduction in the unstandardized coefficients (B) in the third regression compared with the first regression, the greater the potency of the mediator. When all assumptions were satisfied, the indirect effect was determined, which is mathematically equivalent to the drop in the B total effect (path c) after the mediator is in the model (path a ! b). Also, the standard error of the indirect effect was calculated using the Sobel test. Finally, statistical tests for the indirect effects were conducted as suggested by Holmbeck17 to determine the

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percentage of changes in outcome that were accounted by the mediator. A preset a level of .10 was used for all the statistical tests and the regression analysis, which were performed using SPSS statistical software (version 21; SPSS Inc). For potential mediators and outcomes, we used change scores between the end of intervention and the baseline assessments.

RESULTS Sixty-three patients were screened and 31 fulfilled the eligibility criteria and were randomly assigned to the FST group (n = 15) or the ST group (n = 16). The CONSORT diagram with the flowchart of the patients in the study has been reported.2 There was 1 dropout in the FST group during intervention period. Consequently, 30 patients concluded the assessment at the end of the intervention and were therefore used in the statistical analysis. The baseline demographic characteristics and the change scores for the potential mediators and outcomes in both groups are described in Table 1 and Table 2, respectively.

Association Between the Predictor and Potential Outcomes (First Assumption) Intervention condition was negatively associated with changes in kinematics (Table 3). These associations mean that the patients in the FST group performed the singlelegged squat with less trunk ipsilateral inclination, pelvis contralateral depression, and hip adduction when compared with the ST group after the interventions. Consequently, all 3 kinematics variables were considered as outcomes in this study.

TABLE 2 Change in Scores for Eccentric Hip Torque, Trunk Endurance, and Frontal Plane Kinematicsa ST Group Potential mediatorsb D in eccentric hip torque, Nm/kg D in abduction torque D in adduction torque D in lateral rotation torque D in medial rotation torque D in trunk endurance, s D in lateral trunk endurance D in anterior trunk endurance D in posterior trunk endurance Outcomesc D in kinematics in the frontal plane, deg D in trunk ipsilateral/contralateral inclination D in pelvis contralateral depression/elevation D in hip adduction/abduction

0.04 0.06 0.06 0.00

(20.02 to 0.09) (20.04 to 0.15) (0.01 to 0.12) (20.11 to 0.11)

3.18 (20.69 to 7.06) 26.20 (219.54 to 7.14) 22.95 (217.26 to 11.36)

0.14 (21.64 to 1.93) 0.18 (21.44 to 1.81) 21.68 (23.66 to 0.30)

a

FST Group

0.22 0.07 0.08 0.14

(0.09 to 0.35) (20.02 to 0.16) (0.03 to 0.13) (0.03 to 0.25)

32.71 (23.74 to 41.67) 47.84 (31.74 to 63.95) 44.72 (23.40 to 66.05)

23.18 (21.22 to 25.14) 23.98 (21.32 to 2 6.64) 211.27 (28.43 to 214.11)

Data are presented as mean (95% CI). FST, functional stabilization training; ST, standard training. Positive values represent increase (improvement) in eccentric hip torque and trunk endurance after intervention. c Negative values represent reduction (improvement) in trunk ipsilateral inclination, pelvis depression, and hip adduction movement excursions after intervention. b


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TABLE 3 Regression Analysis on the Association Between the Intervention Condition and Frontal Plane Kinematics (First Assumption) and Eccentric Hip Torque and Trunk Endurance (Second Assumption) Total Effect

First assumption Intervention condition ! D in trunk ipsilateral inclination D in pelvis contralateral depression D in hip adduction Second assumption Intervention condition ! D in eccentric hip abduction torque D in eccentric hip adduction torque D in eccentric hip lateral rotation Torque D in eccentric hip medial rotation torque D in trunk lateral endurance D in trunk anterior endurance D in trunk posterior endurance

b

B

SE

P Value

20.45 20.45 20.75

23.34 23.80 29.60

1.24 1.41 1.58

.012 .012 \.001

0.48 0.04 0.09 0.33 0.79 0.73 0.61

0.18 0.01 0.02 0.14 29.52 54.05 47.67

0.06 0.06 0.04 0.07 4.33 9.66 11.77

.007 .824 .649 .071 \.001 \.001 \.001

TABLE 4 Regression Analysis on the Association Between the Potential Mediatorsa and the Outcomes After Controlling for the Predictor (Intervention Condition)—Third Assumption

D in eccentric hip abduction torque ! D in trunk ipsilateral inclination D in pelvis contralateral depression D in hip adduction D in eccentric hip medial rotation torque ! D in trunk ipsilateral inclination D in pelvis contralateral depression D in hip adduction D in trunk lateral endurance ! D in trunk ipsilateral inclination D in pelvis contralateral depression D in hip adduction D in trunk anterior endurance ! D in trunk ipsilateral inclination D in pelvis contralateral depression D in hip adduction D in trunk posterior endurance ! D in trunk ipsilateral inclination D in pelvis contralateral depression D in hip coronal plane

b

B

SE

P Value

0.17 0.14 20.02

3.29 3.18 20.54

3.71 4.25 4.82

.38 .46 .91

20.32 20.43 20.40

25.79 28.92 212.49

3.10 3.33 3.45

.07 .01 .001

20.09 0.08 0.05

20.02 0.02 0.02

0.05 0.06 0.07

.75 .79 .79

20.18 20.19 20.21

20.02 20.02 20.04

0.02 0.03 0.03

.46 .45 .25

20.06 0.18 0.01

20.01 0.02 0.00

0.02 0.02 0.03

.77 .42 .93

a

Determined in the regression analysis for the second assumption.

Association Between the Predictor and the Hypothesized Mediators (Second Assumption) Although the intervention condition was not associated with the changes in eccentric hip adduction and hip lateral rotation torque, it was positively associated with changes in eccentric hip abduction and medial rotation torque, as well as with changes in endurance of the lateral, anterior, and posterior muscles of the trunk (Table 3). This meant that the patients in the FST group showed greater

improvement in these variables when compared with the ST group. Consequently, these 5 variables were considered as potential mediators.

Association Between Potential Mediators and Outcomes When Controlling the Predictor (Third Assumption) When controlling for intervention, only changes in eccentric hip medial rotation torque demonstrated an association




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TABLE 5 Estimates of Indirect Effects of Potential Mediating Variables Indirect Effect Potential Mediating Path Intervention condition ! D in eccentric hip medial rotation torque ! D in trunk ipsilateral inclination D in pelvis contralateral depression D in hip adduction

B

SE

P Value

c Path, %a

20.79 21.21 21.70

0.59 0.79 1.05

.09 .06 .04

24 32 18

a

Percentage of the c path accounted for by the mediator.

with changes in kinematics variables (Table 4). These associations were negative, meaning that the greater the increases in eccentric hip medial rotation torque, the greater the decreases in trunk ipsilateral inclination, pelvis contralateral depression, and hip adduction excursions.

Association Between the Predictor and Outcomes When Controlling the Potential Mediators (Fourth Assumption) As compared with the results from the first regression, when eccentric hip medial rotator torque was controlled in the model, the associations between the intervention condition and changes in kinematics became smaller (trunk inclination, B = 22.55 vs 23.34; pelvic depression, B = 22.59 vs 23.80; and hip adduction, B = 27.90 vs 29.60).

Indirect Effects of Potential Mediating Variables After removing the direct effect of FST on the outcomes of interest, the changes in eccentric hip medial rotator torque showed evidence for a mediating effect (Table 5), meaning that the increases in eccentric hip medial rotation torque observed in the FST group mediated the effect of this intervention in decreasing trunk ipsilateral inclination, pelvis contralateral depression, and hip adduction excursions.

DISCUSSION A recent randomized clinical trial with PFP patients demonstrated that a comprehensive treatment involving trunk and hip strengthening exercises is able to diminish pain, improve trunk and hip strength, and improve frontal plane lower limb kinematics.2 Although increases in trunk and hip strength have been empirically related to improvements in lower limb kinematics, the exact mechanisms responsible for these movement changes have not been determined. To date, it is unknown whether the mechanism for the improved effect on movement is due to increases in strength of the hip muscles or the trunk muscles or perhaps to alternative explanations such as improvement of lower limb coordination and changes in neuromuscular recruitment. Recognizing the mediators would allow clinicians to optimize the interventions and make evidence-based decisions on which exercises should

be emphasized to improve lower limb and trunk frontal plane kinematics. Our results indicate that the reduction of trunk ipsilateral inclination, pelvis contralateral depression, and hip adduction excursions observed in the FST group was mediated by the increase of eccentric hip medial rotation torque. Given the current evidence on the role of the hip lateral rotators muscles on PFP,20,30,37 it may appear intriguing that eccentric hip medial rotation torque, rather than eccentric hip lateral rotation torque, mediated the effect of FST on lower limb and trunk kinematics. This is explained by the test position used in our study for evaluating hip rotation torque. While the gluteus maximus and medius are hip lateral rotators in the upright standing position, they become hip medial rotators in the seated position.5 In a cadaveric study, Delp et al5 verified that the gluteus maximus and medius, which are the primary focused muscles during FST, shifted almost completely from lateral rotation to medial rotation moment arms when the hip was flexed to 90°. As in our study, hip rotation torque was evaluated in 90° of hip flexion, and the test for hip medial rotation mainly assessed the strength of gluteus muscles (minimus, medius, and maximus) and piriformis, while the test for hip lateral rotation assessed the strength of the deep hip muscles (obturators and quadratus femoris). An unexpected finding of the current study was the absence of a mediation effect involving eccentric hip abduction torque on changes to kinematics. This finding may also be explained by the muscles that are active while testing hip abduction. While the hip abduction test assesses the gluteus medius, gluteus minimus, and tensor fascia latae torque generation capacity, the hip medial rotation test at 90° of hip flexion simultaneously assesses the function of the muscles cited above in addition to the gluteus maximus. FST targeted the gluteus muscles, including the gluteus maximus, very intensely. The gluteus medius and maximus (mainly its superior portion) eccentrically control hip adduction, maintain the pelvis level during single-limb activities, and may help to prevent compensatory movements, such as ipsilateral trunk inclination.24,35 However, the gluteus maximus activity during lying hip abduction with the hip in a neutral position (0° hip flexion) has been shown to be small.9 This could imply that, in the test position used in this study for evaluating hip abductor torque, the gluteus maximus was not contributing


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significantly for torque generation, but an electromyographic evaluation would be necessary to confirm this. Therefore, in summary, it is possible that the function of the gluteus maximus may have been the reason why hip medial rotation torque mediated the effect of FST on lower extremity kinematics whereas hip abductor torque did not. Perhaps the evaluation of the hip extensor torque could help to confirm this assumption. These results have important clinical relevance. They demonstrate that increasing the strength of the gluteus muscles (with training programs such as FST) can modify a movement pattern that has been associated with the development of PFP. Several previous studies demonstrated that patients with PFP have greater hip adduction and trunk ipsilateral inclination movements when compared with healthy subjects.29,42,43 A recent prospective study also verified that subjects performing landing activities with greater external knee abduction moment are more likely to develop PFP.27 Abnormal movement patterns during single-legged squat have been shown to reflect abnormal movements during jump landings.14,40 An increased external knee abduction moment during functional activities may have detrimental consequences while increasing the lateral forces acting on the patella. It has been suggested that the magnitude of the external knee abduction moment is influenced by the amount knee abduction and hip adduction movements.35 Also, a greater trunk ipsilateral inclination during single-legged landings has been shown to correlate with greater external knee abduction moments.6 Our results indicate that the strengthening of the gluteus muscles was one of the mechanisms by which FST decreased hip adduction, pelvis contralateral depression, and trunk ipsilateral inclination. This movement pattern involving greater control of the frontal plane trunk, pelvis, and hip movements may result in a smaller external knee abduction moment and patellofemoral stress, consequently reducing the patient’s symptoms. In this study, increases in endurance of the anterior, posterior, and lateral trunk muscles showed no mediating effects on changes to kinematics. Previous studies showed that, during limb movements, the trunk muscles are either anticipatorily activated to stabilize the spine or are recruited after the displacement of the center of mass resultant from body movements.15,16 In our study, the trunk muscles were emphasized in the PFP treatment to improve spine stabilization and avoid abnormal movements of the trunk. However, Powers35 suggested that dynamic trunk stability cannot exist without pelvic stability. Weakness of the gluteus muscles may cause contralateral pelvic depression and compensatory ipsilateral trunk adjustments. The current results indicate that improving endurance of the trunk muscles do not seem to prevent the compensatory trunk motions that are likely caused by weakness of the hip muscles. This study has limitations that should be acknowledged. First, the mediator effect of the eccentric hip medial rotation torque on the improvement of trunk and lower limb kinematics ranged from 18% to 32%. These results, although clinically relevant, imply that additional factors also contribute to the effects of FST on kinematics. Other

factors might include increases in the strength of the trunk muscles and/or the hip extensor muscles, variables that have been related to PFP28,36 but were not evaluated in this study. Also, improvements in muscle activation deficits could have explained the effects of FST on trunk and lower limb kinematics. Women with PFP were shown to have abnormal gluteus muscle recruitment (delayed and/ or smaller activation) during running44 and squatting30 when compared with asymptomatic controls. An electromyographic evaluation could further investigate these effects. Improvements in motor control and kinesthetic awareness might also have contributed to our results. For instance, Noehren et al34 verified that real-time kinematics feedback during running is effective for reducing hip adduction and knee pain in patients with PFP, even without the addition of strengthening exercises. It is important to mention that the extrapolation of the current findings to men with PFP should be done with caution, since only women participated in this study. Finally, the small sample size might have biased the results. While the results demonstrated that we were sufficiently powered to establish some mediator effects, we may not have been powered to detect additional mediators. However, all nonsignificant results obtained in this study (P . .4) demonstrated very small associations that would likely not be considered clinically important.

CONCLUSION Our results indicate that the improvements in eccentric hip medial rotation torque in patients with PFP present mediation effects of 18% to 32% on changes to frontal plane kinematics that were observed after FST. Although the mediation effects are considered small, these findings suggest that strengthening exercises for the gluteus muscles should be included in the rehabilitation programs of PFP patients, as they may improve frontal plane lower limb and trunk kinematics.

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Trunk and Lower Extremity Kinematics During Stair Descent in Women With or Without Patellofemoral Pain.

Relationship between hip strength and trunk, hip, and knee kinematics during a jump-landing task in individuals with patellofemoral pain.

Trunk biomechanics and its association with hip and knee kinematics in patients with and without patellofemoral pain.

Trunk and lower extremity segment kinematics and their relationship to pain following movement instruction during a single-leg squat in females with dynamic knee valgus and patellofemoral pain.

Low back pain affects trunk as well as lower limb movements during walking and running.

Does anterior knee pain severity and function relate to the frontal plane projection angle and trunk and hip strength in women with patellofemoral pain?

Effects of functional stabilization training on pain, function, and lower extremity biomechanics in women with patellofemoral pain: a randomized clinical trial.

Q-angle in patellofemoral pain: relationship with dynamic knee valgus, hip abductor torque, pain and function.

Muscular Activity and Fatigue in Lower-Limb and Trunk Muscles during Different Sit-To-Stand Tests.

Differences in Lower Extremity and Trunk Kinematics between Single Leg Squat and Step Down Tasks.

Trunk kinematics during locomotor activities.

Changes in postural and trunk muscles responses in patients with chronic nonspecific low back pain during sudden upper limb loading.

Hip muscle strength and endurance in females with patellofemoral pain: a systematic review with meta-analysis.

A comprehensive evaluation of trunk response to asymmetric trunk motion.

The effect of exercise training on lower trunk muscle morphology.

Activation of back and lower limb muscles during squat exercises with different trunk flexion.

Contributions of lower extremity kinematics to trunk accelerations during moderate treadmill running.

Effects of femoral rotational taping on pain, lower extremity kinematics, and muscle activation in female patients with patellofemoral pain.

Trunk muscle activation during different quadruped stabilization exercises in individuals with chronic low back pain.

Varied response to mirror gait retraining of gluteus medius control, hip kinematics, pain, and function in 2 female runners with patellofemoral pain.

Contribution of altered hip, knee and foot kinematics to dynamic postural impairments in females with patellofemoral pain during stair ascent.

Effect of changes in orientation and position of external loads on trunk muscle activity and kinematics in upright standing.

Trunk kinematics and muscle activities during arm elevation.

Effect of thoracic movement-mediated training on back pain and trunk range of motion in a patient with lower back pain.