Sie sind auf Seite 1von 9

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 Fábio Viadanna Serrão,yz PT, PhD
Investigation performed at Federal University of São Carlos, São 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 func-
tional 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 strength-
ening 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 fron-
tal 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 over- control, and these alterations to kinematics have been asso-
use disorders of the knee treated in general practice.39 ciated with increased patellofemoral joint stress and
Patients with a history of PFP have an increased risk for pain.19,29,30,32 Specifically, in the frontal plane, patients
developing patellofemoral osteoarthritis.41 Additionally, with PFP exhibit increased hip adduction, contralateral pel-
up to 91% of patients with a diagnosis of PFP will complain vis depression, and ipsilateral trunk inclination during
of knee pain and limited physical function several years weightbearing activities when compared with healthy sub-
after initial presentation.38 Studies have shown that jects.29,42,43 Excessive hip adduction is thought to increase
patients with PFP have poor trunk and hip movement the quadriceps angle and the lateral pressure on the patel-
lofemoral joint.19 Excessive trunk ipsilateral inclination is
thought to be a compensatory movement, performed to pre-
vent contralateral pelvis depression. However, during
The American Journal of Sports Medicine, Vol. 43, No. 6
DOI: 10.1177/0363546515574690 single-legged activities, excessive ipsilateral trunk inclina-
Ó 2015 The Author(s) tion moves the ground-reaction force laterally to the knee

1486 Baldon et al The American Journal of Sports Medicine

joint and increases the external knee abduction moment analog scale for a minimum of 8 weeks; (2) anterior or ret-
and the quadriceps angle, contributing to PFP.6,35 ropatellar knee pain during at least 3 of the following acti-
Given that the hip abductor, lateral rotator, and exten- vities—ascending/descending stairs, squatting, running,
sor muscles, along with the trunk muscles, control the kneeling, jumping and prolonged sitting; and (3) insidious
movements of the hip joint and the trunk in closed kinetic onset of symptoms unrelated to trauma. The exclusion cri-
chain activities, it has been commonly assumed that teria adopted in the study were the following: previous sur-
improving the strength of these muscles is associated gery in the lower limbs, presence of intra-articular
with improvements in lower limb and trunk kinemat- pathologic abnormalities, involvement of the collateral or
ics.10,11,21,31 However, previous research has reported cruciate ligaments, patellar instability, Sinding-Larsen-
that improvements in hip and trunk strength do not neces- Johansson or Osgood-Schlatter syndrome, knee joint effu-
sarily affect lower extremity kinematics,8,13 suggesting sion, hip pain, or palpation of the iliotibial band, patellar
that factors other than muscle strength might play a rele- tendon, or pes anserinus tendons that reproduced the
vant role in frontal plane kinematics. patient’s pain.4,30
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 Randomization
hip and trunk strengthening—named functional stabiliza-
Randomization was done in blocks of 4. Consecutively num-
tion training (FST)—successfully improved lower limb
bered opaque envelopes were prepared ahead of time with
kinematics in the frontal plane in comparison to a more
the randomization scheme using a computer-generated table
traditional training program—named standard training
of random numbers. A person unaware of any information
(ST)—focused on quadriceps strengthening. Although we
about the patients performed the randomization and pro-
hypothesized that the strengthening of the hip muscles
vided the assignment to the treating physical therapist. Ran-
might have been associated with these changes to kinemat-
domization was performed after the baseline assessment,
ics, a mediator analysis was necessary to confirm or reject
and the patients were blinded to group allocation.
this hypothesis.
Treatment mediators identify possible mechanisms
through which a treatment might achieve its effects and Procedures
that could be considered causal links between treatment
and outcome.22 Understanding the mechanisms through All patients read and signed an informed consent form.
which a treatment operates facilitates the development of This study was approved by the Ethics Committee for
interventions where efficient components might be rein- Research on Human Subjects of the Federal University of
forced and refined and where redundant components could São Carlos.
be discarded. Thus, this study aimed to examine the mech- Patients attended a baseline assessment, followed by 2
anisms by which a training program focusing on hip and months of intervention, and were then reassessed. The
trunk strengthening (in this case, the previously reported assessments consisted of an evaluation of trunk, pelvis,
FST) leads to changes in kinematics. Specifically, we tested and lower extremity kinematics during a single-legged
if the increases in hip strength and trunk endurance as squat task. They also involved trunk muscle endurance
a result of the participation in FST were mediators of tests and eccentric hip isokinetic torque evaluations. All
changes in hip adduction, pelvis depression, and trunk assessments were performed on the most painful limb
ipsilateral inclination observed in patients with PFP. according to the patient’s perception.

Outcome Measures
Kinematics Evaluation. Trunk, pelvis, and lower
Patients extremity kinematics in the frontal plane were assessed
during a single-legged squat task using the Flock of Birds
This study used data from a previous randomized controlled electromagnetic tracking system (Ascension Technology
single-blind study (for details, see Baldon Rde et al2). Corp) integrated with the MotionMonitor software (Inno-
Thirty-one female recreational athletes between 18 and vative Sports Training Inc). The single-legged squat was
30 years of age with PFP were randomly assigned to the chosen because it is a task frequently used in research to
FST (n = 15) or ST (n = 16) group. Patients were recruited assess lower limb biomechanics in people with PFP.12,30
between March and November of 2012. Eligibility criteria Also, altered movement patterns during the single-legged
included (1) anterior knee pain of at least 3 cm on a visual squat task have been shown to reflect poor movement

Address correspondence to Fábio Viadanna Serrão, PT, PhD, Department of Physiotherapy, Federal University of São Carlos, Rodovia Washington
Luis, km 235, CEP: 13565-905, São Carlos, SP, Brasil (e-mail:
*Department of Physiotherapy, Federal University of São Carlos, São Carlos, Brazil.
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
Coordenacxão de Aperfeicxoamento de Pessoal de Nı́vel Superior (CAPES).
Vol. 43, No. 6, 2015 Gluteal Strength as Mediator of Improvement in Kinematics 1487

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 kine-
matic variables studied were trunk ipsilateral/contralateral
inclination, pelvis contralateral elevation/depression, and
hip adduction/abduction (Figure 1B). Trunk ipsilateral incli-
nation, 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
Figure 1. (A) Patient performing the single-legged squat kinematics data were processed using custom MATLAB
task. (B) Real-time visualization during the kinematic evalua- software (MathWorks Inc).
tion and definitions of the kinematic variables of interest.

Potential Mediators
control in other functional activities, such as running Trunk Muscle Endurance Evaluation. Trunk muscle
and jump landings.40,42 Before testing, 5 electromagnetic endurance was defined as the time that a patient could
tracking sensors were attached to the sternum, sacrum hold a predefined static position. The endurance of the pos-
(S2), and midlateral thighs and medial to the tibial tuber- terior trunk muscles was assessed with the patients lying
osity using double-sided adhesive tape. The kinematics prone with the lower body fixed to the test bench at the
data were collected at a sampling rate of 90 Hz.30 knees and hips. Before testing, the upper body of the patient
Before dynamic testing, the medial and lateral malleoli was held out of the test bench with the arms resting on the
and femoral epicondyles were digitized to determine the ground. At the beginning of the test, each patient was
ankle and knee joint centers, respectively. The hip joint instructed to extend her upper body and hold it horizontal
center was estimated using the functional approach to the floor with upper limbs across the chest.26
described elsewhere.23 The C7-T1, T12-L1, and L5-S1 joint Endurance of the anterior trunk muscles was assessed
spaces were also digitized, and the trunk and pelvis angles with the patient holding the body in a straight line while
were designated by the sternal and sacral sensors. A static supported only by both forearms and feet.7 Endurance of
frame was taken with the patient standing on both legs to the lateral muscles of the trunk was quantified with the
determine the neutral alignment angles of the joints. Then, patients in a side-lying position on the affected side.
the patients were asked to stand on the affected lower Each patient was instructed to support herself only on 1
limb, with the knee of the contralateral limb at 90° of flex- forearm and her feet and to lift her hips off the test bench
ion, hip in neutral position, and the arms crossed in front of and sustain the full body straight. The arm of the unin-
the thorax (single-legged static position) (Figure 1A) for volved side was held beside the trunk. The tests were con-
the anatomic frame. Kinematics variables were calculated ducted in a random order, and all tests were interrupted
using the data collected in this position as reference. when the patients were not able to sustain the position.
Patients were then asked to squat from the static posi- A single trial of each position was performed with a
tion to at least 60° of knee flexion and then return to the 2-minute rest interval between positions. The duration of
starting position. To ensure that the desired knee flexion time in seconds that the patients could hold the positions
had been reached, the task was visually inspected in real was used for the statistical analysis. Reliability of these
time using the MotionMonitor software (Innovative Sports tests has been reported to be excellent, with ICCs ranging
Training Inc). The execution time of the single-legged from 0.95 to 0.99 and standard errors of measurement
squat was standardized at 2.0 6 0.3 seconds. Each patient ranging from 3.40 to 9.93 seconds.7,26
completed 3 attempts for familiarization and 5 acceptable Eccentric Hip Torque Evaluation. The eccentric hip tor-
trials for data analysis, with a 1-minute rest interval que variables were quantified in a random order using an
between trials. If any of the evaluation requirements isokinetic dynamometer Biodex Multi-Joint System 2 (Bio-
were violated or if the patients lost balance during the dex Medical System Inc) at an angular speed of 30 deg/s.
task, the attempt was invalidated and repeated. The aver- Data were recorded using the Biodex Advantage Software
age kinematics data obtained from 5 acceptable trials were 4.0 at a sampling rate of 100 Hz. Eccentric torque evalua-
used for the statistical analysis. tions were chosen because they better represent the muscle
1488 Baldon et al The American Journal of Sports Medicine

action necessary during functional weightbearing activi-

ties. 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 Figure 2. The 3-variable framework showing the direct (c)
frontal plane, and the lever arm was laterally attached to and indirect (a ! b) paths.
the thigh under test, 5 cm proximal to the base of the
patella. The test was from 0° (neutral) to 30° of hip abduc-
tion.1 The main muscles that generate eccentric hip abduc- and 6. During the exercises, the knee pain could not be
tor torque at this position are all fibers of the gluteus higher than 3 on a scale of 0 to 10. The loads were pro-
medius, gluteus minimus, and tensor fasciae latae. The gressed when the patients were able to perform the set of
main muscles generating eccentric hip adductor torque exercises without exacerbation of knee pain or excessive
are the pectineus, adductor longus, gracilis, adductor brevis, fatigue and if they had no more local muscle pain 48 hours
and adductor magnus (both anterior and posterior heads).33 after the previous training session.
For the eccentric test of the hip medial and lateral rota- The FST consisted of weightbearing and nonweight-
tor muscles, patients were placed in sitting position with bearing exercises to enhance the strength of the trunk
their knees and hips flexed at 90°. The rotational axis of and hip muscles. The main objective of the first 2 weeks
the dynamometer was aligned with the center of the (phase 1) was to improve motor control of the trunk and
patella and the lever arm attached 5 cm proximal to the lat- hip muscles mainly using nonweightbearing exercises.
eral malleolus. The distal thigh of the lower limb under test For the next 3 weeks (phase 2), the main objective was to
and the trunk were stabilized with straps. The range of increase strength of the trunk and hip muscles using
motion of this test was from 10° of hip medial rotation to weightbearing activities. In the final 3 weeks of treatment
20° of hip lateral rotation.1 The main muscles responsible (phase 3), patients were continually educated to perform
for producing eccentric hip medial rotator torque with the the functional exercises with the lower extremities in neu-
hip positioned in 90° of flexion are all fibers of the gluteus tral frontal alignment and to avoid quadriceps dominance
medius, gluteus minimus, tensor fasciae latae, piriformis, by leaning the trunk forward, with hinging at the hips.
and most portions of the gluteus maximus. The muscles pro- The ST consisted of stretching exercises of the hamstrings,
ducing eccentric hip lateral rotator torque in this position ankle plantar flexors, quadriceps, lateral retinaculum, and
are the deep hip muscles, which include the obturator exter- iliotibial band, as well as traditional weightbearing and
nus, obturator internus, and quadratus femoris.5,33 nonweightbearing exercises for quadriceps strengthening.
Before testing, the patients performed 5 submaximal and For a detailed description of the exercises with their pro-
2 maximal reciprocal eccentric contractions of each test for gression for both groups, see Baldon Rde et al.2
familiarization. After 3 minutes of rest, the patients per-
formed 2 series of 5 maximal repetitions with a 3-minute
rest period between them. Verbal encouragement was pro- Statistical Analysis
vided to stimulate the patients to produce maximum torque.
To correct for the influence of gravity on the torque data, the Data were analyzed with respect to their distribution and
limb was weighed before each test according to the instruc- homogeneity of variance using the Shapiro-Wilk and Lev-
tions manual of the dynamometer. For statistical analysis, ene tests, respectively. To assess mediation effects, we fol-
the peak torque from either the first or second series lowed the 3-variable framework described by MacKinnon
normalized by body mass (Nm/kg) was used. Reliability of et al25 (Figure 2). In this model, the intervention condition
these tests are adequate, with ICC3,1 ranging from 0.78 to FST versus ST (predictor) is assumed to have both direct
0.97.1 and indirect paths to the changes in frontal plane kinemat-
ics (outcomes). As shown in Figure 2, c is considered the
direct path, whereas a ! b is the indirect path passing
Interventions through the isokinetic hip torque and endurance trunk
variables (potential mediators). According to Baron and
Treatment started 3 to 5 days after baseline isokinetic Kenny,3 4 conditions must be present for a variable to be
assessment. Patients from both groups performed the considered a mediator: (1) the predictor must be signifi-
training protocol 3 times per week for 8 weeks with at least cantly associated with the outcome, (2) the predictor
24 hours between intervention sessions. All sessions were must be significantly associated with the hypothesized
supervised by a physical therapist. For both groups, the mediator, (3) the mediator must be significantly associated
initial loads for most strengthening exercises were based with the outcome after controlling for the predictor, and (4)
on the 1-repetition maximum performed at the beginning the effect of the predictor on the outcome must be small
of week 1 and repeated at the beginning of the weeks 3 after controlling for the mediator.
Vol. 43, No. 6, 2015 Gluteal Strength as Mediator of Improvement in Kinematics 1489

TABLE 1 percentage of changes in outcome that were accounted by

Demographic Characteristics of Randomized the mediator. A preset a level of .10 was used for all the
Patients at Baselinea statistical tests and the regression analysis, which were
performed using SPSS statistical software (version 21;
Variable ST Group FST Group SPSS Inc). For potential mediators and outcomes, we
Age, y 22.78 6 3.31 21.31 6 2.65 used change scores between the end of intervention and
Height, m 1.66 6 0.08 1.62 6 0.06 the baseline assessments.
Mass, kg 57.37 6 8.41 58.31 6 7.29
Body mass index, kg/m2 20.73 6 2.09 22.27 6 2.52

Data are presented as mean 6 SD. FST, functional stabiliza-
tion training; ST, standard training.
Sixty-three patients were screened and 31 fulfilled the eli-
gibility criteria and were randomly assigned to the FST
The assumptions above were tested with 3 multiple group (n = 15) or the ST group (n = 16). The CONSORT dia-
regression analysis as suggested by Holmbeck.18 The first gram with the flowchart of the patients in the study has
regression tested the association between the predictor been reported.2 There was 1 dropout in the FST group dur-
and the outcomes (first assumption), and the second ing intervention period. Consequently, 30 patients con-
regression tested the association between the predictor cluded the assessment at the end of the intervention and
and the potential mediators (second assumption). The were therefore used in the statistical analysis. The base-
third regression tested the association between the poten- line demographic characteristics and the change scores
tial mediators and the outcomes after controlling for the for the potential mediators and outcomes in both groups
predictor (third assumption). Then, it was observed are described in Table 1 and Table 2, respectively.
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 assump- Association Between the Predictor and
tion). Specifically, the greater the reduction in the unstan- Potential Outcomes (First Assumption)
dardized coefficients (B) in the third regression compared
with the first regression, the greater the potency of the Intervention condition was negatively associated with
mediator. When all assumptions were satisfied, the indi- changes in kinematics (Table 3). These associations mean
rect effect was determined, which is mathematically equiv- that the patients in the FST group performed the single-
alent to the drop in the B total effect (path c) after the legged squat with less trunk ipsilateral inclination, pelvis
mediator is in the model (path a ! b). Also, the standard contralateral depression, and hip adduction when com-
error of the indirect effect was calculated using the Sobel pared with the ST group after the interventions. Conse-
test. Finally, statistical tests for the indirect effects were quently, all 3 kinematics variables were considered as
conducted as suggested by Holmbeck17 to determine the outcomes in this study.

Change in Scores for Eccentric Hip Torque, Trunk Endurance, and Frontal Plane Kinematicsa

ST Group FST Group

Potential mediatorsb
D in eccentric hip torque, Nm/kg
D in abduction torque 0.04 (20.02 to 0.09) 0.22 (0.09 to 0.35)
D in adduction torque 0.06 (20.04 to 0.15) 0.07 (20.02 to 0.16)
D in lateral rotation torque 0.06 (0.01 to 0.12) 0.08 (0.03 to 0.13)
D in medial rotation torque 0.00 (20.11 to 0.11) 0.14 (0.03 to 0.25)
D in trunk endurance, s
D in lateral trunk endurance 3.18 (20.69 to 7.06) 32.71 (23.74 to 41.67)
D in anterior trunk endurance 26.20 (219.54 to 7.14) 47.84 (31.74 to 63.95)
D in posterior trunk endurance 22.95 (217.26 to 11.36) 44.72 (23.40 to 66.05)
D in kinematics in the frontal plane, deg
D in trunk ipsilateral/contralateral inclination 0.14 (21.64 to 1.93) 23.18 (21.22 to 25.14)
D in pelvis contralateral depression/elevation 0.18 (21.44 to 1.81) 23.98 (21.32 to 2 6.64)
D in hip adduction/abduction 21.68 (23.66 to 0.30) 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.
Negative values represent reduction (improvement) in trunk ipsilateral inclination, pelvis depression, and hip adduction movement
excursions after intervention.
1490 Baldon et al The American Journal of Sports Medicine

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
b B SE P Value

First assumption
Intervention condition !
D in trunk ipsilateral inclination 20.45 23.34 1.24 .012
D in pelvis contralateral depression 20.45 23.80 1.41 .012
D in hip adduction 20.75 29.60 1.58 \.001
Second assumption
Intervention condition !
D in eccentric hip abduction torque 0.48 0.18 0.06 .007
D in eccentric hip adduction torque 0.04 0.01 0.06 .824
D in eccentric hip lateral rotation Torque 0.09 0.02 0.04 .649
D in eccentric hip medial rotation torque 0.33 0.14 0.07 .071
D in trunk lateral endurance 0.79 29.52 4.33 \.001
D in trunk anterior endurance 0.73 54.05 9.66 \.001
D in trunk posterior endurance 0.61 47.67 11.77 \.001

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

b B SE P Value

D in eccentric hip abduction torque !

D in trunk ipsilateral inclination 0.17 3.29 3.71 .38
D in pelvis contralateral depression 0.14 3.18 4.25 .46
D in hip adduction 20.02 20.54 4.82 .91
D in eccentric hip medial rotation torque !
D in trunk ipsilateral inclination 20.32 25.79 3.10 .07
D in pelvis contralateral depression 20.43 28.92 3.33 .01
D in hip adduction 20.40 212.49 3.45 .001
D in trunk lateral endurance !
D in trunk ipsilateral inclination 20.09 20.02 0.05 .75
D in pelvis contralateral depression 0.08 0.02 0.06 .79
D in hip adduction 0.05 0.02 0.07 .79
D in trunk anterior endurance !
D in trunk ipsilateral inclination 20.18 20.02 0.02 .46
D in pelvis contralateral depression 20.19 20.02 0.03 .45
D in hip adduction 20.21 20.04 0.03 .25
D in trunk posterior endurance !
D in trunk ipsilateral inclination 20.06 20.01 0.02 .77
D in pelvis contralateral depression 0.18 0.02 0.02 .42
D in hip coronal plane 0.01 0.00 0.03 .93

Determined in the regression analysis for the second assumption.

Association Between the Predictor and the improvement in these variables when compared with the
Hypothesized Mediators (Second Assumption) ST group. Consequently, these 5 variables were considered
as potential mediators.
Although the intervention condition was not associated
with the changes in eccentric hip adduction and hip lateral Association Between Potential Mediators and
rotation torque, it was positively associated with changes Outcomes When Controlling the Predictor
in eccentric hip abduction and medial rotation torque, as (Third Assumption)
well as with changes in endurance of the lateral, anterior,
and posterior muscles of the trunk (Table 3). This meant When controlling for intervention, only changes in eccentric
that the patients in the FST group showed greater hip medial rotation torque demonstrated an association
Vol. 43, No. 6, 2015 Gluteal Strength as Mediator of Improvement in Kinematics 1491

Estimates of Indirect Effects of Potential Mediating Variables

Indirect Effect
Potential Mediating Path B SE P Value c Path, %a

Intervention condition ! D in eccentric hip medial rotation torque !

D in trunk ipsilateral inclination 20.79 0.59 .09 24
D in pelvis contralateral depression 21.21 0.79 .06 32
D in hip adduction 21.70 1.05 .04 18

Percentage of the c path accounted for by the mediator.

with changes in kinematics variables (Table 4). These asso- be emphasized to improve lower limb and trunk frontal
ciations were negative, meaning that the greater the plane kinematics.
increases in eccentric hip medial rotation torque, the Our results indicate that the reduction of trunk ipsilat-
greater the decreases in trunk ipsilateral inclination, pelvis eral inclination, pelvis contralateral depression, and hip
contralateral depression, and hip adduction excursions. adduction excursions observed in the FST group was medi-
ated by the increase of eccentric hip medial rotation tor-
Association Between the Predictor and que. Given the current evidence on the role of the hip
Outcomes When Controlling the Potential Mediators lateral rotators muscles on PFP,20,30,37 it may appear
(Fourth Assumption) intriguing that eccentric hip medial rotation torque, rather
than eccentric hip lateral rotation torque, mediated the
As compared with the results from the first regression, effect of FST on lower limb and trunk kinematics. This is
when eccentric hip medial rotator torque was controlled in explained by the test position used in our study for evalu-
the model, the associations between the intervention condi- ating hip rotation torque. While the gluteus maximus and
tion and changes in kinematics became smaller (trunk incli- medius are hip lateral rotators in the upright standing
nation, B = 22.55 vs 23.34; pelvic depression, B = 22.59 vs position, they become hip medial rotators in the seated
23.80; and hip adduction, B = 27.90 vs 29.60). 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
Indirect Effects of Potential Mediating Variables from lateral rotation to medial rotation moment arms
when the hip was flexed to 90°. As in our study, hip rota-
After removing the direct effect of FST on the outcomes of
tion torque was evaluated in 90° of hip flexion, and the
interest, the changes in eccentric hip medial rotator torque
test for hip medial rotation mainly assessed the strength
showed evidence for a mediating effect (Table 5), meaning
of gluteus muscles (minimus, medius, and maximus) and
that the increases in eccentric hip medial rotation torque
piriformis, while the test for hip lateral rotation assessed
observed in the FST group mediated the effect of this inter-
the strength of the deep hip muscles (obturators and quad-
vention in decreasing trunk ipsilateral inclination, pelvis
ratus femoris).
contralateral depression, and hip adduction excursions.
An unexpected finding of the current study was the
absence of a mediation effect involving eccentric hip abduc-
tion torque on changes to kinematics. This finding may
also be explained by the muscles that are active while test-
A recent randomized clinical trial with PFP patients dem- ing hip abduction. While the hip abduction test assesses
onstrated that a comprehensive treatment involving trunk the gluteus medius, gluteus minimus, and tensor fascia
and hip strengthening exercises is able to diminish pain, latae torque generation capacity, the hip medial rotation
improve trunk and hip strength, and improve frontal plane test at 90° of hip flexion simultaneously assesses the func-
lower limb kinematics.2 Although increases in trunk and tion of the muscles cited above in addition to the gluteus
hip strength have been empirically related to improve- maximus. FST targeted the gluteus muscles, including
ments in lower limb kinematics, the exact mechanisms the gluteus maximus, very intensely. The gluteus medius
responsible for these movement changes have not been and maximus (mainly its superior portion) eccentrically
determined. To date, it is unknown whether the mecha- control hip adduction, maintain the pelvis level during
nism for the improved effect on movement is due to single-limb activities, and may help to prevent compensa-
increases in strength of the hip muscles or the trunk tory movements, such as ipsilateral trunk inclination.24,35
muscles or perhaps to alternative explanations such as However, the gluteus maximus activity during lying hip
improvement of lower limb coordination and changes in abduction with the hip in a neutral position (0° hip flexion)
neuromuscular recruitment. Recognizing the mediators has been shown to be small.9 This could imply that, in the
would allow clinicians to optimize the interventions and test position used in this study for evaluating hip abductor
make evidence-based decisions on which exercises should torque, the gluteus maximus was not contributing
1492 Baldon et al The American Journal of Sports Medicine

significantly for torque generation, but an electromyo- factors might include increases in the strength of the trunk
graphic evaluation would be necessary to confirm this. muscles and/or the hip extensor muscles, variables that
Therefore, in summary, it is possible that the function of have been related to PFP28,36 but were not evaluated in
the gluteus maximus may have been the reason why hip this study. Also, improvements in muscle activation defi-
medial rotation torque mediated the effect of FST on lower cits could have explained the effects of FST on trunk and
extremity kinematics whereas hip abductor torque did not. lower limb kinematics. Women with PFP were shown to
Perhaps the evaluation of the hip extensor torque could have abnormal gluteus muscle recruitment (delayed and/
help to confirm this assumption. or smaller activation) during running44 and squatting30
These results have important clinical relevance. They when compared with asymptomatic controls. An electro-
demonstrate that increasing the strength of the gluteus myographic evaluation could further investigate these
muscles (with training programs such as FST) can modify effects. Improvements in motor control and kinesthetic
a movement pattern that has been associated with the awareness might also have contributed to our results. For
development of PFP. Several previous studies demon- instance, Noehren et al34 verified that real-time kinematics
strated that patients with PFP have greater hip adduction feedback during running is effective for reducing hip adduc-
and trunk ipsilateral inclination movements when com- tion and knee pain in patients with PFP, even without the
pared with healthy subjects.29,42,43 A recent prospective addition of strengthening exercises. It is important to men-
study also verified that subjects performing landing activ- tion that the extrapolation of the current findings to men
ities with greater external knee abduction moment are with PFP should be done with caution, since only women
more likely to develop PFP.27 Abnormal movement pat- participated in this study. Finally, the small sample size
terns during single-legged squat have been shown to might have biased the results. While the results demon-
reflect abnormal movements during jump landings.14,40 strated that we were sufficiently powered to establish
An increased external knee abduction moment during some mediator effects, we may not have been powered to
functional activities may have detrimental consequences detect additional mediators. However, all nonsignificant
while increasing the lateral forces acting on the patella. results obtained in this study (P . .4) demonstrated very
It has been suggested that the magnitude of the external small associations that would likely not be considered clini-
knee abduction moment is influenced by the amount knee cally important.
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 strength-
ening of the gluteus muscles was one of the mechanisms by Our results indicate that the improvements in eccentric
which FST decreased hip adduction, pelvis contralateral hip medial rotation torque in patients with PFP present
depression, and trunk ipsilateral inclination. This move- mediation effects of 18% to 32% on changes to frontal plane
ment pattern involving greater control of the frontal plane kinematics that were observed after FST. Although the
trunk, pelvis, and hip movements may result in a smaller mediation effects are considered small, these findings sug-
external knee abduction moment and patellofemoral stress, gest that strengthening exercises for the gluteus muscles
consequently reducing the patient’s symptoms. should be included in the rehabilitation programs of PFP
In this study, increases in endurance of the anterior, patients, as they may improve frontal plane lower limb
posterior, and lateral trunk muscles showed no mediating and trunk kinematics.
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 REFERENCES
resultant from body movements.15,16 In our study, the
1. Baldon Rde M, Lobato DF, Carvalho LP, Wun PY, Santiago PR,
trunk muscles were emphasized in the PFP treatment to Serrão FV. Effect of functional stabilization training on lower limb bio-
improve spine stabilization and avoid abnormal move- mechanics in women. Med Sci Sports Exerc. 2012;44(1):135-145.
ments of the trunk. However, Powers35 suggested that 2. Baldon Rde M, Serrão FV, Scattone Silva R, Piva SR. Effects of func-
dynamic trunk stability cannot exist without pelvic stabil- tional stabilization training on pain, function, and lower extremity bio-
ity. Weakness of the gluteus muscles may cause contralat- mechanics in females with patellofemoral pain: a randomized clinical
trial. J Orthop Sports Phys Ther. 2014;44(4):240-251.
eral pelvic depression and compensatory ipsilateral trunk
3. Baron RM, Kenny DA. The moderator-mediator variable distinction in
adjustments. The current results indicate that improving social psychological research: conceptual, strategic, and statistical
endurance of the trunk muscles do not seem to prevent considerations. J Pers Soc Psychol. 1986;51(6):1173-1182.
the compensatory trunk motions that are likely caused 4. Cowan SM, Crossley KM, Bennell KL. Altered hip and trunk muscle
by weakness of the hip muscles. function in individuals with patellofemoral pain. Br J Sports Med.
This study has limitations that should be acknowledged. 2009;43(8):584-588.
First, the mediator effect of the eccentric hip medial rota- 5. Delp SL, Hess WE, Hungerford DS, Jones LC. Variation of rotation
moment arms with hip flexion. J Biomech. 1999;32(5):493-501.
tion torque on the improvement of trunk and lower limb
6. Dempsey AR, Elliott BC, Munro BJ, Steele JR, Lloyd DG. Whole body
kinematics ranged from 18% to 32%. These results, kinematics and knee moments that occur during an overhead catch
although clinically relevant, imply that additional factors and landing task in sport. Clin Biomech (Bristol, Avon). 2012;27(5):
also contribute to the effects of FST on kinematics. Other 466-474.
Vol. 43, No. 6, 2015 Gluteal Strength as Mediator of Improvement in Kinematics 1493

7. Durall CJ, Greene PF, Kernozek TW. A comparison of two isometric 26. McGill SM, Childs A, Liebenson C. Endurance times for low back sta-
tests of trunk flexor endurance. J Strength Cond Res. 2012;26(7): bilization exercises: clinical targets for testing and training from a nor-
1939-1944. mal database. Arch Phys Med Rehabil. 1999;80(8):941-944.
8. Earl JE, Hoch AZ. A proximal strengthening program improves pain, 27. Myer GD, Ford KR, Barber Foss KD, et al. The incidence and poten-
function, and biomechanics in women with patellofemoral pain syn- tial pathomechanics of patellofemoral pain in female athletes. Clin
drome. Am J Sports Med. 2011;39(1):154-163. Biomech (Bristol, Avon). 2010;25(7):700-707.
9. Fujisawa H, Suzuki H, Yamaguchi E, Yoshiki H, Wada Y, Watanabe A. 28. Nakagawa TH, Maciel CD, Serrão FV. Trunk biomechanics and its
Hip muscle activity during isometric contraction of hip abduction. association with hip and knee kinematics in patients with and without
J Phys Ther Sci. 2014;26(2):187-190. patellofemoral pain. Man Ther. 2015;20(1):189-193.
10. Fukuda TY, Melo WP, Zaffalon BM, et al. Hip posterolateral muscu- 29. Nakagawa TH, Moriya ET, Maciel CD, Serrão AF. Frontal plane bio-
lature strengthening in sedentary women with patellofemoral pain mechanics in males and females with and without patellofemoral
syndrome: a randomized controlled clinical trial with 1-year follow- pain. Med Sci Sports Exerc. 2012;44(9):1747-1755.
up. J Orthop Sports Phys Ther. 2012;42(10):823-830. 30. Nakagawa TH, Moriya ET, Maciel CD, Serrão FV. Trunk, pelvis, hip, and
11. Fukuda TY, Rossetto FM, Magalhaes E, Bryk FF, Lucareli PR, de knee kinematics, hip strength, and gluteal muscle activation during
Almeida Aparecida Carvalho N. Short-term effects of hip abductors a single-leg squat in males and females with and without patellofemoral
and lateral rotators strengthening in females with patellofemoral pain syndrome. J Orthop Sports Phys Ther. 2012;42(6):491-501.
pain syndrome: a randomized controlled clinical trial. J Orthop Sports 31. Nakagawa TH, Muniz TB, Baldon Rde M, Dias Maciel C, de Menezes
Phys Ther. 2010;40(11):736-742. Reiff RB, Serrão FV. The effect of additional strengthening of hip
12. Graci V, Salsich GB. Trunk and lower extremity segment kinematics abductor and lateral rotator muscles in patellofemoral pain syndrome:
and their relationship to pain following movement instruction during a randomized controlled pilot study. Clin Rehabil. 2008;22(12):
a single-leg squat in females with dynamic knee valgus and patello- 1051-1060.
femoral pain [published online April 26, 2014]. J Sci Med Sport. 32. Nakagawa TH, Serrão FV, Maciel CD, Powers CM. Hip and knee
doi:10.1016/j.jsams.2014.04.011 kinematics are associated with pain and self-reported functional sta-
13. Herman DC, Weinhold PS, Guskiewicz KM, Garrett WE, Yu B, Padua tus in males and females with patellofemoral pain. Int J Sports Med.
DA. The effects of strength training on the lower extremity biome- 2013;34(11):997-1002.
chanics of female recreational athletes during a stop-jump task. 33. Neumann DA. Kinesiology of the hip: a focus on muscular actions.
Am J Sports Med. 2008;36(4):733-740. J Orthop Sports Phys Ther. 2010;40(2):82-94.
14. Herrington L. Knee valgus angle during single leg squat and landing 34. Noehren B, Scholz J, Davis I. The effect of real-time gait retraining on
in patellofemoral pain patients and controls. Knee. 2014;21(2): hip kinematics, pain and function in subjects with patellofemoral pain
514-517. syndrome. Br J Sports Med. 2011;45(9):691-696.
15. Hodges PW, Richardson CA. Feedforward contraction of transversus 35. Powers CM. The influence of abnormal hip mechanics on knee injury:
abdominis is not influenced by the direction of arm movement. Exp a biomechanical perspective. J Orthop Sports Phys Ther. 2010;40(2):
Brain Res. 1997;114(2):362-370. 42-51.
16. Hodges PW, Richardson CA. Transversus abdominis and the super- 36. Souza RB, Powers CM. Differences in hip kinematics, muscle
ficial abdominal muscles are controlled independently in a postural strength, and muscle activation between subjects with and without
task. Neurosci Lett. 1999;265(2):91-94. patellofemoral pain. J Orthop Sports Phys Ther. 2009;39(1):12-19.
17. Holmbeck GN. Post-hoc probing of significant moderational and 37. Souza RB, Powers CM. Predictors of hip internal rotation during run-
mediational effects in studies of pediatric populations. J Pediatr Psy- ning: an evaluation of hip strength and femoral structure in women
chol. 2002;27(1):87-96. with and without patellofemoral pain. Am J Sports Med. 2009;37(3):
18. Holmbeck GN. Toward terminological, conceptual, and statistical 579-587.
clarity in the study of mediators and moderators: examples from 38. Stathopulu E, Baildam E. Anterior knee pain: a long-term follow-up.
the child-clinical and pediatric psychology literatures. J Consult Rheumatology (Oxford). 2003;42(2):380-382.
Clin Psychol. 1997;65(4):599-610. 39. Taunton JE, Ryan MB, Clement DB, McKenzie DC, Lloyd-Smith DR,
19. Huberti HH, Hayes WC. Patellofemoral contact pressures: the influ- Zumbo BD. A retrospective case-control analysis of 2002 running
ence of q-angle and tendofemoral contact. J Bone Joint Surg Am. injuries. Br J Sports Med. 2002;36(2):95-101.
1984;66(5):715-724. 40. Ugalde V, Brockman C, Bailowitz Z, Pollard CD. Single leg squat test
20. Ireland ML, Willson JD, Ballantyne BT, Davis IM. Hip strength in and its relationship to dynamic knee valgus and injury risk screening
females with and without patellofemoral pain. J Orthop Sports Phys [published online August 8, 2014]. PM R. doi:10.1016/j.pmrj
Ther. 2003;33(11):671-676. .2014.08.361
21. Khayambashi K, Mohammadkhani Z, Ghaznavi K, Lyle MA, Powers 41. Utting MR, Davies G, Newman JH. Is anterior knee pain a predispos-
CM. The effects of isolated hip abductor and external rotator muscle ing factor to patellofemoral osteoarthritis? Knee. 2005;12(5):362-365.
strengthening on pain, health status, and hip strength in females with 42. Willson JD, Davis IS. Lower extremity mechanics of females with and
patellofemoral pain: a randomized controlled trial. J Orthop Sports without patellofemoral pain across activities with progressively
Phys Ther. 2012;42(1):22-29. greater task demands. Clin Biomech (Bristol, Avon). 2008;23(2):
22. Kraemer HC, Wilson GT, Fairburn CG, Agras WS. Mediators and 203-211.
moderators of treatment effects in randomized clinical trials. Arch 43. Willson JD, Davis IS. Lower extremity strength and mechanics during
Gen Psychiatry. 2002;59(10):877-883. jumping in women with patellofemoral pain. J Sport Rehabil.
23. Leardini A, Cappozzo A, Catani F, et al. Validation of a functional 2009;18(1):76-90.
method for the estimation of hip joint centre location. J Biomech. 44. Willson JD, Kernozek TW, Arndt RL, Reznichek DA, Scott Straker J.
1999;32(1):99-103. Gluteal muscle activation during running in females with and without
24. Lyons K, Perry J, Gronley JK, Barnes L, Antonelli D. Timing and rel- patellofemoral pain syndrome. Clin Biomech (Bristol, Avon).
ative intensity of hip extensor and abductor muscle action during 2011;26(7):735-740.
level and stair ambulation: an EMG study. Phys Ther. 1983;63(10): 45. Wu G, Siegler S, Allard P, et al. ISB recommendation on definitions of
1597-1605. joint coordinate system of various joints for the reporting of human
25. MacKinnon DP, Fairchild AJ, Fritz MS. Mediation analysis. Annu Rev joint motion: part I. Ankle, hip, and spine. International Society of Bio-
Psychol. 2007;58:593-614. mechanics. J Biomech. 2002;35(4):543-548.

For reprints and permission queries, please visit SAGE’s Web site at