Relationship between knee abduction moment with patellofemoral joint reaction force, stress and self-reported pain during stair descent in women with patellofemoral pain

Accepted Manuscript Relationship between knee abduction moment with patellofemoral joint reaction force, stress and self-reported pain during stair descent in women with patellofemoral pain

Marina Cabral Waiteman, Ronaldo Valdir Briani, Marcella Ferraz Pazzinatto, Amanda Schenatto Ferreira, Deisi Ferrari, Danilo de Oliveira Silva, Fábio Mícolis de Azevedo PII: DOI: Reference:

S0268-0033(18)30146-3 doi:10.1016/j.clinbiomech.2018.09.012 JCLB 4601

To appear in:

Clinical Biomechanics

Received date: Accepted date:

21 February 2018 10 September 2018

Please cite this article as: Marina Cabral Waiteman, Ronaldo Valdir Briani, Marcella Ferraz Pazzinatto, Amanda Schenatto Ferreira, Deisi Ferrari, Danilo de Oliveira Silva, Fábio Mícolis de Azevedo , Relationship between knee abduction moment with patellofemoral joint reaction force, stress and self-reported pain during stair descent in women with patellofemoral pain. Jclb (2018), doi:10.1016/j.clinbiomech.2018.09.012

This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

ACCEPTED MANUSCRIPT

RELATIONSHIP BETWEEN KNEE ABDUCTION MOMENT WITH PATELLOFEMORAL JOINT REACTION FORCE, STRESS AND SELFREPORTED PAIN DURING STAIR DESCENT IN WOMEN WITH PATELLOFEMORAL PAIN

PT

Marina Cabral Waiteman PT1, Ronaldo Valdir Briani PT, MSc1, Marcella Ferraz Pazzinatto1,2

São Paulo State University, School of Science and Technology, Physical Therapy

Department, Presidente Prudente, Brazil

La Trobe Sports and Exercise Medicine Research Centre, School of Allied Health, La Trobe

MA

2

NU

1

SC

Silva1,2 PT, MSc, Fábio Mícolis de Azevedo1 PT, PhD

RI

PT, MSc, Amanda Schenatto Ferreira1 PT, Deisi Ferrari3,4 PT, PhD, Danilo de Oliveira

University, Bundoora, Victoria, Australia

Educational Faculty of Francisco Beltrão, Physical Therapy Department, Francisco Beltrão,

D

3

4

PT E

Brazil

Cascavel Educational Center, Physical Therapy Department, Cascavel, Brazil

Corresponding author:

CE

Fábio Mícolis de Azevedo

AC

Sao Paulo State University (UNESP) - School of Science and Technology - Physical Therapy Department - Laboratory of Biomechanics and Motor Control (LABCOM). Rua Roberto Simonsen, 305 Presidente Prudente – SP - Brazil Postal Code: 19060-900 e-mail: [email protected] Abstract count: 250 Main Text count: 3873

ACCEPTED MANUSCRIPT

ABSTRACT Background: Increased external knee abduction moment has been proposed as a risk factor for patellofemoral pain. This alteration is thought to be associated with elevated patellofemoral joint reaction force and stress, however these relationships remain poorly explored. Therefore,

PT

this study aimed at comparing knee abduction moment parameters (peak, rate of moment development and impulse), patellofemoral joint reaction force and stress of women with

RI

patellofemoral pain and pain-free controls during stair descent; and investigating the

SC

relationship among these variables with self-reported pain. Methods: Kinetic data was obtained by inverse-dynamics equations and a previously reported algorithmic model was

NU

used to determine patellofemoral joint reaction force and stress. Participants’ worst pain in the

MA

last month and pain level during stair descent were evaluated using a visual analogue scale. Findings: Women with patellofemoral pain presented higher peak, rate of moment

D

development and impulse of the external knee abduction moment, patellofemoral joint

PT E

reaction force and stress (p = 0.005 to 0.04, effect size = 0.52 to 0.96) during stair descent than pain-free controls. Only knee abduction moment impulse presented positive moderate correlations with worst pain level in the last month (r = 0.53, p < 000.1), pain level during

CE

stair descent (r = 0.33, p = 0.042), patellofemoral joint reaction force (r = 0.65, p < 000.1) and

AC

stress (r = 0.58, p < 000.1). Interpretation: These findings indicate that strategies aimed at decreasing external knee abduction moment impulse could reduce the load over the patellofemoral joint and improve pain of women with patellofemoral pain. Keywords: Knee abduction moment, knee, anterior knee pain, kinetics, biomechanics.

ACCEPTED MANUSCRIPT

1. INTRODUCTION Patellofemoral pain (PFP) is a common knee disorder, aggravated by repetitive activities loading the patellofemoral joint (PFJ) such as stair negotiation, squatting and running (Briani et al., 2017; Crossley et al., 2016). PFP has an annual prevalence of 22.7% in

PT

the general population (Smith et al., 2018), from which women are 2.23 times more likely to develop PFP than men (Boling et al., 2010). Individuals with PFP present a poor prognosis

RI

with 56.7% reporting unfavorable outcomes 5-8 years after treatment (Lankhorst et al., 2015).

etiology remains unknown (Powers et al., 2017).

SC

Several biomechanical studies have investigated the underlying causes of PFP, however, its

NU

Alterations in knee frontal plane kinetics have been found in individuals with PFP

MA

(Aminaka et al., 2011; Myer et al., 2015; Stefanyshyn et al., 2006). High knee frontal plane moments have been identified in different activities such as running (Stefanyshyn et al., 2006)

D

and drop vertical jump (Myer et al., 2010). More specifically, a higher peak external knee

PT E

abduction moment (KAbdM) than 15 Nm during drop vertical jump has been proposed as a risk factor for PFP in a recent prospective study (Myer et al., 2015). However, only one study (Aminaka et al., 2011) has investigated knee frontal plane moments during stair ambulation,

CE

which is a daily task that exacerbates PFP (Briani et al., 2018, 2017). The authors have found

AC

a higher external knee adduction moment in women with PFP compared to controls (Aminaka et al., 2011), which is in contrast to the literature that suggests a valgus knee orientation and a higher external KAbdM in individuals with PFP (Myer et al., 2015; Powers, 2010). They suggested this might have been a compensatory strategy to provide stability of the lower extremity during a dynamic task. However, further investigation is needed to better understand this conflicting mechanical behavior (Aminaka et al., 2011). There seems to be a direct relation between a knee valgus orientation and moment with PFJ contact pressures (Li et al., 2004). Studies suggest that a valgus knee orientation and 3

ACCEPTED MANUSCRIPT

moment may increase the lateral forces acting on the patella, which would be expected to elevate the lateral pressures within the PFJ (Huberti and Hayes, 1984; Powers, 2010). This is supported by the findings of Huberti and Hayes (1984), who have found that a 10° increase towards a knee valgus orientation increased the PFJ stress by 45%. A knee valgus orientation

PT

may also reduce the PFJ contact area (Davis et al., 2017; Liao et al., 2015), increasing PFJ reaction force and stress (Davis et al., 2017; Powers, 2010). Although elevated PFJ reaction

RI

force and stress have been recently proposed as contributor factors to PFP (Powers et al.,

SC

2017), no study has investigated the relationship between the external KAbdM with PFJ reaction force, stress and self-reported pain during a daily task such as stair descent in women

NU

with PFP.

MA

The aims of this study were: (1) to compare external KAbdM parameters (peak, rate of moment development and impulse), PFJ reaction force and stress of women with PFP and

D

sex-matched pain-free controls during stair descent; (2) to investigate the relationship between

PT E

peak, rate of moment development and impulse of the external KAbdM with PFJ reaction force, PFJ stress and self-reported pain in women with PFP.

CE

2. METHODS

AC

2.1. Participants

Sixty-four women aged 18 to 35 years were recruited via advertisements at universities, public places for physical activity practice, gyms and social media. Participants were divided into two groups: PFP group (n = 32) and pain-free group (n = 32). Prior to data collection, all participants provided written informed consent and the experimental protocol was approved by the Institutional Review Board of the University’s Human Ethics Committee (1.484.129).

4

ACCEPTED MANUSCRIPT

Diagnosis of PFP was confirmed by a clinician (> five years’ experience) based on definitions used in previous studies (Crossley et al., 2016). The following inclusion criteria for PFP participants were considered: (1) anterior knee pain when performing at least two of the following activities: sitting for prolonged time, squatting, kneeling, running, ascending

PT

and descending stairs, jumping and landing; (2) insidious onset symptoms lasting at least 4 months; (3) the worst pain level in the previous month corresponding to at least 3 cm in the

RI

visual analogue pain scale (VAS). Women were included in the pain-free group if they had no

SC

signs or symptoms of PFP or other neurological or musculoskeletal condition. Exclusion criteria for both PFP and pain-free groups were as follow: sign or symptoms of any other knee

NU

dysfunction, history of surgery in any lower limb joint, history of patellar subluxation or

MA

clinical evidence of meniscal injury or ligament instability, and referred pain coming from the

PT E

2.2. Instrumentation

D

lumbar spine.

Data collection included lower-limb kinetic and kinematic evaluation, during stair descent, of each participant’s symptomatic limb (those with unilateral symptoms) or most

CE

symptomatic limb (in those with bilateral symptoms) for PFP group, and dominant limb for

AC

pain-free group (De Oliveira Silva et al., 2016). Stair descent was chosen since it is a daily task that exacerbates pain and increase the load in the PFJ joint of women with PFP (Brechter and Powers, 2002; Briani et al., 2017). Kinetic data were collected using a force plate (Bertec Corporation, Columbus, OH, model FP4060) at a sampling frequency of 4000 Hz. A threedimensional motion analysis system (Vicon Motion Systems Inc. Denver EUA) combined with 9 cameras (type Bonita®B10) operating at a sampling frequency of 100 Hz was used to obtain kinematic data. The force plate and motion system were synchronized by the Vicon Lock® device. The experimental design included a seven step staircase, each step being 28 5

ACCEPTED MANUSCRIPT

cm deep and 18 cm high (De Oliveira Silva et al., 2016). To ensure a natural stair descent pattern, participants were not made aware of the force plate, which was covered by a rubberized fabric (De Oliveira Silva et al., 2016; Ferrari et al., 2018). Participants’ worst pain in the last month and pain level at the moment of data

PT

collection (during stair descent) were evaluated using a 10 cm VAS. The extreme left side of the VAS indicated “no pain” whereas the extreme right side indicated “worst pain

RI

imaginable.” Participants drew a perpendicular line on the scale at the position that most

SC

likely described their pain. This scale has been validated and it is reliable for assessing women with PFP (Crossley et al., 2004). Additionally, duration of knee-related symptoms

MA

NU

(months) and self-reported knee function (anterior knee pain scale - AKPS) were obtained.

2.3. Procedure

D

Demographic data were collected prior to testing, including age, body mass, height,

PT E

length of the lower limbs (distance from the anterior superior iliac spine to the inferior surface of the medial malleolus), width of the ankle and knee joints (through a universal pachymeter 150mm 0,02mm - Digimess®). Afterwards, the biomechanical model (combination of oxford-

CE

foot-model with plug-in gait - PiG to lower limbs) with 29 markers (9 mm of diameter) was

AC

positioned by the same investigator in specific anatomic points (De Oliveira Silva et al., 2016b). Markers placed on the right and left side were: anterior superior iliac spine, posterior superior iliac spine, lateral aspect of the femur, estimated average axis of rotation of the knee joint, lateral aspect of tibia, lateral malleolus, heel posterior face and over the second metatarsal head. Markers placed only on the tested limb were: head of fibula, tibial tuberosity, anterior aspect of the shin, posterior end of the calcaneus, lateral aspect of the calcaneus, sustentaculum tali, base of first metatarsal, head of fifth metatarsal, base of fifth metatarsal

6

ACCEPTED MANUSCRIPT

and hallux. Medial malleolus, posterior calcaneus proximal and head of first metatarsal were used for static calibration only. After positioning the markers, a relaxed standing calibration trial was then captured. Then, participants performed three practice stair descent trials to allow familiarization with

PT

the instrumentation and environment; the participants were not able to use handrails. Five successful trials were collected for each participant and the mean value of these five trials was

RI

used for data analyses in order to attenuate the influence of speed, intra-subject variability,

SC

and other external factors (Winter, 2009). A trial was considered successful when the tested limb touched the fourth step (where force plate was allocated) and the participant had

NU

performed the stair descent at their natural comfortable speed (Jordan et al., 2007). If the trial

MA

was not considered valid, an additional trial was performed. Just the kinematic and kinetic

PT E

2.4. Data analysis

D

data of the fourth step was considered in the analyses.

Link-segment models and inverse-dynamics equations were used (Vicon Nexus 2.0® Software) to obtain kinetic data of the lower limbs (Winter, 2009). To be consistent with

CE

previous literature (Myer et al., 2015, 2010; Stefanyshyn et al., 2006), kinematic and kinetic

AC

data were filtered with a fourth-order Butterworth low-pass filter with a cutoff frequency of 12 Hz (Winter, 2009). The calculation of external KAbdM was performed using the software (Vicon Nexus 2.0® Software). Afterwards, peak, rate of moment development and impulse of the KAbdM were obtained by custom-written codes in MATLAB® (The Math Works, Inc, Natick, MA). Peak of the external KAbdM was determined by the maximum value reached during the stance phase and was normalized by the body weight of each participant (Myer et al., 2015). The stance phase was defined as time while the foot was in contact with the force plate (fourth step) (De Oliveira Silva et al., 2016). The initial and the end of the stance phase 7

ACCEPTED MANUSCRIPT

were determined when the vertical ground reaction force exceeded 10N up and down, respectively (De Oliveira Silva et al., 2016). The rate of moment development of the external KAbdM was calculated as the change between each point of the KAbdM and time signals from the foot initial contact until the peak KAbdM. Then, the change in the KAbdM was

PT

divided by the respective change in time and the mean was calculated (Morgenroth et al., 2014). External KAbdM impulse (total area under the curve) was quantified by integrating the

RI

moment-time curve, it represents the cumulative twisting load during the entire stance phase

SC

(Stefanyshyn et al., 2006). In addition, the stance time for one entire gait cycle was obtained while the participant was crossing over the force plate in the fourth step (Briani et al., 2018;

NU

Ferreira et al., 2018). Each event was inspected manually by viewing the animated

MA

visualization of the motion data.

A previously reported algorithmic model was used to determine PFJ reaction force and

D

PFJ stress (Sinclair and Selfe, 2015). This algorithm has already been used to detect

PT E

differences in PFJ reaction force and PFJ stress between individuals with PFP and pain-free controls during stair descent (Brechter and Powers, 2002). The detailed description of the algorithm can be found in appendix 1. These variables were extracted from the entire stance

AC

CE

phase and then averaged for statistical analysis.

2.5. Statistics analysis All analyses were conducted using Statistical Software for the Social Sciences 18.0 program (SPSS Inc, Chicago, IL). Based on calculations made in sample-power with data from Sinclair et al. (Sinclair and Selfe, 2015), a sample size of 28 individuals per group was indicated to evaluate differences in PFJ stress with a statistical power of 85%, observing a minimum difference of 1.31 MPa between means, a standard deviation of 1.36 MPa and a significance level of 5%. PCP was chosen for sample-power calculation because it was the 8

ACCEPTED MANUSCRIPT

kinetic parameter with the highest standard deviation and the smallest difference between groups (Field, 2013). The data were analyzed with respect to their distribution, and homogeneity using the Shapiro-Wilk and Levene’s tests, respectively. As all variables were found to be normally

PT

distributed, demographics data were compared between groups with independent t tests. To account for the possible influence of speed on kinetic parameters (Jordan et al., 2007),

RI

analyses of covariance were performed to provide between-group comparisons adjusted for

SC

the stance time of the participants. The Bonferroni post hoc test was performed for pairwise comparisons. Effect sizes were calculated for pairwise comparisons according to equations

NU

previously described, and the guidelines for interpreting the Cohen's d are: 0 to 0.40 small

MA

effect, 0.41 to 0.70 moderate effect, 0.71 or higher large effect (Field, 2013). A Pearson correlation matrix was used to investigate relationships among peak, rate of moment

D

development and impulse of the external KAbdM with the self-reported pain (worst pain in

PT E

the last month and pain during stair descent), PFJ reaction force and PFJ stress in women with PFP. For these analyses, the magnitude of correlation were interpreted as: 0.00 to 0.25 little or no correlation; 0.25 to 0.50 fair correlation; 0.50 to 0.75 moderate to good correlation; and

AC

CE

more than 0.75 excellent correlation (Portney and Watkins, 2009).

3. RESULTS

Independent t-tests revealed no differences between groups for age, height, body mass and BMI (Table 1). Symptoms duration and self-reported knee function of women with PFP are described in table 1. Women with PFP presented higher peak (F = 4.911, p = 0.010, d = 0.60), rate of moment development (F = 5.975, p = 0.005, d = 0.78) and impulse (F = 7.737, p < 0.001, d = 0.96) of the external KAbdM during stair descent than pain-free controls (Table 2). In 9

ACCEPTED MANUSCRIPT

addition, women with PFP presented higher PFJ reaction force (F = 4.392, p = 0.040, d = 0.52) and PFJ stress (F = 5.472, p = 0.015, d = 0.73) than pain-free controls. Stance time was not significantly associated with the kinetic parameters (p = 0.841 to 0.202). There were no correlations between peak and rate of moment development of the

PT

external KAbdM with worst pain level in the last month (Figure 1). On the other hand, there was a positive moderate correlation (r = 0.53, p < 000.1) between external KAbdM impulse

RI

and worst pain level in the last month (Figure 1). Likewise, peak (r = 0.032, p = 0.432) and

SC

rate of moment development (r = 0.034, p = 0.427) of the external KAbdM did not correlate with pain level during stair descent, but external KAbdM impulse had positive fair correlation

NU

(r = 0.33, p = 0.042). Peak and rate of moment development of the external KAbdM did not

MA

correlate PFJ reaction force and PFJ stress, but external KAbdM impulse had positive moderate correlation with PFJ reaction force (r = 0.65, p < 000.1) and PFJ stress (r = 0.58, p <

PT E

D

000.1) (Figure 2).

4. DISCUSSION

Our findings demonstrated that women with PFP present higher peak, rate of moment

CE

development and impulse of the external KAbdM compared to pain-free controls. Moreover,

AC

women with PFP presented higher PFJ reaction force and PFJ stress than pain-free controls while descending stairs. Only higher external KAbdM impulse was related with PFJ reaction force, stress and self-reported pain, that is, the higher the external KAbdM impulse, the higher the PFJ reaction force, stress and self-reported pain of women with PFP. Dynamic external KAbdM has been suggested to contribute to the onset of PFP (Myer et al., 2010). Previous studies reported that women with PFP present higher external KAbdM (Myer et al., 2010) and those who demonstrate a peak external KAbdM above 15.4 Nm during drop vertical jump have an increased risk of developing PFP (Myer et al., 2015). Our 10

ACCEPTED MANUSCRIPT

results are in accordance with these findings, demonstrating that women with PFP present higher peak, rate of moment development and impulse of the external KAbdM during stair descent than pain-free controls. However, this is in contrast to some studies that found greater external knee adduction moment in individuals with PFP during walking and running (Bazett-

PT

Jones et al., 2013; Paoloni et al., 2010; Stefanyshyn et al., 2006), which might be explained by the different tasks being evaluated. On the other hand, Aminaka et al. (2011) showed that

RI

individuals with PFP presented higher external knee adduction moment during stair

SC

ambulation. The differences in the participants included in our and Aminaka's et al. (2011) study may explain the discrepant findings. While we included only women with PFP, men

NU

and women with PFP were included in Aminaka's et al. (2011) study. Men were shown to

MA

present knee varus orientation during stair descent (Baldon et al., 2013), greater peak external knee adduction moment during running (Willy et al., 2013) and higher peak knee varus

D

moment during drop vertical jump (Kernozek et al., 2005), which might have influenced their

PT E

findings. In addition, the authors have stated that the higher external knee adduction moment might have been be a compensatory strategy used by individuals with PFP to provide stability to the lower extremity in order to reduce external KAbdM and pain (Aminaka et al., 2011).

CE

Therefore, women with PFP present increased external KAbdM during stair descent

AC

compared to pain-free controls, but further studies are needed to investigate this mechanical behavior in a population of men with PFP. The moderate correlation between external KAbdM impulse with PFJ stress found in our study may corroborate with the theory that alterations in the frontal plane might be related with higher PFJ stress (Huberti and Hayes, 1984; Li et al., 2004). The elevated external KAbdM impulse found in women with PFP was positively correlated with PFJ reaction force and stress. As previously shown (Schulthies et al., 1995), the patella has a natural tendency to experience laterally directed forces as a result of the valgus orientation and moment of the 11

ACCEPTED MANUSCRIPT

lower extremity due to changes in the quadriceps angle (Q-angle). As the Q-angle reflects the frontal plane forces acting on the patella, an increase in knee valgus would elevate the Qangle, which would be expected to increase the lateral pressures within the PFJ (Powers, 2010). This is in line with Huberti and Hayes (1984) who reported that a 10° increase in the

PT

Q-angle resulted in a 45% increase in peak contact pressure on the lateral aspect of the PFJ. Therefore, besides knee extensor moment and knee flexion which are known to influence PFJ

RI

reaction force and stress (Atkins et al., 2018; Brechter and Powers, 2002), it seems that knee

SC

frontal plane alterations such as high external KAbdM may also be associated with elevated PFJ reaction force and stress, which suggests they should be considered into clinical practice

NU

and biomechanical models.

MA

Increased PFJ reaction force and stress have been proposed as main contributors to PFP (Powers et al., 2017). Peak PFJ reaction force was recently shown to be the best

D

predictor of the rate of change in pain in women with PFP after repetitive impact landings

PT E

(Atkins et al., 2018). Considering that our results showed a relationship between external KAbdM impulse with PFJ reaction force and stress, it is not surprising that the elevated external KAbdM impulse found in women with PFP was also associated with higher reports

CE

of pain. Therefore, it seems that high external KAbdM impulse is associated with elevated

AC

PFJ reaction force and stress and, consequently, knee pain. Interestingly, all parameters of the external KAbdM were higher in women with PFP, but only external KAbdM impulse was related to PFJ stress and self-reported pain. Probably this happened because the impulse represents the cumulative twisting load during the entire stance phase and is more representative of the loading in the knee joint than the other variables (Aminaka et al., 2011; Stefanyshyn et al., 2006). Therefore, treatments aimed at decreasing external KAbdM impulse may have positive effects in managing PFJ reaction force, stress and pain in women with PFP. Biomechanical alterations in the frontal plane appear to play a role in the events that 12

ACCEPTED MANUSCRIPT

lead to the initiation and progression of osteoarthritis (Cahue et al., 2004; Elahi et al., 2000; Guilak, 2011). A previous study (Elahi et al., 2000) showed that knees with PFJ osteoarthritis are more likely to have excessive valgus angulation, and consequently higher external KAbdM (Powers, 2010). In addition, Cahue et al. (2004) have found that those with knee

PT

valgus orientation have higher odds of lateral PFJ space narrowing progression. These findings suggest that an increase in the external KAbdM may lead to an increase in the load of

RI

the PFJ, which may have important implications for the progression of degenerative joint

SC

disease. In this direction, a recent narrative review investigated the biomechanical link between PFP and PFJ osteoarthritis (Wyndow et al., 2016). They reported mechanical factors,

NU

shared by both disorders, that may act altering joint loads and increasing PFJ stress (Wyndow

MA

et al., 2016). However, the contribution of the KAbdM in this context has still not been explored. Thus, further research is warranted to investigate the contribution of high external

PT E

D

KAbdM to the possible continuum between PFP and PFJ osteoarthritis.

4.1. Clinical implications

The findings of this study highlight that clinicians should consider interventions

CE

aiming to reduce external KAbdM impulse during functional gestures as it is related with PFJ

AC

reaction force, stress and self-reported pain. For instance, flat flexible shoes have been indicated to minimize increased knee impulse in the frontal plane (Paterson et al., 2017). In addition to footwear usage, strategies to reduce the knee valgus position of women with PFP, and consequently the external KAbdM impulse, PFJ reaction force and stress, may be indicated such as general hip abductors and external rotators strengthening, verbal and visual feedback (Powers, 2010). Proximal strengthening has been shown to improve knee pain and function, increase strength of hip abductors and external rotators muscles and reduce KAbdM (Earl and Hoch, 2011). Moreover, strengthening of the knee flexors and extensors may 13

ACCEPTED MANUSCRIPT

provide balanced co-contraction, compress the joint and potentially limit high external KAbdM impulse during dynamic tasks (Myer et al., 2015). Therefore, adequate programs with strengthening, verbal and visual feedback and changes in footwear may be effective in reducing external KAbdM impulse and could be applied in women with PFP, if efficacy is

PT

proved in further randomized controlled trials (RCTs). Despite providing insights about which interventions could be beneficial to women with PFP, the design of this study does not allow

SC

RI

intervention prescription, but it highlights the need for new RCTs exploring this subject.

4.2. Limitations

NU

There are some limitations in this study that should be acknowledged. Firstly, a

MA

potential drawback of the current study is that PFJ stress was quantified using a mathematical model. The model used in this study includes estimates of patellofemoral contact area and

D

quadriceps moment arm that are not specific to our participants. Secondly, since this is the

PT E

first study that has investigated the relationship between frontal plane kinetics with PFJ reaction force and stress in women with PFP, we have used a common model that only considers sagittal plane inputs to calculate PFJ reaction force and stress. Therefore,

CE

considering our findings, future studies are warranted to investigate the importance of adding

AC

frontal plane kinetics in the calculation of PFJ reaction force and stress. Lastly, although women with PFP is the subgroup that is the most likely to suffer from PFP (Boling et al., 2010), since our study included only women the results cannot be generalizable to the entire population of individuals with PFP (e.g. adolescents, man).

5. CONCLUSION Women with PFP presented higher peak, rate of moment development and impulse of the external KAbdM. Moreover, women with PFP presented higher PFJ reaction force and 14

ACCEPTED MANUSCRIPT

stress than pain-free controls while descending stairs. However, only the external KAbdM impulse was positively correlated with PFJ reaction force, stress and self-reported pain. Therefore, strategies aimed at decreasing external KAbdM impulse could be important for

PT

reducing the load over the PFJ and improving pain of women with PFP.

6. ACKNOWLEDGEMENT

RI

This work was supported by the FAPESP – São Paulo Research Foundation [Grants

SC

number: 2016/09665-3; 2014/24939-7]

NU

7. REFERENCES

MA

Aminaka, N., Pietrosimone, B.G., Armstrong, C.W., Meszaros, A., Gribble, P.A., 2011. Patellofemoral pain syndrome alters neuromuscular control and kinetics during stair J.

Electromyogr.

Kinesiol.

21,

645–651.

D

ambulation.

PT E

https://doi.org/10.1016/j.jelekin.2011.03.007 Atkins, L.T., James, C.R., Yang, H.S., Sizer, P.S., Brismée, J.M., Sawyer, S.F., Powers, C.M., 2018. Changes in patellofemoral pain resulting from repetitive impact landings are

CE

associated with the magnitude and rate of patellofemoral joint loading. Clin. Biomech.

AC

53, 31–36. https://doi.org/10.1016/j.clinbiomech.2018.02.006 Baldon, R.D.M., Lobato, D.F.M., Furlan, L., Serrão, F. V., 2013. Gender differences in lower limb kinematics during stair descent. J. Appl. Biomech. 29, 413–420. Bazett-Jones, D.M., Cobb, S.C., Huddleston, W.E., O’Connor, K.M., Armstrong, B.S.R., Earl-Boehm, J.E., 2013. Effect of patellofemoral pain on strength and mechanics after an exhaustive

run.

Med.

Sci.

Sports

Exerc.

45,

1331–1339.

https://doi.org/10.1249/MSS.0b013e3182880019 Boling, M., Padua, D., Marshall, K., Guskiewicz, K., Pyne, S., Beutler, A., 2010. Gender 15

ACCEPTED MANUSCRIPT

differences in the incidence and prevalence of patellofemoral pain syndrome. Scand. J. Med. Sci. Sport. 20, 725–730. https://doi.org/10.1111/j.1600-0838.2009.00996.x.Gender Brechter, J.H., Powers, C.M., 2002. Patellofemoral joint stress during stair ascent and descent in persons with and without patellofemoral pain. Gait Posture 16, 115–123.

PT

https://doi.org/10.1016/S0966-6362(02)00090-5 Briani, R.V., Pazzinatto, M.F., Waiteman, M.C., de Oliveira Silva, D., de Azevedo, F.M.,

RI

2018. Association between increase in vertical ground reaction force loading rate and

SC

pain level in women with patellofemoral pain after a patellofemoral joint loading protocol. Knee 25, 398–405. https://doi.org/10.1016/j.knee.2018.03.009

NU

Briani, R. V., Pazzinatto, M.F., Silva, D.O., Azevedo, F.M., 2017. Different pain responses to

MA

distinct levels of physical activity in women with patellofemoral pain. Brazilian J. Phys. Ther. 21, 138–143. https://doi.org/10.1016/j.bjpt.2017.03.009

D

Cahue, S., Dunlop, D., Hayes, K., Song, J., Torres, L., Sharma, L., 2004. Varus-valgus

PT E

alignment in the progression of patellofemoral osteoarthritis. Arthritis Rheum. 50, 2184– 2190. https://doi.org/10.1002/art.20348 Crossley, K.M., Bennell, K.L., Cowan, S.M., Green, S., 2004. Analysis of outcome measures

CE

for persons with patellofemoral pain: Which are reliable and valid? Arch. Phys. Med.

AC

Rehabil. 85, 815–822. https://doi.org/10.1016/S0003-9993(03)00613-0 Crossley, K.M., Stefanik, J.J., Selfe, J., Collins, N.J., Davis, I.S., Powers, C.M., Mcconnell, J., Vicenzino, B., Bazett-jones, D.M., Esculier, J., Morrissey, D., Callaghan, M.J., 2016. 2016 Patellofemoral pain consensus statement from the 4th International Patellofemoral Pain Research Retreat, Manchester. Part 1: Terminology, definitions, clinical examination, natural history, patellofemoral osteoarthritis and patient-reported outcome m. Br. J. Sports Med. 50, 839–843. https://doi.org/10.1136/bjsports-2016-096384 Davis, I., Powers, C., Tenforde, A., Singh, J.R., 2017. A Tale of Two Treatments for 16

ACCEPTED MANUSCRIPT

Patellofemoral Pain. Pm&R 9, 1283–1289. https://doi.org/10.1016/j.pmrj.2017.10.012 De Oliveira Silva, D., Barton, C.J., Pazzinatto, M.F., Briani, R.V., De Azevedo, F.M., 2016a. Proximal mechanics during stair ascent are more discriminate of females with patellofemoral

pain

than

distal

mechanics.

Clin.

Biomech.

35,

56–61.

PT

https://doi.org/10.1016/j.clinbiomech.2016.04.009 De Oliveira Silva, D., Magalhães, F.H., Pazzinatto, M.F., Briani, R.V., Ferreira, A.S., Aragão,

RI

F.A., de Azevedo, F.M., 2016b. Contribution of altered hip, knee and foot kinematics to

SC

dynamic postural impairments in females with patellofemoral pain during stair ascent. Knee 23, 376–381. https://doi.org/10.1016/j.knee.2016.01.014

NU

Earl, J.E., Hoch, A.Z., 2011. A proximal strengthening program improves pain, function, and

MA

biomechanics in women with patellofemoral pain syndrome. Am. J. Sports Med. 39, 154–163. https://doi.org/10.1177/0363546510379967

D

Elahi, S., Cahue, S., Felson, D.T., Engelman, L., Sharma, L., 2000. The association between

PT E

varus-valgus alignment and patellofemoral osteoarthritis. Arthritis Rheum. 43, 1874– 1880. https://doi.org/10.1002/1529-0131(200008)43:8<1874::AID-ANR25>3.0.CO;2-2 Ferrari, D., Briani, R.V., de Oliveira Silva, D., Pazzinatto, M.F., Ferreira, A.S., Alves, N., de

CE

Azevedo, F.M., 2018. Higher pain level and lower functional capacity are associated

AC

with the number of altered kinematics in women with patellofemoral pain. Gait Posture 60, 268–272. https://doi.org/10.1016/j.gaitpost.2017.07.034 Ferreira, A.S., de Oliveira Silva, D., Briani, R.V., Ferrari, D., Aragão, F.A., Pazzinatto, M.F., de Azevedo, F.M., 2018. Which Is the Best Predictor of Excessive Hip Internal Rotation in Women With Patellofemoral Pain: Rearfoot Eversion or Hip Muscle Strength? Exploring

Subgroups.

Gait

Posture

62,

366–371.

https://doi.org/10.1016/j.gaitpost.2018.03.037 Field, A., 2013. Discovering statistics using IBM SPSS statistics, 4a. ed. Sage, London. 17

ACCEPTED MANUSCRIPT

Guilak, F., 2011. Biomechanical factors in osteoarthtitis. Best Pract. Res. Clin. Rheumatol. 25, 815–823. https://doi.org/10.1016/j.berh.2011.11.013 Huberti, H.H., Hayes, W.C., 1984. Patellofemoral contact pressures: The influence of Q-angle and tendofemoral contact. J. bone Jt. Surg. 66, 715–724.

PT

Jordan, K., Challis, J.H., Newell, K.M., 2007. Walking speed influences on gait cycle variability. Gait Posture 26, 128–134. https://doi.org/10.1016/j.gaitpost.2006.08.010

RI

Kernozek, T.W., Torry, M.R., Van Hoof, H., Cowley, H., Tanner, S., 2005. Gender

SC

differences in frontal and sagittal plane biomechanics during drop landings. Med. Sci. Sports Exerc. 37, 1003–1012. https://doi.org/10.1249/01.mss.0000171616.14640.2b

NU

Lankhorst, N.E., van Middelkoop, M., Crossley, K.M., Bierma-Zeinstra, S.M.A., Oei, E.H.G.,

MA

Vicenzino, B., Collins, N.J., 2015. Factors that predict a poor outcome 5–8 years after the diagnosis of patellofemoral pain: a multicentre observational analysis. Br. J. Sports

D

Med. 50, 881–886. https://doi.org/10.1136/bjsports-2015-094664

PT E

Li, G., DeFrate, L.E., Zayontz, S., Park, S.E., Gill, T.J., 2004. The effect of tibiofemoral joint kinematics on patellofemoral contact pressures under simulated muscle loads. J. Orthop. Res. 22, 801–806. https://doi.org/10.1016/j.orthres.2003.11.011

CE

Liao, T.C., Yang, N., Ho, K.Y., Farrokhi, S., Powers, C.M., 2015. Femur Rotation Increases

AC

Patella Cartilage Stress in Females with Patellofemoral Pain. Med. Sci. Sports Exerc. 47, 1775–1780. https://doi.org/10.1249/MSS.0000000000000617 Morgenroth, D.C., M., J.R., Mahyo, S., Czerniecki, J.M., 2014. The Relationship between Knee Joint Loading Rate During Walking and Degenerative Changes on Magnetic Resonance Imaging. Clin. Biomech. 29, 664–670. https://doi.org/10.1038/jid.2014.371 Myer, G.D., Ford, K.R., Di Stasi, S.L., Foss, K.D.B., Micheli, L.J., Hewett, T.E., 2015. High knee abduction moments are common risk factors for patellofemoral pain (PFP) and anterior cruciate ligament (ACL) injury in girls: is PFP itself a predictor for subsequent 18

ACCEPTED MANUSCRIPT

ACL injury? Br. J. Sports Med. 49, 118–122. https://doi.org/10.1136/bjsports-2013092536 Myer, G.D., Ford, K.R., Foss, K.D.B., Goodman, A., Ceasar, A., Rauh, M.J., Facsm, M.P.H., Divine, J.G., Hewett, T.E., 2010. The incidence and potencial pathomecanics of Pain

in

female

athletes.

Clin.

https://doi.org/10.1016/j.clinbiomech.2010.04.001.The

Biomech.

25,

700–707.

PT

Patellofemoral

RI

Paoloni, M., Mangone, M., Fratocchi, G., Murgia, M., Maria Saraceni, V., Santilli, V., 2010.

More

than

a

sagittal

SC

Kinematic and kinetic features of normal level walking in patellofemoral pain syndrome: plane

alteration.

J.

Biomech.

43,

1794–1798.

NU

https://doi.org/10.1016/j.jbiomech.2010.02.013

MA

Paterson, K.L., Bennell, K.L., Wrigley, T. V., Metcalf, B.R., Kasza, J., Hinman, R.S., 2017. Effects of footwear on the knee adduction moment in medial knee osteoarthritis:

D

classification criteria for flat flexible vs stable supportive shoes. Osteoarthr. Cartil. 25,

PT E

234–241. https://doi.org/10.1016/j.joca.2016.10.001 Portney, L., Watkins, M., 2009. Foundations of clinical research: applications to practice, 3 o. ed. Pearson Prentice Hall, New Jersey.

CE

Powers, C.M., 2010. The influence of abnormal hip mechanics on knee injury: a perspective.

J.

Orthop.

Sports

Phys.

Ther.

40,

42–51.

AC

biomechanical

https://doi.org/10.2519/jospt.2010.3337 Powers, C.M., Witvrouw, E., Davis, I.S., Crossley, K.M., 2017. Evidence-based framework for a pathomechanical model of patellofemoral pain: 2017 patellofemoral pain consensus statement from the 4th International Patellofemoral Pain Research Retreat, Manchester, UK: Part 3. Br. J. Sports Med. 51, 1713–1723. https://doi.org/10.1136/bjsports-2017098717 Schulthies, S.S., Francis, R.S., Fisher, A.G., Van de Graaff, K.M., 1995. Does the Q angle 19

ACCEPTED MANUSCRIPT

reflect the force on the patella in the frontal plane? Phys. Ther. 75, 24–30. Sinclair, J., Selfe, J., 2015. Sex differences in knee loading in recreational runners. J. Biomech. 48, 2171–2175. https://doi.org/10.1016/j.jbiomech.2015.05.016 Smith, B., Selfe, J., Thacker, D., Hendrick, P., Bateman, M., Moffatt, F., Rathleff, M., Smith,

and

meta-analysis.

PLoS

https://doi.org/10.1371/journal.pone.0190892

One

13,

e0190892.

RI

review

PT

T., Logan, P., 2018. Incidence and prevalence of patellofemoral pain: a systematic

SC

Stefanyshyn, D.J., Stergiou, P., Lun, V.M.Y., Meeuwisse, W.H., Worobets, J.T., 2006. Knee angular impulse as a predictor of patellofemoral pain in runners. Am. J. Sports Med. 34,

NU

1844–1851. https://doi.org/10.1177/0363546506288753

MA

Willy, R.W., Manal, K.T., Witvrouw, E.E., Davis, I.S., 2013. Are mechanics different between male and female runners with patellofemoral pain? Med Sci Sport. Exerc. 44,

D

2165–2171. https://doi.org/10.1249/MSS.0b013e3182629215.Are

PT E

Winter, D., 2009. Biomechanics and motor control of human movement, 4st ed. New Jersey. Wyndow, N., Collins, N., Vicenzino, B., Tucker, K., Crossley, K., 2016. Is There a Biomechanical Link Between Patellofemoral Pain and Osteoarthritis? A Narrative

AC

0545-6

CE

Review. Sport. Med. 46, 1797–1808. https://doi.org/https://doi.org/10.1007/s40279-016-

20

ACCEPTED MANUSCRIPT

Figure 1 – Correlation between peak, rate of moment development and impulse of the

MA

NU

SC

RI

PT

external KAbdM with worst pain level in the last month of women with PFP.

AC

CE

PT E

D

Abbreviations: KAbdM – external knee abduction moment; PFP - patellofemoral pain.

21

ACCEPTED MANUSCRIPT

Figure 2 – Correlation between peak, rate of moment development and impulse of the

CE

PT E

D

MA

NU

SC

RI

PT

external KAbdM with PFJ reaction force and PFJ stress of women with PFP.

joint

AC

Abbreviations: KAbdM – external knee abduction moment; PFP - patellofemoral pain; PFJ – patellofemoral

22

ACCEPTED MANUSCRIPT

Table 1. Demographic characteristics of the participants. Pain-free controls

Mean (SD)

Mean (SD)

Age (y)

21.6 (2.9)

21.8 (3.0)

0.88

Height (m)

1.6 (0.5)

1.6 (0.5)

0.71

59.9 (8.8)

60.6 (9.6)

0.74

BMI (kg/m )

22.5 (3.7)

23.4 (3.0)

0.82

Worst pain level in the last month (VAS)

5.2 (2.9)

NA

NA

NA

NA

NA

NA

Body Mass (kg) 2

58.4 (54.1)

Self-reported function (AKPS)

71.3 (12.5)

p-value

SC

RI

Symptoms duration (months)

PT

PFPG

Variable

Abbreviations: PFPG - patellofemoral pain group; SD - standard deviation; BMI – body mass index; VAS -

AC

CE

PT E

D

MA

NU

visual analogue scale (0 - 10 cm); AKPS - anterior knee pain scale (0 – 100); NA - not applicable.

23

ACCEPTED MANUSCRIPT

Table 2. Knee abduction moment parameters, patellofemoral joint reaction force and stress of women with PFP and pain-free controls during stair descent. PFPG

Pain-free controls

Mean Difference

Mean (SD)

Mean (SD)

(95% CI)

0.57 (0.18)

0.47 (0.15)

0.10 (0.17 to 0.09)*

2.41 (1.7)

1.20 (1.1)

Impulse - KAbdM (Nm.kg .s)

30.7 (9.0)

22.6 (7.7)

Patellofemoral joint reaction force (N/Kg)

3.84 (2.1)

2.75 (2.0)

Patellofemoral joint stress (MPa)

12.5 (5.1)

9.2 (3.8)

Variable Peak - KAbdM (Nm.kg-1) -1

Rate of moment development - KAbdM (Nm.kg /s) -1

D E

-1

Effect size (95% CI) -0.5 0 0.5 1

1.5

C S U

N A

M

I R

T P

1.21 (1.84 to 0.45)* 8.1 (12.1 to 4.01)* 1.08 (2.12 to 0.5)*

3.31 (5.50 to 1.11)* Lower in PFP

Higher in PFP

Abbreviations: PFPG - patellofemoral pain group; KAbdM – external knee abduction moment; SD - standard deviation; CI - confidential interval. * Represents significant

T P E

differences between groups (p < 0.05).

C C

A

24

ACCEPTED MANUSCRIPT

Highlights 1. Women with patellofemoral pain present higher knee abduction moment 2. Patellofemoral joint reaction force and stress is elevated in patellofemoral pain

PT

3. Knee abduction moment impulse is associated with patellofemoral pain

AC

CE

PT E

D

MA

NU

SC

RI

4. Knee abduction moment impulse is associated with patellofemoral joint stress

25