Patellofemoral pain presents as diffuse pain of insidious onset in the anterior portion of the knee in approximately 25% of the general U.S. population.1,2 It is characterized by pain with daily activities such as stair ascent and descent, squatting, walking, and running.1 Although not fully understood, one suggested etiology for patellofemoral pain is the increase in patellofemoral joint pressure over time due to abnormal tracking of the patella within the intercondylar groove of the femur.3,4 Abnormal patellar tracking may be attributed by various factors, including structural abnormalities and malalignment5,6 and dynamic malalignment due to neuromuscular and biomechanical alterations.7,8 In addition, abnormal frontal plane hip and knee kinematics9,10 and imbalance in frontal plane muscle strength11 are thought to contribute to patellofemoral joint malalignment during dynamic movement.
Previous studies have found delayed and shorter electromyographic (EMG) activation of gluteal and vasti muscles,12–15 as well as EMG activation imbalances between the medial (hip adductors) and lateral (gluteus medius) hip musculature,16 in participants with patellofemoral pain compared with their healthy counterparts. Altered functions of the hip abductors and adductors should be considered in individuals with patellofemoral pain. Internal hip abduction movement created by the gluteus medius, one of the primary hip abductors, is considered an important contributor for stabilizing the pelvis and lower extremities.17 The hip adductor group also serves as the hip stabilizer and helps control the lower limb alignment because of its role in assisting hip rotation, flexion, and extension.18 Dysfunctions of activity of these muscles may be associated with patellofemoral dynamic malalignment due to increased femoral adduction and lateral pull on the patella, which may further increase patellofemoral joint stress.19
Recent studies have demonstrated that higher levels of pain may be associated with greater neuromuscular alterations in individuals with patellofemoral pain, as depicted by an increased normalized activity and an increased complexity of the vastus lateralis muscle.20 Previous research demonstrated that pain21–25 in different body regions may have varying effects on neuromuscular characteristics. Specifically, these studies suggest that pain can contribute to hyperexcitability and increased muscle activity, possibly to increase muscle stiffness and provide joint stability. Although not related to the patellofemoral region, one study23 demonstrated that increased pain and disability are associated with increased coactivation of neck flexor/extensor muscles in those with neck pain. The relationship between pain and neuromuscular alterations observed from the above studies suggests that individuals may exhibit different levels and characteristics of neuromuscular alterations at varying levels of pain. However, the association between patellofemoral pain and neuromuscular and kinematic alterations must be further investigated, specifically related to the muscles that contribute to frontal plane motions. As stated earlier, patellofemoral pain is proposed to arise from increased patellofemoral joint pressure, possibly due to frontal plane malalignment and neuromuscular imbalance. Stair descent is one of the common activities of daily living that requires a great amount of hip and lower extremity stabilization from various muscles, including hip abductors and adductors, and is known to exacerbate painful symptoms associated with patellofemoral pain.1
This study assessed the association between pain-related measures and lower extremity muscle activation and frontal plane kinematics in those with patellofemoral pain during stair descent. Because previous studies12,15,26,27 found delayed activation onset and shorter duration of the lower extremity muscles (vastus medialis and gluteus medius) during stair descent, we hypothesized that increased pain levels would be associated with delayed activation onset and shorter activation duration of the vastus medialis, adductor longus, and gluteus medius muscles. Also, we hypothesized that increased pain levels would be associated with increased hip adduction and knee abduction. Investigating the association between pain and the extent of biomechanical alterations may help clinicians further understand what biomechanical alterations may be present in association with patellofemoral pain.
Twenty participants with patellofemoral pain (13 women/7 men; mean age = 21.45 ± 3.90 years; height = 169.96 ± 10.47 cm; mass = 71.30 ± 14.50 kg; duration of symptoms = 5.02 ± 3.82 years) volunteered for the study. All participants met the following inclusion criteria adopted from other studies28,29: (1) a previous patellofemoral pain diagnosis by a physician, athletic trainer, or physical therapist; (2) diffuse anterior knee pain for at least 8 weeks; and (3) increased knee pain when ascending and descending stairs and during at least one of the following activities: going up or down hills, after sitting for a prolonged period of time, walking, running, and squatting.
A proportion of the participants (12 of 20) complained of bilateral pain. In this case, the leg with the more painful symptoms was used for data collection. Participants were required to score 85 (of 100) or below on the Kujala Anterior Knee Pain Scale (AKPS). A lower AKPS score would indicate more functional impairments related to pain.30 The average AKPS score from our participants was 72.00 ± 9.57. The AKPS scores and the duration of patellofemoral pain symptoms were also used in statistical analyses. The exclusion criteria included the history of previous major lower extremity injury (other than patellofemoral pain), orthopedic surgery to the lower extremity (including arthroscopy), and participating in lower extremity rehabilitation within 12 months. Participants read and signed a university consent form approved by a biomedical institutional review board.
All testing took place in a motion analysis research laboratory in a single session. Prior to testing, participants warmed up on a stationary bicycle (Monark Ergomedic 828E Exercise Test Cycle; Monark Exercise AB, Vansbro, Sweden) for 5 minutes at a self-selected resistance and speed (50 to 60 RPM). The participant's skin was shaved if necessary, cleaned with alcohol pads, and lightly debrided with sandpaper. A total of 33 retroreflective markers with a diameter of 2.5 cm were applied on the lower extremities with double-sided adhesive tape using the following marker set placements: sacrum, anterior superior iliac spine, posterior superior iliac spine, greater trochanter, anterior thigh cluster consisting of two medial and two lateral markers, lateral femoral condyle, anterior shank cluster consisting of two medial and two lateral markers, lateral malleolus, heel at the posterior calcaneal tuberosity, fifth metatarsal head, and first metatarsal head.31 Markers at the medial malleolus and medial femoral condyle were placed during a static trial. Pairs of disposable 0.8-cm diameter Ag/AgCl surface electrodes with a center-to-center inter-electrode distance of 1.5 cm (Noraxon U.S.A., Inc., Scottsdale, AZ) were placed for surface electromyography (EMG) recording over the gluteus medius at the halfway distance between the highest part of the iliac crest and the greater trochanter,32,33 adductor longus at the distal one-third of the distance between the pubis symphysis and adductor's tubercle, on the anterior medial thigh,32 and vastus medialis oblique at 4 cm proximal to the superior medial angle of the patella at 55° relative to the imaginary line of the femur32,34 of the affected limb. An 8-channel telemetered surface EMG system (Telemyo; Noraxon U.S.A., Inc.) was used for data collection, with amplification gain of 1,000, baseline noise of greater than 1 microvolt, input impedance of greater than 100 Ohms, and a common-mode rejection ratio of greater than 100 dB.
The baseline EMG measures of the gluteus medius, adductor longus, and vastus medialis oblique were collected during the 5-second double-limb quiet standing. The participant performed five stair descent trials at a self-selected pace.12 The second step of the custom-made four-step staircase (rise of 17 cm and run of 25 cm) contained a solid box that was custom constructed to fit on the force plate (AMTI OR6-5; Advanced Motion Technology, Inc., Watertown, MA) to identify the beginning and end of the stance phase of the step. Specifically, the beginning (initial contact) and end (toe off) of the stance phase were determined if the force exerted on the force plate was above or below 10 N, respectively. The data were collected at or around the second step of each stair descent trial, and were averaged across trials. To minimize fatigue, up to 1 minute of rest was given between trials. At the completion of all stair descent trials, the participant was asked to rate the worst pain experienced during the descent on the 10-cm visual analog scale, with higher scores indicating more pain. Knee and hip frontal plane kinematic data were collected using the three-dimensional motion analysis system (Twelve Eagle digital cameras; Motion Analysis Corporation, Santa Rosa, CA) and Cortex software (Motion Analysis Corporation) at 100 Hz. All EMG data and force plate data were collected with a sampling frequency of 1,000 Hz using Cortex software integrated with the three-dimensional motion capture system.
All data were processed using Visual 3D Basic/RT (C-Motion, Inc., Germantown, MD) and smoothed with the Butterworth filter using a 10-Hz cut-off frequency. The mean knee abduction (the frontal plane motion of the shank relative to the thigh) and mean hip abduction (the frontal plane motion of the thigh relative to the pelvis) at the first 30% of the stance phase were obtained.
The EMG signals for quiet standing and stair ambulation trials were full-wave rectified, band-pass filtered between 20 and 500 Hz,35 and processed using the root mean square calculation over a 55-msec window.26 Activation onset (milliseconds) for the gluteus medius and adductor longus during the stair ambulation trials was defined as the time when the EMG amplitude exceeded 3 standard deviations (SDs) of baseline for each participant for a minimum of 25 msec, relative to the initial foot contact.12,35,36 A positive value in the activation onset indicated the EMG activation onset occurred after foot contact (delayed), whereas a negative value indicated the EMG activation onset occurred before foot contact (early). Activation duration (milliseconds) for the gluteus medius and adductor longus were defined as the time between the activation onset and when the EMG amplitude fell below 3 SDs of baseline for a minimum of 25 msec. The threshold for the vastus medialis oblique activation onset and duration was set as 10% of the mean peak amplitude across the descending trials for each participant. A previous study37 used two thresholds for identifying activation onset of a single muscle due to erratic onset timings with one method. Therefore, we determined that using a different threshold value for the vastus medialis oblique would be acceptable.
Pearson product-moment correlation coefficients (r) were calculated to assess the association between pain-related measures (visual analog scale scores, AKPS scores, and duration of symptoms) and muscle activation/duration and knee/hip kinematics during stair descent. Normality of data was tested using the Shapiro–Wilk test. The results of the Shapiro–Wilk test indicated that the data for the adductor longus activation onset and adductor longus duration were not normally distributed. Therefore, the association between pain-related measures and these two variables (adductor longus activation onset and duration) was tested using Spearman's rho (ρ). Also, data were further assessed for outliers using stem and leaf plots. We considered any data points greater than 2.5 SDs to be statistical outliers, and the outliers were removed from the data set for further analyses. This occurred for the adductor longus activation onset and duration, which contained one outlier. The strength of association was determined from positive or negative correlation values and interpreted as: very weak (< 0.25), weak (0.25 to 0.5), moderate (0.5 to 0.75), and strong (> 0.75).38 IBM SPSS Statistics software (version 21.0; IBM Corporation, Armonk, NY) was used for data analysis. The alpha level was set a priori at a P value of less than .05.
The graphs with descriptive data (mean ± SD) for EMG activation onset and duration of the vastus medialis oblique, adductor longus, and gluteus medius are presented in Figures 1–2. The mean hip and knee frontal plane angles during the first 30% of the stance phase were 3.53° ± 3.90° for hip abduction and 1.55° ± 3.94° for knee abduction. Average maximum pain (visual analog scale) experienced during the task was 2.2 ± 1.8 cm. As previously stated, the average duration of patellofemoral pain symptoms was 5.02 ± 3.82 years, and the average AKPS score was 72.00 ± 9.57. The results of the Pearson product-moment correlation and Spearman's rho analyses are presented in Table 1. There was a moderate negative association between visual analog scale pain and vastus medialis oblique activation (r = −0.611; P = .007; Figure 3). There was also a weak negative association between visual analog scale pain and adductor longus activation (ρ = −0.490; P = .028; Figure 3). Visual analog scale pain was weakly associated with less knee abduction (r = −0.488; P = .029; Figure 4). Furthermore, a higher AKPS score (indicating fewer functional deficits related to pain) was associated with a later onset of adductor longus activation (ρ = 0.495; P = .027; Figure 5). There was no significant association between the duration of the patellofemoral pain symptoms and any neuromuscular or kinematic characteristics.
Lower extremity muscle onset during stair descent.
Lower extremity muscle activation duration during stair descent.
Association Between Pain-related Measures and Neuromuscular and Kinematic Variables
Scatterplots of statistically significant associations between visual analog scale (VAS) pain and neuromuscular functions. (A) Moderate negative association (r = −0.611) between pain and vastus medialis oblique (VMO) activation. (B) Weak negative association (ρ = −0.490) between pain and adductor longus (AL) activation.
Scatterplot of the significant association between visual analog scale (VAS) pain and knee abduction angle. Weak negative association (r = −0.488) between VAS and knee abduction during the stance phase.
Scatterplots of statistically significant associations between Anterior Knee Pain Scale (AKPS) and adductor longus (AL) activation. Weak positive association (ρ = 0.495) between AKPS and AL onset.
The current study is one of the few to assess the association between pain-related measures and lower extremity muscle activation in individuals with patellofemoral pain, and the first study to date that has assessed the association between pain and frontal plane muscles (gluteus medius and adductor longus). We initially expected that the adductor longus would behave like other muscles, with shorter and delayed activation associated with more patient-reported knee pain. Although the strength of the associations was low to moderate, our results supported our hypothesis and demonstrated the relationship between pain and muscle activations. However, the directions of association were unexpected because the results yielded that pain was correlated with an earlier vastus medialis oblique activation onset, earlier adductor longus activation onset, and less knee abduction during stair descent. Other studies have demonstrated that the adductor longus has an earlier onset16 and adductor group strength is higher11 in those with patellofemoral pain compared to healthy, pain-free individuals. The results regarding the vastus medialis oblique activation were also unexpected because previous studies reported delayed vastus medialis oblique activation onset during stair descent in those with patellofemoral pain.12,16,27,39 Additionally, earlier activation of the vastus medialis oblique and adductor longus in association with pain also was observed concurrently with less knee abduction. A comparable study16 that included all three muscles (vastus medialis oblique, adductor longus, and gluteus medius) demonstrated that healthy individuals with no pain demonstrated with earlier adductor longus and gluteus medius activation onset and longer activation duration of the vastus medialis oblique and gluteus medius compared to the individuals with patellofemoral pain. Therefore, it is interesting that the participants in our study demonstrated the association between pain and earlier activation of the vastus medialis oblique and adductor longus.
Although our results seem to contradict the previous studies investigating the effects of patellofemoral pain on neuromuscular and kinematic changes, they indicate that individuals with patellofemoral pain are using a compensatory strategy during the stair descending task, possibly in an attempt to control the patellofemoral joint loading. Our kinematics results indicate that although the frontal plane hip motion seems to be unrelated to different levels of pain, those with more pain seemed to demonstrate protective compensation of less knee abduction, possibly in an attempt to avoid valgus collapse during weight bearing.
Our EMG results could also explain a possible compensatory strategy exercised by individuals with patellofemoral pain. Although it may be natural to expect diminished neuromuscular control due to pain,40–42 those with chronic pain such as patellofemoral pain may have lower vastus medialis oblique and vastus lateralis activity but higher excitability of these muscles, suggesting that chronic knee pain may alter the excitability of corticomotor pathways.24 The only other study that investigated the relationship between patellofemoral pain and neuromuscular control found that higher pain levels were associated with more complex neuromuscular control of the vastus lateralis but not the vastus medialis.20 We speculate that those with pain may demonstrate a protective neuromuscular strategy by activating some key muscles (presumably the vastus medialis oblique and adductor longus in our case) and “bracing” the legs to provide further stability at foot contact during the stair descending maneuver.
Gutierrez et al.43 discussed the possibility of anticipatory muscle activation for increasing ankle stability, consistent with other studies that have observed increased muscle activation and/or excitability in those with chronic pain.21–23,44 These studies suggest that the heightened muscle activation may be a protective strategy in an attempt to increase stability of the joints. Although the protective patterns of early muscle activation, as observed in our study, can be a beneficial strategy for enhancing joint stiffness and stability in the short term, they may not provide beneficial kinematic changes for improving function, which may become detrimental in the long term.44 Increased adductor activity and strength may be attributed to further neuromuscular and kinematic imbalance, functional deficits, and pain in the patellofemoral pain population.11 However, our study cannot establish cause and effect. In other words, we cannot state whether pain leads to earlier and longer activation of some muscles and reduced knee adduction or whether the aforementioned neuromuscular and kinematic alterations have led to pain. Because this is the first study that we are aware of examining the association between pain and hip muscle activation, additional research, especially longitudinal studies, is warranted to fully establish the relationship between the presence of pain and neuromuscular alterations. Future studies that evaluate kinetics such as joint stress and stiffness may also be helpful in determining the threshold of muscle activation onset and duration that are deemed safe and beneficial for achieving optimal joint stability.
Interestingly, we did not observe a significant association between pain and gluteus medius activation in contrast to previous results that found delayed and shorter gluteus medius activation in the population with patellofemoral pain.12,13 Perhaps the different levels of pain may not affect the activation onset and timing of the lateral hip muscle (eg, gluteus medius) activation levels, but may more noticeably affect the activation onset and timing of the medial knee/hip muscles such as the vastus medialis oblique and adductor longus. Also, we did not observe a significant association between the duration of pain and neuromuscular characteristics. Because all of the participants were considered to be currently experiencing chronic pain (longer than 2 months), overall severity of pain may play a larger role in altered neuromuscular function in this population.
We should caution that the participants with patellofemoral pain in our study experienced minimum to mild levels of pain on the leg with patellofemoral pain (mean ± SD = 2.2 ± 1.8 cm) during the task. Although we included the exacerbation of pain during stair ambulation and lower AKPS score in the inclusion criteria, it is possible that stair descent may not be the most painful activity for individuals with patellofemoral pain. The baseline level of pain was 1.2 ± 1.3 cm and therefore the increase of 1 cm in the “worst” pain during the stair descent was not minimally clinically important.45,46 A higher level of pain may enhance the strength of the associations, and therefore future studies should consider only including those who experience more pain during the specific activities. Also, we observed that our participants complained of increased pain during or after a prolonged activity. Because the study involved repetitive stair ambulation for a total of 10 trials on the four-step staircase, participants may not have developed a significant amount of pain during the data collection period. Other studies with low intensity and low pain-provoking activities seem to demonstrate no to minimum neuromuscular and kinematic changes.47–49 There is evidence that more pronounced biomechanical and strength deficits occur during a prolonged activity50 or a more intense or demanding task,51,52 so it may be of interest in the future to investigate associations between pain and neuromuscular and kinematics alterations at the beginning and the end of a longer-duration stair ambulation exercise, or during a more physically demanding task.
The overall weakness of association is another limitation. Although we observed that pain-related measures were associated with some biomechanical characteristics, these associations were weak to moderate. Large standard deviations may be attributed to this limitation, which may result from individual variations in neuromuscular adaptation to pain. Muscle activation onset and duration, as well as frontal plane joint angles, tend to display more inter-subject variability, and a larger sample size in future studies may further enhance the strength of association. Also, it is a consistent challenge to determine the best EMG processing procedure because published studies use different equipment, sampling rate, and processing and normalization techniques. Of particular note, the need for normalizing the time domain during a part of a task that consists of a short time period has been debated. We were interested in each participant's natural muscle activation patterns at a self-selected pace, and therefore decided not to normalize the time domain of the EMG activity for determining the onset timing and activation duration. It is possible that our decision may have contributed to the limitation of large standard deviations. Overall, however, we used what we determined to be the most appropriate procedure for representing each muscle's activation pattern.
Implications for Clinical Practice
The overall low level of pain with the specific task (stair descent) may warrant caution on clinical applications. However, our study demonstrated that an increase in pain during stair descent was weakly and moderately associated with altered neuromuscular and kinematic functions that may provide additional protection and stability to the lower extremity. Although the observed association between pain and neuromuscular and kinematic functions could be the result of a compensatory mechanism to successfully execute the task and protect the lower extremity, it is unknown whether the compensation is beneficial or detrimental to individuals with patellofemoral pain in the long term.
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Association Between Pain-related Measures and Neuromuscular and Kinematic Variables
|Measure||Mean ± SD||VAS Pain Score (2.2 ± 1.8 cm)||AKPS (72.00 ± 9.57)||Duration of Symptoms (5.02 ± 3.82 years)|
|r (or ρ)||P||r (or ρ)||P||r (or ρ)||P|
|VMO onset||−34.76 ± 126.15 msec||−0.611||.007a||0.388||.091||−0.080||.739|
|VMO duration||754.91 ± 319.34 msec||0.337||.172||0.059||.806||0.132||.578|
|AL onsetb||22.85 ± 58.69 msec||−0.49||.028a||0.495||.027a||−0.238||.312|
|AL durationb||422.69 ± 274.89 msec||0.219||.355||−0.072||.764||0.210||.373|
|GMed onset||38.38 ± 49.05 msec||−0.218||.355||0.265||.259||−0.086||.719|
|GMed duration||274.43 ± 115.00 msec||0.219||.354||0.080||.738||0.036||.880|
|Hip abduction angle||3.53° ± 3.90°||0.137||.565||−0.208||.379||−0.196||.407|
|Knee abduction angle||1.55° ± 3.94°||−0.488||.029a||0.244||.300||0.280||.232|