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Kinematic and electromyographic analysis in patients with patellofemoral pain syndrome during single leg triple hop test
Gait & Posture 49 (2016) 246–251
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Kinematic and electromyographic analysis in patients with patellofemoral pain syndrome during single leg triple hop test Marcelo Martins Kalytczak, Paulo Roberto Garcia Lucareli, Amir Curcio dos Reis, André Serra Bley, Daniela Aparecida Biasotto-Gonzalez, João Carlos Ferrari Correa, Fabiano Politti* Department of Rehabilitation Science, Human Motion Analysis Laboratory, Universidade Nove de Julho, São Paulo, Brazil
A R T I C L E I N F O
Article history: Received 9 February 2016 Received in revised form 16 June 2016 Accepted 18 July 2016 Keywords: Patellofemoral pain syndrome Electromyography Hop test Kinematics
A B S T R A C T
Possible delays in pre-activation or deficiencies in the activity of the dynamic muscle stabilizers of the knee and hip joints are the most common causes of the patellofemoral pain syndrome (PFPS). The aim of the study was to compare kinematic variables and electromyographic activity of the vastus lateralis, biceps femoris, gluteus maximus and gluteus medius muscles between patients with PFPS and health subjects during the single leg triple hop test (SLTHT). This study included 14 female with PFPS (PFPS group) and 14 female healthy with no history of knee pain (Healthy group). Kinematic and EMG data ware collected through participants performed a single session of the SLTHT. The PFPS group exhibited a significant increase (p < 0.05) in the EMG activity of the biceps femoris and vastus lateralis muscles, when compared with the healthy group in pre-activity and during the stance phase. This same result was also found for the vastus lateralis muscle (p < 0.05) when analyzing the EMG activity during the eccentric phase of the stance phase. In kinematic analysis, no significant differences were found between the groups. These results indicate that biceps femoris and vastus lateralis muscles mainly during the preactivation phase and stance phases of the SLTHT are more active in PFPS group among healthy group. ã 2016 Elsevier B.V. All rights reserved.
1. Introduction Patellofemoral pain syndrome (PFPS) is a common disorder of the knee joint complex. It is mainly characterized by retro or peripatellar pain [1] and an absence of any other type of associated injury (e.g. chondromalacia, cartilage fissures, osteoarthritis or arthritis). The clinical issue can worsen in the following situations: climbing and descending stairs; performing squats; jumping; remaining seated for a long time or palpating the lateral facet of the patella [2,3]. PFPS is the most common knee injury among active women [4] aged between 18 and 35 years, regardless of whether they are athletes or not. It is more common among women than among men [5–7]. Although the cause of PFPS is multi-factorial,
* Corresponding author at: Rua Vergueiro, 2355 – Liberdade, São Paulo 01504-001, SP, Brazil. E-mail addresses: [email protected] (M.M. Kalytczak), [email protected] (P.R.G. Lucareli), acrfi[email protected] (A.C. dos Reis), [email protected] (A.S. Bley), [email protected] (D.A. Biasotto-Gonzalez), [email protected] (J.C.F. Correa), [email protected] (F. Politti). http://dx.doi.org/10.1016/j.gaitpost.2016.07.020 0966-6362/ã 2016 Elsevier B.V. All rights reserved.
biomechanical abnormalities are considered to play a role in the worsening of this joint disorder. Kinematic abnormalities of the lower limbs, known as medial collapse, is one of the most common of the abovementioned biomechanical factors [8]. This condition is characterized by internal rotation and excessive adduction of the femur, contralateral pelvic drop and knee abduction, which can lead to poor alignment and diminish the congruence between the patella and the femoral trochlea, reducing the area of contact through lateral patellar displacement and increasing patellofemoral pressure [9– 12]. Possible delays in pre-activation or deficiencies in the activity of the dynamic muscle stabilizers of the knee and hip joints are the most common causes of PFPS [13–16]. Delays in muscle activation, differences in the time of activation and different gluteus medius (GMed) muscle activity have been previously proven during the ascent and descent of stairs [13], weight bearing tasks [16] and running tests [15], based on comparisons of healthy women and women with PFPS. However, these results have not been confirmed in studies with similar tasks [17–20]. Controversial results have also been found in relation to the activity of the gluteus maximus (GM) muscle in both healthy
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individuals and those with PFPS while running and descending steps [15,17,20]. When comparing healthy individuals to those with PFPS, greater activity of the patella stabilizer muscles (vastus medialis oblique – VMO and vastus lateralis muscles – VL) was only observed among healthy individuals during tests that involved descending steps [21]. No differences were recorded for the same tests in a similar study [13] and during sprint [20]. However, evidence suggests that abnormal neuromuscular control of the VMO and VL muscles, as well as the reduced strength of the quadriceps, are likely contributors to the development of PFPS [22]. Previous studies have suggested a possible impaired VMO function in cases of PFPS, based on assessments of the EMG signal magnitude [23,24]. However, this finding has not been consistent across all studies [13,20]. Although a greater VMO ratio has previously been linked with PFPS [23,24], abnormal neuromuscular control of the VL muscle was significantly correlated with the Knee Injury and Outcome Score (pain subscale) and the EMG activity of the VL muscle in adolescent female PFPS patients while descending stairs [25]. These results suggest that the neuromuscular control of the VL muscle requires further investigations. Therefore, the influence of the neuromuscular control of hip and knee stabilizers in the genesis and worsening of PFPS remains inconclusive, since these results could be associated with the type of tasks performed during the tests. Very few studies [18,19,26,27] have investigated the biomechanical behavior of lower limbs during tasks of high-intensity, such as the single leg vertical jump, the drop landing task and the unilateral squat. However, no studies have been found addressing the activity of the stabilizer muscles of the hip and knee during the single leg triple hop test (SLTHT). The SLTHT involves the performance of three consecutive unipodal forward jumps. The aim of the test is to achieve the greatest possible distance. It is used to assess the functional performance of lower limbs based on the total of the three jumps, neuromuscular coordination and joint stability [28]. It also enables comparisons between the distances reached when using asymptomatic and symptomatic lower limbs [28–30]. This test can be used to: assess the therapeutic treatment of lower limbs [31]; detect asymmetry or muscle weaknesses in healthy individuals [32,33]; assess the dynamic stabilization of the knee joint [34]; or analyze the strength, power and balance of the lower limbs of patients and athletes [28,29,31,35–37]. The functional phases of the SLTHT place different demands on the knee joint. One of these phases is the preparation phase [38], which is considered a relatively low-impact activity. Another phase is known as the landing phase, which is characterized as a highimpact activity [39]. The speed and intensity of the movements requested in the execution of the SLTHT can generate increased muscle activity, as is the case with sprints of different intensities [40,41], in relation to tasks of less intensity, such as climbing and descending stairs, walking and the step down test. Thus, the SLTHT can involve a significant neuromuscular demand, which can increase the possible differences in the intensity of muscle contractions among individuals with and without PFPS. These differences can be analyzed using surface electromyography (EMG). The intensity of the EMG signal provides a reliable estimate of the volume of the recruited muscle [42]. Hence, the hypothesis of this study was that the speed and intensity of the movements requested in the execution of the SLTHT could also clarify possible differences between the muscle activity of healthy individuals and those with PFPS. The aim of the study was to compare kinematic variables and electromyographic activity of the vastus lateralis, biceps femoris, gluteus maximus and gluteus medius muscles between patients
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with PFPS and health subjects during the single leg triple hop test (SLTHT). 2. Methods 2.1. Subjects This study included 14 individuals with PFPS (PFPS group) and 14 healthy individuals (Healthy group) recruited from the surrounding community and the university by an experienced physiotherapist [6]. The present study was approved by the local Human Research Ethics Committee (CAAE: 02290412.0.0000.5511). The Numerical Rating Scale for Pain (NRS) and the Anterior Knee Pain Scale (AKPS) were used as the diagnostic criteria of PFPS. The NRS is an 11-point scale, ranging from 0 (absence of pain) to 10 (worst possible pain), which has been previously used to assess the pain intensity of PFPS subjects [43]. The AKPS is a self-report questionnaire consisting of 13 questions for which items are differentially weighted for a maximum score of 100, with higher scores indicating better function. This scale has previously been used to assess the severity of pain and disability [44]. The PFPS group contained individuals aged 18–35 years [26] with at least three months of retropatellar pain and a score of between 3 and 6 points on the NRS in the previous three months. These individuals also exhibited a clear increase in symptoms during at least two of the following activities [45]: climbing and descending stairs; squatting; jumping; remaining seated for a long time; maximal isometric voluntary contraction (MIVC) of the quadriceps at 60 of knee flexion; or pain on palpation of the lateral facet of the patella. The inclusion criteria for the healthy group were as follows: physically active women in the same age range as the PFPS group, with no history of knee pain (Table 1). Women with any of the following were excluded from the present study: any neurological disorder; pain in the lower back, sacrum, hip or ankle; a history of surgical procedures on the lower limbs, or other associated pathologies, such as patellofemoral luxation or subluxation; absence of clinical signs of patellar tendinitis and ligament injuries of knee; discrepancies of more than 1 cm in the length of lower limbs (distance between the anterior superior iliac spine and the medial malleolus). Pregnant women and former practitioners of a high performance sport (e.g. practitioners volleyball, basketball, running) were also excluded. 2.2. Instruments The EMG signal was digitalized by a 16-bit A/D converter and synchronized with the kinematic data. A 4-channel telemeterized surface EMG system (FREE EMG, BTS, Italy) recorded muscle activity at 1 kHz per channel. This activity was detected using bipolar surface circular electrodes (Ag/AgCl, Medical Trace1) with 10 mm diameter, center-to-center inter-electrode distance of 2 cm, connected to a portable amplifier with a common-mode rejection
Table 1 Demographics data.
Age (years) Heigth (m) Body mass (Kg) BMI (Kg/m2) Pain score (NRS) AKPS (score)
Health group
PFPS group
P-Value
23.14 3.35 1.62 0.06 55.93 7.15 21.33 2.71 0 99.50 1.29
23.50 2.02 1.66 0.05 56.00 5.23 20.47 1.98 5.05 1.63 80.43 4.78
0.73 0.09 0.97 0.34 – <0.001*
BMI: Body mass index. NRS: numerical rate scale of pain. AKPS: anterior knee pain scale. PFPS: patellofemoral pain syndrome. * Statistically significant difference (p < 0.05: Independent t test).
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ratio >100 dB, an output impedance exceeding 10 MV, a cutoff frequency of 20–500 Hz and a gain of 1000. The surface electrodes were positioned based on the mid-point between the following: the sacrum and the greater trochanter for the muscle GM muscle; the iliac crest and the greater trochanter for the GMed muscle; the head of the fibula and the ischial tuberosity for the biceps femoris muscle (BF). For the VL muscle, the lower third between the base of the patella and the anterosuperior iliac spine was considered [36]. An infrared camera passive marker system (SMART-D BTS1, Milan Italy) recorded the participant’s trunk and lower limb movements, with sampling at 100 Hz. Twenty-five spherical markers were attached to the skin with double-faced adhesive tape, based on the Vicon Plug-in Gait biomechanical model [46,47] (Fig. 1).
counterbalanced to avoid any potential bias. The figure with this information can be found in Supplementary data. After these procedures, the participants were familiarized with the SLTHT, which consists of three consecutive one-leg hops, the aim of which is to reach the maximum possible distance [48]. The reflective markers were fixed in the previously described locations. All of the participants wore shorts and tops and performed the test barefoot in order to prevent different models of sneakers, as well as the different materials used to make them, from distorting the results. For the SLTHT, the volunteers were positioned in the collection area and the helped to perform the test from a one-leg static standing position. The SLTHT was repeated 3 times, with a one-minute rest period between tests. 2.4. Processing
2.3. Procedure The participants performed a single session of the test. The first procedures adopted involved the collection of anthropometric data, as well as the NRS and AKPS scores. The affected limb (or most affected limb) was tested in the PFPS group. The dominant limb of the participants in the healthy group was analyzed. Prior to the kinematic and EMG data collection, a warm-up exercise was performed on a treadmill for 10 min at 1.5 m/s. After an interval of one minute, disposable electrodes were attached for the collection of the EMG signal. Each individual initially performed three MIVC for each muscle during 5-s, with two-minute intervals between the collections. The first and last second of the EMG signal recorded were disregarded (total 3-s) and the highest value observed among the three contractions was used to normalize the data obtained during the jumps. The following tests were used to obtain the MVIC of each muscle against a fixed resistance offered by a non- elastic strap directly attached to the test table at the following positions: GM) patient in the prone position, with the lower limb to be tested at 90 knee flexion, resistance on the distal region of the thigh and the pelvis in a stabilized position; GMed) patient lying on her side, the knee was extended and the hip was placed in slight extension and abduction, with resistance on the shin distal region; BF) the hip was positioned in slight lateral rotation and the knee was flexed at 60 , with resistance on the distal region of the shin; VL) patient in sitting position with the knee flexed at 60 and resistance on the shin distal region. Verbal encouragement was given during all MVIC’s. The order of the MVIC’s was
The present study only considered the EMG activity of the GM, GMed, BF and VL muscles during the stance phase of the second jump in the SLTHT. The first jump of the SLTHT was disregarded due to the difficulty of standardization in relation to the preparation phase that proceeds the propulsion of the test (joint angle, position of the trunk and head). The third jump of the SLTHT was shown to be less motivating for many individuals and thus, the results of this phase could have provided less reliable results than the second phase. Therefore, the stance phase used in the analysis was defined as the first and last contact of the foot during the landing and takeoff of the sole, respectively (Fig. 2). The peak knee and hip flexion values were obtained from the kinematic data recorded during the stance phase of the second jump in the SLTHT. The coordinates of the kinematic data were then smoothed with a Woltring filtering routine, using a 10 Hz cut-off frequency (Vicon Nexus software). All raw EMG data recorded during the MIVC and SLTHT were linear enveloped by rectifying and low-pass filtering (4th order Butterworth, 10 Hz cut-off). The amplitude (intensity) of the EMG signal (iEMG) for each muscle was estimated by calculating the area below the curve, using trapezoidal integration. For the normalization of the EMG signal, the iEMG recorded during the SLTHT was expressed as the percentage of the MIVC (%MIVC). Previous studies have shown that during jumping, the medial gastrocnemius, rectos femoris and vastus lateralis muscles are activated approximately 100 m/s before landing [49,50]. Thus, the iEMG was calculated during the 100 m/s before the initial foot contact, labeled “pre-activity” (PRE-iEMG), and during the stance phase (STP-iEMG). The peak knee flexion (kinematic values) was used to divide the stance phase in order to calculate the iEMG of the eccentric (EXC-iEMG) and concentric phases (CON-iEMG) (Fig. 2). EMG signals were processed by performing specific routines with Matlab software (MathWorks Inc., Natick, Massachusetts, USA). 2.5. Statistical analysis The Shapiro–Wilk test was used to determine the distribution of the data. The independent t-test or the Mann-Whitney test were used for intergroup comparisons. The level of significance was set at 5% (p < 0.05). All data were analyzed using the Statistical Package for Social Sciences (SPSS), version 20.0. 3. Results
Fig. 1. Kinematic marker locations. CLAV: over the manubrium; STR: xiphoid process; RBACK: right scapula; RSHO and Professionanterosuperior iliac spines; RPSI and LPSI: posterosuperior iliac spine; RTHI1 and LTHI1: side of thigh; RTHI and LTHI: lateral face of the base of the patella; RKNE and LKNE: lateral femoral epicondyle; RTIB and LTIB: side of shin; RANK and LANK: lateral malleolus; RTOE and LTOE: middle third of the foot between the 2nd and 3rd metatarsals; RHEE and LHEE: calcaneus.
The anthropometric data (age, stature, body mass and BMI) were similar in the healthy volunteers and those with PFPS (p > 0.05). Differences between the groups related to clinical characteristics were recorded on the same day of the tests before the SLTHT using the Numerical Rating Scale for Pain (NRS) and the Anterior Knee Pain Scale (AKPS) (Table 1). The values recorded for
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Fig. 2. Time course during single leg triple hop test. STP: Stance phase. Foot strikes the ground; Foot leaves the ground; Peak knee flexion; STP: stance phase.
the variables PRE-iEMG, STP-iEMG, EXC-iEMG, CON-iEMG of the GM, GMed, BF and VL muscles were expressed as %MIVC. The peak knee flexion and peak hip flexion variables were displayed in degrees (Table 2).
Table 2 Muscle activation data (EMG). Health group
PFPS group
P-Value
Gluteus maximus muscle PRE-iEMG (%MIVC) STP-iEMG (%MIVC) EXC-iEMG (%MIVC) CON-iEMG (%MIVC)
2.33 1.23 12.81 8.65 8.56 4.41 5.10 4.82
2.35 0.89 12.59 5.16 8.81 4.36 5.51 4.20
0.96 0.69 0.92 0.50
3.2. Kinematic data
Gluteus medius muscle PRE-iEMG (%MIVC) STP-iEMG (%MIVC) EXC-iEMG (%MIVC) CON-iEMG (%MIVC)
2.49 1.40 10.99 5.27 7.39 3.24 4.86 2.74
2.29 1.10 11.69 5.27 8.26 4.00 5.54 3.13
0.62 0.72 0.52 0.54
The peak knee and hip flexion values obtained from the kinematic analysis, as well as the combination of flexion angles of these joints, were compared between the groups, with no significant differences recorded (p > 0.05) (Table 3).
Biceps femoris muscle PRE-iEMG (%MIVC) STP-iEMG (%MIVC) EXC-iEMG (%MIVC) CON-iEMG (%MIVC)
2.17 1.23 6.96 2.53 4.48 2.51 2.90 1.35
2.90 1.46 10.34 5.01 6.48 3.17 3.67 2.88
0.04* 0.04* 0.07 0.37
4. Discussion
Vastus lateralis muscle PRE-iEMG (%MIVC) STP-iEMG (%MIVC) EXC-iEMG (%MIVC) CON-iEMG (%MIVC)
2.75 1.89 13.40 5.75 9.82 5.65 7.10 5.44
3.61 1.20 18.52 7.01 13.54 4.66 8.07 5.59
0.02* 0.04* 0.04* 0.53
3.1. Muscle activation data (EMG) Table 2 displays the results of the EMG data. For PRE-iEMG and STP-iEMG, the PFPS group exhibited a significant increase (p < 0.05) in the EMG signal of the BF and VL muscles, when compared with the healthy group. This same result was also found for the VL muscle (p < 0.05) when analyzing the EMG activity during the eccentric phase (EXC-iEMG) of the stance phase.
The initial hypothesis was that the SLTHT would highlight any possible abnormalities in muscle activity among individuals with PFPS, when compared to healthy individuals. This hypothesis was partially confirmed by the results of the present study. Only the muscles involved in the movement of the knee (BF and VL) exhibited elevated activity compared to the healthy control subjects. The activity of the muscles that are associated with the hip (GM and GMed) was similar in both groups.
Abbreviations: PFPS, patellofemoral pain syndrome; PRE-iEMG, pre-activation; STPiEMG, stance phase; EXC-iEMG, eccentric phase; CON-iEMG, concentric phase; MIVC, maximal isometric voluntary contraction. Integral signal (iEMG) of each muscle. EMGs normalized utilizing the maximally voluntary contraction (%MVC). * Statistically significant difference (p < 0.05: Independent t test and MannWhitney test, used for parametric and non-parametric data, respectively).
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Table 3 Mean and standard deviation (SD) of the kinematics data.
Peak hip flexion (degrees) Peak knee flexion (degrees) Peak hip/knee flexion (degrees)
Health group
PFPS group
P-Value
63.84 11.84 54.91 7.65 118.75 15.86
58.35 7.70 51.22 6.49 109.57 12.53
0.16 0.18 0.10
Independent t test were used for intergroup comparisons.
These results add further information in the discussion of the possibility that PFPS is caused by a deficiency in the control of hip muscles during isometric and dynamic activities, as described in previous studies [8,51,52]. Previous studies have reported significant differences between healthy individuals and those with PFPS, in terms of activity patterns (beginning and duration of activation) of the GMed muscle while climbing and descending stairs [13,14,16] and running [15]. However, when the same muscle was assessed during activities that demand a greater muscular effort, such as the single leg vertical jump [18] and the drop jump [17], no differences were found between the groups. This same observation can also be applied to the GM muscle. During the performance of tasks such as the step down test and sprinting, the activity of the GM muscle was greater among individuals with PFPS. No differences were noted in the drop jump tests [17]. The differences found in the two groups analyzed for the BF and VL muscles indicate that there could be an association between the activity of the muscles involved in the articulation of the knee and PFPS during activities of high intensity, such as the SLTHT. In the present study, the significant increase in the pre-activation and activity of the BF and VL muscles found among women with PFPS may have been caused by a compensation or protection mechanism associated with the pain felt by individuals with this disorder. In general, these muscles help to control the lower limb and the dynamic stabilization of the knee prior to an event of high intensity [53]. Therefore, the greater activity of these muscles could be associated with the need for a greater stability and protection of the joint, due to the impact that occurs during the SLTHT. The activity of the BF muscle during the STP-iEMG also increased in the PFPS group when compared with the healthy group. This difference has previously been demonstrated among cyclists with PFPS [54], who exhibited a greater activation of the hamstrings (BF and semitendinosus) than cyclists without pain. This increase in activity may have generated an increase in the load imposed by the muscle on the joint, thereby contributing to the poor patellar alignment and consequent increase in joint pressure [55]. The greater activation of the VL muscle in the STP-iEMG and EXC-iEMG in the PFPS group could be associated with the decreased angle of hip and knee flexion, when compared with the healthy women. Although this difference was not significant in the present study, this association has previously been demonstrated during the execution of the drop landing task [26,27]. A number of previous studies have reported that the greater EMG activity found in the hip and/or knee extensor muscles of individuals with PFPS could reflect a weakness in these muscles [17,56,57] described the higher VMO (vastus medialis obliquus) and VL amplitudes observed in individuals with PFPS (from patella instability) while walking and climbing/descending stairs, as well as greater GMed and VMO EMG activity during the loading response and single leg stance intervals while descending stairs [57]. Abnormal GMed muscle activity in patients with PFPS has also been described during demanding activities (e.g. running, drop landings and a step-down maneuver) [17]. One explanation for these results is that weaker muscles may reflect the need for increased neuromuscular activity to complete the task. This idea is
strengthened by the decreased amplitude of the EMG signals in the VMO and VL muscles of PFPS patients after exercise therapy [58]. Based on these findings, it is possible that the increased EMG activity of the VL (in the STP-iEMG and EXC-iEMG) and BF (in the STPiEMG) muscles were due to possible weaknesses in these muscles. In the present study, it was possible to confirm that during activities of high intensity, such as the SLTHT, the muscles that act directly on the knee (BF and VL) are more active among individuals with PFPS. These results, although insufficient to form a therapeutic approach, indicate that the muscles responsible for the movement and stabilization of the knee should not be neglected during the assessment and treatment of PFPS patients. The analysis of only four muscles, due to the specifics of the electromyography used, was a limitation of the present study. It is suggested that further studies should also record the activity of the medial vastus, rectus femoris and semitendinosus muscles, as well as those assessed in the present study. The data concerning the joint activity of these muscles should enable more accurate biomechanical analysis of the different strategies adopted by healthy individuals and those with PFPS in the stance phase of the SLTHT. 5. Conclusions In tasks that involve a high muscular demand such as the single leg triple hop test, the muscles that act directly on the knee joint (biceps femoris and vastus lateralis) are more active among women with patellofemoral pain syndrome during the preactivation phase and stance phase than among healthy women. These differences were not observed for the muscles that act on the hip (gluteus maximus and gluteus medius). Competing interests The authors declare that they have no competing interests. Author’s contributions MMK: data collection, analysis, manuscript writing and critical revision PRGL: conception and design, manuscript writing ACR: data collection ASB: data collection DAB: conception design and critical revision JCFC: data analysis and critical revision FP: conception and design, data analysis and manuscript writing Acknowledgements The authors are grateful to all involved in the study, the team and participants. This study is supported by the Universidade Nove de Julho (UNINOVE, Brazil) and the Brazilian fostering agencies Fundação de Amparo a Pesquisa (FAPESP; process number 2013/ 13839-9). Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j. gaitpost.2016.07.020. References [1] K. Crossley, K. Bennell, S. Green, J. McConnell, A systematic review of physical interventions for patellofemoral pain syndrome, Clin. J. Sport Med. 11 (2001) 103–110.
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Full length article
Kinematic and electromyographic analysis in patients with patellofemoral pain syndrome during single leg triple hop test Marcelo Martins Kalytczak, Paulo Roberto Garcia Lucareli, Amir Curcio dos Reis, André Serra Bley, Daniela Aparecida Biasotto-Gonzalez, João Carlos Ferrari Correa, Fabiano Politti* Department of Rehabilitation Science, Human Motion Analysis Laboratory, Universidade Nove de Julho, São Paulo, Brazil
A R T I C L E I N F O
Article history: Received 9 February 2016 Received in revised form 16 June 2016 Accepted 18 July 2016 Keywords: Patellofemoral pain syndrome Electromyography Hop test Kinematics
A B S T R A C T
Possible delays in pre-activation or deficiencies in the activity of the dynamic muscle stabilizers of the knee and hip joints are the most common causes of the patellofemoral pain syndrome (PFPS). The aim of the study was to compare kinematic variables and electromyographic activity of the vastus lateralis, biceps femoris, gluteus maximus and gluteus medius muscles between patients with PFPS and health subjects during the single leg triple hop test (SLTHT). This study included 14 female with PFPS (PFPS group) and 14 female healthy with no history of knee pain (Healthy group). Kinematic and EMG data ware collected through participants performed a single session of the SLTHT. The PFPS group exhibited a significant increase (p < 0.05) in the EMG activity of the biceps femoris and vastus lateralis muscles, when compared with the healthy group in pre-activity and during the stance phase. This same result was also found for the vastus lateralis muscle (p < 0.05) when analyzing the EMG activity during the eccentric phase of the stance phase. In kinematic analysis, no significant differences were found between the groups. These results indicate that biceps femoris and vastus lateralis muscles mainly during the preactivation phase and stance phases of the SLTHT are more active in PFPS group among healthy group. ã 2016 Elsevier B.V. All rights reserved.
1. Introduction Patellofemoral pain syndrome (PFPS) is a common disorder of the knee joint complex. It is mainly characterized by retro or peripatellar pain [1] and an absence of any other type of associated injury (e.g. chondromalacia, cartilage fissures, osteoarthritis or arthritis). The clinical issue can worsen in the following situations: climbing and descending stairs; performing squats; jumping; remaining seated for a long time or palpating the lateral facet of the patella [2,3]. PFPS is the most common knee injury among active women [4] aged between 18 and 35 years, regardless of whether they are athletes or not. It is more common among women than among men [5–7]. Although the cause of PFPS is multi-factorial,
* Corresponding author at: Rua Vergueiro, 2355 – Liberdade, São Paulo 01504-001, SP, Brazil. E-mail addresses: [email protected] (M.M. Kalytczak), [email protected] (P.R.G. Lucareli), acrfi[email protected] (A.C. dos Reis), [email protected] (A.S. Bley), [email protected] (D.A. Biasotto-Gonzalez), [email protected] (J.C.F. Correa), [email protected] (F. Politti). http://dx.doi.org/10.1016/j.gaitpost.2016.07.020 0966-6362/ã 2016 Elsevier B.V. All rights reserved.
biomechanical abnormalities are considered to play a role in the worsening of this joint disorder. Kinematic abnormalities of the lower limbs, known as medial collapse, is one of the most common of the abovementioned biomechanical factors [8]. This condition is characterized by internal rotation and excessive adduction of the femur, contralateral pelvic drop and knee abduction, which can lead to poor alignment and diminish the congruence between the patella and the femoral trochlea, reducing the area of contact through lateral patellar displacement and increasing patellofemoral pressure [9– 12]. Possible delays in pre-activation or deficiencies in the activity of the dynamic muscle stabilizers of the knee and hip joints are the most common causes of PFPS [13–16]. Delays in muscle activation, differences in the time of activation and different gluteus medius (GMed) muscle activity have been previously proven during the ascent and descent of stairs [13], weight bearing tasks [16] and running tests [15], based on comparisons of healthy women and women with PFPS. However, these results have not been confirmed in studies with similar tasks [17–20]. Controversial results have also been found in relation to the activity of the gluteus maximus (GM) muscle in both healthy
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individuals and those with PFPS while running and descending steps [15,17,20]. When comparing healthy individuals to those with PFPS, greater activity of the patella stabilizer muscles (vastus medialis oblique – VMO and vastus lateralis muscles – VL) was only observed among healthy individuals during tests that involved descending steps [21]. No differences were recorded for the same tests in a similar study [13] and during sprint [20]. However, evidence suggests that abnormal neuromuscular control of the VMO and VL muscles, as well as the reduced strength of the quadriceps, are likely contributors to the development of PFPS [22]. Previous studies have suggested a possible impaired VMO function in cases of PFPS, based on assessments of the EMG signal magnitude [23,24]. However, this finding has not been consistent across all studies [13,20]. Although a greater VMO ratio has previously been linked with PFPS [23,24], abnormal neuromuscular control of the VL muscle was significantly correlated with the Knee Injury and Outcome Score (pain subscale) and the EMG activity of the VL muscle in adolescent female PFPS patients while descending stairs [25]. These results suggest that the neuromuscular control of the VL muscle requires further investigations. Therefore, the influence of the neuromuscular control of hip and knee stabilizers in the genesis and worsening of PFPS remains inconclusive, since these results could be associated with the type of tasks performed during the tests. Very few studies [18,19,26,27] have investigated the biomechanical behavior of lower limbs during tasks of high-intensity, such as the single leg vertical jump, the drop landing task and the unilateral squat. However, no studies have been found addressing the activity of the stabilizer muscles of the hip and knee during the single leg triple hop test (SLTHT). The SLTHT involves the performance of three consecutive unipodal forward jumps. The aim of the test is to achieve the greatest possible distance. It is used to assess the functional performance of lower limbs based on the total of the three jumps, neuromuscular coordination and joint stability [28]. It also enables comparisons between the distances reached when using asymptomatic and symptomatic lower limbs [28–30]. This test can be used to: assess the therapeutic treatment of lower limbs [31]; detect asymmetry or muscle weaknesses in healthy individuals [32,33]; assess the dynamic stabilization of the knee joint [34]; or analyze the strength, power and balance of the lower limbs of patients and athletes [28,29,31,35–37]. The functional phases of the SLTHT place different demands on the knee joint. One of these phases is the preparation phase [38], which is considered a relatively low-impact activity. Another phase is known as the landing phase, which is characterized as a highimpact activity [39]. The speed and intensity of the movements requested in the execution of the SLTHT can generate increased muscle activity, as is the case with sprints of different intensities [40,41], in relation to tasks of less intensity, such as climbing and descending stairs, walking and the step down test. Thus, the SLTHT can involve a significant neuromuscular demand, which can increase the possible differences in the intensity of muscle contractions among individuals with and without PFPS. These differences can be analyzed using surface electromyography (EMG). The intensity of the EMG signal provides a reliable estimate of the volume of the recruited muscle [42]. Hence, the hypothesis of this study was that the speed and intensity of the movements requested in the execution of the SLTHT could also clarify possible differences between the muscle activity of healthy individuals and those with PFPS. The aim of the study was to compare kinematic variables and electromyographic activity of the vastus lateralis, biceps femoris, gluteus maximus and gluteus medius muscles between patients
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with PFPS and health subjects during the single leg triple hop test (SLTHT). 2. Methods 2.1. Subjects This study included 14 individuals with PFPS (PFPS group) and 14 healthy individuals (Healthy group) recruited from the surrounding community and the university by an experienced physiotherapist [6]. The present study was approved by the local Human Research Ethics Committee (CAAE: 02290412.0.0000.5511). The Numerical Rating Scale for Pain (NRS) and the Anterior Knee Pain Scale (AKPS) were used as the diagnostic criteria of PFPS. The NRS is an 11-point scale, ranging from 0 (absence of pain) to 10 (worst possible pain), which has been previously used to assess the pain intensity of PFPS subjects [43]. The AKPS is a self-report questionnaire consisting of 13 questions for which items are differentially weighted for a maximum score of 100, with higher scores indicating better function. This scale has previously been used to assess the severity of pain and disability [44]. The PFPS group contained individuals aged 18–35 years [26] with at least three months of retropatellar pain and a score of between 3 and 6 points on the NRS in the previous three months. These individuals also exhibited a clear increase in symptoms during at least two of the following activities [45]: climbing and descending stairs; squatting; jumping; remaining seated for a long time; maximal isometric voluntary contraction (MIVC) of the quadriceps at 60 of knee flexion; or pain on palpation of the lateral facet of the patella. The inclusion criteria for the healthy group were as follows: physically active women in the same age range as the PFPS group, with no history of knee pain (Table 1). Women with any of the following were excluded from the present study: any neurological disorder; pain in the lower back, sacrum, hip or ankle; a history of surgical procedures on the lower limbs, or other associated pathologies, such as patellofemoral luxation or subluxation; absence of clinical signs of patellar tendinitis and ligament injuries of knee; discrepancies of more than 1 cm in the length of lower limbs (distance between the anterior superior iliac spine and the medial malleolus). Pregnant women and former practitioners of a high performance sport (e.g. practitioners volleyball, basketball, running) were also excluded. 2.2. Instruments The EMG signal was digitalized by a 16-bit A/D converter and synchronized with the kinematic data. A 4-channel telemeterized surface EMG system (FREE EMG, BTS, Italy) recorded muscle activity at 1 kHz per channel. This activity was detected using bipolar surface circular electrodes (Ag/AgCl, Medical Trace1) with 10 mm diameter, center-to-center inter-electrode distance of 2 cm, connected to a portable amplifier with a common-mode rejection
Table 1 Demographics data.
Age (years) Heigth (m) Body mass (Kg) BMI (Kg/m2) Pain score (NRS) AKPS (score)
Health group
PFPS group
P-Value
23.14 3.35 1.62 0.06 55.93 7.15 21.33 2.71 0 99.50 1.29
23.50 2.02 1.66 0.05 56.00 5.23 20.47 1.98 5.05 1.63 80.43 4.78
0.73 0.09 0.97 0.34 – <0.001*
BMI: Body mass index. NRS: numerical rate scale of pain. AKPS: anterior knee pain scale. PFPS: patellofemoral pain syndrome. * Statistically significant difference (p < 0.05: Independent t test).
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ratio >100 dB, an output impedance exceeding 10 MV, a cutoff frequency of 20–500 Hz and a gain of 1000. The surface electrodes were positioned based on the mid-point between the following: the sacrum and the greater trochanter for the muscle GM muscle; the iliac crest and the greater trochanter for the GMed muscle; the head of the fibula and the ischial tuberosity for the biceps femoris muscle (BF). For the VL muscle, the lower third between the base of the patella and the anterosuperior iliac spine was considered [36]. An infrared camera passive marker system (SMART-D BTS1, Milan Italy) recorded the participant’s trunk and lower limb movements, with sampling at 100 Hz. Twenty-five spherical markers were attached to the skin with double-faced adhesive tape, based on the Vicon Plug-in Gait biomechanical model [46,47] (Fig. 1).
counterbalanced to avoid any potential bias. The figure with this information can be found in Supplementary data. After these procedures, the participants were familiarized with the SLTHT, which consists of three consecutive one-leg hops, the aim of which is to reach the maximum possible distance [48]. The reflective markers were fixed in the previously described locations. All of the participants wore shorts and tops and performed the test barefoot in order to prevent different models of sneakers, as well as the different materials used to make them, from distorting the results. For the SLTHT, the volunteers were positioned in the collection area and the helped to perform the test from a one-leg static standing position. The SLTHT was repeated 3 times, with a one-minute rest period between tests. 2.4. Processing
2.3. Procedure The participants performed a single session of the test. The first procedures adopted involved the collection of anthropometric data, as well as the NRS and AKPS scores. The affected limb (or most affected limb) was tested in the PFPS group. The dominant limb of the participants in the healthy group was analyzed. Prior to the kinematic and EMG data collection, a warm-up exercise was performed on a treadmill for 10 min at 1.5 m/s. After an interval of one minute, disposable electrodes were attached for the collection of the EMG signal. Each individual initially performed three MIVC for each muscle during 5-s, with two-minute intervals between the collections. The first and last second of the EMG signal recorded were disregarded (total 3-s) and the highest value observed among the three contractions was used to normalize the data obtained during the jumps. The following tests were used to obtain the MVIC of each muscle against a fixed resistance offered by a non- elastic strap directly attached to the test table at the following positions: GM) patient in the prone position, with the lower limb to be tested at 90 knee flexion, resistance on the distal region of the thigh and the pelvis in a stabilized position; GMed) patient lying on her side, the knee was extended and the hip was placed in slight extension and abduction, with resistance on the shin distal region; BF) the hip was positioned in slight lateral rotation and the knee was flexed at 60 , with resistance on the distal region of the shin; VL) patient in sitting position with the knee flexed at 60 and resistance on the shin distal region. Verbal encouragement was given during all MVIC’s. The order of the MVIC’s was
The present study only considered the EMG activity of the GM, GMed, BF and VL muscles during the stance phase of the second jump in the SLTHT. The first jump of the SLTHT was disregarded due to the difficulty of standardization in relation to the preparation phase that proceeds the propulsion of the test (joint angle, position of the trunk and head). The third jump of the SLTHT was shown to be less motivating for many individuals and thus, the results of this phase could have provided less reliable results than the second phase. Therefore, the stance phase used in the analysis was defined as the first and last contact of the foot during the landing and takeoff of the sole, respectively (Fig. 2). The peak knee and hip flexion values were obtained from the kinematic data recorded during the stance phase of the second jump in the SLTHT. The coordinates of the kinematic data were then smoothed with a Woltring filtering routine, using a 10 Hz cut-off frequency (Vicon Nexus software). All raw EMG data recorded during the MIVC and SLTHT were linear enveloped by rectifying and low-pass filtering (4th order Butterworth, 10 Hz cut-off). The amplitude (intensity) of the EMG signal (iEMG) for each muscle was estimated by calculating the area below the curve, using trapezoidal integration. For the normalization of the EMG signal, the iEMG recorded during the SLTHT was expressed as the percentage of the MIVC (%MIVC). Previous studies have shown that during jumping, the medial gastrocnemius, rectos femoris and vastus lateralis muscles are activated approximately 100 m/s before landing [49,50]. Thus, the iEMG was calculated during the 100 m/s before the initial foot contact, labeled “pre-activity” (PRE-iEMG), and during the stance phase (STP-iEMG). The peak knee flexion (kinematic values) was used to divide the stance phase in order to calculate the iEMG of the eccentric (EXC-iEMG) and concentric phases (CON-iEMG) (Fig. 2). EMG signals were processed by performing specific routines with Matlab software (MathWorks Inc., Natick, Massachusetts, USA). 2.5. Statistical analysis The Shapiro–Wilk test was used to determine the distribution of the data. The independent t-test or the Mann-Whitney test were used for intergroup comparisons. The level of significance was set at 5% (p < 0.05). All data were analyzed using the Statistical Package for Social Sciences (SPSS), version 20.0. 3. Results
Fig. 1. Kinematic marker locations. CLAV: over the manubrium; STR: xiphoid process; RBACK: right scapula; RSHO and Professionanterosuperior iliac spines; RPSI and LPSI: posterosuperior iliac spine; RTHI1 and LTHI1: side of thigh; RTHI and LTHI: lateral face of the base of the patella; RKNE and LKNE: lateral femoral epicondyle; RTIB and LTIB: side of shin; RANK and LANK: lateral malleolus; RTOE and LTOE: middle third of the foot between the 2nd and 3rd metatarsals; RHEE and LHEE: calcaneus.
The anthropometric data (age, stature, body mass and BMI) were similar in the healthy volunteers and those with PFPS (p > 0.05). Differences between the groups related to clinical characteristics were recorded on the same day of the tests before the SLTHT using the Numerical Rating Scale for Pain (NRS) and the Anterior Knee Pain Scale (AKPS) (Table 1). The values recorded for
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Fig. 2. Time course during single leg triple hop test. STP: Stance phase. Foot strikes the ground; Foot leaves the ground; Peak knee flexion; STP: stance phase.
the variables PRE-iEMG, STP-iEMG, EXC-iEMG, CON-iEMG of the GM, GMed, BF and VL muscles were expressed as %MIVC. The peak knee flexion and peak hip flexion variables were displayed in degrees (Table 2).
Table 2 Muscle activation data (EMG). Health group
PFPS group
P-Value
Gluteus maximus muscle PRE-iEMG (%MIVC) STP-iEMG (%MIVC) EXC-iEMG (%MIVC) CON-iEMG (%MIVC)
2.33 1.23 12.81 8.65 8.56 4.41 5.10 4.82
2.35 0.89 12.59 5.16 8.81 4.36 5.51 4.20
0.96 0.69 0.92 0.50
3.2. Kinematic data
Gluteus medius muscle PRE-iEMG (%MIVC) STP-iEMG (%MIVC) EXC-iEMG (%MIVC) CON-iEMG (%MIVC)
2.49 1.40 10.99 5.27 7.39 3.24 4.86 2.74
2.29 1.10 11.69 5.27 8.26 4.00 5.54 3.13
0.62 0.72 0.52 0.54
The peak knee and hip flexion values obtained from the kinematic analysis, as well as the combination of flexion angles of these joints, were compared between the groups, with no significant differences recorded (p > 0.05) (Table 3).
Biceps femoris muscle PRE-iEMG (%MIVC) STP-iEMG (%MIVC) EXC-iEMG (%MIVC) CON-iEMG (%MIVC)
2.17 1.23 6.96 2.53 4.48 2.51 2.90 1.35
2.90 1.46 10.34 5.01 6.48 3.17 3.67 2.88
0.04* 0.04* 0.07 0.37
4. Discussion
Vastus lateralis muscle PRE-iEMG (%MIVC) STP-iEMG (%MIVC) EXC-iEMG (%MIVC) CON-iEMG (%MIVC)
2.75 1.89 13.40 5.75 9.82 5.65 7.10 5.44
3.61 1.20 18.52 7.01 13.54 4.66 8.07 5.59
0.02* 0.04* 0.04* 0.53
3.1. Muscle activation data (EMG) Table 2 displays the results of the EMG data. For PRE-iEMG and STP-iEMG, the PFPS group exhibited a significant increase (p < 0.05) in the EMG signal of the BF and VL muscles, when compared with the healthy group. This same result was also found for the VL muscle (p < 0.05) when analyzing the EMG activity during the eccentric phase (EXC-iEMG) of the stance phase.
The initial hypothesis was that the SLTHT would highlight any possible abnormalities in muscle activity among individuals with PFPS, when compared to healthy individuals. This hypothesis was partially confirmed by the results of the present study. Only the muscles involved in the movement of the knee (BF and VL) exhibited elevated activity compared to the healthy control subjects. The activity of the muscles that are associated with the hip (GM and GMed) was similar in both groups.
Abbreviations: PFPS, patellofemoral pain syndrome; PRE-iEMG, pre-activation; STPiEMG, stance phase; EXC-iEMG, eccentric phase; CON-iEMG, concentric phase; MIVC, maximal isometric voluntary contraction. Integral signal (iEMG) of each muscle. EMGs normalized utilizing the maximally voluntary contraction (%MVC). * Statistically significant difference (p < 0.05: Independent t test and MannWhitney test, used for parametric and non-parametric data, respectively).
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Table 3 Mean and standard deviation (SD) of the kinematics data.
Peak hip flexion (degrees) Peak knee flexion (degrees) Peak hip/knee flexion (degrees)
Health group
PFPS group
P-Value
63.84 11.84 54.91 7.65 118.75 15.86
58.35 7.70 51.22 6.49 109.57 12.53
0.16 0.18 0.10
Independent t test were used for intergroup comparisons.
These results add further information in the discussion of the possibility that PFPS is caused by a deficiency in the control of hip muscles during isometric and dynamic activities, as described in previous studies [8,51,52]. Previous studies have reported significant differences between healthy individuals and those with PFPS, in terms of activity patterns (beginning and duration of activation) of the GMed muscle while climbing and descending stairs [13,14,16] and running [15]. However, when the same muscle was assessed during activities that demand a greater muscular effort, such as the single leg vertical jump [18] and the drop jump [17], no differences were found between the groups. This same observation can also be applied to the GM muscle. During the performance of tasks such as the step down test and sprinting, the activity of the GM muscle was greater among individuals with PFPS. No differences were noted in the drop jump tests [17]. The differences found in the two groups analyzed for the BF and VL muscles indicate that there could be an association between the activity of the muscles involved in the articulation of the knee and PFPS during activities of high intensity, such as the SLTHT. In the present study, the significant increase in the pre-activation and activity of the BF and VL muscles found among women with PFPS may have been caused by a compensation or protection mechanism associated with the pain felt by individuals with this disorder. In general, these muscles help to control the lower limb and the dynamic stabilization of the knee prior to an event of high intensity [53]. Therefore, the greater activity of these muscles could be associated with the need for a greater stability and protection of the joint, due to the impact that occurs during the SLTHT. The activity of the BF muscle during the STP-iEMG also increased in the PFPS group when compared with the healthy group. This difference has previously been demonstrated among cyclists with PFPS [54], who exhibited a greater activation of the hamstrings (BF and semitendinosus) than cyclists without pain. This increase in activity may have generated an increase in the load imposed by the muscle on the joint, thereby contributing to the poor patellar alignment and consequent increase in joint pressure [55]. The greater activation of the VL muscle in the STP-iEMG and EXC-iEMG in the PFPS group could be associated with the decreased angle of hip and knee flexion, when compared with the healthy women. Although this difference was not significant in the present study, this association has previously been demonstrated during the execution of the drop landing task [26,27]. A number of previous studies have reported that the greater EMG activity found in the hip and/or knee extensor muscles of individuals with PFPS could reflect a weakness in these muscles [17,56,57] described the higher VMO (vastus medialis obliquus) and VL amplitudes observed in individuals with PFPS (from patella instability) while walking and climbing/descending stairs, as well as greater GMed and VMO EMG activity during the loading response and single leg stance intervals while descending stairs [57]. Abnormal GMed muscle activity in patients with PFPS has also been described during demanding activities (e.g. running, drop landings and a step-down maneuver) [17]. One explanation for these results is that weaker muscles may reflect the need for increased neuromuscular activity to complete the task. This idea is
strengthened by the decreased amplitude of the EMG signals in the VMO and VL muscles of PFPS patients after exercise therapy [58]. Based on these findings, it is possible that the increased EMG activity of the VL (in the STP-iEMG and EXC-iEMG) and BF (in the STPiEMG) muscles were due to possible weaknesses in these muscles. In the present study, it was possible to confirm that during activities of high intensity, such as the SLTHT, the muscles that act directly on the knee (BF and VL) are more active among individuals with PFPS. These results, although insufficient to form a therapeutic approach, indicate that the muscles responsible for the movement and stabilization of the knee should not be neglected during the assessment and treatment of PFPS patients. The analysis of only four muscles, due to the specifics of the electromyography used, was a limitation of the present study. It is suggested that further studies should also record the activity of the medial vastus, rectus femoris and semitendinosus muscles, as well as those assessed in the present study. The data concerning the joint activity of these muscles should enable more accurate biomechanical analysis of the different strategies adopted by healthy individuals and those with PFPS in the stance phase of the SLTHT. 5. Conclusions In tasks that involve a high muscular demand such as the single leg triple hop test, the muscles that act directly on the knee joint (biceps femoris and vastus lateralis) are more active among women with patellofemoral pain syndrome during the preactivation phase and stance phase than among healthy women. These differences were not observed for the muscles that act on the hip (gluteus maximus and gluteus medius). Competing interests The authors declare that they have no competing interests. Author’s contributions MMK: data collection, analysis, manuscript writing and critical revision PRGL: conception and design, manuscript writing ACR: data collection ASB: data collection DAB: conception design and critical revision JCFC: data analysis and critical revision FP: conception and design, data analysis and manuscript writing Acknowledgements The authors are grateful to all involved in the study, the team and participants. This study is supported by the Universidade Nove de Julho (UNINOVE, Brazil) and the Brazilian fostering agencies Fundação de Amparo a Pesquisa (FAPESP; process number 2013/ 13839-9). Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j. gaitpost.2016.07.020. References [1] K. Crossley, K. Bennell, S. Green, J. McConnell, A systematic review of physical interventions for patellofemoral pain syndrome, Clin. J. Sport Med. 11 (2001) 103–110.
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