Agonist versus antagonist muscle fatigue effects on

Available online at www.sciencedirect.com

Journal of Electromyography and Kinesiology 19 (2009) 55–64 www.elsevier.com/locate/jelekin

Agonist versus antagonist muscle fatigue effects on thigh muscle activity and vertical ground reaction during drop landing Eleftherios Kellis *, Vasiliki Kouvelioti Laboratory of Neuromuscular Control and Therapeutic Exercise, Department of Physical Education and Sports Sciences at Serres Aristotle University of Thessaloniki, TEFAA Serres, Serres 62100, Greece Received 11 May 2007; received in revised form 3 August 2007; accepted 3 August 2007

Abstract Background: Agonist and antagonist co-activation plays an important role for stabilizing the knee joint, especially after fatigue. However, whether selective fatigue of agonists or antagonist muscles would cause different changes in muscle activation patterns is unknown. Hypothesis: Knee extension fatigue would have a higher influence on landing biomechanics compared with a knee flexion protocol. Study design: Repeated-measures design. Methods: Twenty healthy subjects (10 males and 10 females) performed two sets of repeated maximal isokinetic concentric efforts of the knee extensors (KE) at 120 s 1 until they could no longer consistently produce 30% of maximum torque. On a separate day, a similar knee flexion (KF) fatigue protocol was also performed. Single leg landings from 30 cm drop height were performed before, in the middle and after the end of the fatigue test. The mean normalized electromyographic (EMG) signal of the vastus medialis (VM), vastus lateralis (VL), biceps femoris (BF) and gastrocnemius (GAS) at selected landing phases were determined before, during and after fatigue. Quadriceps:hamstrings (Q:H) EMG ratio as well as sagittal hip and knee angles and vertical ground reaction force (GRF) were also recorded. Results: Two-way analysis of variance designs showed that KE fatigue resulted in significantly lower GRF and higher knee flexion angles at initial contact while maximum hip and knee flexion also increased (p < 0.05). This was accompanied by a significant decline of BF EMG, unaltered EMG of vastii and GAS muscles and increased Q:H ratio. In contrast, KF fatigue had no effects on vGRFs but it was accompanied by increased activation of VM, BF and GAS while the Q:H increased during before landing and decreased after impact. Conclusion: Fatigue responses during landing are highly dependent on the muscle which is fatigued. 2007 Elsevier Ltd. All rights reserved. Keywords: Electromyography; Anterior cruciate ligament; Co-activation; Injury prevention

1. Introduction Landing from a jump is a common activity in sport and work environments. The vertical ground reaction force (GRF) during single-leg landings is high and it can reach 11 times body weight (McNitt-Gray, 1991). This mechanical shock must be attenuated by the musculoskeletal system. However, when the external loads are very high for the body to adequately attenuate, the probability of injury *

Corresponding author. Tel.: +30 2310 991053/991044; fax: +30 2310 991053. E-mail address: [email protected] (E. Kellis). 1050-6411/$ - see front matter 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.jelekin.2007.08.002

increases (Devita and Skelly, 1992; Dufek et al., 1990; Dufek and Bates, 1991; Gross and Nelson, 1988; James et al., 2000; Kovacs et al., 1999). Fatigue has been hypothesized to alter the biomechanical and neuromuscular factors associated with the risk of sustaining musculoskeletal injury (Christina et al., 2001; Rozzi et al., 1999a). Epidemiological and experimental studies indicate that fatigue combined with extreme loads, may lead to injury (Pettrone and Ricciardelli, 1987; Urabe et al., 2005). Fatigue affects reaction time (Hakkinen and Komi, 1986), movement co-ordination and motor control precision (Sparto et al., 1997), and reduces the muscle force generation capacity (Nicol et al., 1991a).

56

E. Kellis, V. Kouvelioti / Journal of Electromyography and Kinesiology 19 (2009) 55–64

The ground reaction force (GRF) provides an indication of the loading of the musculoskeletal system after fatigue; more importantly, because the GRF is greater during a stiffer landing, GRF has be used to identify changes in landing stiffness (Madigan and Pidcoe, 2003; Padua et al., 2006; Tillman et al., 2004). Research has shown that vertical GRF during single-leg landing decreases after fatigue (Madigan and Pidcoe, 2003) while vertical leg stiffness remains unaltered (Padua et al., 2006). The reduction of vertical GRF after fatigue is indicative of the subject effort to reduce the mechanical shock due to landing. Since landing is a multiarticular task, subjects may use altered activation and movement strategies to account for fatigue effects. Previous research has shown that post-fatigue landing is characterised by increased flexion of the knee (Coventry et al., 2006; Madigan and Pidcoe, 2003) and the hip (Coventry et al., 2006) and decreased ankle plantarflexion (Coventry et al., 2006). An increase in knee flexion acceleration has also been reported (Fagenbaum and Darling, 2003). Fatigue also caused a re-distribution of work produced around the lower limb joints, as hip joint work increased, knee joint remained unaltered while ankle work decreased after fatigue (Coventry et al., 2006; Madigan and Pidcoe, 2003). The alterations in kinetics and kinematics after fatigue may be the result of alterations in muscle activation profiles of the associated musculature. Despite this, only a few studies have examined muscle activation profiles during single-leg landings after fatigue (Padua et al., 2006; Rozzi et al., 1999b). Particularly, increased co-contraction of antagonistic musculature around the knee and the ankle (Padua et al., 2006) and alterations in contraction onset of knee and ankle muscles (Rozzi et al., 1999b) have been reported. Among numerous strategies available, Padua et al. (2006) identified three strategies to control joint motion after fatigue: the ankle-dominant strategy where individuals place greater reliance on the ankle musculature; the antagonist inhibition strategy which is characterised by a decline in antagonist muscle activation patterns upon landing and, finally, the quadriceps-dominant strategy where subjects place greater reliance on quadriceps muscles after fatigue. It seems, therefore, muscle activation responses to fatigue mainly focus around the activity patterns of the quadriceps and hamstrings. However, it is known that these co-contraction of the agonist–antagonist muscle groups around the knee is an important determinant of knee joint stability (Kellis, 1998). For these reasons, examination of fatigue effects on activation of agonist–antagonist couple of muscles is worthwhile. Evidence suggests that agonist fatigue affects movement kinematics more than antagonist muscle fatigue (Jaric et al., 2000; Rodacki et al., 2002). For example, Rodacki et al. (2002) reported that fatiguing the knee flexor muscles did not change the kinematic, kinetic, and electromyographic profiles of counter movement jumps. In contrast, knee extensor fatigue caused the subjects to adjust several variables of the movement. These results, however, apply

to countermovement jumps where individuals aim to maximize jumping performance. This differs compared with drop landings where safe landing is the main priority. Single-leg landings are characterised by high pre-activation of vastus medialis, hamstrings and lateral gastrocnemius muscles (Cowling and Steele, 2001; Tillman et al., 2004) in order to stabilize the knee and the ankle in preparation for landing. The majority of previous studies examined landing biomechanics after fatiguing mainly the knee extensor musculature (Fagenbaum and Darling, 2003; Madigan and Pidcoe, 2003; Padua et al., 2006; Rozzi et al., 1999b; Wikstrom et al., 2004). To our knowledge, muscle activation and kinematics during singe leg landing following different muscle fatigue protocols have not been examined. Taken into account the potentially different roles of agonist and antagonist muscle action during landing, it can be assumed that selective fatigue of either of them would cause different changes in movement biomechanics. Such information may provide an insight on the way the neuromuscular system adjusts the movement co-ordination pattern used during landing under fatigue of different muscles. The objective of this study was to compare the effects of a knee extension (KE) and flexion (KF) fatigue protocol on vertical GRF and EMG characteristics during landing. It was hypothesized that KE fatigue would have a higher influence on vertical GRF, kinematic and EMG variables compared with KF protocol. 2. Methods 2.1. Design A single two-group pre-post test design was applied. The subjects visited the laboratory three days, a week apart. The aim of the first visit was to familiarize the subjects with isokinetic dynamometer and landing technique. Day 1 was a familiarisation session whereas the KE (agonist) and KF (antagonist) isokinetic fatigue protocols were performed on the next two sessions on a random basis. Vertical GRF, muscle EMGs and hip and knee kinematics were recorded prior to and after fatigue. 2.2. Subjects Ten males (age 24.3 ± 1.25 yr, height 181.3 ± 8.27 cm, body mass 79 ± 8.21 kg) and ten females (age 23.5 ± 1.43 yr, height 168.9 ± 8.38 cm, body mass 59.82 ± 6.25 kg) who were physical education students volunteered to participate. The participants had no history of serious lower-extremity injury. Subjects signed informed written consent prior to their participation. The study was approved by the Aristotle University Ethics Committee. 2.3. Instrumentation All drop landings were performed on a customized uni-axial force plate (600 · 400 cm). The platform uses a strain gauge (Model LC4204 – K600, A&D Co. Ltd., Tokyo, Japan) capable to measure vertical ground reaction force (linearity 110 db at 50/60 Hz, bandwidth = 10–500 Hz; gain = 1000) was used for EMG data collection. Bipolar surface electrodes were placed on vastus medialis (VM), vastus lateralis (VL), biceps femoris (BF) and gastrocnemius (GAS) were recorded using a TEL100D (Biopac Systems, Inc., Goleta, CA) remote system. The EMG electrode locations were prepared by shaving the skin of each electrode site and cleaning it with alcohol wipes. The skin resistance was always checked using a simple DC ohmmeter and it was less than 5 kX. These locations were identified during a maximal voluntary isometric effort from the seated (VM, VL, GAS) and prone (BF) positions. For the VM, electrodes were located approximately 5 cm medial to a point that was 25% of the distance from the superior aspect of the patella to the anterior superior iliac spine. For the VL, the position of the electrodes was lateral to the rectus femoris, half way between the lateral femoral epicondyle and greater trochanter. The BF electrodes were placed 2.5 cm medial to the midpoint of a line from the ischial tuberosity to the mid-popliteal crease. For the GAS, electrodes were directly placed over the lateral head, at approximately 25% of the distance from the fibular head to the middle of the calcaneal tendon. The ground electrode was positioned on the bony surface on the lateral epicondyle. The position of the electrodes was not altered during each testing session. A Cybex Norm dynamometer (Lumex Corporation, Ronkonkoma, NY) was used for isometric and isokinetic measurements. All (Cybex, EMG, force platform) systems were interfaced to a Biopac MP100 Data Acquisition unit (Biopac Systems, Inc., Goleta, CA) and converted into digital form at a rate of 2000 Hz. All signals were displayed on the monitor and stored for further analysis. Two-dimensional movement kinematics were recorded using a video camera (JVC 9800, frame rate 120 Hz with a high-speed shutter). Skin reflective markers (radius 10 mm) were placed on the head of fifth metatarsal, the heel, lateral malleolus, greater trochanter and shoulder of the dominant side. The dominant limb was defined as the limb that the subject used to kick a soccer ball (Wikstrom et al., 2006). The camera was placed perpendicular to the movement plane at a focal distance of 8 m. The lens was then adjusted by zooming on the performing in order to reduce perspective error. For synchronization of the force and video data, the computer triggered a stroboscopic light which was visible on the camera’s field of view. The video image of a calibration frame (1.80 m · 2.40 m) was recorded prior to each measurement and eight calibration points were digitized in order to determine the 2-D position of any point in space. 2.4. Procedures 2.4.1. Landing In each visit, subjects first warmed up by cycling for 10 min at a low workload of 75 W. All subjects were asked to perform several single-leg landings from 30 cm drop height on the force plate. Particularly, the subjects jumped from a stand on the

57

platform on their dominant leg, with their hands on their hips while they wear no shoes. The starting position was with the knee at 0 (full extension) and positive knee angles indicate knee flexion. No verbal or visual reinforcement was provided during the tests. Landings were performed prior to, between the first and the second set of the fatigue protocol, and after fatigue. 2.5. Maximal and fatigue tests Isokinetic and isometric tests were performed from the seated position (hip flexion angle of 85). The trunk, waist and thigh of the right leg of the subjects were stabilised with Velcro straps. The axis of rotation of the dynamometer was carefully aligned with the approximate center of rotation of the knee, on the posterior aspect of the lateral femoral condyle. The leg was positioned horizontally to the ground and full extension (0) was checked by aligning a level indicator posteriorly on the medial femoral epicondyle and malleolus. During day 1, each subject performed three extension/flexion efforts at 120 s 1 to determine maximum extension and flexion torque. The motion ranged from 0 (full extension) to 90 of knee flexion. The subjects were instructed to exert maximal effort throughout the whole range of motion. Maximum values were then used to set the target levels of fatigue tests performed on subsequent days. During days 2 and 3, the subjects were asked to perform three (5 s) maximal isometric efforts of the knee extensors and flexors at an angle of 65 and 35, respectively (full knee extension = 0). These tests were performed in order to normalize the surface EMG signals. For each subject, the EMG activity of each muscle was filtered using a digital high-pass filter at 10.0 Hz with zero phase shift. It was then rectified and the average value for a period of 2 s during which the recorded torque was relatively consistent (± 5%). The fatigue test included performance of two sets of consecutive concentric efforts of the knee extensors (day 2) or flexors (day 3) at 120 s 1 until the subjects could no longer produce 30% of the maximum moment. During the test subjects received standardized verbal instructions to maintain maximal effort throughout the test. When the first fatiguing session ended, the subject immediately got off the dynamometer and then performed the landing tasks as quickly as possible to reduce the effects of recovery from muscular fatigue. The subject then returned to the dynamometer and performed the second set of repetitions until fatigue occurred. Each subject then repeated the same jumping sequence as quickly as possible. 2.6. Data analysis Each drop landing was divided into three phases: the preparatory phase (PR) defined as the period 100 ms before initial ground contact, the initial loading response (LR) phase, defined as the 100-ms interval immediately after ground contact (LR1), and the main LR phase (LR2) defined as the period between 100 and 200 ms after ground contact. Ground contact was determined from the vertical GRF tracings. For each subject, vertical GRF data was expressed in times body weight (BW). For each individual force–time tracing the mean value during each landing phase was estimated. Further, the maximum GRF was also used for further analysis. EMG data were filtered using a digital high-pass filter at 10.0 Hz with zero

58


phase shift to attenuate movement artefacts. Following rectification, the EMG amplitude signals were normalized as percentage of EMG values recorded during maximum voluntary contraction and computed for each phase of the landing. The quadriceps:hamstrings co-activation was also computed as the sum of quadriceps (VM and VL) (agonist) activity divided by the BF (antagonist) activity for each phase (Q:H ratio). The level of antagonist co-activation is considered an important indicator of muscle imbalances around the knee. We used this specific co-activation index in order to compare our results with recent findings on fatigue effects on landing biomechanics (Padua et al., 2006). Q:H ratios of 1.0 indicate equal activation of the agonist and antagonist muscles while co-activation ratios greater than 1.0 indicate increased agonist (quadriceps) activation compared with the antagonist (hamstring) muscles and vice versa(Padua et al., 2006). The recorded video sequences were digitized using a videobased software (Kwon 3-D, Yoon Kwon and Visol Inc., Korea). The resulting displacement–time data of each marker were filtered using a second-order Butterworth digital filter with zero-order phase lag. Optimal cut-off frequencies were chosen by comparing the residuals of the difference between filtered and unfiltered signals at several cut-off frequencies. Sagittal plane joint angles were calculated for the right hip and knees. The measured kinematic variables included the knee joint angle at impact (ICKNEE) and the maximum angle (MaxKNEE) during the movement. The same angles for the hip (ICHIP and MaxHIP) were calculated. 2.7. Statistical analysis Separate, mixed-model, repeated-measures analyses of variance (ANOVA) for each of the dependent variables were used to determine whether fatigue had an effect on the variables tested. Knee and hip angles involved two within-subject variables: time (three levels: pre-fatigue, middle-fatigue, post-fatigue) and fatigue protocol (KE, KF). Similar ANOVAs were used to examine fatigue and fatigue protocol effects on muscle activation amplitude of the GAS, BF, VM and VL, vertical GRF as well as the quadriceps:hamstrings co-activation ratio for each phase of landing. The Tukey honestly significant difference method was used to perform post-hoc analyses on all significant main effects and interactions. A significance level of a < .05 was set a priori for all analyses.

3. Results The ANOVA results are presented in Table 1. Significant fatigue · protocol interaction effects were found for GRF values, MAXHIP, EMGBF during the PR and LR1 phases, EMGVM and EMGVL during the PR phase, EMGGAS during the LR1 and LR2 phases and quadriceps:hamstrings co-activation ratio during the LR1 phase. 3.1. Vertical GRFs and joint angles Maximum GRFs and joint angle values for each testing condition are presented in Table 2. Post-hoc Tukey tests indicated that maximum GRF decreased significantly (p < 0.05) with KE fatigue. After fatigue, subjects landed with significantly greater knee flexion angle than they did pre-fatigue (Table 2). With regards to the hip angle (Table 2), post-hoc

Table 1 F-ratio values resulting from ANOVA designs used to examine the effects of fatigue, type of protocol (extension–flexion) and their interaction effect on each dependent variable Parameters

Fatigue

Protocol

Degrees of freedom (within, residual)

2, 36

1, 18

Fatigue X protocol 2, 36

6.18* 6.48* 5.08*

0.21 4.93 0.12

3.72* 6.49* 10.81*

15.34* 24.94* 2.17 33.37*

4.59 0.93 0.04 5.63

3.25 0.96 0.82 8.49*

Biceps femoris EMG PR LR1 LR2

3.21 1.79 2.29

2.37 3.09 2.94

4.16* 4.07* 1.79

Gastrocnemius EMG PR LR1 LR2

0.06 1.51 2.15

0.12 1.73 0.15

0.26 3.98* 4.03*

Vastus medialis EMG PR LR1 LR2

3.52* 1.27 0.13

0.47 4.32* 4.52*

5.27* 0.79 2.67

Vastus lateralis EMG PR LR1 LR2

10.10* 1.52 0.71

0.52 4.04 1.19

9.19* 0.14 0.38

0.24 3.21* 0.48

2.15 7.29* 0.23

Ground reaction forces GRF max GRF LR1 GRF LR2 Angular position kinematics ICKNEE MAXKNEE ICHIP MAXHIP

Quadriceps:hamstrings co-activation ratio PR 20.01* 0.48 LR1 LR2 1.67 *

Significant at p < 0.05; PR = 100 ms before impact; LR1 = 0–100 ms after impact; LR2 = 100–200 ms after impact; GRF = ground reaction force; ICKNEE = knee angle at impact; MAXKNEE = maximum knee angle; ICHIP = HIP angle at impact; MAXHIP = maximum hip angle.

analysis indicated that MaxHIP flexion angle increased only after the KE fatigue protocol (p < 0.05). The post-hoc analysis also indicated that GRFLR1 (Fig. 1) decreased an average of 12.0% with KE fatigue, from 2.15 ± 0.16 times body weight (BW) to 1.90 ± 0.17 BW (p < 0.05). In contrast, GRFLR1 (2.15 ± 0.20 BW) before KF fatigue was not significantly different compared with the post-fatigue value (2.11 ± 0.18 BW). The GRFLR2 following KE fatigue also significantly declined from 1.76 ± 0.17 BW to 1.55 ± 0.16 BW (p < 0.05). The GRFLR2 was 1.77 ± 0.18 BW prior to KF fatigue and 1.68 ± 0.19 BW after KF fatigue. 3.2. Biceps femoris and gastrocnemius EMG KE fatigue caused a 23.5% decrease in EMGBF (Fig. 2) only during the PR phase from 21.3 ± 4.8% MVC to

E. Kellis, V. Kouvelioti / Journal of Electromyography and Kinesiology 19 (2009) 55–64 Table 2 Maximal vertical GRF (mean ± SD), knee and hip flexion angle at contact and maximum values during landing prior to (Pre), before (Pre), between the two sets of fatigue (Mid) and after fatigue (Post)

4.19 ± 0.40 3.83 ± 0.48 3.73 ± 0.47*

4.09 ± 0.41 4.01 ± 0.45 3.98 ± 0.48

Knee angle at contact Pre 10.62 ± 2.58 Mid 14.50 ± 3.39 Post 18.50 ± 4.09*

9.75 ± 2.29 12.53 ± 2.94 15.00 ± 3.74*

Maximum knee angle Pre 47.37 ± 9.35 Mid 57.00 ± 13.34 Post 61.46 ± 9.77*

47.17 ± 9.77 52.84 ± 8.37 57.84 ± 11.68*

Maximum hip angle Pre 32.00 ± 7.97 Mid 40.50 ± 10.37* Post 40.91 ± 9.83* *

3 2.5 2 1.5

Pre

2.82 ± 0.57 2.87 ± 0.64 2.99 ± 0.95 33.29 ± 5.93 36.39 ± 8.32 34.93 ± 9.56

Significantly different compared with pre-fatigue values, p < 0.05.

16.9 ± 5.5% MVC (after fatigue). In contrast, KF fatigue caused a 29.44% increase (p < 0.05) in EMGBF during the LR1 phase, from 31.4 ± 6.2% MVC prior to fatigue to 44.4 ± 9.4% MVC post-fatigue. KF fatigue caused a significant (p < 0.05) increase in EMGGAS during the LR1 from 65.7 ± 34.1% MVC before fatigue to 84.3 ± 36.9% MVC after fatigue (Fig. 2). Similarly, the EMG during the LR2 phase increased from a pre-fatigue value of 45.4 ± 25.2% MVC to 63.51 ± 28.4% MVC after fatigue.

*

*

Mid

Post

1

2.2

Hip angle at contact Pre 2.75 ± 0.84 Mid 3.01 ± 1.04 Post 3.16 ± 1.01

KE fatigue KF fatigue

GRF / BodyWeight

Maximum GRF Pre Mid Post

Flexion protocol

LR1

3.5

LR2

2

GRF / BodyWeight

Extension protocol

4

59

1.8 1.6 1.4

* 1.2

*

1 Pre

Mid

Post

Fig. 1. Vertical ground reaction force (times body weight) during landing before (Pre), between the two sets of fatigue (Mid) and after fatigue (Post). (LR1: initial landing phase; LR2: main landing phase; KE: knee extension; KF = knee flexor; error bars indicated standard deviation; * significantly different compared with pre-fatigue value at p < 0.05).

4. Discussion 3.3. Vastus medialis and lateralis EMG No alterations in EMG of the vastii muscles after KE fatigue were observed (Fig. 3). In contrast, KF fatigue caused a significant increase (p < 0.05) in EMGVM (Fig. 3) during the pre-activation phase from 32.61 ± 12.71% MVC (before fatigue) to 41.47 ± 17.91% MVC (after fatigue). The EMGVL (Fig. 3) during the PR phase increased significantly (p < 0.05) from 16.15 ± 7.6% MVC prior to KF fatigue to 32.07 ± 17.92% MVC after fatigue. 3.4. Quadriceps:hamstrings co-activation ratio Fatigue (collapsed across protocols) caused a significant (p > 0.05) increase in Q:H ratio during the PR phase (Table 3). In contrast, during the LR1 phase, the co-activation ratio increased after the KE protocol while it decreased following the KF protocol.

The primary finding of this study is that landing responses to fatigue differ between KE and KF fatigue protocols. KE fatigue caused a decline in GRF values, increased knee flexion angle and reduced hamstrings activation, unaltered activation of vastii muscles and increased Q:H ratio. In contrast, KF fatigue did not alter GRF values but it caused alterations in VM, GAS and BF activity while the Q:H declined during the loading response phase. 4.1. Agonist versus antagonist fatigue effects on GRF and joint angles The present results showed a decline of vertical GRF following KE fatigue (Fig. 1) which is in agreement with some studies during single-leg landing (Madigan and Pidcoe, 2003) and running (Bruggemann, 1996; Christina et al., 2001; Nicol et al., 1991b) following various fatigue

60


Biceps Femoris 50

KE fatigue

PR

170

KF fatigue

40 35 30 25 20 15

*

10

*

Muscleactivation (% MVC)


45

Gastrocnemius

130 110 90 70 50 30

Pre

Mid

Pre

Post

Mid

100

60

*

40 30 20

*

10


50

Post

*

LR1

*

LR1 Muscleactivation (% MVC)

KF fatigue

150

5 0

90 80 70 60 50 40 30

0 Pre

Mid

Pre

Post

Mid

Post

100

60



KE fatigue

PR

50 40 30 20 10

90 80

*

*

70 60 50 40 30

0 Pre

Mid

Post

Pre

Mid

Post

Fig. 2. Normalized (% MVC) biceps femoris and gastrocnemius EMG during landing before (Pre), between the two sets of fatigue bouts (Mid) and after fatigue (Post). (PR: pre-activation phase; LR1: initial landing phase; LR2: main landing phase; KE: knee extension; KF = knee flexor; error bars indicated standard deviation; * significantly different compared with pre-fatigue value at p < 0.05).

protocols while others have reported opposite results (Nyland et al., 1997, 1994). These studies, though, involve different activities (running, rapid stop, crossover cutting) and different fatigue patterns (general fatigue, quadriceps

muscles fatigue, dorsiflexor muscles fatigue), thus making comparisons among studies difficult. Given that the ICHIP remained unaltered after fatigue (Table 2), the reduction in GRF after KE fatigue is primar-


Vastus Medialis KE fatigue

PR

90

80 70 60

*

50 40 30 20 10 Pre

Mid

70 60 50

*

40

*

30 20 10 Pre

Post

150

Mid

Post

Pre

Mid

Post

Pre

Mid

Post

150

LR1

LR1

130



KF fatigue

80

0

0

110 90 70 50 30

130 110 90 70 50 30

Pre

Mid

Post

150

150

LR2

LR2

130



KE fatigue

PR

KF fatigue


Muscleactivation (% mVC)

Vastus Lateralis 100

100 90

61

110 90 70 50 30

130 110 90 70 50 30

Pre

Mid

Post

Fig. 3. Normalized (% MVC) vastus medialis EMG during landing before (Pre), between the two sets of fatigue (Mid) and after fatigue (Post). (PR: Preactivation phase; LR1: initial landing phase; LR2: main landing phase; KE: knee extension; KF = knee flexor; error bars indicated standard deviation; * significantly different compared with pre-fatigue value at p < 0.05).

ily due to the increase of knee flexion angle at impact during landing (Table 2). This is in agreement with previous findings (Coventry et al., 2006; Hewett et al., 1996; Louw et al., 2006; McNair et al., 2000) and provides support to previous suggestions that more knee flexion during the

landing phase will reduce the chances of injury due to lower GRFs and better shock absorption (Coventry et al., 2006; Derrick, 2004; Hewett et al., 1996; Louw et al., 2006; Riemann and Lephart, 2002). It has been shown that the increase in knee flexion angle causes a reduction in

62


Table 3 Quadriceps:hamstrings co-activation ratios (mean ± SD) during the three landing phases prior to (Pre), before (Pre), between the two sets of fatigue (Mid) and after fatigue (Post) Landing phase

Fatigue condition

Extension protocol

Flexion protocol

Pre-activation

Pre Mid Post

1.12 ± 0.53 1.20 ± 0.53 1.87 ± 0.76*

1.08 ± 0.45 1.55 ± 0.51 1.75 ± 0.73*

Loading response 1

Pre Mid Post

2.45 ± 0.82 2.52 ± 0.82 3.14 ± 0.81*

2.60 ± 0.92 2.28 ± 0.87 2.06 ± 1.10*

Loading response 2

Pre Mid Post

2.32 ± 0.81 2.40 ± 0.88 2.64 ± 0.77

2.22 ± 1.01 2.55 ± 0.84 2.44 ± 1.05

*

Significantly different compared with pre-fatigue value, p < 0.05.

body-effective axial stiffness and consequential improvement shock attenuation functions of the body (Derrick, 2004; Lafortune et al., 1996). Further, Lafortune at al. (Lafortune et al., 1996) showed that while the loading rate and the impact shock were not altered after fatigue, the vertical GRF declined. Using simulation, Gerritsen et al. (1995) reported that a 1 change in the leg angle led to a 68 N (0.1 BW) change in impact forces. In the present study, ICKNEE was reduced by approximately 4–6 which may explain the mean reduction 0.35 BW after KE fatigue. Our results, however, are in disagreement with other studies (Fagenbaum and Darling, 2003; Wikstrom et al., 2004) which reported no significant alterations of knee joint kinematics following fatigue. In the present study a non-significant effect of KF fatigue on vertical GRF during landing was found (Fig. 1). Previous studies have shown that upon impact the BF muscle mainly has a stabilizing effect for the knee joint (Coventry et al., 2006; McNitt-Gray et al., 2001; Urabe et al., 2005; Zhang et al., 2000). Therefore, fatiguing of these muscles may have had less effect on the position of the body during landing compared with the KE fatigue protocol. This is confirmed by the smaller changes in knee and hip (Table 2) flexion angles after KF fatigue compared with KE fatigue. 4.2. Agonist versus antagonist fatigue effects on muscle activity In the present study, fatigue responses were different between the two protocols. To our knowledge, this is the first study which compared the effects of localized KF and KE fatigue protocols on muscle activation patterns during landing. Our results support previous findings (Jaric et al., 2000; Rodacki et al., 2002) and suggest that fatigue responses may differ depending on whether the muscle acts as agonist or antagonist around a joint. The reduction in EMGBF (Fig. 2) and maintenance of quadriceps activation (Fig. 3) after KE fatigue were evident during the pre-activation and early loading phase of the

landing. Subjects placed greater reliance on quadriceps muscles after KE fatigue (Fig. 3) which is in agreement with the quadriceps-dominant strategy reported in the literature (Padua et al., 2006). Such a strategy was also evident after the KF fatigue protocol where fatigue resulted in increased EMGVM (Fig. 3) prior to ground contact. The maintenance of quadriceps muscle activation as they lengthen may be indicative of the attempt of neuromuscular system to control the knee as well as the hip during landing. Another strategy to compensate for fatigue effects is the decline in antagonist activation patterns of the knee and the ankle (Padua et al., 2006). We also observed a decline in BF activity following KE fatigue which supports this suggestion (Fig. 2). In contrast, KF fatigue caused unaltered BF activity during the pre-contact phase and increased activation in the loading response phase (Fig. 2). The net outcome of the above changes was a different behaviour of the Q:H ratio after the two protocols (Table 3): while the Q:H ratio increased after the KE protocol, KF fatigue caused an increase in this ratio in the PR phase and a decline in the LR1 phase (Table 3). Previous research (Coventry et al., 2006; Madigan and Pidcoe, 2003; Padua et al., 2006) reported that subjects placed higher reliance on the ankle musculature (increased GAS activation) and less to the knee musculature after fatigue. However, these studies applied functional fatigue protocols which load not only the knee musculature (agonists and antagonists) but also the ankle joint muscles. This load differs compared with the localized muscle fatigue protocols applied in this study. Our results indicated increased GAS activity only after the KF fatigue protocol while we found non-significant alteration of GAS activation after KE fatigue (Fig. 2). This might suggest that alterations in GAS activation are due to fatigue of the antagonist muscles and not due to fatigue of the agonists (quadriceps). However, since we did not measure ankle joint kinematics as well as the antagonist muscle activation around this joint and no conclusions regarding the role of ankle musculature during landing are possible. Minimizing knee joint loading is of particular interest especially when an individual is fatigued. For example, many studies have suggested that minimizing the ACL strain and injury requires an increase in antagonist hamstring activity to counteract quadriceps muscle forces (Kellis, 1998; Solomonow and Krogsgaard, 2001). Our results suggest that fatiguing the quadriceps muscles may increase injury risk, as the subjects demonstrated higher Q:H ratios when fatigued. These was accompanied by altered GRFs and knee flexion angle, in order to reduce injury risk. In contrast, fatiguing the antagonist muscles had less effect on movement patterns, but it did result in an increase of Q:H ratio in the pre-activation phase. This may demonstrate the importance of quadriceps muscle function during the preparatory landing phase, irrespective of the muscle being fatigued. The decline of Q:H ratio in the main landing phase may be


seen as attempt of the neuromuscular system to compensate for the fatigue of the antagonist muscle. In the present study, only sagittal plane motion of the hip and knee were examined. Movement pattern alterations may have occurred in the transverse or frontal planes of motion at these joints as well as in all planes of hip joint motion. Furthermore, muscle activation patterns of gluteus muscles as well as tibialis anterior muscles were not examined. It is possible that fatigue may have altered activation of these muscles in order to compensate for fatigue and maintain balance. Furthermore, we examined the effects of fatigue on the magnitude of the muscle EMGs and GRFs was recorded, by dividing landing into three phases. Instantaneous development of maximum GRF and associated muscle activation during landing is also important for shock attenuation at impact (Cowling et al., 2003) and its examination under fatigue conditions deserves further attention in the future. Biomechanical characteristics of single-leg landings may also be affected by perception (Santello et al., 2001). It is possible that fatigue may have affected subject ability to estimate touchdown time or their ability to visualize the movement after fatigue. Unfortunately perception or ability to respond to various stimuli was not examined in the present study. Our observations from the experimental sessions showed that subject perception might have been affected more after the KE fatigue protocol compared with KF fatigue efforts. We can speculate that this may be due to the large size and significant contribution of the knee extensor muscle group during landing. However, further research is needed to verify the above finding. In conclusion, this study showed that KE fatigue, individuals landed with lower vGRFs and higher knee flexion angle. This was accompanied by an antagonist inhibition strategy around the knee and a quadriceps-dominant strategy. In contrast, KF fatigue had no effects on vGRFs but it was accompanied by increased activation of VM, BF and GAS and increased Q:H ratio during the pre-activation phase. It is concluded that fatigue responses during landing are highly dependent on the muscle which is fatigued. References Bruggemann G. Influence of fatigue on lower extremity function. In: XIV symposium on biomechanics in sports. Funchal, Portugal: Universidade Tecnica de Lisboa; 1996. Christina KA, White SC, Gilchrist LA. Effect of localized muscle fatigue on vertical ground reaction forces and ankle joint motion during running. Human Mov Sci 2001;20:257–76. Coventry E, O’Connor KM, Hart BA, Earl JA, Ebersole KT. The effect of lower extremity fatigue on shock attenuation during single leg landing. Clin Biomech 2006;21:1090–7. Cowling EJ, Steele JR. Is lower limb muscle synchrony during landing affected by gender? Implications for variations in ACL injury rates. J Electromyogr Kinesiol 2001;11:263–8. Cowling EJ, Steele JR, McNair PJ. Effect of verbal instructions on muscle activity and risk of injury to the anterior cruciate ligament during landing. Brit J Sport Med 2003;37:126–30.

63

Derrick TR. The effects of knee contact angle on impact forces and accelerations. Med Sci Sport Exerc 2004;36:832–7. Devita P, Skelly W. Effect of landing stiffness on joint kinetics and energetics in the lower extremity. Med Sci Sport Exerc 1992;24:108–15. Dufek JS, Bates BT. Biomechanical factors associated with injury during landing in jump sports. Sport Med 1991;12:326–37. Dufek J, Schot P, Bates B. Lower extremity moments of force during landings. Med Sci Sport Exerc 1990;22:S17. Fagenbaum R, Darling WG. Jump landing strategies in male and female college athletes and the implications of such strategies for anterior cruciate ligament injury. Am J Sport Med 2003;31:233–40. Gerritsen KG, van den Bogert AJ, Nigg BM. Direct dynamics simulation of the impact phase in heel-toe running. J Biomech 1995;28:661–8. Gross T, Nelson R. The shock attenuation role of the ankle during landing from a vertical jump. Med Sci Sport Exerc 1988;20:506–14. Hakkinen K, Komi PV. Electromyographic and force production characteristics of leg extensor muscles of elite weight lifters during isometric, concentric and various stretch-shortening cycle exercises. Int J Sport Med 1986;7:144–51. Hewett T, Stroupe A, Nance T, Noyes F. Plyometric training in female athletes. Decreased impact forces and hamstring torques. Am J Sport Med 1996;24:765–73. James CR, Dufek JS, Bates BT. Effects of injury proneness and task difficulty on joint kinetic variability. Med Sci Sport Exerc 2000;32:1833–44. Jaric S, Blesic S, Milanovic S, Radovanovic S, Ljubisavljevic M, Anastasijevic R. Changes in movement final position associated with agonist and antagonist muscle fatigue. Eur J Appl Phys 2000;80:379–85. Kellis E. Quantification of quadriceps and hamstring antagonist activity. Sport Med 1998;26:37–62. Kovacs I, Tihanyi J, Devita P, Racz L, Barrier J, Hortobagyi T. Foot placement modifies kinematics and kinetics during drop jumping. Med Sci Sport Exerc 1999;31:708–16. Lafortune MA, Lake MJ, Hennig EM. Differential shock transmission response of the human body to impact severity and lower limb posture. J Biomech 1996;29:1531–7. Louw Q, Grimmer K, Vaughan C. Knee movement patterns of injured and uninjured adolescent basketball players when landing from a jump: a case-control study. BMC Musculoskel Disord 2006;7:22. Madigan M, Pidcoe P. Changes in landing biomechanics during a fatiguing landing activity. J Electromyogr Kinesiol 2003;13:491–8. McNair PJ, Prapavessis H, Callender K. Decreasing landing forces: effects of instruction. Brit J Sport Med 2000;34:293–6. McNitt-Gray J. Kinematics and impulse characteristics of drop landings from three heights. Int J Sport Biomech 1991;7:201–24. McNitt-Gray JL, Hester DM, Mathiyakom W, Munkasy BA. Mechanical demand and multijoint control during landing depend on orientation of the body segments relative to the reaction force. J Biomech 2001;34:1471–81. Nicol C, Komi P, Marconnet P. Fatigue effects of marathon running on neuromuscular performance. I. Changes in muscle force and stiffness characteristics. Scan J Med Sci Sport 1991a;1:10–7. Nicol C, Komi P, Marconnet P. Fatigue effects of marathon running on neuromuscular performance. II changes in force, integrated electromyographic activity and endurance capacity. Scan J Med Sci Sport 1991b;1:18–24. Nyland JA, Shapiro R, Stine RL, Horn TS, Ireland ML. Relationship of fatigued run and rapid stop to ground reaction forces, lower extremity kinematics, and muscle activation. J Orthop Sport Phys Ther 1994;20:132–7. Nyland J, Shapiro R, Caborn D, Nitz A, Malone T. The effect of quadriceps, hamstring, and placebo eccentric fatigue on knee and ankle dynamics during crossover cutting. J Orthop Sport Phys Ther 1997;25:171–84. Padua DA, Arnold BL, Perrin DH, Gansneder BM, Carcia CR, Granata KP. Fatigue, vertical leg stiffness, and stiffness control strategies in males and females. J Athl Train 2006;41:294–304.

64


Pettrone F, Ricciardelli E. Gymnastic injuries: the Virginia experience 1982–1983. Am J Sport Med 1987;15:59–62. Riemann BL, Lephart SM. Sensorimotor system part 1: physiological basis of joint stability. J Athl Train 2002;37:71–9. Rodacki ALF, Fowler NE, Bennet SJ. Vertical jump coordination: fatigue effects. Med Sci Sport Exerc 2002;34:105–16. Rozzi S, Lephart S, Fu F, Gear W. Effects of muscular fatigue on knee joint laxity and neuromuscular characteristics of male and female athletes. J Athl Train 1999a;34:106–14. Rozzi S, Lephart S, Gear W, Fu F. Knee joint laxity and neuromuscular characteristics of male and female soccer and basketball players. Am J Sport Med 1999b;27:312–9. Santello M, McDonagh MJN, Challis JH. Visual and non-visual control of landing movements in humans. J Physiol 2001;537(1):313–27. Solomonow M, Krogsgaard M. Sensorimotor control of knee stability: a review. Scan J Med Sci Sport 2001;11:64–80. Sparto P, Parniarpour M, Reinsel T, Simon S. The effect of fatigue on multijoint kinematics, coordination and postural stability during a repetitive lifting test. J Orthop Sport Phys Ther 1997;25: 3–12. Tillman MD, Criss RM, Brunt D, Hass CJ. Landing constraints influence ground reaction forces and lower extremity EMG in female volleyball players. J Appl Biomech 2004;20:38–51. Urabe Y, Kobayashi R, Sumida S, Tanaka K, Yoshida N, Nishiwaki GA, et al. Electromyographic analysis of the knee during jump landing in male and female athletes. Knee 2005;12:129–34. Wikstrom EA, Powers ME, Tillman MD. Dynamic stabilization time after isokinetic and functional fatigue. J Athl Train 2004;39:247–53. Wikstrom EA, Tillman MD, Kline KJ, Borsa PA. Gender and limb differences in dynamic postural stability during landing. Clin J Sport Med 2006;16:311–5.

Zhang SN, Bates BT, Dufek JS. Contributions of lower extremity joints to energy dissipation during landings. Med Sci Sport Exerc 2000;32: 812–9. Eleftherios Kellis completed his B.Ed. in Physical Education and Sport Sciences, at the Aristotle University of Thessaloniki, Greece (1993) and his Ph.D. at the Department of Movement Sciences and Physical Education, University of Liverpool, England (1996). From 1996 to 1999 he was a Lecturer in Sports Biomechanics in the Division of Sport Sciences at the University of Northumbria at Newcastle, England. In 2001, he joined the Department of Physical Education and Sports Sciences at Serres at the Aristotle University of Thessaloniki, where currently teaches statistics and biomechanics. His main research interests are in the area of muscle co-ordination via electromyography in clinical and sport applications. Vasiliki Kouvelioti completed her B.Ed. in Physical Education and Sports Sciences (2001) and received her Master degree on Exercise and Health from the Department of Physical Education and Sports Sciences at Serres, Aristotle University of Thessaloniki, Greece (2004). She is currently a Doctoral student at the same department and her main research interest is in the biomechanics of therapeutic exercises, fatigue effects on performance and clinical biomechanics applications.