Article
The Use of Hamstring Fatigue to Reduce Quadriceps Inhibition After Anterior Cruciate Ligament Reconstruction
Perceptual and Motor Skills 0(0) 1–12 ! The Author(s) 2017 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/0031512517735744 journals.sagepub.com/home/pms
Timothy Lowe1 and Xuanliang Neil Dong1
Abstract Arthrogenic muscle inhibition, an inability to fully activate the quadriceps muscles, has been persistently observed after anterior cruciate ligament reconstruction (ACLr) surgery. Reductions in quadriceps activation may be partly due to the flexion reflex pathway, hamstrings activation, and reciprocal quadriceps inhibition. Since central fatigue has been shown to modify hamstring excitability and change the hamstring reflex response, hamstring fatigue might alleviate quadriceps muscle inhibition by counteracting the flexion reflex. In this study, nine young adult athletes (age: M ¼ 19.9 years, SD ¼ 1.7) with unilateral ACLr and nine control athletes (age: M ¼ 24.0 years, SD ¼ 2.4) with no previous history of knee injury performed tempo squats to induce fatigue. The ACLr group tended to use hamstrings for more hip flexion and trunk forward flexion than the control group. We assessed each participant’s quadriceps inhibition through the central activation ratio (CAR), measured by twitch interpolation, before and after the induced fatigue. A mixed analysis of variance was used to examine the effect of fatigue on the CAR between pre- and post-fatigue and for both ACLr and control groups. The ACLr group showed significantly (p ¼ .010) greater CAR of the quadriceps post-fatigue (M ¼ 96.0%, SD ¼ 7.6%) than pre-fatigue (M ¼ 81.2%, SD ¼ 15.8%), while the control group showed no significant (p ¼ .969) pre-fatigue (M ¼ 96.9%, SD ¼ 9.6%) and postfatigue (M ¼ 97.0%, SD ¼ 17.1%) differences. Thus, fatigue training may be used as a
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Department of Health and Kinesiology, The University of Texas at Tyler, TX, USA
Corresponding Author: Xuanliang Neil Dong, Department of Health and Kinesiology, The University of Texas at Tyler, 3900 University Boulevard, Tyler, TX 75799, USA. Email: [email protected]
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rehabilitation strategy to restore normal quadriceps function at the knee joint following ACL reconstruction by relaxing the hamstrings and overcoming quadriceps inhibition. Keywords anterior cruciate ligament, fatigue, quadriceps, arthrogenic muscle inhibition, central activation ratio
Introduction Anterior cruciate ligament (ACL) injuries are among the most common lower extremity athletic injuries (Lyman et al., 2009), with more than 175,000 ACL injury cases in the United States yearly (American Orthopaedic Society for Sports Medicine, 2007; Spindler & Wright, 2008). Serious ACL injuries require surgery to restore normal knee functions, costing more than $2 billion in the United States per year (Gottlob, Baker, Pellissier, & Colvin, 1999; Spindler & Wright, 2008). Long-term effects from ACL injury changes in knee kinematics and the unloading of knee joint tissue may include early-onset posttraumatic osteoarthritis (Palmieri-Smith & Thomas, 2009). Post-ACL reconstruction (ACLr) patients shift their joint torques from the knee to the adjacent hip (Oberlander, Bruggemann, Hoher, & Karamanidis, 2012, 2013) due to arthrogenic muscle inhibition (AMI) in which they are unable to voluntarily activate all motor units in the quadriceps. The quantification of AMI can be implemented through either the burst superimposition (Hart, Pietrosimone, Hertel, & Ingersoll, 2010; Snyder-Mackler, De Luca, Williams, Eastlack, & Bartolozzi, 1994) or twitch interpolation technique (Behm, St-Pierre, & Perez, 1996; Drechsler, Cramp, & Scott, 2006; Pfeifer & Banzer, 1999; Urbach, Nebelung, Becker, & Awiszus, 2001). The central activation ratio (CAR), the percentage of the quadriceps motor neuron pool that can be volitionally activated, averages 85.0% among post-ACLr patients and 98.5% for healthy control groups, suggesting a muscle activation deficit in ACLr patients (Hart et al., 2010). Muscle inhibition in the quadriceps persists for years, even after ACLr surgery (Jones, Jones, & Newham, 1987; Rice & McNair, 2010; Snyder-Mackler et al., 1994). Posttraumatic osteoarthritis due to muscle inhibition poses a particular clinical challenge for younger patients for whom total knee joint replacement is neither appropriate nor acceptable (Palmieri-Smith & Thomas, 2009). Thus, any rehabilitation strategies to overcome quadriceps muscle inhibition hold promise for restoring normal joint mechanics and slowing down the onset of posttraumatic osteoarthritis in younger patients. Although the underlying mechanism for AMI is not clearly understood, it is generally accepted that AMI may stem from changes in discharges of sensory
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receptors in the injured knee joint (Behm et al., 1996; Drechsler et al., 2006; Hart et al., 2010; Snyder-Mackler et al., 1994). Factors such as swelling, inflammation, joint laxity, and a loss of output from articular sensory receptors may cause these afferent discharge changes (Rice & McNair, 2010), and changed joint afferent discharges may, in turn, greatly increase the excitability of certain central nervous system (CNS) pathways, such as flexion reflex (Rice, McNair, Lewis, & Dalbeth, 2015). Flexion reflex involves the facilitation of flexor muscles, such as hamstrings, and the reciprocal inhibition of extensor muscles, such as quadriceps (Solomonow, Baratta, & D’Ambrosia, 1989; Solomonow et al., 1987; Stokes & Young, 1984; Young, 1993). Solomonow et al. (1987, 1989) have proposed a flex arc between the ACL and hamstrings. Animal studies in cats and rats have also shown that the CNS receives excitatory sensory input from joint afferent discharges and then enhances flexion reflex excitability (Ferrell, Wood, & Baxendale, 1988; Rice et al., 2015; Schaible, Schmidt, & Willis, 1986; Woolf & Wall, 1986). If CNS-mediated hamstring excitability can be lessened, the inhibition of quadriceps may be suppressed. Muscle fatigue, the inability to maintain a desired force output (Basmajian & De Luca, 1985), has been shown to modify hamstring excitability and change the hamstring reflex response (Behrens et al., 2015; Melnyk & Gollhofer, 2007; Wojtys, Wylie, & Huston, 1996). Therefore, we hypothesized that inducing hamstring muscle fatigue might be a means of counteracting the flexion reflex pathway and alleviating the quadriceps muscle inhibition. To test this hypothesis, we assessed the effect of fatigue on the CAR of quadriceps muscles in young athletes with ACLr and compared them with a control group of young adults with no previous history of knee injury.
Method Participants Through convenience sampling, we recruited nine adult athletes (age: M ¼ 19.9 years, SD ¼ 1.7; six males, three females; Table 1) who had undergone unilateral ACLr. All subjects sustained their injuries during high performance in sports, including football (four), basketball (three), soccer (one), and volleyball (one). The average post-surgery time for subjects with ACLr was 17.6 months (range: 5–54 months, SD ¼ 15.9). We also recruited nine athletes (age: M ¼ 24.0 years, SD ¼ 2.4; five males, four females; Table 1) with no previous history of knee injury as a control group. Control group participants had played sports such as basketball, soccer, and baseball. All experimental procedures were approved by the institutional review board from the participating institution. All participants gave informed written consent prior to testing.
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Table 1. Descriptive Statistics (Mean SD) of ACLr and Control Groups.
ACLr (n ¼ 9) Control (n ¼ 9)
Age (years)
Height (cm)
Weight (kg)
BMI (kg/m2)
19.9 1.7 24.0 2.4
184.2 9.3 176.3 10.6
93.9 15.9 84.2 17.2
27.6 3.4 26.9 4.0
Note. ACLr ¼ anterior cruciate ligament reconstruction; BMI ¼ body mass index.
Central Activation Ratio Each participant’s quadricepts inhibition was measured through the CAR before and after fatigue inducement. The CAR was measured by comparing the force produced by the quadriceps from a maximal voluntary contraction (MVC) and the force from an interpolated twitch which electrically stimulated the nerve to fully activate the quadriceps muscle during an MVC (Behm, Power, & Drinkwater, 2001; Behm et al., 1996; Drechsler et al., 2006). We used the interpolated twitch technique rather than the burst superimposition method in which electrical stimulation is delivered percutaneously to the muscles, since a confounding factor for the burst superimposition technique is that the skin and subcutaneous tissues must be penetrated by electrical stimulation to recruit all motor neurons (Park & Hopkins, 2011). In this study, the maximal isometric quadriceps extension force was measured through a chair built for this (Figure 1(a)). The participant was seated upright with knee and hips flexed at 90 . A Velcro strap, attached by a hightension wire to a load cell (LCCA 200; Omega Engineering Inc., Stamford, CT), was placed approximately 2 in. above the malleolus of each participant. The participant was first asked to perform an MVC of the quadriceps and the force was measured by the load cell attached to the chair (Figure 1(b)). Then, a 2-Hz, single square wave stimuli of 0.3 ms duration was given to the intramuscular branches of the femoral nerve using two electrodes placed on the proximal and distal portions of the rectus femoris and a portable electrical stimulator (Empi 300PV; Empi, CA, USA). The portable electrical stimulator (Empi 300PV) has been shown to produce adequate force for the quadriceps femoris muscle and to be comparable to a clinical electrical stimulator, VersaStim 380 (Lyons, Robb, Irrgang, & Fitzgerald, 2005). In each testing session, the particpants performed three or more MVCs (5-s duration) of the quadriceps femoris, with a 2-min rest period between each MVC (Drechsler et al., 2006). For each MVC, consistent instruction and verbal encouragement were given to push as hard as possible against the resistance pad. The first two MVCs were trial attempts, undertaken without stimulation. On the third occasion, the portable electrical stimulator delivered 2-Hz stimuli for 5 seconds to the relaxed muscle; the participant then performed an MVC (Drechsler et al.,
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(a)
(b) E-Sm
10.0
EMG
0.0
Volts
EMG
5.0
-5.0
380.0
Load Cell
Steel Wire
FMVC
FIT
Velcro Strap
180.0
N
Force
280.0
80.0 -20.0 10.0
80.0
150.0 seconds
220.0
Figure 1. (a) A custom-built chair to measure the isometric quadriceps extension force through a load cell connecting to a steel wire and a Velcro strap, a portable electrical stimulator was used to provide an interpolated twitch, and electromyography (EMG) was used to monitor electrical activity of the quadriceps muscles. (b) Superimposition of an interpolated twitch during a voluntary contraction to estimate the central activation ratio, FMVC was the extension force of the quadriceps muscles during the MVC, and FIT was the force produced during the interpolated twitch with the MVC. MVC ¼ maximal voluntary contraction.
2006). The CAR was calculated from the MVC force, first without and then with stimulation, using the following equation: CAR ¼ 100
FIT FMVC 100 FMVC
ð1Þ
where FMVC is the force produced during the MVC without stimulation and FIT is the force produced from the MVC with the twitch interpolation (Figure 1(b)). We measured CARs of the quadriceps muscles for both ACLr and control groups before and after the fatigue inducement protocol.
Fatigue Inducement Protocol After a 5-minute warm-up exercise of between 70 and 80 revolutions per minute (rpm) with low resistance on a cycle ergometer (Ergomedic 894E Peak Bike; Monar, Sweden), participants were instructed to perform tempo squats to a height of approximately 0.45 meters from the ground at the rate of one squat every 2 seconds until participants rating of perceived exertion (RPE) was 15 out
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of 20, or ‘‘hard.’’ In addition, we monitored the participant’s heart rate (using Biosig Instruments, Insta-heart rate monitor 105). Subjects were considered fatigued when their RPE reached 15 and their heart rate was approximately 150 beats per minute. The mean number of tempo squats performed by the ACLr and control groups was 134 (SD ¼ 36) and 153 (SD ¼ 40), respectively.
Statistical Analyses A mixed-design analysis of variance was used to compare ACLr and control groups on repeated measures differences for pre- and post-fatigue CARs of the quadriceps. The two independent variables were pre- or post-fatigue and ACLr or control group participants. Statistical analyses were performed using SPSS statistical software (version 20, IBM, Armonk, NY). An a level of .05 was used to indicate statistical significance for all comparisons.
Results On pre-fatigue trials, the ACLr group showed a statistically nonsignificant trend toward less CAR than the control group (M ¼ 81.2%, SD ¼ 15.8% vs. M ¼ 97.0%, SD ¼ 17.1%, p ¼ .067). On post-fatigue trials, there were no significant CAR differences between ACLr and control groups (M ¼ 96.0%, SD ¼ 7.6% vs. M ¼ 96.9%, SD ¼ 9.6%, p ¼ .838). With regard to pre- and post-fatigue group differences, there was a significant interaction between fatigue status (pre-fatigue vs. post-fatigue) and group membership (ACLr vs. control), F(1, 15) ¼ 4.75, p ¼ .046. Simple main effects were used to examine the effect of one independent variable (fatigue status) within each level of a second independent variable (participant group). The CAR of the quadriceps of the ACLr group was significantly higher (p ¼ .010, Figure 2), postfatigue (M ¼ 96.0%, SD ¼ 7.6%) versus pre-fatigue (M ¼ 81.2%, SD ¼ 15.8%), while there was no significant difference (p ¼ .969) between the quadriceps CAR of the control group, pre-fatigue (M ¼ 97.0%, SD ¼ 17.1%) and post-fatigue (M ¼ 96.9%, SD ¼ 9.6%).
Discussion This study sought to determine whether induced hamstring fatigue might represent a rehabilitation strategy for alleviating problematic quadriceps muscle inhibition following ACLr, associated with joint movement shifting (knee to hip) and long-term adverse effects, particularly among young athletes with ACL injuries. We found a pre-fatigue, nonsignificant trend toward higher quadriceps CAR among ACLr versus control participants, suggesting possible evidence of AMI in the quadriceps of the participants in the ACLr group, although this trend will require more definitive replication with a larger sample.
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Pre Fatigue
140 120
*
Post Fatigue
p=0.010
CAR(%)
100 80 60 40 20 0 ACLr
Control
Figure 2. Comparison of central activiation ratios (CAR) for the ACLr group and control group before and after fatigue. The CAR was significantly (p ¼ .007) different between preand postfatigue for ACLr group but not for the control group (p ¼ .969). ACLr ¼ anterior cruciate ligament reconstruction.
Importantly, significant group differences in pre- and post-fatigue CAR with greater reduction in quadriceps muscle inhibition in the ACLr group, relative to the control group, affirm our hypothesis that our hamstring fatigue-inducement protocol was an effective rehabilitation treatment. Returning to our finding of a nonsignificant trend toward greater pre-fatigue muscle inhibition in the quadriceps muscles of the ACLr group relative to the control group (CAR: M ¼ 81.2%, SD ¼ 15.8% and CAR: M ¼ 97.0%, SD ¼ 17.1%, respectively), our small group samples (nine participants per group) probably left our study statistically underpowered, suggesting that future studies with larger samples may redress this limitation and reveal statistically significant group differences; indeed, prior studies have quantified muscle inhibition with this CAR method (Behm et al., 1996; Drechsler et al., 2006; Pfeifer & Banzer, 1999; Urbach et al., 2001), and one reported that CARs of the quadriceps were lower in an ACLr group (M ¼ 74.9%, SD ¼ 3.5%) relative to a healthy control group (M ¼ 91%, SD ¼ 0.9%; Urbach et al., 2001). Again, of most importance, our study showed that ACLr participants had significantly higher CARs in the quadriceps post- versus pre-fatigue in our protocol (Figure 2), demonstrating that the induced hamstring fatigue alleviated quadricep muscle by more muscle recruitment. As this finding was not evident among healthy control participants, induced hamstring fatigue appears to be an effective rehabilitation strategy for ACLr patients. This approach was able to change problematic muscle inhibition of quadriceps muscles in ACLr participants through the spinal reflex pathway (Rice et al., 2015; Snyder-Mackler et al.,
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1994; Stokes & Young, 1984; Young, 1993). Of note, as previously reported (Kuenze, Hertel, & Hart, 2013; McHugh, Tyler, Nicholas, Browne, & Gleim, 2001; Snyder-Mackler et al., 1993), ACLr subjects have greater fatigability compared with healthy controls, perhaps due to selective atrophy of fast twitch fibers during prolonged exercise since lower initial median frequency and smaller decline in median frequency were observed in EMG analysis of quadriceps fatigue after ACL reconstruction (McHugh et al., 2001). ACLr patients adapt by partially transferring the load at the knee to the hip, modifying their posture throughout the movement (Oberlander et al., 2012, 2013). This adaptation may help maintain lower extremity function during prolonged exercise (Gokeler et al., 2014; Kuenze et al., 2013). In support of this theorized adaption, during our fatigue protocol, we observed that ACLr participants tended to lean their trunk forward, rather than hold it erect, while performing squats (Figure 3). When an individual performs a squat with the trunk kept relatively erect (Figure 3(a)), there are larger external flexion torques at the knee than at the hip (Oatis, 2016). On the other hand, leaning the trunk
(a)
(b)
Figure 3. External flexion torques are created at both the hip and knee during a squat. (a) When the trunk is held upright, the moment arm is longer at the knee than at the hip; consequently, the external flexion torque is greater at the knee. (b) When the trunk leans forward, the moment arm decreases at the knee and increases at the hip; therefore, the external flexion torque is greater at the hip.
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forward during the squat moves the center of mass of the head, arms, and trunk anteriorly and changes the moment arm (Figure 3(b)). The external flexion torques increase at the hip and decrease at the knee because of changes in the length of moment arms at the hip and knee. Decreasing the external flexion torque at the knee requires less quadriceps force and puts less stress on the ACL. This may be the adaptation experienced by subjects with quadriceps inhibition after ACLr. Meanwhile, an increased external flexion torque at the hip requires the additional use of hamstrings muscles for ACLr participants. After the fatigue protocol, our ACLr participants were no longer able to use the hamstring muscles to compensate because of hamstring fatigue. Hamstring fatigue may then counteract the inhibition of quadriceps muscles with likely involvement of the flexion reflex pathway (Rice et al., 2015; Snyder-Mackler et al., 1994; Stokes & Young, 1984; Young, 1993). In the absence of hamstring muscle activity, more motor units in the quadriceps are activated, as reflected by the higher post-fatigue CAR of the quadriceps observed among ACLr but not control participants. Among several study limitations was the aforementioned small sample size that likely left this study statistically underpowered for clearly demonstrating greater quadriceps muscle inhibition for the ACLr group. As noted, future studies should utilize larger samples and random sampling that might also permit comparisons of male and female and older and younger participants. Second, we did not differentiate the choice of graft material for ACL reconstruction in this study. Patellar tendon and hamstring tendon were two major types of replacement materials for ACLr surgery (Magnussen, Carey, & Spindler, 2011; Pinczewski, Deehan, Salmon, Russell, & Clingeleffer, 2002; Xergia, McClelland, Kvist, Vasiliadis, & Georgoulis, 2011). Future studies might compare the effects of fatigue training on muscle inhibition in ACLr participants with patellar tendon and hamstring tendon grafts. Despite its limitations, our study suggested possible greater quadriceps muscle inhibition in the ACLr group relative to controls before fatigue trials as might be expected. Of most importance, following hamstring fatigue trials, our ACLr group showed at least temporary alleviation of problematic quadriceps muscle inhibition, supporting our hypothesis and providing critical support for a promising new rehabilitation strategy for restoring normal quadriceps functioning at the knee joint following ACL reconstruction by overcoming quadriceps muscle inhibition and recruiting more quadricep motor units. Acknowledgment The authors gratefully acknowledge the editorial contributions of J. D. Ball, PhD.
Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
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Funding The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by an Academic Year Research Award from The University of Texas at Tyler.
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Magnussen, R. A., Carey, J. L., & Spindler, K. P. (2011). Does autograft choice determine intermediate-term outcome of ACL reconstruction? Knee Surgery Sports Traumatology Arthroscopy, 19(3), 462–472. McHugh, M. P., Tyler, T. F., Nicholas, S. J., Browne, M. G., & Gleim, G. W. (2001). Electromyographic analysis of quadriceps fatigue after anterior cruciate ligament reconstruction. Journal of Orthopaedic & Sports Physical Therapy, 31(1), 25–32. Melnyk, M., & Gollhofer, A. (2007). Submaximal fatigue of the hamstrings impairs specific reflex components and knee stability. Knee Surgery, Sports Traumatology, Arthroscopy, 15(5), 525–532. Oatis, C. A. (2016). Kinesiology: The mechanics and pathomechanics of human movement. Baltimore, MD: Lippincott Williams and Wilkins. Oberlander, K. D., Bruggemann, G. P., Hoher, J., & Karamanidis, K. (2012). Reduced knee joint moment in ACL deficient patients at a cost of dynamic stability during landing. Journal of Biomechanics, 45(8), 1387–1392. Oberlander, K. D., Bruggemann, G. P., Hoher, J., & Karamanidis, K. (2013). Altered landing mechanics in ACL-reconstructed patients. Medicine and Science in Sports and Exercise, 45(3), 506–513. Palmieri-Smith, R. M., & Thomas, A. C. (2009). A neuromuscular mechanism of posttraumatic osteoarthritis associated with ACL injury. Exercise and Sports Sciences Reviews, 37(3), 147–153. Park, J., & Hopkins, J. T. (2011). Quadriceps activation normative values and the affect of subcutaneous tissue thickness. Journal of Electromyography and Kinesiology, 21, 136–140. Pfeifer, K., & Banzer, W. (1999). Motor performance in different dynamic tests in knee rehabilitation. Scandinavian Journal of Medicine & Science in Sports, 9(1), 19–27. Pinczewski, L. A., Deehan, D. J., Salmon, L. J., Russell, V. J., & Clingeleffer, A. (2002). A five-year comparison of patellar tendon versus four-strand hamstring tendon autograft for arthroscopic reconstruction of the anterior cruciate ligament. The American Journal of Sports Medicine, 30(4), 523–536. Rice, D. A., & McNair, P. J. (2010). Quadriceps arthrogenic muscle inhibition: Neural mechanisms and treatment perspectives. Seminars in Arthritis and Rheumatism, 40(3), 250–266. Rice, D. A., McNair, P. J., Lewis, G. N., & Dalbeth, N. (2015). The effects of joint aspiration and intra-articular corticosteroid injection on flexion reflex excitability, quadriceps strength and pain in individuals with knee synovitis: A prospective observational study. Arthritis Research & Therapy, 17, 191. Schaible, H. G., Schmidt, R. F., & Willis, W. D. (1986). Responses of spinal cord neurones to stimulation of articular afferent fibres in the cat. Journal of Physiology, 372, 575–593. Snyder-Mackler, L., Binder-Macleod, S. A., & Williams, P. R. (1993). Fatigability of human quadriceps femoris muscle following anterior cruciate ligament reconstruction. Medicine & Science in Sports & Exercise, 25(7), 783–789. Snyder-Mackler, L., De Luca, P. F., Williams, P. R., Eastlack, M. E., & Bartolozzi, A. R. III (1994). Reflex inhibition of the quadriceps femoris muscle after injury or reconstruction of the anterior cruciate ligament. Journal of Bone & Joint Surgery American Volume, 76(4), 555–560.
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Author Biographies Timothy Lowe is currently a Lecturer at the University of Texas at Tyler. He received his Master’s from the University of Texas at Tyler. Xuanliang Neil Dong is currently a Professor of Health and Kinesiology at The University of Texas at Tyler. He received his PhD degree from Columbia University. Dr. Dong is interested in neuromuscular training strategies for prevention and treatment of knee joint injuries in athletes.
The Use of Hamstring Fatigue to Reduce Quadriceps Inhibition After Anterior Cruciate Ligament Reconstruction
Perceptual and Motor Skills 0(0) 1–12 ! The Author(s) 2017 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/0031512517735744 journals.sagepub.com/home/pms
Timothy Lowe1 and Xuanliang Neil Dong1
Abstract Arthrogenic muscle inhibition, an inability to fully activate the quadriceps muscles, has been persistently observed after anterior cruciate ligament reconstruction (ACLr) surgery. Reductions in quadriceps activation may be partly due to the flexion reflex pathway, hamstrings activation, and reciprocal quadriceps inhibition. Since central fatigue has been shown to modify hamstring excitability and change the hamstring reflex response, hamstring fatigue might alleviate quadriceps muscle inhibition by counteracting the flexion reflex. In this study, nine young adult athletes (age: M ¼ 19.9 years, SD ¼ 1.7) with unilateral ACLr and nine control athletes (age: M ¼ 24.0 years, SD ¼ 2.4) with no previous history of knee injury performed tempo squats to induce fatigue. The ACLr group tended to use hamstrings for more hip flexion and trunk forward flexion than the control group. We assessed each participant’s quadriceps inhibition through the central activation ratio (CAR), measured by twitch interpolation, before and after the induced fatigue. A mixed analysis of variance was used to examine the effect of fatigue on the CAR between pre- and post-fatigue and for both ACLr and control groups. The ACLr group showed significantly (p ¼ .010) greater CAR of the quadriceps post-fatigue (M ¼ 96.0%, SD ¼ 7.6%) than pre-fatigue (M ¼ 81.2%, SD ¼ 15.8%), while the control group showed no significant (p ¼ .969) pre-fatigue (M ¼ 96.9%, SD ¼ 9.6%) and postfatigue (M ¼ 97.0%, SD ¼ 17.1%) differences. Thus, fatigue training may be used as a
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Department of Health and Kinesiology, The University of Texas at Tyler, TX, USA
Corresponding Author: Xuanliang Neil Dong, Department of Health and Kinesiology, The University of Texas at Tyler, 3900 University Boulevard, Tyler, TX 75799, USA. Email: [email protected]
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rehabilitation strategy to restore normal quadriceps function at the knee joint following ACL reconstruction by relaxing the hamstrings and overcoming quadriceps inhibition. Keywords anterior cruciate ligament, fatigue, quadriceps, arthrogenic muscle inhibition, central activation ratio
Introduction Anterior cruciate ligament (ACL) injuries are among the most common lower extremity athletic injuries (Lyman et al., 2009), with more than 175,000 ACL injury cases in the United States yearly (American Orthopaedic Society for Sports Medicine, 2007; Spindler & Wright, 2008). Serious ACL injuries require surgery to restore normal knee functions, costing more than $2 billion in the United States per year (Gottlob, Baker, Pellissier, & Colvin, 1999; Spindler & Wright, 2008). Long-term effects from ACL injury changes in knee kinematics and the unloading of knee joint tissue may include early-onset posttraumatic osteoarthritis (Palmieri-Smith & Thomas, 2009). Post-ACL reconstruction (ACLr) patients shift their joint torques from the knee to the adjacent hip (Oberlander, Bruggemann, Hoher, & Karamanidis, 2012, 2013) due to arthrogenic muscle inhibition (AMI) in which they are unable to voluntarily activate all motor units in the quadriceps. The quantification of AMI can be implemented through either the burst superimposition (Hart, Pietrosimone, Hertel, & Ingersoll, 2010; Snyder-Mackler, De Luca, Williams, Eastlack, & Bartolozzi, 1994) or twitch interpolation technique (Behm, St-Pierre, & Perez, 1996; Drechsler, Cramp, & Scott, 2006; Pfeifer & Banzer, 1999; Urbach, Nebelung, Becker, & Awiszus, 2001). The central activation ratio (CAR), the percentage of the quadriceps motor neuron pool that can be volitionally activated, averages 85.0% among post-ACLr patients and 98.5% for healthy control groups, suggesting a muscle activation deficit in ACLr patients (Hart et al., 2010). Muscle inhibition in the quadriceps persists for years, even after ACLr surgery (Jones, Jones, & Newham, 1987; Rice & McNair, 2010; Snyder-Mackler et al., 1994). Posttraumatic osteoarthritis due to muscle inhibition poses a particular clinical challenge for younger patients for whom total knee joint replacement is neither appropriate nor acceptable (Palmieri-Smith & Thomas, 2009). Thus, any rehabilitation strategies to overcome quadriceps muscle inhibition hold promise for restoring normal joint mechanics and slowing down the onset of posttraumatic osteoarthritis in younger patients. Although the underlying mechanism for AMI is not clearly understood, it is generally accepted that AMI may stem from changes in discharges of sensory
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receptors in the injured knee joint (Behm et al., 1996; Drechsler et al., 2006; Hart et al., 2010; Snyder-Mackler et al., 1994). Factors such as swelling, inflammation, joint laxity, and a loss of output from articular sensory receptors may cause these afferent discharge changes (Rice & McNair, 2010), and changed joint afferent discharges may, in turn, greatly increase the excitability of certain central nervous system (CNS) pathways, such as flexion reflex (Rice, McNair, Lewis, & Dalbeth, 2015). Flexion reflex involves the facilitation of flexor muscles, such as hamstrings, and the reciprocal inhibition of extensor muscles, such as quadriceps (Solomonow, Baratta, & D’Ambrosia, 1989; Solomonow et al., 1987; Stokes & Young, 1984; Young, 1993). Solomonow et al. (1987, 1989) have proposed a flex arc between the ACL and hamstrings. Animal studies in cats and rats have also shown that the CNS receives excitatory sensory input from joint afferent discharges and then enhances flexion reflex excitability (Ferrell, Wood, & Baxendale, 1988; Rice et al., 2015; Schaible, Schmidt, & Willis, 1986; Woolf & Wall, 1986). If CNS-mediated hamstring excitability can be lessened, the inhibition of quadriceps may be suppressed. Muscle fatigue, the inability to maintain a desired force output (Basmajian & De Luca, 1985), has been shown to modify hamstring excitability and change the hamstring reflex response (Behrens et al., 2015; Melnyk & Gollhofer, 2007; Wojtys, Wylie, & Huston, 1996). Therefore, we hypothesized that inducing hamstring muscle fatigue might be a means of counteracting the flexion reflex pathway and alleviating the quadriceps muscle inhibition. To test this hypothesis, we assessed the effect of fatigue on the CAR of quadriceps muscles in young athletes with ACLr and compared them with a control group of young adults with no previous history of knee injury.
Method Participants Through convenience sampling, we recruited nine adult athletes (age: M ¼ 19.9 years, SD ¼ 1.7; six males, three females; Table 1) who had undergone unilateral ACLr. All subjects sustained their injuries during high performance in sports, including football (four), basketball (three), soccer (one), and volleyball (one). The average post-surgery time for subjects with ACLr was 17.6 months (range: 5–54 months, SD ¼ 15.9). We also recruited nine athletes (age: M ¼ 24.0 years, SD ¼ 2.4; five males, four females; Table 1) with no previous history of knee injury as a control group. Control group participants had played sports such as basketball, soccer, and baseball. All experimental procedures were approved by the institutional review board from the participating institution. All participants gave informed written consent prior to testing.
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Table 1. Descriptive Statistics (Mean SD) of ACLr and Control Groups.
ACLr (n ¼ 9) Control (n ¼ 9)
Age (years)
Height (cm)
Weight (kg)
BMI (kg/m2)
19.9 1.7 24.0 2.4
184.2 9.3 176.3 10.6
93.9 15.9 84.2 17.2
27.6 3.4 26.9 4.0
Note. ACLr ¼ anterior cruciate ligament reconstruction; BMI ¼ body mass index.
Central Activation Ratio Each participant’s quadricepts inhibition was measured through the CAR before and after fatigue inducement. The CAR was measured by comparing the force produced by the quadriceps from a maximal voluntary contraction (MVC) and the force from an interpolated twitch which electrically stimulated the nerve to fully activate the quadriceps muscle during an MVC (Behm, Power, & Drinkwater, 2001; Behm et al., 1996; Drechsler et al., 2006). We used the interpolated twitch technique rather than the burst superimposition method in which electrical stimulation is delivered percutaneously to the muscles, since a confounding factor for the burst superimposition technique is that the skin and subcutaneous tissues must be penetrated by electrical stimulation to recruit all motor neurons (Park & Hopkins, 2011). In this study, the maximal isometric quadriceps extension force was measured through a chair built for this (Figure 1(a)). The participant was seated upright with knee and hips flexed at 90 . A Velcro strap, attached by a hightension wire to a load cell (LCCA 200; Omega Engineering Inc., Stamford, CT), was placed approximately 2 in. above the malleolus of each participant. The participant was first asked to perform an MVC of the quadriceps and the force was measured by the load cell attached to the chair (Figure 1(b)). Then, a 2-Hz, single square wave stimuli of 0.3 ms duration was given to the intramuscular branches of the femoral nerve using two electrodes placed on the proximal and distal portions of the rectus femoris and a portable electrical stimulator (Empi 300PV; Empi, CA, USA). The portable electrical stimulator (Empi 300PV) has been shown to produce adequate force for the quadriceps femoris muscle and to be comparable to a clinical electrical stimulator, VersaStim 380 (Lyons, Robb, Irrgang, & Fitzgerald, 2005). In each testing session, the particpants performed three or more MVCs (5-s duration) of the quadriceps femoris, with a 2-min rest period between each MVC (Drechsler et al., 2006). For each MVC, consistent instruction and verbal encouragement were given to push as hard as possible against the resistance pad. The first two MVCs were trial attempts, undertaken without stimulation. On the third occasion, the portable electrical stimulator delivered 2-Hz stimuli for 5 seconds to the relaxed muscle; the participant then performed an MVC (Drechsler et al.,
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(a)
(b) E-Sm
10.0
EMG
0.0
Volts
EMG
5.0
-5.0
380.0
Load Cell
Steel Wire
FMVC
FIT
Velcro Strap
180.0
N
Force
280.0
80.0 -20.0 10.0
80.0
150.0 seconds
220.0
Figure 1. (a) A custom-built chair to measure the isometric quadriceps extension force through a load cell connecting to a steel wire and a Velcro strap, a portable electrical stimulator was used to provide an interpolated twitch, and electromyography (EMG) was used to monitor electrical activity of the quadriceps muscles. (b) Superimposition of an interpolated twitch during a voluntary contraction to estimate the central activation ratio, FMVC was the extension force of the quadriceps muscles during the MVC, and FIT was the force produced during the interpolated twitch with the MVC. MVC ¼ maximal voluntary contraction.
2006). The CAR was calculated from the MVC force, first without and then with stimulation, using the following equation: CAR ¼ 100
FIT FMVC 100 FMVC
ð1Þ
where FMVC is the force produced during the MVC without stimulation and FIT is the force produced from the MVC with the twitch interpolation (Figure 1(b)). We measured CARs of the quadriceps muscles for both ACLr and control groups before and after the fatigue inducement protocol.
Fatigue Inducement Protocol After a 5-minute warm-up exercise of between 70 and 80 revolutions per minute (rpm) with low resistance on a cycle ergometer (Ergomedic 894E Peak Bike; Monar, Sweden), participants were instructed to perform tempo squats to a height of approximately 0.45 meters from the ground at the rate of one squat every 2 seconds until participants rating of perceived exertion (RPE) was 15 out
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of 20, or ‘‘hard.’’ In addition, we monitored the participant’s heart rate (using Biosig Instruments, Insta-heart rate monitor 105). Subjects were considered fatigued when their RPE reached 15 and their heart rate was approximately 150 beats per minute. The mean number of tempo squats performed by the ACLr and control groups was 134 (SD ¼ 36) and 153 (SD ¼ 40), respectively.
Statistical Analyses A mixed-design analysis of variance was used to compare ACLr and control groups on repeated measures differences for pre- and post-fatigue CARs of the quadriceps. The two independent variables were pre- or post-fatigue and ACLr or control group participants. Statistical analyses were performed using SPSS statistical software (version 20, IBM, Armonk, NY). An a level of .05 was used to indicate statistical significance for all comparisons.
Results On pre-fatigue trials, the ACLr group showed a statistically nonsignificant trend toward less CAR than the control group (M ¼ 81.2%, SD ¼ 15.8% vs. M ¼ 97.0%, SD ¼ 17.1%, p ¼ .067). On post-fatigue trials, there were no significant CAR differences between ACLr and control groups (M ¼ 96.0%, SD ¼ 7.6% vs. M ¼ 96.9%, SD ¼ 9.6%, p ¼ .838). With regard to pre- and post-fatigue group differences, there was a significant interaction between fatigue status (pre-fatigue vs. post-fatigue) and group membership (ACLr vs. control), F(1, 15) ¼ 4.75, p ¼ .046. Simple main effects were used to examine the effect of one independent variable (fatigue status) within each level of a second independent variable (participant group). The CAR of the quadriceps of the ACLr group was significantly higher (p ¼ .010, Figure 2), postfatigue (M ¼ 96.0%, SD ¼ 7.6%) versus pre-fatigue (M ¼ 81.2%, SD ¼ 15.8%), while there was no significant difference (p ¼ .969) between the quadriceps CAR of the control group, pre-fatigue (M ¼ 97.0%, SD ¼ 17.1%) and post-fatigue (M ¼ 96.9%, SD ¼ 9.6%).
Discussion This study sought to determine whether induced hamstring fatigue might represent a rehabilitation strategy for alleviating problematic quadriceps muscle inhibition following ACLr, associated with joint movement shifting (knee to hip) and long-term adverse effects, particularly among young athletes with ACL injuries. We found a pre-fatigue, nonsignificant trend toward higher quadriceps CAR among ACLr versus control participants, suggesting possible evidence of AMI in the quadriceps of the participants in the ACLr group, although this trend will require more definitive replication with a larger sample.
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Pre Fatigue
140 120
*
Post Fatigue
p=0.010
CAR(%)
100 80 60 40 20 0 ACLr
Control
Figure 2. Comparison of central activiation ratios (CAR) for the ACLr group and control group before and after fatigue. The CAR was significantly (p ¼ .007) different between preand postfatigue for ACLr group but not for the control group (p ¼ .969). ACLr ¼ anterior cruciate ligament reconstruction.
Importantly, significant group differences in pre- and post-fatigue CAR with greater reduction in quadriceps muscle inhibition in the ACLr group, relative to the control group, affirm our hypothesis that our hamstring fatigue-inducement protocol was an effective rehabilitation treatment. Returning to our finding of a nonsignificant trend toward greater pre-fatigue muscle inhibition in the quadriceps muscles of the ACLr group relative to the control group (CAR: M ¼ 81.2%, SD ¼ 15.8% and CAR: M ¼ 97.0%, SD ¼ 17.1%, respectively), our small group samples (nine participants per group) probably left our study statistically underpowered, suggesting that future studies with larger samples may redress this limitation and reveal statistically significant group differences; indeed, prior studies have quantified muscle inhibition with this CAR method (Behm et al., 1996; Drechsler et al., 2006; Pfeifer & Banzer, 1999; Urbach et al., 2001), and one reported that CARs of the quadriceps were lower in an ACLr group (M ¼ 74.9%, SD ¼ 3.5%) relative to a healthy control group (M ¼ 91%, SD ¼ 0.9%; Urbach et al., 2001). Again, of most importance, our study showed that ACLr participants had significantly higher CARs in the quadriceps post- versus pre-fatigue in our protocol (Figure 2), demonstrating that the induced hamstring fatigue alleviated quadricep muscle by more muscle recruitment. As this finding was not evident among healthy control participants, induced hamstring fatigue appears to be an effective rehabilitation strategy for ACLr patients. This approach was able to change problematic muscle inhibition of quadriceps muscles in ACLr participants through the spinal reflex pathway (Rice et al., 2015; Snyder-Mackler et al.,
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1994; Stokes & Young, 1984; Young, 1993). Of note, as previously reported (Kuenze, Hertel, & Hart, 2013; McHugh, Tyler, Nicholas, Browne, & Gleim, 2001; Snyder-Mackler et al., 1993), ACLr subjects have greater fatigability compared with healthy controls, perhaps due to selective atrophy of fast twitch fibers during prolonged exercise since lower initial median frequency and smaller decline in median frequency were observed in EMG analysis of quadriceps fatigue after ACL reconstruction (McHugh et al., 2001). ACLr patients adapt by partially transferring the load at the knee to the hip, modifying their posture throughout the movement (Oberlander et al., 2012, 2013). This adaptation may help maintain lower extremity function during prolonged exercise (Gokeler et al., 2014; Kuenze et al., 2013). In support of this theorized adaption, during our fatigue protocol, we observed that ACLr participants tended to lean their trunk forward, rather than hold it erect, while performing squats (Figure 3). When an individual performs a squat with the trunk kept relatively erect (Figure 3(a)), there are larger external flexion torques at the knee than at the hip (Oatis, 2016). On the other hand, leaning the trunk
(a)
(b)
Figure 3. External flexion torques are created at both the hip and knee during a squat. (a) When the trunk is held upright, the moment arm is longer at the knee than at the hip; consequently, the external flexion torque is greater at the knee. (b) When the trunk leans forward, the moment arm decreases at the knee and increases at the hip; therefore, the external flexion torque is greater at the hip.
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forward during the squat moves the center of mass of the head, arms, and trunk anteriorly and changes the moment arm (Figure 3(b)). The external flexion torques increase at the hip and decrease at the knee because of changes in the length of moment arms at the hip and knee. Decreasing the external flexion torque at the knee requires less quadriceps force and puts less stress on the ACL. This may be the adaptation experienced by subjects with quadriceps inhibition after ACLr. Meanwhile, an increased external flexion torque at the hip requires the additional use of hamstrings muscles for ACLr participants. After the fatigue protocol, our ACLr participants were no longer able to use the hamstring muscles to compensate because of hamstring fatigue. Hamstring fatigue may then counteract the inhibition of quadriceps muscles with likely involvement of the flexion reflex pathway (Rice et al., 2015; Snyder-Mackler et al., 1994; Stokes & Young, 1984; Young, 1993). In the absence of hamstring muscle activity, more motor units in the quadriceps are activated, as reflected by the higher post-fatigue CAR of the quadriceps observed among ACLr but not control participants. Among several study limitations was the aforementioned small sample size that likely left this study statistically underpowered for clearly demonstrating greater quadriceps muscle inhibition for the ACLr group. As noted, future studies should utilize larger samples and random sampling that might also permit comparisons of male and female and older and younger participants. Second, we did not differentiate the choice of graft material for ACL reconstruction in this study. Patellar tendon and hamstring tendon were two major types of replacement materials for ACLr surgery (Magnussen, Carey, & Spindler, 2011; Pinczewski, Deehan, Salmon, Russell, & Clingeleffer, 2002; Xergia, McClelland, Kvist, Vasiliadis, & Georgoulis, 2011). Future studies might compare the effects of fatigue training on muscle inhibition in ACLr participants with patellar tendon and hamstring tendon grafts. Despite its limitations, our study suggested possible greater quadriceps muscle inhibition in the ACLr group relative to controls before fatigue trials as might be expected. Of most importance, following hamstring fatigue trials, our ACLr group showed at least temporary alleviation of problematic quadriceps muscle inhibition, supporting our hypothesis and providing critical support for a promising new rehabilitation strategy for restoring normal quadriceps functioning at the knee joint following ACL reconstruction by overcoming quadriceps muscle inhibition and recruiting more quadricep motor units. Acknowledgment The authors gratefully acknowledge the editorial contributions of J. D. Ball, PhD.
Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
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Funding The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by an Academic Year Research Award from The University of Texas at Tyler.
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Author Biographies Timothy Lowe is currently a Lecturer at the University of Texas at Tyler. He received his Master’s from the University of Texas at Tyler. Xuanliang Neil Dong is currently a Professor of Health and Kinesiology at The University of Texas at Tyler. He received his PhD degree from Columbia University. Dr. Dong is interested in neuromuscular training strategies for prevention and treatment of knee joint injuries in athletes.
