The Knee 17 (2010) Contents lists available at ScienceDirect. The Knee

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1 The Knee 17 (2010) Contents lists available at ScienceDirect The Knee Increasing pre-activation of the quadriceps muscle protects the anterior cruciate ligament during the landing phase of a jump: An in vitro simulation Javad Hashemi a,d,, Ryan Breighner a, Taek-Hyun Jang a, Naveen Chandrashekar b, Stephen Ekwaro-Osire a, James R. Slauterbeck c a Texas Tech University, Lubbock, TX, United States b University of Waterloo, Ontario, Canada c University of Vermont, Burlington, VT, United States d Texas Tech University Health Sciences Center, United States article info abstract Article history: Received 10 April 2009 Received in revised form 1 September 2009 Accepted 26 September 2009 Keywords: Anterior cruciate ligament ACL Quadriceps ACL strain In vitro simulation ACL injury mechanism We hypothesize that application of an unopposed quadriceps force coupled with an impulsive ground reaction force may induce anterior cruciate ligament (ACL) injury. This situation is similar to landing from a jump if only the quadriceps muscle is active; an unlikely but presumably dangerous circumstance. The purpose of this study was to test our hypothesis using in vitro simulation of jump landing. A jump-landing simulator was utilized. Nine cadaveric knees were tested at an initial flexion angle of 20. Each ACL was instrumented with a differential variable reluctance transducer (DVRT). Quadriceps pre-activation forces (QPFs) ranging from 25 N to 700 N were applied to each knee, followed by an impulsive ground reaction force produced by a carriage-mounted drop weight (7 kg) that impulsively drove the ankle upward. ACL strain was monitored before landing due to application of QPF (pre-activation strain) and at landing due to application of the ground reaction force (landing strain). No ACLs were injured. Pre-activation strains exhibited a positive correlation with QPF (r=0.674, pb0.001) while landing strains showed a negative correlation (r= 0.235, p=0.032). Total ACL strain (pre-activation +landing strain) showed no correlation with QPF (r =0.023, p=0.428). Our findings indicate that elevated QPF increases pre-activation strain but reduces the landing strain and is therefore protective post-landing. Overall, there is a complete lack of correlation between total ACL strain and QPF suggesting that the total strain in the ACL is independent of the QPF under the simulated conditions Elsevier B.V. All rights reserved. 1. Introduction The human anterior cruciate ligament (ACL) primarily serves as a restraint against anterior tibial translation at low flexion angles. There are an estimated 80,000 to 250,000 cases annually where the stability of the knee is compromised and the ACL fails [1,2]. Additionally, about 70% of these failures are classified as non-contact [3]. Activities in which non-contact ACL injuries occur include pivoting or side step cutting, decelerating while the knee is in an extended position, or landing from a jump with the latter being the most often cited [4].No consensus as to the root cause of these injuries exists among researchers in the field [2]. Despite a lack of agreement as to the cause, many risk factors for noncontact ACL injury have been proposed. Among these, sex is the most widely cited with females exhibiting a 4 6 fold greater incidence of ACL Corresponding author. Department of MechanicalEngineering, TexasTechUniversity, MS1021, Lubbock, TX 79409, United States. Tel.: ; fax: address: javad.hashemi@ttu.edu (J. Hashemi). injury [1]. In addition to sex, environmental, anatomical, hormonal, and neuromuscular risk factors have also been identified [2]. A frequently cited mechanism of ACL injury is a process in which the quadriceps muscle force is applied at an exceptionally aggressive level to cause severe anterior tibial translation and subsequent ACL injury. An abundance of evidence in the literature supports this plausible theory [5 13]. The proponents of the theory suggest that a combination of low knee flexion, strong quadriceps muscle contraction, and a posteriorly directed ground reaction force can increase ACL loading and cause injury [6,8,10,12]. AposteriorlydirectedGRF tends to increase the flexion of the knee post-landing and, for the body to resist excessive flexion of the knee, the quadriceps load has to increase; this additional increase in the quadriceps force is believed to increase the ACL strain and potentially cause injury [12,24]. Some argue that hamstring co-contraction will resist anterior tibial translation induced by the aggressive quadriceps pull. However, proponents of the quadriceps pull mechanism contend that at low flexion angles (less than 15 ), hamstring co-contraction does not significantly reduce anterior tibial translation and is therefore not protective of the ACL [9,14] /$ see front matter 2009 Elsevier B.V. All rights reserved. doi: /j.knee

2 236 J. Hashemi et al. / The Knee 17 (2010) To address this controversy, we posed the question, Can an unopposed quadriceps force (without the aid of the hamstring muscle), at a knee flexion angle of 20 o, increase ACL strain to injurious levels when assisted by an impulsive GRF (encountered at landing) during a simulated jump-landing task? In vivo study of the strain in the ACL during non-impulsive activities has been reported in the literature [9]. However, such measurements during more aggressive and dynamic activities are very rare and controversial. The only other feasible approach to understand ACL loading would be through descriptive laboratory studies by performing simulations of highly dynamic/ impulsive activities, in vitro. Thus, we tested our hypotheses through in vitro simulation of the vertical jump-landing process in a dynamic loading simulator. We postulate that as the unopposed quadriceps preactivation force is increased during simulated jump landing (when an impulsive ground reaction force is superimposed), 1) the strain in the ACL would also increase (both prior to and during the landing phase of a jump) and 2) this would lead to ACL injury. 2. Methods This was a descriptive laboratory study design intended to assess the effect of quadriceps pre-activation force (QPF) on ACL strain both prior to landing (under the anticipatory application of muscle forces), and during landing (during the application of impulsive forces). We also aimed to assess the overall effect of QPF throughout the landing process in vitro. To this end, cadaveric knees were installed in a dynamic loading simulator and muscle forces were applied, followed by an impulsive ground reaction force. Strain in the ACL was monitored during both stages Subjects Nine fresh frozen cadaver knees (five male, four female) were obtained from the University of Texas Southwestern Medical Center Willed Body Program (Dallas, TX), free of any prior injury. The average subject age was 55.1 years (SD 11.0). The specimens were stored at 20 C until dissection. The knees were dissected, leaving all ligaments intact, but removing all muscle and adipose tissue. Following dissection, the knees were refrozen until 12 h prior to testing Experimental setup The vertical jump-landing simulator used in this study integrated both artificial hip and ankle joints with cadaveric knees. The simulator allowed for simulation of the various stages of jump-landing including: muscle pre-activation in preparation for landing, impulsive loading at heel contact, post-landing flexion of the knee, and lastly post-landing muscle-induced stabilization of the lower extremity. The pre-landing angle of the hip and knee was varied through adjustment of tibia and femur lengths and, to a lesser extent, varying the positions of the hip and ankle joints. This was accomplished by varying the length of the coupler rods (Fig. 1a). The simulator allowed for the application of quadriceps muscle forces via a servo-electric actuator and programmable controller (TC3 Series actuator, B8962 controller, Danaher Motion, Radford, VA) attached to the patella with a 6 mm diameter steel cable (McMaster-Carr, Atlanta, GA). Elongation of the ACL was measured in the antero-medial bundle of the anterior cruciate ligament by means of a differential variable reluctance transformer (DVRT, Microstrain, Burlington, Vermont). The QPF and the subsequent increase in quadriceps force during the landing phase were measured using a single axis load cell (Honeywell-Sensotec, Columbus, Ohio). All strain and force signals were acquired and logged at 1 khz using a model USB bit data acquisition device and the NI Labview 8.2 software (National Instruments, Austin, Texas). The DVRT measured displacements were converted to strain based on the length of the instrument with the knee at approximately 20 of flexion and zero muscle force Simulation protocol Prior to testing, each specimen was potted both proximally and distally in steel cups using Cerrobend (Purity Casting Alloys, Surry, B.C., Canada), a low melt point casting alloy. After potting, the knee/ pot construct was installed in the jump-landing simulator (Fig. 1a). The system was adjusted to place the knee at an initial flexion angle of approximately 20. The hip joint was generally placed 50 to 75 mm posterior the ankle joint. At this point, the DVRT was installed on the ACL and its length was used as the gage length for subsequent strain calculation. Two small holes were drilled through the patella, in the anterior posterior direction, in order to attach the cable through which simulated quadriceps forces were applied (Fig. 1b). Following preparation, instrumentation, and installation of the knees in the simulator, each knee was subjected to a quadriceps preactivation force. To create the most hazardous conditions for the ACL, no hamstring forces were applied as it is established that hamstring forces protect the ACL by resisting anterior tibial translation [9,14]. It is important to note that the application of an unopposed quadriceps load will obviously tend to extend the knee; Fig. 1. The jump-landing simulator. (a) The full simulator showing the drop-weight carriage and the position of the knee in the simulator. (b) The sagittal view of the loaded knee showing the quadriceps cable, load cells, and actuators.

3 J. Hashemi et al. / The Knee 17 (2010) however, the pre-landing knee extension is resisted in our system by preventing anterior translation of the ankle joint during the quadriceps pre-activation stage. This simulates the contribution of the hamstring in flexing the knee joint without resisting anterior tibial translation. To simulate the landing phase, the knee was loaded impulsively upward after quadriceps pre-activation. Impact-induced flexion was generated through the use of a carriage-mounted drop weight (7 kg) which impacted a lever to drive the ankle upward, simulating a ground reaction force as is experienced during jump landing (Fig. 1a). This process simulates landing in reverse and is accepted as a viable method of landing simulation [13,15 17]. The height of the drop was fixed at 60 cm. The elongation in the ACL measured by the DVRT was recorded during the application of the pre-activation force as well as during the application of the impulsive force. Each knee was tested using the same impulsive landing force at seven different QPFs ranging from 25 N to 700 N. Once the QPF was applied, the actuator was placed in locked-displacement mode, i.e. as the ground reaction force was applied impulsively, the knee underwent flexion and extended the quadriceps cable attached to the patella (simulating eccentric contraction of the quadriceps). This increased the force in the cable because the actuator did not allow rigid body displacement of the cable. 3. Analysis Correlation analyses were performed to test the extent of a linear relationship between QPF and ACL strain in each knee. These tests were conducted for ACL strain before simulated landing (preactivation strain) and ACL strain during the application of the impulsive force (landing strain). In each knee, the pre-activation and landing strains corresponding to each QPF were added to find the total strain in the ACL under the given QPF. A correlation analysis was also performed to assess the extent of a linear relationship between the QPF and the total strain in each knee. At each QPF, the preactivation strains in all knees were pooled and a correlation analysis was performed for the whole sample (all subjects). Similarly, the landing and total strains were pooled and tested for correlation with QPF. 4. Results None of the ACLs were injured after simulated jump landing with an unopposed quadriceps force at any tested QPF level. In all nine knees, there was a positive correlation between QPF and ACL pre-activation strain as presented in Table 1. Sevenkneesshowed statistically significant correlations. The correlation for the pooled results of all knees was also found to be significant and positive (Fig. 2). A negative correlation between QPF and ACL landing strain was found in seven out of nine knees (four correlations were statistically significant, Table 2). Two knees showed positive correlations. The correlation for the pooled results of all knees was found to be negative and significant (Fig. 3). Fig. 2. Linear trendline for pre-activation strain versus QPF for pool of all knees (strains measured prior to landing). Mean±standard error of the mean. r=0.674, pb In Fig. 4, the total strain at each QPF is plotted for the pooled results. Seven knees showed no significant positive correlation between QPF and total ACL strain in any of the individual knees (Table 3). Similarly, no correlation was observed for the pooled results. 5. Discussion The strain in the ACL during the quadriceps pre-activation stage, presumably occurring in anticipation of landing, produces what we call the pre-activation strain. There are no reports of the level of QPF during landing from a jump. As a result, we used a maximum quadriceps pre-activation of 700 N, approximately the weight of a 70 kg subject. Our results show that unopposed pre-activation of the quadriceps prior to landing will increase pre-activation strain in the ACL. This is supported by an in vivo case study reported by Cerulli et al. [18] that showed that nearly 60% of the strain in the ACL was produced during the in-flight phase of the activity (the percentage is estimated from Fig. 2 in their report). The authors report strain levels close to 3.5% in the ACL just before landing. Based on Cerulli's in vivo results and using our Fig. 2, we may extrapolate that on average, one would need close to 900 N of QPF to create 3.5% pre-activation strain in the ACL. Thus the 700 N maximum pre-activation force used in this study is reasonable. As the QPF increases, the tibia moves anteriorly relative to the femur. This is clearly confirmed in Fig. 5a where the QPF is approximately 700 N (resulting in a longer and more vertically oriented patellar tendon) and Fig. 5b where the QPF is 150 N (resulting in a shorter, more anteriorly directed tendon) in the same knee. As the tibia moves anteriorly, it will put the ACL in tension. If the QPF is small, then the pre-activation strain in the ACL will also be small and conversely, large pre-activation forces will yield large preactivation ACL strains (Fig. 2). Table 1 Correlational statistics for pre-activation strain versus QPF. Table 2 Correlational statistics for landing strain versus QPF. Pre-activation Strain r Landing strain r p-value p-value K K b0.001 K b0.001 K K b0.001 K K b0.001 K K Pooled b0.001 For individual knees: r critical=0.669; α=0.05, for pooled r critical= K K K K K K K b0.001 K K Pooled For individual knees: r critical= 0.669; α=0.05, for pooled r critical=

4 238 J. Hashemi et al. / The Knee 17 (2010) Table 3 Correlational statistics for total strain versus QPF. Total strain r p-value K K K K K K K K K Pooled For individual knees: r critical=0.669; α=0.05, for pooled r critical= Fig. 3. Linear trendline for landing strain versus QPF for pool of all knees (peak strains measured during upward impulse). Mean±standard error of the mean. r= 0.235, p= The dynamic component of strain (landing strain) in the ACL is produced during landing. As an individual lands from a jump, the ground reaction force will induce knee flexion and the quadriceps force will necessarily increase through initial eccentric contraction to decelerate knee flexion and then through concentric contraction, to extend the knee, in order for the individual to regain an upright posture. Based on Cerulli et al.'s in vivo work [18], the landing strain is approximately 2% (estimated from their Fig. 2 at 40% of the total strain). Our results show that the landing strain in the ACL generally decreases with increasing QPF (Fig. 3). Thus when QPF is low, the pre-activation strain remains low (Fig. 2), but the induced landing strain in the ACL will be high, relative to the pre-activation strain (see Figs. 2 and 3). This is because at low QPFs, the knee is less stable and the tibia can translate more freely relative to the femur. We define stability as the measure of the resistance of the joint to anterior tibial translation. Conversely, as QPF increases, the pre-activation strain will become larger (Fig. 2) but the landing strain induced during landing will be reduced (Fig. 3). Landing strain will be smaller because large QPFs will increase joint stability. Large QPFs will also reduce knee flexion postlanding due to the body's downward momentum. This does not mean that greater knee extension at landing is safer for the individual, but rather that greater pre-activation of the quadriceps will inhibit flexion Fig. 4. Linear trendline for total strain (pre-activation+landing) in each knee versus quadriceps pre-avtivation force. Mean±standard error of the mean. r=0.023, p= during landing. Our results also show that the total strain observed in the ACL (the sum of pre-activation strain and landing strain) does not vary considerably with increasing QPFs (Fig. 4). Generally speaking, if landing strain had shown an increasing trend with greater quadriceps pre-activation, one might conclude that a mechanism by which the quadriceps forces could cause ACL injury does exist, but this was not the case. Our results indicate that even unopposed QPFs aided by an impulsive ground reaction force cannot injure the ACL. Under the loading conditions in this study, the ACL in each knee appeared to have a constant level of total strain at landing. This signature strain value most likely depends upon the geometry of the knee and the ACL, as well as other subject specific variables such as the stiffness of the ligament. This signature strain was not substantially deviated from at any of the quadriceps pre-activation levels for each knee (Fig. 4). The question arises: Under these extreme conditions, exactly what prevents ACL strain from reaching injurious levels? The answer to this question, we believe, is the slope and geometry of the tibial plateau. There are two ways that the tibial plateau's slope and geometry could help protect the ACL. First, one could make the argument that joint compressive loads, heightened with large muscle forces, induce snug positioning of the convex medial femoral condyle in the concave medial tibial plateau [19,23] and this snug fit (joint conformity) produces the primary restraint against anterior tibial translation at low flexion angles along with menisci (similar to a locking mechanism). In other words, the deeper the medial tibial plateau, the more resistant to anterior tibial translation the joint will be [23]. Second, it is reported that the slope of the medial tibial plateau is directed posteriorly ranging from 0 to 10 [19]. The lateral plateau has a slightly steeper slope. As a result of the posterior slope of the tibial plateau, a fully extended knee (zero knee flexion) will experience a joint compressive force that will have an anteriorly directed shear component acting on the tibia (see red arrow in Fig. 6 note no hamstring force). The force transmitted through the patellar tendon will also have an anterior shear component. In this situation, a knee extension moment will be generated by the quadriceps about the tibiofemoral articulation point, forcing the tibia to move anteriorly, increasing strain in the ACL and potentially causing ACL injury. However, as soon as the contact phase of the landing is initiated, the ground reaction force creates a significantly larger and opposing knee flexion moment, Fig. 7. Under this moment, the knee flexion increases rapidly and the quadriceps force also increases to reduce this flexion moment and eventually generates an extension moment. The point that is often ignored, however, is that increased knee flexion due to ground contact will cause the tibia to angulate posterior to the femur and place the tibial plateau at an anteriorly decreasing angle relative to the femur, Fig. 7. This will change the direction of the joint reaction force so it has a posteriorly directed shear component. At moderate flexion angles, secondary soft tissue restraints such as the

5 J. Hashemi et al. / The Knee 17 (2010) Fig. 5. The sagittal image of the knee under a QPF of (a) 700 N and (b) 150 N. Note the orientation and length of the patellar tendon in the two scenarios. collateral ligaments also resist anterior tibial translation. Many researchers ignore the critical effect of the changing direction of the joint reaction force as knee flexion increases. After a small amount of knee flexion, the posteriorly directed shear component of the joint reaction force will serve as a crucial element protecting the ACL by pushing the tibia posteriorly relative to the femur. As quadriceps force increases, the joint compressive force also increases and the posterior component of the force becomes larger and more protective. At this position, the anterior tibial translation produced by the patellar tendon will be diminished or even stopped by the anterior slope of the tibial plateau, and the ACL will be safe. For these reasons non-contact ACL injury is rarely observed at higher flexion angles. Here, it is important to compare our approach and results to that of Withrow et al. [13] since they also used the concept of a jumplanding simulator and studied the role of the quadriceps force in loading the ACL, in vitro. The ACL strain that Withrow et al. report is equivalent to the landing strain reported here as Withrow et al. did not measure the pre-activation strain. The other major differences between our work and Withrow et al. are that they used a low QPF of 180 N for all their cases and a fixed hamstring and gastrocnemius force of 70 N. In our work, we did not simulate the hamstring muscles because we intended to discount any protective effects that the hamstring muscle may have (in other words create a more injurious condition for the ACL). Gastrocnemius does play a role in loading the ACL but only near full knee extension [20] (less than 15 ). In Withrow Fig. 6. A schematic of the tibiofemoral joint at full extension under the application of an unopposed quadriceps force just before impact: Note the direction of the JCF, the joint reaction force. Fig. 7. A schematic of the tibiofemoral joint at moderate flexion under the application of an unopposed quadriceps force after impact: Note the direction of the JCF, the joint reaction force.

6 240 J. Hashemi et al. / The Knee 17 (2010) et al.'s work, any impact that this muscle had on the ACL strain was experienced before the application of the impulse when the knee was at 25 o of flexion but Withrow et al. did not report the strain before the application of the impulsive ground reaction force. Thus, to compare the observed ACL strain in our work and that of Withrow et al.'s, we must compare their reported strain, under approximately 180 N of QPF, with our results at the same QPF. From Fig. 3, we can estimate our overall average landing strain under a QPF of 180 N to be approximately 4% which is higher than the overall average of 2.9% in Withrow et al.'s work (calculated based on values reported in Table 1 of Withrow et al). This difference is probably due to the absence of a hamstring force in our simulation and differences in the magnitude of the imparted impulse. What is incontrovertible, however, is that neither Withrow et al. nor our group was able to cause ACL injury (although their peak quadriceps force after impulse reached as high as 1578 N). We also believe that had Withrow et al. increased the quadriceps pre-activation force to above 180 N, they would have observed a similar downward trend in their measured ACL strain as we have reported here. We therefore cannot verify Withrow et al.'s conclusion that when the balance between large muscle forces is temporarily lost (i.e. there is a large quadriceps force but smaller hamstring force), ACL injury may occur. It is also important to compare our results and conclusions with that of DeMorat et al. also as they suggest that high quadriceps loads of around 4500 N can cause ACL injury. We do not disagree with their conclusion. If the knee flexion angle is fixed (in their case at 20 ) and quadriceps load is increased monotonically, a large joint compressive force will be produced that could fail the ACL. We agree that their results may be applicable during activities that external forces and moments create circumstances under which quadriceps force will increase rapidly and concentrically but knee extension is resisted such as weight lifting or alpine skiing [24]. However, after ground contact during jump landing, the quadriceps force increases eccentrically (lengthening) to resist excessive flexion of the knee. Can this eccentric increase in the quadriceps also cause ACL injury? The answer is yes but only if there is enough time for the eccentric increase in muscle force to reach the force levels that DeMorat et al. suggest (~4500 N). Based on video evidence, it has been shown that ACL injury in noncontact injuries probably occurs from 17 to 50 ms after initial ground contact [21]. Thus, for DeMorat's ACL injury theory to be valid in activities such as landing from a jump, a sudden increase in quadriceps force (from low pre-activation levels to 4500 N), in less than 50 ms after landing, must be produced. The question now becomes Is this rate of eccentric muscle loading possible? Grabnier and Owings (2002) reported that in voluntary eccentric activation of the quadriceps there exists a 200 ms delay before the onset of dynamometer motion or muscle lengthening [22]. In the same paper at 50 ms (when the ACL is shown to have already failed [21]), the generated knee moment is minimal; the peak knee extension moment was observed around 600 ms. In addition, there is evidence that the peak vertical ground reaction force during landing occurs between 38 to 65 ms after foot contact [25] following which there is a sharp drop in its magnitude (further evidence that ACL injury occurs in this time frame). Thus, the combination of the above findings [21,22,25], produces a strong case against the viability of the aggressive quadriceps contraction alone as a mechanism of ACL injury during jump landing. There is not enough time for the quadriceps force to reach ACL-injurious levels. Some could argue that there may be significant pre-activation of the quadriceps prior to landing but that is exactly what we investigated in this paper and could not show that strong pre-activation of the quadriceps causes injurious levels of ACL strain. Our results and analysis here support some of the arguments made by McLean et al (2005) against this sagittal plane mechanism of ACL injury [24]. Limitations of this study are primarily related to the use of cadaveric specimens and the quadriceps forces used. The hip muscles were not included in the simulation. We believe that the hip muscles are crucial to the developed strain in the ACL and could actually cause increased ACL strain. The effect of muscle forces on knee joint kinematics was also not examined and this is important to make sure that we are simulating appropriate kinematics. These deficiencies should be corrected in future in vitro research efforts as they could affect our conclusions. 6. Conclusion Our in vitro simulation results show that even an unopposed quadriceps force aided by an impulsive ground reaction force cannot cause ACL injury during the landing phase of the jump-landing activity when the initial flexion angle is around 20. There are various means of protection against such a mechanism of injury including pressure-induced joint conformity, hamstring co-contraction, and an anteriorly tilted tibial plateau, all of which will reduce relative movement between the femur and the tibia. 7. Conflicts of Interest None of the authors report any conflict of interest. References [1] Arendt E, Dick R. Knee injury patterns among men and women in collegiate basketball and soccer: NCAA data and review of literature. Am J Sports Med 1995;23: [2] Griffin LY, Albohm MJ, Arendt EA, Bahr R, Beynnon BD, DeMaio M, et al. Understanding and preventing noncontact anterior cruciate ligament injuries: a review of the hunt valley II meeting, January Am J Sports Med 2006;34: [3] McNair PJ, Marshall RN, Matheson JA. Important features associated with acute anterior cruciate ligament injury. NZ Med J 1990;103: [4] Shimokochi Y, Shultz SJ. Mechanisms of non-contact anterior cruciate ligament injury. J Athl Train 2008;43: [5] Arms SW, Pope MH, Johnson RJ, Fischer RA, Arvidsson I, Eriksson E. The biomechanics of anterior cruciate ligament rehabilitation and reconstruction. Am J Sports Med 1984;12:8 18. [6] Draganich LF, Vahey JW. An in vitro study of anterior cruciate ligament strain induced by quadriceps and hamstring forces. J Orthop Res 1990;8: [7] Berns GS, Hull ML, Patterson HA. Strain in the anteromedial bundle of the anterior cruciate ligament under combination loading. J Orthop Res 1992;10: [8] Durselen L, Claes L, Kiefer H. The influence of muscle forces and external loads on cruciate ligament strain. Am J Sports Med 1995;23: [9] Beynnon BD, Fleming BC, Johnson RJ, Nichols CE, Renstrom PA, Pope MH. Anterior cruciate ligament strain behavior during rehabilitation exercises in vivo. Am J Sports Med 1995;23: [10] Markolf KL, Burchfield DM, Shapiro MM, Shepard MF, Finerman GA, Slauterbeck JL. Combined knee loading states that generate high anterior cruciate ligament forces. J Orthop Res 1995;13: [11] Fleming BC, Renstrom PA, Beynnon BD, Engstrom B, Peura GD, Badger GJ, et al. The effect of weightbearing and external loading on anterior cruciate ligament strain. J Biomech 2001;34: [12] Demorat G, Weinhold P, Blackburn T, Chudik S, Garrett W. Aggressive quadriceps loading can induce noncontact anterior cruciate ligament injury. Am J Sports Med 2004;32: [13] Withrow TJ, Huston LJ, Wojtys EM, Ashton-Miller JA. The relationship between quadriceps muscle force, knee flexion, and anterior cruciate ligament strain in an in vitro simulated jump landing. Am J Sports Med 2006;34: [14] Li G, Rudy TW, Sakane M, Knamori A, Ma CB, Woo SL. The importance of quadriceps and hamstring muscle loading on knee kinematics and in-situ forces in the ACL. J Biomech 1999;32: [15] Hashemi J, Chandrashekar N, Jang T-H, Karpat F, Oseto M, Ekwaro-Osire S. An alternative mechanism of non-contact anterior cruciate ligament injury during jump-landing: in vitro simulation. Exp Mech 2007;47: [16] Withrow TJ, Huston LJ, Wojtys EM, Ashton-Miller JA. The effect of an impulsive knee valgus moment on in vitro relative ACL strain during a simulated jump landing. Clin Biomech 2006;21: [17] Withrow TJ, Huston LJ, Wojtys EM, Ashton-Miller JA. Effect of varying hamstring tension on anterior cruciate ligament strain during in vitro impulsive knee flexion and compression loading. J Bone Jt Surg Am Vol 2008;90: [18] Cerulli G, Benoit DL, Lamontagne M, Caraffa A, Liti A. In vivo anterior cruciate ligament strain behaviour during a rapid deceleration movement: case report. Knee Surg Sports Traumatol Arthrosc 2003;11: [19] Hashemi J, Chandrashekar N, Gill B, Beynnon BD, Slauterbeck JR, Schutt RC, et al. The geometry of the tibial plateau and its influence on the biomechanics of the tibiofemoral joint. J Bone Jt Surg Am Vol 2008;90:

7 J. Hashemi et al. / The Knee 17 (2010) [20] Fleming BC, Renstrom PA, Ohlen G, Johnson RJ, Peura GD, Beynnon BD, et al. The gastrocnemius muscle is an antagonist of the anterior cruciate ligament. J Orthop Res Nov 2001;19(6): [21] Krosshaug T, Nakamae A, Boden BP, Engebretsen L, Smith G, Slauterbeck JR, et al. Mechanisms of anterior cruciate ligament injury in basketball: video analysis of 39 cases. Am J Sports Med Mar 2007;35(3): [22] Grabnier MD, Owings TM. EMG differences between concentric and eccentric maximum voluntary contractions are evident prior to movement onset. Exp Brain Res 2002;145: [23] Hashemi J, Chandrashekar N, Mansouri H, Gill B, Slauterbeck JR, Schutt RC, et al. Shallow medial tibial plateau and steep medial and lateral tibial slopes: new risk factors for anterior cruciate ligament injuries. Am J Sports Med 2010;38(1): [24] McLean SG, Andrish JT, van den Bogert AJ. Comment on: Aggressive quadriceps loading can induce noncontact anterior cruciate ligament injury. Am J Sports Med Jul 2005;33(7):1106. [25] Seegmiller JG, McCaw ST. Ground reaction forces among gymnasts and recreational athletes in drop landings. J Athl Train 2003;38(4):311 4.