Archives of Physical Medicine and Rehabilitation
Volume 89, Issue 12 , Pages 2324-2331, December 2008

Dynamic Restraint Capacity of the Hamstring Muscles Has Important Functional Implications After Anterior Cruciate Ligament Injury and Anterior Cruciate Ligament Reconstruction

  • Adam L. Bryant, PhD

      Affiliations

    • Centre for Health, Exercise and Sports Medicine, School of Physiotherapy, The University of Melbourne, Melbourne, Australia
    • Corresponding Author InformationCorrespondence to Adam L. Bryant, PhD, Centre for Health, Exercise and Sports Medicine, School of Physiotherapy, Faculty of Medicine, Dentistry and Health Sciences, The University of Melbourne, Victoria, Australia 3010
    • ,
  • Mark W. Creaby, PhD

      Affiliations

    • Centre for Health, Exercise and Sports Medicine, School of Physiotherapy, The University of Melbourne, Melbourne, Australia
    • ,
  • Robert U. Newton, PhD

      Affiliations

    • School of Exercise, Biomedical and Health Sciences, Edith Cowan University, Joondalup, Australia
    • ,
  • Julie R. Steele, PhD

      Affiliations

    • Biomechanics Research Laboratory, University of Wollongong, Wollongong, Australia

Article Outline

Abstract 

Bryant AL, Creaby MW, Newton RU, Steele JR. Dynamic restraint capacity of the hamstring muscles has important functional implications after anterior cruciate ligament injury and anterior cruciate ligament reconstruction.

Objective

The purpose of this study was to investigate the relation between knee functionality of anterior cruciate ligament deficient (ACLD) and anterior cruciate ligament reconstruction (ACLR) patients and hamstring antagonist torque generated during resisted knee extension.

Design

Cross-sectional.

Setting

Laboratory based.

Participants

Male ACLD subjects (n=10) (18–35y) and 27 matched males who had undergone ACLR (14 patella tendon [PT] grafts and 13 combined semitendinosus/gracilis tendon grafts).

Interventions

Not applicable.

Main Outcome Measures

Knee functionality was rated (0- to 100-point scale) by using the Cincinnati Knee Rating System. Using electromyography data from the semitendinosus (ST) and biceps femoris muscles, we created a mathematical model to estimate the opposing torque generated by the hamstrings during isokinetic knee extension in 10° intervals from 80° to 10° knee flexion.

Results

Pearson product-moment correlations revealed that more functional ACLD subjects generated significantly (P<.05) higher hamstring antagonist torque throughout knee extension. In contrast, more functional PT subjects produced significantly lower hamstring antagonist torque at 80° to 70° knee flexion, whereas no significant associations were found between hamstring antagonist torque and knee functionality for the ST/gracilis tendon subjects.

Conclusions

An increased hamstring antagonist torque generated by the more functional ACLD subjects, reflective of increased hamstring contractile force, is thought to represent a protective mechanism to compensate for mechanical instability. The restoration of anterior knee stability through ACLR negates the need for augmented hamstring antagonist torque.

Key Words: Anterior cruciate ligament, Rehabilitation

List of Abbreviations: ACL, anterior cruciate ligament, ACLD, anterior cruciate ligament deficient, ACLR, anterior cruciate ligament reconstruction, ANOVA, analysis of variance, ATT, anterior tibial translation, BF, biceps femoris, EMG, electromyography, G, gracilis, iEMG, integrated electromyography, PCSA, physiologic cross-sectional area, PT, patella tendon, ROM, range of motion, SM, semimembranosus, ST, semitendinosus

 

BY INSERTING ON THE posterior aspect of the tibia and fibular head, the hamstrings can impart a posterior draw force on the knee. For this reason, the hamstrings are-commonly referred to as ACL agonists and cocontract with the quadriceps during knee extension to reduce ATT.1, 2, 3 The magnitude of hamstring cocontraction has been used to predict the antagonist torque generated by the hamstrings of healthy subjects during isokinetic knee extension.1, 4 Using EMG-driven mathematical models, Baratta1 and Kellis,4 and colleagues reported that the hamstrings play an active role in maintaining knee joint stability, particularly when the knee extensors are working concentrically.

Given their capacity to generate considerable antagonist force, the hamstrings emerge as the principal structure contributing to reduced knee joint laxity after ACL injury.5, 6, 7 Indeed, there is some evidence from cadaveric6 and computer models7 to suggest that contraction of the hamstring muscles in ACLD knees reduces knee joint laxity. In addition, More et al6 also showed in situ the importance of hamstring contraction after ACLR in that the application of a 90-N hamstring force unloaded the ACL graft between 90° knee flexion and near terminal extension. Although it is the hamstring force applied to the tibia and fibula that opposes ATT, the torque generated by the hamstrings during active knee flexion is easily measured by using isokinetic dynamometry and is typically the mechanical parameter used to characterize hamstrings force output.1, 4 However, no research to date has examined whether the level of hamstring antagonist torque during isokinetic knee extension is an important determinant of in vivo function after ACL injury or ACLR.

The process of harvesting the ACL substitute from the medial hamstrings (ie, ST/gracilis tendon graft) might cause neural inhibition and/or altered mechanics of the donor musculotendinous unit,8 which may alter hamstring antagonist torque during knee extension. Alternatively, harvesting the ACL graft from the extensor mechanism (ie, PT graft), and thus preserving integrity of the hamstring musculotendinous structures might produce a different response. Hence, there may not be a single optimal hamstring response that extends to all ACLR patients. Although a number of studies9, 10 have investigated hamstring concentric torque after ACLR, no research was located examining the effect of the ACL graft harvest site on hamstring antagonist torque or how this affects knee functionality in ACLR patients. Therefore, the purpose of this study was to investigate the relation between knee functionality of ACLD and ACLR (PT and ST/gracilis tendon grafts) patients and hamstring antagonist torque generated during resisted knee extension throughout the operational range of the quadriceps muscles.

Back to Article Outline

Methods 

Subjects 

Subjects for this study were recruited from a potential pool of 113 ACLD and ACLR patients. After the application of the inclusion criteria, 10 male ACLD patients together with 14 ACLR patients who had undergone reconstruction by using the PT graft and 13 ACLR subjects reconstructed by using the ST/gracilis tendon graft were recruited to participate in this study. Subjects in the PT and ST/gracilis tendon groups were matched for time since reconstructive surgery. Female subjects were excluded because hormonal fluctuations can affect joint dynamics, including joint laxity11, 12, 13, 14 and the viscoelastic properties of the lower-limb musculature.15 For the ACLD subjects, isolated complete rupture of the ACL was confirmed by previous arthroscopy, and the initial injury occurred at least 1 year before testing.16, 17 These ACLD subjects were identified early after injury as having good potential to dynamically stabilize the injured knee18 and were therefore advised by the surgeon that they were good candidates for conservative treatment. All subjects were reexamined by the same consulting surgeon before participating in the study, and ACLR subjects had to be stable in flexion and extension to be included. ACLD and ACLR subjects also met the following inclusion criteria: aged from 18 to 35 years; no evidence of collateral ligament, posterior cruciate ligament, or meniscal damage or repair at the time of arthroscopy/surgery; no evidence of collateral ligament, posterior cruciate ligament, or meniscal damage on clinical examination; no previous ACL surgery or subsequent knee surgery on the involved leg; no history of surgery or traumatic injury to the contralateral knee; frequent participation (ie, 4–7 d/wk) in sporting activities that involve running, jumping, cutting, and lateral motion before injury; and at least moderate participation (ie, 1–3/mo) in sporting activities that require running, twisting, and turning after injury/surgery.

The protocol was approved by the university human ethics committee (reference no. 02/09–74), and all subjects read and signed an approved consent document before participating in the study.

Surgical Procedure and Rehabilitation 

All ACL reconstructions were performed by the same orthopedic surgeon using arthroscopically assisted 2-incision techniques. The bone-patellar tendon-bone graft (10mm wide) was constructed from the central third of the tendon of the ipsilateral knee. Along with the tendon strip, bone blocks (20 × 10mm) were removed with the graft on either end, leaving bony defects in the patella and tibial tuberosity. Tibial and femoral tunnels (drilled using a 4.5-mm gauge drill) were fashioned with guide pins, and a notchplasty was performed as required to ensure that graft impingement did not occur in the intercondylar notch region. The graft was passed into the joint, and the bone plug was fixed at the femoral site with an interference screw. Similarly, the tibial bone plug fixation was accomplished with an interference screw at 10° of knee flexion. The graft was observed under a final arthroscopic examination to determine its ability to resist anterior displacement during a Lachman test.10, 19, 20

The ipsilateral ST and G tendons were harvested through an oblique incision over the pes anserinus. A tendon stripper was used to harvest the 4 strands of hamstring tendon, each being about 20cm long. The muscle fibers on the proximal ends of the tendons, together with excess fascia, were debrided. The defect in the hamstrings was repaired by suturing the ST and G muscle fascia to each other and/or to the semimembranosus muscle. The 4 tendon strands were whip stitched together and tensioned through a sizing block. The average size of the combined grafts was 7 to 10mm. Preparation of the tibial and femoral tunnels was the same as that described for the PT technique, although access to the distal femur was achieved through a 3- to 4-cm straight, lateral thigh incision. Femoral fixation of the graft was performed with an interference screw. After femoral fixation, traction was placed on the tibial end of the graft, and the knee was cycled through a full ROM 20 to 30 times to ensure stress relaxation of the graft and uniform tension of all the limbs of the graft.21 The tibial end of the graft was fixed using an interference screw, and the final arthroscopic examination was the same as that described for the PT technique.

All ACLR subjects participated in the same standard accelerated physical therapy rehabilitation program as originally described by Shelbourne and Nitz22 for the injured knee after knee surgery. Progression through the various activities in rehabilitation (as determined by the physiotherapist) was essentially similar for the PT and ST and gracilis tendon subjects; however, PT subjects had a slightly more rapid progression to riding an exercise bike, riding a road bike, and both closed and open kinetic chain quadriceps strengthening.23, 24 On average, ACLR subjects underwent supervised rehabilitation for 12 weeks postsurgery and then entered the “return to sport” phase in which they gradually increased the complexity and intensity of activities. ACLD subjects were also subjected to an accelerated protocol with immediate training of ROM and weight bearing. Supervised rehabilitation continued for 8 to 10 weeks after injury and primarily consisted of quadriceps/hamstring muscle strengthening (open and closed kinetic chain) together with agility skill training and sport-specific training in the latter part of the program.

Experimental Protocol 

Knee functionality rating 

Knee function was rated using the questionnaire and functional test components of the Cincinnati Knee Rating System.25 The questionnaire components pertaining to symptoms (pain, swelling, partial and full giving way), activities of daily living (walking, stairs, kneeling), and sports (level of participation, running, jumping and hard twists, cuts, pivots) were completed. Each subject also completed 3 trials of 3 single-leg functional tests, including the vertical jump, long hop, and timed hop, with the noninvolved limb tested before the involved limb.25

Hamstring isokinetic torque and EMG activity 

After standard preparation to reduce cutaneous impedance below 5 kappa omega (Metex M–3650 impedance metera), silver-silver chloride preamplified surface electrodes (Quantecb, 5-mm diameter) were placed over the bellies of the ST and BF muscles of the involved limb in a bipolar electrode configuration (interelectrode distance=20mm).26 A reference electrode was placed equidistant with respect to the differential electrodes.27 Saline gel was placed between each electrode and the skin to enhance conductivity.

After a standardized warm-up (5 minutes of low-resistance ergometer cycling [60 RPM at 1 kpm] and 5min of slow static quadriceps and hamstring muscle stretching), each subject was positioned on the testing bench of the Cybex Isokinetic Dynamometerc after the standard subject positioning protocol.28 Before data collection, subjects performed 5 to 10 submaximal and then 4 maximal knee extension and flexion repetitions for their involved limb. These trials served as a specific knee extension-knee flexion warm-up and also familiarized the subjects with the testing protocol. The warm-up phase was followed by 2 minutes of rest to reduce fatigue from impairing performance. Each subject then performed 2 sets of 5 maximal extension and flexion repetitions at 180°/s. This test velocity was selected because previous researchers29, 30, 31 have established a close relationship between torque produced during knee extension and flexion at this speed and performance in functional tasks such as jumping and landing. A standardized script of verbal encouragement was provided to all subjects to facilitate maximum performance.

Preamplified EMG data were relayed to an amplifier (Quantec, gain=10,000, common mode rejection >120dB, input bias current <40 pA, input impedance >1012Ω). Electromyographic data from the Quantec amplifiers, together with raw isokinetic torque and knee joint displacement data from the Cybex Isokinetic Dynamometer, were recorded using an AMLABd signal-acquisition system. Data were relayed to the AMLAB alternating current amplifiers (gain=10,000; common mode rejection >120 dB; input bias current <40 pA; input impedance >1012Ω). After amplification, the data were analog to digital converted (12-bit, 1000Hz) by the AMLAB system.

Data Analysis 

Knee functionality 

Like a number of previous studies,25, 32, 33, 34 an overall knee functionality score was calculated for each subject by summing the points awarded for their symptoms, ability to perform daily and sports activities, and single-leg functional testing. A maximum of 20 points was possible for the rating of symptoms, 15 points for functional daily and sports activities, and 10 points for single-limb functional testing.25 The score for each subject was summed, and the overall total was converted to a score out of 100.

Hamstring antagonist EMG activity and torque 

The preamplified EMG signals from the ST and BF muscles were filtered using a fourth-order 0-phase shift Butterworth filter (high pass fc=15Hz; low-pass fc=250Hz).35 To create a linear envelope (m·V), the filtered EMG data were full wave rectified and then filtered again using a fourth-order 0-phase shift Butterworth low-pass filter (fc=30 Hz). To convert any negative values arising at the extreme ends, the linear envelope was again full-wave rectified.36

Consistent with methods described in the literature,1, 4 iEMG signals were averaged in 10° intervals from 80° to 10° knee flexion, leading to a total number of 7 averaged iEMG and moment values. Antagonist iEMG activity for the ST and BF muscles were normalized as a percentage of the iEMG activity of the same muscle, at the same angle, and angular velocity when the muscle was acting as an agonist.1, 4, 37 In accordance with the findings of Kellis and Baltzopoulos4 who also investigated open kinetic chain knee extension, the relation between hamstring iEMG and the moments generated at each knee flexion interval was assumed to be linear. However, unlike Kellis4 who used the activity from a single hamstring muscle and assumed this to be representative of the entire muscle group, the moment contribution of the medial and lateral hamstrings was based on a stress distribution approach whereby the force generated by each of the hamstring muscles was calculated to be proportional to the muscle's PCSA. Data pertaining to the hamstring PCSA were derived from Wickiewicz et al.38 For the purposes of this model and several previous studies,1, 39, 40 the moment arm for each hamstring muscle was assumed to be equal, and, thus, the contribution of each hamstring muscle toward the net knee joint flexion-extension moment was also assumed to be proportional to the PCSA. Because EMG data were not available for the SM muscle, the activity of the other medial hamstring (ie, ST muscle) was assumed to approximate that of the SM. Using this approach, hamstring antagonist torque at each 10° knee flexion interval was obtained by using the following equation:

where HamTORQUE=hamstring antagonist torque in N·m, TOR=estimated torque (N·m) generated by the individual hamstrings, and PCSA=physiologic cross-sectional area of the hamstrings in mm2.

Hamstring torque at each flexion interval was normalized to the net extension torque for that interval. Data from all 10 trials of each subject's test limb were averaged. Custom-written softwaree was used to analyze the data.

Statistical Analysis 

Descriptive statistics for the age, height, body mass, time since injury or surgery, and overall knee functionality scores for each subject group were calculated. After confirming normality (Kolmogorov-Smirnov test with Lilliefor's correction) and equal variance (Levene Median Test), a 1-way ANOVA design was then used to compare these variables among the ACLD, PT, and ST/gracilis tendon groups.

Means and SDs were calculated for the hamstring antagonist torque generated in the 7 intervals between 80° and 10° knee flexion. Pearson product-moment correlation coefficients were used to establish the strength of the relation between the knee functionality scores and the hamstring antagonist torque values. A level of significance P less than .05 was selected in all analyses. It is recognized that numerous variables were correlated for each subject group, and, hence, there is an increased risk of type 1 error. The cost of incurring a type 1 error was, nevertheless, deemed minimal and therefore appropriate given the exploratory nature of the study. All analyses were conducted using statistical package, SPSS version 12.0.f

Back to Article Outline

Results 

Descriptive data pertaining to the physical characteristics and overall knee functionality scores of the ACLD, PT, and ST/gracilis tendon subjects, together with F ratios and alpha levels derived for each source of variance in the 1-way ANOVA, are presented in table 1. Statistical analysis revealed a significant main effect of subject group for age, time since injury or surgery, and overall knee functionality scores. Post hoc comparisons for age revealed that the ST/gracilis tendon subjects, on average, were significantly younger than their ACLD (P=0.009, mean difference=7.8y) and PT (P=0.004, mean difference=7.9y) counterparts. Despite this difference, the 3 subject groups were considered appropriately matched on the main physiologic variables of height and body mass, although it is acknowledged that there was high variability in the subjects' masses as evident in the high standard deviations. For time since injury or surgery, post hoc contrasts indicated that the ACLD group had incurred their original injury significantly earlier before testing compared with the time between surgery and testing for the PT (P<0.001, mean difference=60.5mo) and ST/gracilis tendon (P=0.001, mean difference=61.4mo) groups. This difference was, however, anticipated given the differences in selection criteria for the ACLD subjects compared with the ACLR subjects. Finally, post hoc contrasts for overall knee functionality scores showed that the PT (P<0.001, mean difference=22.1 points) and ST/gracilis tendon (P<0.001, mean difference=28.5 points) groups rated significantly higher than the ACLD group.

Table 1. Age, Height, Body Mass, Time Since Injury or Surgery, and Overall Knee Functionality Scores
VariableACLDPTSTGTF⁎P⁎
Age (y)30.7(±8.6)30.9(±7.3)22.9(±3.8)5.800.007†‡§
Height(cm)176.2(±5.0)180.2(±4.7)177.6(±5.1)2.063.143
Mass(kg)72.4(±4.8)87.1(±19.6)79.4(±7.3)2.377.080
Time since injury/surgery(mo)75.6(±72.5)15.1(±5.0)14.2(±4.5)6.242.002†‡∥
Overall knee functionality scores(/100)59.0(±16.3)81.1(±16.1)87.5(±11.8)11.629.000†‡∥

NOTE. Mean ± SD of the age, height, body mass, time since injury or surgery, and overall knee functionality scores for the ACLD (n=10), PT (n=14), and SM/gracilis tendon (n=13) subjects, together with F ratios and alpha levels derived for each source of variance.

Abbreviation: STGT, semitendinosus and gracilis tendon.

⁎F values (1) and P values (2) are reported for 1-way ANOVA comparisons between the 3 subject groups for the physiologic characteristics (df=37).

†A significant main effect (P<0.05) of subject group.

‡A significant difference between the ACLD and STGT groups.

§A significant difference between the PT and STGT groups.

∥A significant difference between the ACLD and PT groups.

Hamstring antagonist torque varied as a function of knee joint angle, showing a descending-ascending curve. The average hamstring torque generated across the 7 knee flexion intervals by the ACLD, PT, and ST/gracilis tendon subjects was 12.2%±7.4% net extension torque, 12.4%±6.9% net extension torque, and 14.0%±5.7% net extension torque, respectively. Pearson product-moment correlation coefficients calculated between knee functionality and hamstring antagonist activity are presented in table 2. Statistical analysis revealed moderate to strong positive correlations between hamstring antagonist activity at knee flexion intervals 70° to 60°, 60° to 50°, 50° to 40°, 40° to 30°, 30° to 20°, and 20° to 10° and knee functionality for the ACLD group. Compared with less functional ACLD subjects, more functional ACLD subjects generated higher hamstring antagonist torque throughout the ROM. This is shown for 2 individual subjects in figure 1. For the PT group, a significant moderate negative correlation was identified between the level of hamstring antagonist torque at 80° to 70° knee flexion and knee functionality. No significant associations were found between hamstring antagonist torque across the range of knee flexion motion and knee functionality for the ST/gracilis tendon group.

Table 2. Correlation Coefficients Between Overall Knee Functionality Scores
Knee Flexion IntervalCorrelation Coefficient
ACLDPTSTGT
rPrPrP
80°−70°.230.262−.580.015⁎.388.095
70°−60°.588.048⁎−.394.082.377.102
60°−50°.657.038⁎−.367.098.429.072
50°−40°.784.011⁎−.279.167−.010.487
40°−30°.741.011⁎−.188.260.006.492
30°−20°.702.017⁎−.061.481−.110.360
20°−10°.802.003⁎−.089.382−.257.198

NOTE. Derived from the Cincinnati Knee Rating System (1995) and hamstring antagonist torque generated during knee extension at 180/s for the involved limb of the ACLD (n=10), PT (n=14), and ST/gracilis tendon (n=13) groups.

Abbreviation: STGT, semitendinosus and gracilis tendon.

⁎A significant correlation.

  • View full-size image.
  • Fig 1. 

    Representative curves for hamstring antagonist torque (±SE) for a less functional ACLD subject and a more functional ACLD subject. Knee functionality scores for the less and more functional ACLD subjects were 44 and 88 points, respectively.

Back to Article Outline

Discussion 

Knee Functionality 

Knee functionality scores of the ACLD subjects were comparable to those of other studies that tested ACLD patients with similar characteristics to those included in the present study.41, 42 Therefore, ACLD subjects in the current study represented a cross-section of a typical, chronic ACLD population who were, on average, limited (according to the guidelines of Noyes et al32) to participating in sports involving running, twisting, and turning 1 to 3 times a month. Like the findings of Barber-Westin20 Tibone,43 and colleagues who also used the Cincinnati Knee Rating System, the results of the present study showed that subjects who choose to undergo ACLR can expect greater knee functional ability compared with those who prefer to manage their ACLD limb conservatively.

In accordance with several previous studies44, 45 that have incorporated the Cincinnati Knee Rating System, there were no significant differences between the PT and SM/gracilis tendon groups for knee functionality scores, indicating that both ACLR procedures were equivalent in terms of restoring knee joint function. It is also noteworthy that the average knee functionality scores for the ACLR groups in the present study exceeded 80 points, a common finding of studies incorporating similar ACLR subjects.20, 43, 44, 45 Nevertheless, average knee functionality scores of the ACLR subjects indicated that they had not returned to preinjury functional levels at an average time of 14.6±4.7 months since surgery and were only able to perform sports that involve jumping, hard pivoting, and cutting on a 3-day-a-week basis. Before ACL injury, both ACLR and ACLD subjects were able to participate in sports such as basketball, football, soccer, and field hockey 4 to 7 days a week.

Hamstring Antagonist Torque 

As depicted for representative ACLD subjects in figure 1, the opposing torque generated by the hamstrings at the start of the movement (ie, 80°–70° knee flexion) was very high and is thought to stabilize the knee joint during forceful acceleration of the lower limb. Given that ACL loads are increasing within the range of 40° to 10° knee flexion,46 escalating hamstring antagonist torque in this range would act to decrease ATT/ACL graft strain and provide the necessary dynamic restraint during deceleration of the lower limb.

Relation Between Knee Functionality and Hamstring Antagonist Torque 

Although Stener47 questioned whether rapid, quickly applied stress to the ACL might be successfully negated by the hamstring muscles, Aagaard et al48 speculated that the torque produced by eccentric hamstring contraction might minimize anterior tibial shear forces across the knee joint and thus improve function after ACL rupture. Consistent with the hypothesis of Aagaard et al,3 the results of this study indicated that ACLD subjects who generated higher amounts of hamstring antagonist torque between angles of 70° and 10° knee flexion showed higher levels of knee functionality. An increased opposing torque is thought to represent a protective mechanism mediated by the neuromuscular control apparatus. It is assumed that more functional ACLD patients use sensory feedback to build a new internal model to compensate for mechanical instability rather than relying on reflexive muscular activation in response to stimuli occurring during an activity.49

Although ATT is increased at all flexion angles after ACL rupture,6, 50 most giving-way episodes occur with the knee in a relatively extended position shortly after foot strike when performing locomotor activities such as running, pivoting, and jumping.51 Therefore, those subjects with greater hamstring antagonist torque at knee flexion angles representative of those found at initial contact and during deceleration showed higher levels of knee functionality, presumably because they were better able to restrain motion of the proximal tibia during deceleration of the lower limb under high load. An increased hamstring antagonist torque (ie, greater hamstring activation) would also increase stiffness of the hamstring musculature. A stiffer musculotendinous system is more advantageous than a compliant system in situations in which the ACL is subjected to acute strain15, 52; that is, stiff hamstring muscles are better able to counteract deleterious forces and may shield the secondary restraints within the knee (eg, menisci and collateral ligaments) from bearing the full responsibility of joint stability.53

Knee flexion angles of 70° to 40° are beyond the range of knee flexion typically used during single-limb deceleration.54 However, increased hamstring antagonist torque in this range is thought to control anterior tibial motion and maintain joint stability during tasks such as ascending stairs and during squatting. More et al6 reported that during a simulated squat exercise (to 90° knee flexion) in cadaveric knees, the addition of a hamstring antagonist torque significantly reduced ATT and improved joint stability throughout knee extension in the absence of the ACL. Because the hamstring muscles all meet the tibia at relatively large angles when the knee is flexed between 70° and 40°, the perpendicular projection of the hamstring force is naturally augmented in this range.46, 55 Therefore, an increased antagonist torque would further enhance the ability of the hamstrings to apply a large posterior stabilizing force. From a practical perspective, these associations specify the exact ranges of knee flexion that should be emphasized when implementing open kinetic chain eccentric exercises for the hamstrings in the post-ACL injury period.

Several studies6, 56, 57 have reported that hamstring activation is required to unload the reconstructed ACL during extension. Furthermore, deceleration parameters associated with significant antagonist activation during isokinetic knee extension have been positively correlated with functional performance measures requiring controlled rotation and deceleration after ACLR.31 In contrast, only negative correlations were identified between hamstring activation and knee functionality for the PT group in the present study, indicating that low hamstring torque is associated with higher levels of knee functionality. Nevertheless, knee functionality was only significantly correlated with hamstring antagonist torque generated between 80° and 70° knee flexion. Given that hamstring muscle force is required to guide and restrain knee motion under high loading,56, 57 this result appears contradictory in terms of making the knee stiffer and more difficult to perturb. However, More et al6 reported that, with the addition of low-level hamstrings load in situ, the ACL graft load is greatly reduced.

Unlike the PT group, no significant associations were identified between hamstring antagonist torque and knee functionality for the ST/gracilis tendon group. Hence, there is some evidence to suggest that the functional significance of hamstring antagonist torque after ACLR is graft specific. Attenuated hamstring antagonist torque in more functional PT subjects may be desirable to facilitate generation of the net extension torque, which is often compromised as a result of impaired quadriceps force generation because of ACL graft procurement.58, 59 However, it is important to note that the ST/gracilis tendon subjects were significantly younger and 8.5kg lighter, on average, compared with their PT graft counterparts. These inherent differences may have influenced the strength of the associations between knee functionality and hamstring antagonist torque for the ST/gracilis tendon subjects.

Study Limitations 

There are several limitations associated with this study. First, because of the study design, the subjects in the ACLD and ACLR groups were not entirely homogenous in that the ACLD subjects showed coping strategies (as determined by the surgeon) that may not have been present in the ACLR groups. Nevertheless, these potential differences are likely to be representative of the typical characteristics of these patient populations, and, thus, the findings are considered externally valid. Second, although the mathematical model used to predict hamstring antagonist torque was well justified and was based on methods used in previous studies using uninjured subjects,1, 4 it does not take into account the potential for variable hamstring anatomy. In this respect, although the hamstrings have been deemed functionally intact at 6 months postoperatively after ST/gracilis tendon graft procurement, the anatomy of the regenerated tendon may not exactly mimic that of the native ST tendon.60, 61 Hence, the relation between ST activity and the moment that this muscle generates during knee extension may be different in subjects having undergone ACLR using the ST/gracilis tendon graft. Additional errors may also be introduced when calculating the hamstring antagonist moments for the ST/gracilis tendon subjects given that EMG data from the ST muscle was also used to approximate the contribution of the SM muscle. Magnetic resonance imaging needs to be used in future studies incorporating ST/gracilis tendon subjects to clarify the cross-sectional area and insertional characteristics of the ST muscle so that these potential differences can be considered when estimating the antagonist torque generated by the medial hamstrings.

Third, although the results of the present study suggest that the magnitude of hamstring antagonist torque, for the most part, does not signify part of the successful coping mechanism after ACLR, it is important not to generalize these findings to ACLR subjects who are in the earlier phases of rehabilitation. It may be that the opposing torque generated by the hamstrings during the period in which the ACL graft is maturing and undergoing remodeling and revascularization (ie, during the first 6 months after ACLR62, 63) is particularly important to enhance knee joint stability and unload the ACL graft. Therefore, future studies examining the association between hamstring antagonist torque and knee functionality should be longitudinal in nature to examine these relationships at various time intervals after ACLR.

Finally, given that only male subjects were included in the present study, these results may not be applicable to female subjects given that their hamstring-activation strategies may be different from their male counterparts.64 Hence, studies performed in the future should also include female ACLD and ACLR subjects with similar hormonal characteristics (ie, at a certain phase of their menstrual cycle) to minimize confounding factors such as joint laxity and muscle viscoelastic properties that are a response to estrogen fluctuations.11, 12, 13, 14, 15

Back to Article Outline

Conclusions 

An increased opposing torque generated by the hamstring muscles of more functional ACLD subjects may represent a protective mechanism mediated by the neuromuscular control apparatus to compensate for mechanical instability. The restoration of anterior knee stability through the process of ACLR is thought to negate the need for increased hamstring antagonist torque. These results may assist in formulating treatment-specific training exercises and rehabilitation programs to obtain optimal function after ACL injury and ACLR.

Suppliers

Back to Article Outline

References 

  1. Baratta R, Solomonow M, Zhou BH, Letson D, Chuinard R, D'Ambrosia R. Muscular coactivation: the role of the antagonist in maintaining knee stability. Am J Sports Med. 1988;16:113–122
  2. Solomonow M, Krogsgaard M. Sensorimotor control of knee stability (A review). Scand J Med Sci Sports. 2001;11:64–80
  3. Aagaard P, Simonsen EB, Andersen JL, Magnusson SP, Bojsen-Moller F, Dyhre-Poulsen P. Antagonist muscle coactivation during isokinetic knee extension. Scand J Med Sci Sports. 2000;10:58–67
  4. Kellis E, Baltzopoulos V. The effects of antagonist moment on the resultant knee joint moment during isokinetic testing of the knee extensors. Eur J Appl Physiol Occup Physiol. 1997;76:253–259
  5. Hagood S, Solomonow M, Baratta R, Zhou BH, D'Ambrosia R. The effect of joint velocity on the contribution of the antagonist musculature to knee stiffness and laxity. Am J Sports Med. 1990;18:182–187
  6. More RC, Karras BT, Neiman R, Fritschy D, Woo S, Daniel DM. Hamstrings—an anterior cruciate ligament protagonist (An in vitro study). Am J Sports Med. 1993;21:231–237
  7. Pandy MG, Shelburne KB. Dependence of cruciate-ligament loading on muscle forces and external load. J Biomech. 1997;30:1015–1024
  8. Mattacola CG, Perrin DH, Gansneder BM, Gieck JH, Saliba EN, McCue FC. Strength, functional outcome, and postural stability after anterior cruciate ligament reconstruction. J Athl Train. 2002;37:262–268
  9. Hiemstra LA, Webber S, MacDonald PB, Kriellaars DJ. Knee strength deficits after hamstring tendon and patellar tendon anterior cruciate ligament reconstruction. Med Sci Sports Exerc. 2000;32:1472–1479
  10. Beynnon BD, Johnson RJ, Fleming BC, et al. Anterior cruciate ligament replacement: comparison of bone-patellar tendon-bone grafts with two-strand hamstring grafts (A prospective, randomized study). J Bone Joint Surg Am. 2002;84-A:1503–1513
  11. Hewett TE. Neuromuscular and hormonal factors associated with knee injuries in female athletes: strategies for intervention. Sports Med. 2000;29:313–327
  12. Romani W, Curl LA, Lovering R. The effect of endogenous estradiol levels at three phases of the menstrual cycle on anterior cruciate ligament stiffness in active females. J Athl Train. 2001;2:S62
  13. Romani W, Patrie J, Curl LA, Flaws JA. The correlations between estradiol, estrone, estriol, progesterone, and sex hormone-binding globulin and anterior cruciate ligament stiffness in healthy, active females. J Womens Health (Larchmt). 2003;12:287–298
  14. Shultz SJ, Kirk SE, Johnson ML, Sander TC, Perrin DH. Relationship between sex hormones and anterior knee laxity across the menstrual cycle. Med Sci Sports Exerc. 2004;36:1165–1174
  15. Eiling E, Bryant AL, Petersen W, Murphy A, Hohmann E. Effects of menstrual-cycle hormone fluctuations on musculotendinous stiffness and knee joint laxity. Knee Surg Sports Traumatol Arthrosc. 2007;15:126–132
  16. Gauffin H, Pettersson G, Tropp H. Kinematic analysis of one-legged long hopping in patients with an old rupture of the anterior cruciate ligament. Clin Biomech (Bristol, Avon). 1990;5:41–46
  17. Gauffin H, Tropp H. Altered movement and muscular-activation patterns during the one-legged jump in patients with an old anterior cruciate ligament rupture. Am J Sports Med. 1992;20:182–192
  18. Chmielewski TL, Hurd WJ, Snyder-Mackler L. Elucidation of a potentially destabilizing control strategy in ACL deficient non-copers. J Electromyogr Kinesiol. 2005;15:83–92
  19. Buss DD, Warren RF, Wickiewicz TL, Galinat BJ, Panariello R. Arthroscopically assisted reconstruction of the anterior cruciate ligament with use of autogenous patellar-ligament grafts (Results after twenty-four to forty-two months). J Bone Joint Surg. 1993;75:1346–1355
  20. Barber-Westin SD, Noyes FR, Andrews M. A rigorous comparison between the sexes of results and complications after anterior cruciate ligament reconstruction. Am J Sports Med. 1997;25:514–526
  21. Brown CH, Steiner ME, Carson EW. The use of hamstring tendons for anterior cruciate ligament reconstruction (Technique and results). Clin Sports Med. 1993;12:723–756
  22. Shelbourne KD, Nitz P. Accelerated rehabilitation after anterior cruciate ligament reconstruction. Am J Sports Med. 1990;18:292–299
  23. Corry IS, Webb JM, Clingeleffer AJ, Pinczewski LA. Arthroscopic reconstruction of the anterior cruciate ligament (A comparison of patellar tendon autograft and four-strand hamstring tendon autograft). Am J Sports Med. 1999;27:444–454
  24. MacDonald PB, Hedden D, Pacin O, Huebert D. Effects of an accelerated rehabilitation program after anterior cruciate ligament reconstruction with combined semitendinosus-gracilis autograft and a ligament augmentation device. Am J Sports Med. 1995;23:588–592
  25. Noyes FR. The Noyes knee rating system. Cincinnati: Cincinnati Sportsmedicine and Education Foundation; 1995;
  26. Daanen HA, Mazure M, Holewijn M, Van der Velde EA. Reproducibility of the mean power frequency of the surface electromyogram. Eur J Appl Physiol Occup Physiol. 1990;61:274–277
  27. De Luca CJ. Control properties of motor units. J Exp Biol. 1985;115:125–136
  28. Kannus P. Isokinetic evaluation of muscular performance: Implications for muscle testing and rehabilitation. Int J Sports Med. 1994;15(Suppl 1):S11-S8
  29. Tegner Y, Lysholm J, Lysholm M, Gillquist J. A performance test to monitor rehabilitation and evaluate anterior cruciate ligament injuries. Am J Sports Med. 1986;14:156–159
  30. Wiklander J, Lysholm J. Simple tests for surveying muscle strength and muscle stiffness in sportsmen. Int J Sports Med. 1987;8:50–54
  31. Wilk KE, Romaniello WT, Soscia SM, Arrigo CA, Andrews JR. The relationship between subjective knee scores, isokinetic testing, and functional testing in the ACL-reconstructed knee. J Orthop Sports Phys Ther. 1994;20:60–73
  32. Noyes FR, Barber SB, Mooar LA. A rationale for assessing sports activity levels and limitations in knee disorders. Clin Orthop Relat Res. 1989;246:238–249
  33. McNair PJ, Wood GA, Marshall RN. Stiffness of the hamstring muscles and its relationship to function in anterior cruciate deficient individuals. Clin Biomech (Bristol, Avon). 1992;7:131–173
  34. Bryant AL, Kelly J, Hohmann E. Neuromuscular adaptations and correlates of knee functionality following ACL reconstruction. J Orthop Res. 2008;26:126–135
  35. Winter DA. Biomechanics and motor control of human movement. 2nd ed.. New York: Wiley-Interscience; 1990;
  36. Steele JR, Brown JM. Effects of chronic anterior cruciate ligament deficiency on muscle activation patterns during an abrupt deceleration task. Clin Biomech (Bristol, Avon). 1999;14:247–257
  37. Kellis E, Baltzopoulos V. The effects of normalization method on antagonistic activity patterns during eccentric and concentric isokinetic knee extension and flexion. J Electromyogr Kinesiol. 1996;6:235–245
  38. Wickiewicz TL, Roy RR, Powell PL, Edgerton RV. Muscle architecture of the human lower limb. Clin Orthop Relat Res. 1983;179:275–283
  39. Kellis E, Baltzopoulos V. In vivo determination of the patella tendon and hamstrings moment arms in adult males using videofluoroscopy during submaximal knee extension and flexion. Clin Biomech (Bristol, Avon). 1999;14:118–124
  40. Smidt GL. Biomechanical analysis of knee flexion and extension. J Biomech. 1973;6:79–92
  41. Li RC, Maffulli N, Hsu YC, Chan KM. Isokinetic strength of the quadriceps and hamstrings and functional ability of anterior cruciate deficient knees in recreational athletes. Br J Sports Med. 1996;30:161–164
  42. McNair PJ. Neuromuscular adaptations associated with anterior cruciate ligament deficiency [dissertation]. Perth: University of Western Australia; 1991;
  43. Tibone JE, Antich TJ. A biomechanical analysis of anterior cruciate ligament reconstruction with patellar tendon: A two year followup. Am J Sports Med. 1988;16:332–335
  44. Aune AK, Holm I, Risberg MA, Jensen HK, Steen H. Four-strand hamstring tendon autograft compared with patellar tendon-bone autograft for anterior cruciate ligament reconstruction (A randomized study with two-year follow-up). Am J Sports Med. 2001;29:722–728
  45. Feller JA, Webster KE. A randomized comparison of patellar tendon and hamstring tendon anterior cruciate ligament reconstruction. Am J Sports Med. 2003;31:564–573
  46. Shelburne KB. Modeling the mechanics of the normal and reconstructed knee joint [dissertation]. Austin: University of Texas; 1997;
  47. Stener B. Experimental evaluation of the hypothesis of ligament-muscular protective reflexes I (A method for adequate stimulation of tension receptors in the medial collateral ligament of the knee joint of the cat, and studies of the innervation of the ligament). Acta Physiol Scand. 1959;48(Suppl):5–26
  48. Aagaard P, Simonsen EB, Dyhre-Poulsen P. A noninvasive method for measuring antagonist co-contraction force during isokinetic knee extension and flexion. Scand J Med Sci Sports. 1994;4:286
  49. Swanik CB, Lephart SM, Swanik KA, Stone DA, Fu FH. Neuromuscular dynamic restraint in women with anterior cruciate ligament injuries. Clin Orthop Relat Res. 2004;425:189–199
  50. Pandy MG, Shelburne KB. Theoretical analysis of ligament and extensor-mechanism function in the ACL-deficient knee. Clin Biomech (Bristol, Avon). 1998;13:98–111
  51. McNair PJ, Marshall RN, Matheson JA. Disability and strength of athletes with anterior cruciate ligament deficiency. N Z J Sports Med. 1990;14:537–539
  52. Granata KP, Padua DA, Wilson SE. Gender differences in active musculoskeletal stiffness (Part II. Quantification of leg stiffness during functional hopping tasks). J Electromyogr Kinesiol. 2002;12:127–135
  53. McNair PJ, Marshall RN. Landing characteristics in subjects with normal and anterior cruciate ligament deficient knee joints. Arch Phys Med Rehabil. 1994;75:584–589
  54. McNitt-Gray JL. Kinematics and impulse characteristics of drop landings from three heights. Int J Sport Biomech. 1991;7:201–224
  55. Hirokawa S, Soiomonow M, Luo Z, Lu Y, D-Ambrosia R. Muscular co-contraction and control of knee stability. J Electromyogr Kinesiol. 1991;1:199–208
  56. Draganich LF, Vahey JW. An in vitro study of anterior cruciate ligament strain induced by quadriceps and hamstrings forces. J Orthop Res. 1990;8:57–63
  57. Renstrom P, Arms SW, Stanwyck TS, Johnson RJ, Pope MH. Strain within the anterior cruciate ligament during hamstring and quadriceps activity. Am J Sports Med. 1986;14:83–87
  58. Lephart SM, Perrin OH, Fu FH, Minger K. Functional performance tests for the anterior cruciate ligament insufficient athlete. J Athl Train. 1991;26:44–50
  59. Harter RA, Osternig LR, Standifer LW. Isokinetic evaluation of quadriceps and hamstring symmetry following anterior cruciate ligament reconstruction. Arch Phys Med Rehabil. 1990;71:465–468
  60. Ferretti A, Conteduca F, Morelli F, Masi V. Regeneration of the semitendinosus tendon after its use in anterior cruciate ligament reconstruction: a histologic study of three cases. Am J Sports Med. 2002;30:204–207
  61. Cross MJ, Roger G, Kujawa P, Anderson IF. Regeneration of the semitendinosus and gracilis tendons following their transection for repair of the anterior cruciate ligament. Am J Sports Med. 1992;20:221–223
  62. Kleiner JB, Amiel D, Roux RD, Akeson WH. Origin of replacement cells for the anterior cruciate ligament autograft. J Orthop Res. 1986;4:466–474
  63. Johnson LL. The outcome of a free autogenous semitendinosus tendon graft in human anterior cruciate reconstructive surgery: a histological study. Arthroscopy. 1993;9:131–142
  64. 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;11:263–268
  • a SPSS for Windows, SPSS Inc, 233 S Wacker Dr, 11th Fl, Chicago, IL 60606.
  • b Metex M–3650 impedance meter; Jamwondong 15-4 metex Seo cho gu, Seoul, Korea 137-030.
  • c Quantec, 128 Waterworks Rd, Ashgrove, Queensland, 4060, Australia.
  • d Cybex Isokinetic Dynamometer; CSMI Solutions, 101 Tosca Dr, Stoughton, MA 02072 .
  • e AMLAB signal acquisition system; Associative Measurement, 6 Lyon Park Rd, North Ryde, New South Wales, 2113, Australia.
  • f Visual Basic Version 5.0; Microsoft Corp, One Microsoft Way, Redmond, WA 98052-6399.

 No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit on the authors or on any organization with which the authors are associated.

 Reprints are not available from the author.

PII: S0003-9993(08)00834-4

doi:10.1016/j.apmr.2008.04.027

Archives of Physical Medicine and Rehabilitation
Volume 89, Issue 12 , Pages 2324-2331, December 2008

Article Tools

* Image Usage & Resolution