Rupture of the anterior cruciate ligament (ACL) represents a considerable proportion of sports-related injuries and is associated with various functional adaptations.2,21,22,57,60 Strength deficits have been examined.7,32,37,38,48 The strength profile of the quadriceps and hamstrings is influenced by the neural effects of ACL injury,36,52,53,59 and by disuse of the limb.63,64 Although injury adaptations are time-dependent to a large extent, investigations of thigh muscle weakness after ACL rupture have focused mainly on patients after reconstructive surgery.23,27,49,54 Furthermore, data for patients with ACL deficiencies arise primarily from patients greater than 18 months past injury.7,34,38,48,55,62 Studies examining patients with ACL deficiencies at a shorter time from injury are rare.3,64 Generally, variations have been reported in the level of thigh muscle weakness, ranging from approximately 10%48 to greater than 25%3,64 for the quadriceps and from negligible7,34 to greater than 15%3 for the hamstrings. Side- to-side differences in strength range to as much as 15%, and the effect of time on this variable is not well understood.7,32,37,38,43,55,58 However, a large deficit for the quadriceps and hamstrings (> 25%) appears only in one study with a chronicity of approximately 9 months,3 a time distinctly shorter than for most studies. Also, the percent strength deficit is reported as greater and more persistent in the quadriceps than with the hamstrings.3,7,26,32,38 Differential findings64 could be attributed to study variations, therefore leaving the area of functional muscle adaptations through chronicity open for additional investigation.
Functional performance often is tested via closed kinetic chain activities incorporating hopping or twisting movements.6,17,45,62 However, multijoint testing may obscure substantial and clinically important weakness in a part of the kinetic chain compensated by other joints.18
Those underlying deficits can be revealed by using the highly reliable single-joint isokinetic dynamometry1,48 which is an integral evaluative tool for thigh muscle function.8,12,62 Achieving acceptable levels of quadriceps and hamstrings strength is a key criterion for progressive rehabilitation after ACL rupture,51,61 as strength adaptations partly reflect the stabilizing potential of these muscles for the ACL-deficient knee.5,29,40,44 Identifying strength adaptations at different times after injury would be useful in rehabilitation planning as it would make the goal of strengthening exercise clearer for each time.
Patients' adherence to rehabilitation may be a confounding factor for the functional status of their muscles because protocols vary.19 When regularly performing athletes avoid rehabilitation, the strength deterioration after injury may be more profound compared with individuals who are nonathletic because the intact side of the athletes seems to be affected by limb disuse.9,22 Therefore, we suspect side-to-side differences may not reveal the overall effect of ACL rupture on muscle strength. Comparing amateur athletes who abstained from structured rehabilitation after ACL rupture with healthy amateur athletes of similar activity levels seems to be a reasonable method to measure the effect of ACL rupture on muscle function of the quadriceps and hamstrings at different stages of chronicity.
We hypothesized that quadriceps and hamstrings strength in amateur athletes with ACL deficiencies who abstained from rehabilitation would be less than the strength of control subjects matched for the preinjury level of sports activity. We also studied whether the quadriceps and hamstrings side-to-side asymmetry in strength was consistently different during all stages of chronicity.
MATERIALS AND METHODS
We retrospectively tested the quadriceps and hamstrings strength of 36 patients with unilateral ACL-deficient knees. They were divided into three equal groups (n = 12) according to time from injury (chronicity).64 The short-term group included patients injured for 6 months or less, representing a vulnerable postinjury period. The intermediate-term group included patients 6 to 18 months postinjury who we considered adapted to activities of daily living. The long-term group included patients 18 months or more postinjury. All patients were male athletes regularly participating in amateur leagues of cutting and twisting sports (ie, soccer, basketball, and handball). None of the patients followed any specific rehabilitation intervention after their injury apart from the acute phase strategy of rest, immobilization, compression, and elevation to minimize joint effusion. The reasons for abstaining from structured rehabilitation included difficulty to access physiotherapy clinics or other personal, financial, or professional reasons. These groups were compared with a control group of 12 healthy individuals with physical activity similar to the preinjury status of the patients with ACL deficiencies. All subjects agreed with the testing protocol and gave their consent in accordance with university policies.
Injured participants were tested for arthroscopic reconstruction by one of the authors (ADG). Inclusion criteria consisted of ACL rupture verified by magnetic resonance imaging (MRI), preinjury involvement in soccer, basketball, or handball with at least three training and game-playing sessions per week before injury, and no involvement in physical therapy or structured exercise after injury. Exclusion criteria included serious reinjury requiring immobilization, severe symptoms during testing attributed to any concomitant articular or muscle injury, severe meniscal lesions observed on MRI or clinical examination, any previous knee surgery including the healthy side or other ligaments, instability, and history of serious injury to the lower limbs. Based on previously reported means and standard deviations (SD) of isokinetic tests on athletes with ACL deficiencies,58 we estimated 12 participants in each group would be enough to address the primary research question of comparing quadriceps and hamstrings strength of patients with ACL deficiencies with strength of healthy control subjects to fulfill the power criterion of ≥ 0.80.24 Subsequent power analysis revealed a satisfactory level of at least 0.846 (quadriceps long-term versus control) among comparisons of strength between any of the chronicity groups and the control group.
Isokinetic testing of the thigh muscles was performed using Biodex system-3 (Biodex Corp, Shirley, NY). Each subject completed a 5-minute warmup of stationary cycling at self-selected submaximal intensity followed by 2 minutes of stretching. Subjects were positioned on the isokinetic dynamometer and stabilized according to standard procedures. Range of motion (ROM) of the knee was set from 90° flexion to full extension. A standard warmup consisting of five repetitions of incremental intensity from 50% to 100% was performed using a dynamometer. After 1 minute of complete rest, five extension and flexion cycles of maximal concentric contraction were performed at 60° per second (1.05 rads second−1). The testing order of the knees was randomized. The testing speed of 60° per second was based on evidence that strength deficits tend to be magnified under greater stress levels, which are produced at lower isokinetic speeds.33 Slow isokinetic speeds also provide a longer true isokinetic period, avoiding the inertial effects of acceleration and deceleration periods that might interfere with the validity of the results.30 Additionally, 60° per second is not as stressful as even lower speeds for the knee,33,35 and it is the most routinely used speed which allows for comparisons to be made (Table 1).3,7,25,26,32,34,37,38,47,48,55,58,64 Despite limitations arising from the presence of cocontraction of the antagonist muscles during testing,35 the concentric peak torque of the knee extensors and flexors extracted from the ASCII files was considered the maximal strength of the quadriceps and hamstrings, respectively. Isokinetic testing was performed by the same examiner (ET) who was blinded to grouping. Questionnaires were answered during an interview with another examiner (SR). To confirm the maximum torque for all trials was achieved within the preset angular velocity, we examined all the angular velocity plots provided by the dynamometer.35 The dependent variable was the peak torque value normalized for body mass (BM) to guard against possible interference of intergroup BM differences.48
Additional tests were performed (ET) to complete the patients' profiles. Static anterior tibial translation was measured by the standard method of arthrometry with the KT-1000 arthrometer (MEDmetric® Corp, San Diego, CA), and laxity was represented by side-to-side differences in millimeters. Both knees were tested randomly with a manual maximum pull by the same experienced examiner (ET). Knee function was assessed via the 100-grade Lysholm questionnaire. It was used to determine pain, effusion, instability, and functional aspects such as stair climbing or deep squatting.42 The level of physical activity was estimated by the 10-point Tegner scale. It was used to classify patients according to their involvement in knee-loading activities. The lowest score starts from inability to walk and increases toward cutting and twisting activities; the highest score corresponds to the level of elite soccer.56 Leg dominance was assessed through a previously reported questionnaire consisting of six questions regarding leg preference during dynamic, skillful, or mixed activities (eg, jumping, balancing on a beam, or kicking a ball).58
The level of significance was set at the α = 0.05 level. One-way analysis of variance (ANOVA) was used to compare the demographic characteristics to identify the degree of similarity across the tested groups. The functional characteristics (Lysholm score, Tegner scale preinjury, Tegner scale preinjury/postinjury differences, and KT-1000 side-to-side differences) were compared using the nonparametric Kruskal-Wallis test for independent samples. The experimental groups were compared according to the proportion of injury occurrence to the dominant versus the nondominant knee using a chi square test. This was done to ensure leg dominance had minimal influence on the results. The strength of the injured side of the three experimental groups (short term, intermediate term, long term) against the control group was tested via one-way ANOVA followed by Dunnett's post hoc analysis. The differences between the three groups were tested via one-way ANOVA followed by Bonferroni's post hoc analysis. The same statistics were used when the percent side-to-side difference was the tested variable. The strength deficits were expressed as (1) percentages of the healthy knee strength, and the asymmetry in the control group was expressed as (2) a percentage of the dominant knee strength: (1) (healthy-ACL-deficient)*100/healthy and (2) (dominant- nondominant)*100/dominant.
In the three experimental groups, the quadriceps and ham- strings strength did not fully recover at any time after injury. The short-term, intermediate-term, and long-term groups produced lower peak torque (PT) values adjusted for BM (PT/BM) than the control group for knee extension (F = 9.834; p = 0) by 32%, 30.5%, and 21.8%, respectively (p = 0, p = 0, p = 0.011, respectively). The short-term, intermediate-term, and long-term groups also produced lower PT/BM values than the control group for knee flexion (F = 6.642; p = 0.001) by 30.3%, 24.5%, and 21%, respectively (p = 0, p = 0.005, p = 0.006, respectively) (Fig 1).
The side-to-side strength deficits during knee extension of 23.5%, 15.9%, and 10% for the short-term, intermediate-term, and long-term groups were greater (F = 10.956: p = 0) than the 2.7% strength asymmetry in the control group (p = 0, p = 0.001, p = 0.027, respectively). During knee flexion, the strength asymmetry in the respective groups was 14%, 8%, and 0.4%, and it was greater (p = 0.003) only in the short-term group compared with the control group (5.7%). The long-term group had lower deficits than the short-term group in extension (p = 0.023) and flexion (p = 0.037). There were no other differences among the three chronicity groups (Fig 2). An obvious trend was toward reduction of the percent deficits with time expressed by a linearity for knee extension (F = 6.647; p = 0.015) and flexion (F = 5.356; p = 0.027). In addition to the quantitative differences among the three experimental groups, there also were obvious qualitative differences of clinical importance (Figs 3, 4). Hamstrings testing showed more patients were close to a balanced strength between the injured and the uninjured sides, and some were even stronger on the affected side.
All groups were similar in terms of age, BM, and height (Table 2). The Lysholm scores were not different among the experimental groups, but all were lower (p < 0.001) than the scores of the control group. The Tegner scale values before injury were similar among the experimental groups, but the ACL rupture caused decreased (p < 0.001) Tegner scores which did not differ across groups. Knee anterior laxity was similar in all groups and greater (p < 0.001) than that of the control group (Table 3). The proportion of injury to the dominant limb did not differ among groups. The strength of the dominant and nondominant sides in the control group was not different for extension or flexion.
We isokinetically tested the strength of the thigh muscles of three different groups of amateur athletes with ACL deficiencies who abstained from structured rehabilitation.
Those groups represented injury chronicity of short term (< 6 months), intermediate term (6-18 months), and long term (> 18 months). We hypothesized that quadriceps and hamstrings strength in patients with ACL deficiencies would be less than the strength of healthy control subjects. We also questioned whether the quadriceps and hamstrings side-to-side asymmetry in strength would be consistent in all stages of chronicity.
The retrospective design of the study is a limitation related to the chronicity of patients in the long-term group (mean, 56 months). However, we think its effect was minimized after careful matching of the control group with the patients. By confirming the postinjury reduction of physical activity did not differ across chronicity groups, we excluded different levels of detraining from influencing the results. Another limitation is that study participants were not tested against patients with ACL deficiencies after specific rehabilitation. However, this does not compromise the importance of our results because it establishes a basis for future studies. Statistical power was satisfactory for any comparison between knees with ACL deficiencies and healthy knees of control subjects because it exceeded 0.80. On the contrary, side-to-side comparisons among groups were underpowered because of the normally high variability of these values. The persistent deficit of the quadriceps in contrast to the regained symmetry of the hamstrings strength in the subacute phase is clinically important7,8,12,61 regardless of statistical significance. Patients' performance was tested only isokinetically; however, this mode holds a key role in functional assessment,62 and changes in muscle strength have been shown to reflect a global improvement in muscle properties including neural changes.10 This is supported by how quadriceps strength is connected with functional ability,20,39,41 whereas hamstring strength has been associated with ACL injury prevention,28 improved performance,47,58,65 and return to physical activity after ACL injury.50 Additionally, weakness of both muscle groups has been connected with increased tibiofemoral instability in patients with ACL deficiencies during running.11
Our findings provide a basis for strength testing of athletes with ACL deficiencies at different times of injury chronicity. Despite that isokinetic data for ACL-deficient knees are abundant, crucial differences in methods make comparisons difficult. In numerous studies,7,25,26,32,34,37,38,47,48,55,58 with one exception,3 patients were examined at a mean of at least 1.5 years after ACL rupture. In only one study were patients examined at different times after ACL rupture.64 Only a few studies compared the strength of patients with ACL deficiencies with the strength of healthy control subjects at 60° per second (Table 1).3,37,47,48,64
Quadriceps and hamstrings weakness existed in all chronic stages after ACL rupture in untreated amateur athletes formerly involved in cutting and twisting sports. We can make limited comparisons with the literature because only one study has a similar design.64 The strength difference from the control subjects ranged from 21% to 32% depending on the muscle group and level of chronicity. This degree of weakness compares with the greatest levels reported in the literature. These included a study examining patients with the least chronicity (9 months)3 and a study comparing patients with control subjects who exercised more systematically than subjects in the other studies.58 Some studies show lesser degrees of weakness,37,47,48 but all were greater than 7.2%.64 We think our data are important because the control group was exercising regularly at a high level (median Tegner scale, 7), whereas in other studies, control subjects were sedentary or only exercised recreationally.3,20,48
We used the same separation criteria (6 and 18 months) for time grouping as used by Wojtys and Huston.64 We also found quadriceps and hamstrings were weaker after ACL rupture regardless of the time since injury. However, strength difference between patients and control subjects decreased with time in our study. This contradiction, which was exaggerated in the hamstrings, can be explained by how Wojtys and Huston examined patients with the best and the worst function in each time group separately. Their chronic group consisted of a large proportion of patients with poor performance (84%), affecting the mean strength considerably. Differences in the proportion of men and women between groups also might have interfered with their results.
The majority of isokinetic studies on patients with ACL deficiencies focus on side-to-side deficits, neglecting the effects of the usual postinjury reduction of physical activity on the intact limb.7,25,26,32,34,38,55 Side-to-side strength difference revealed asymmetry in the quadriceps and hamstrings strength vanished with time, leading to a more symmetric and economic performance.4 However, the adaptation pattern was different between muscle groups with time. The mean quadriceps deficit was important in all groups, especially in the long-term patients who had a fourfold difference compared with the natural symmetry of the control group. The hamstrings revealed a different profile of adaptation as the deficit was significant only within 6 months after injury. After that time, it approximated the level of normal asymmetry and was reversed in many patients. This observation supports the clinical importance of side-to-side differences. Our findings generally agreed with the percentages reported for side-to-side differences, with the greatest asymmetry measured in the patients with the shortest chronicity (Table 1).3
The quadriceps muscle was affected to a greater degree possibly because of postinjury neural inhibition from the loss of afferent feedback from the ACL to gamma moto-neurons,36,52 the adaptation toward a quadriceps avoidance gait pattern2,60 to prevent anterior subluxation,5,29 and because limited loading of limbs promoted quadriceps weakness in patients with ACL deficiencies.31 The greater atrophy of the quadriceps (10% versus 4%) reported even 1 year after injury22 might additionally explain their higher deficit compared with the hamstrings. In contrast, there is evidence that the hamstrings are recruited in weightbearing activities in a subconscious attempt to counteract anterior shear forces.53,59 This stimulus might have assisted with the improvements in our patients. Evidence in the literature also supports the development of subtle electro-physiologic modifications in patients with ACL deficiencies that retune the hamstrings and preprogram their muscle activation strategies to optimize shear force dissipation during injured knee loading.12-14,16,43 The strength asymmetry of the quadriceps was in accordance with reported strength.7,32,37,38,48 Full symmetry of the hamstrings can be expected15 or even a reverse favoring of the affected side.46
Although the effect of a structured exercise program on muscle strength in patients with ACL deficiencies was not investigated directly, the resulting weakness could be attributed to the lack of adequate training along with the reduction of physical activity to safer levels. Organized rehabilitation could prevent this weakness because it has been proven beneficial for muscles41 and has enabled some patients to return to the preinjury level of physical activity.17 Zatterstrom et al65 found supervised training induced improvements ranging from 8.4% to 11.6% in strength and endurance to the quadriceps and hamstrings after ACL rupture treated nonoperatively. Almost ½ their patients who started a self-monitored program required supervision during the process, indicating the need for organized and guided exercise.
A structured rehabilitation program might provide more complete strength recovery after ACL injury. The rehabilitation program should strive to limit thigh muscle weakness after ACL rupture, reduce the quadriceps side- to-side deficit to clinically acceptable levels, and assist the hamstrings to regain strength faster. These benefits could enhance the natural reaction of the body against anterior knee instability. The effect of organized rehabilitation protocols on the course of strength adaptations after ACL injury has yet to be examined. A promising research area is investigating whether early and intensive postinjury strengthening of the hamstrings will allow more patients with ACL deficiencies to cope. Similarly, it could be investigated whether this intervention improves knee function before ACL reconstruction, optimizing the functional background for the operation or enhancing functional recovery.
We thank the Prefecture of Ioannina for research support.
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