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CLINICAL SCIENCES: Clinically Relevant

Tibialis Anterior Volumes and Areas in ACL-Injured Limbs Compared with Unimpaired

BINDER-MACLEOD, BENJAMIN I.; BUCHANAN, THOMAS S.

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Medicine & Science in Sports & Exercise: September 2006 - Volume 38 - Issue 9 - p 1553-1557
doi: 10.1249/01.mss.0000227642.06478.8f
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Abstract

Most patients cannot return to normal levels of activity after a full ACL tear. They lose knee stability, and their knees give way during activities that prevent them from participating in active sports (6,8). These patients are commonly called noncopers because they cannot cope with their injuries unless they have surgery. There is, however, a small percentage of patients who sustain a full ACL tear but are able to go back to normal activity without surgery. They can participate in sports that involve loading the knee, such as sideways cutting and jumping, without incidence of giving way. These are called copers because they can cope with their injury (14,20).

It would be beneficial to determine how the copers cope with their injuries and how they are different from noncopers. Much research has been conducted on the muscles that control the knee of ACL-deficient patients. It has been shown that muscles that control the knee are affected by the ACL injuries more in the noncopers than in the copers, but the underlying mechanism for this is still being debated (2,20,22). Although it has been argued that people with ACL deficiencies avoid using their quadriceps (2,7), others have argued that this is not the case for noncopers (4,9,15). Nevertheless, it has been shown that the muscles of the quadriceps greatly atrophy after an ACL injury in noncopers, whereas the quadriceps of copers do not atrophy compared with uninjured subjects (24,23). However, no atrophy for either group was noted in the hamstrings (23). Thus, it has been established that the muscles of the knee are affected differently in each muscle group. However, it is plausible that the muscle groups at the ankle of ACL-injured people might also show size differences, because it is known that the gait patterns are different between injured and uninjured people (1,13). Studies have shown that during different movements including walking, the angle of flexion and moments of the ankle are less in injured subjects than in uninjured subjects (3,21). It has also been shown that the moments and angles of the joints in the lower leg of copers are similar to those of the uninjured, whereas noncopers continue to have smaller moments and flexion angles (17).

The purpose of this study was to discover how the muscles that control the ankle are affected by an ACL injury in both copers and noncopers by finding their volumes and cross-sectional areas (CSA). Differences in the CSA and volume of the muscle are indicators that the muscles may play different functional roles in these groups. We hypothesized that muscles that control the ankle of the ACL-deficient leg in the noncopers will atrophy like the muscles of the knee. We believe this potential atrophy could be caused by the smaller moments and angular articulation, which would cause a decrease and change in the use of the muscles that control the ankle. We also hypothesized that the muscles that control the ankle for the copers will not atrophy and will be similar to those of uninjured people.

METHODS

Subjects.

This study included 27 subjects who volunteered to participate in the study (nine ACL-deficient noncopers, nine ACL-deficient copers, and nine subjects with no history of knee injury). All subjects participated regularly (≥ 50 h·yr−1) in activities that challenge the knee joint with jumping and/or quick changes in direction. Each group consisted of both males and females, age 27.67 ± 11.28. The uninjured group comprised three females and six males, age 21 ± 7.14. The copers consisted of two females and seven males; four of these subjects had injured their dominant leg, and five had injured their nondominant leg, age 37.22 ± 8.69. The noncopers consisted of three females and six males, five who had injured their dominant leg and four who had injured their nondominant leg, age 24.78 ± 11.18.

All ACL tears were diagnosed by an orthopedic surgeon and were confirmed with magnetic resonance imaging (MRI) and knee arthrometry. An established screening process, which differentiates people who may be able to cope with an ACL injury and those who are not able to cope, was used to identify the noncopers (10). Prerequisites for this screening examination included the resolution of physical and functional impairments such as joint effusions, gait abnormalities, and range of motion deficits. Copers were defined as those who have returned to level 1 or level 2 activities, have not had any episodes of giving way for at least a year, and have had less than one episode of giving way since the injury (0.22 ± 0.44 of episodes of giving way). Also, copers had to report a high level of knee function (≥ 80 score) on the Knee Outcomes Survey Activities of Daily Living (12) and global rating knee function scales (12,25). Enrollment exclusion criteria included previous ACL injury, concomitant ligament pathology, fractures, greater than a trace knee joint effusion, an abnormal gait pattern, and the presence of hip or ankle pathology. Those who failed the coper screen test were labeled as noncopers. The noncopers all had recent ACL injuries to prevent confounding effects from knee instability (1.94 ± 1.70 months, range = 0.5-6 months). In contrast, copers were required to have had the injury for at least 1 yr (66.25 ± 70.10 months, range = 14-216 months) to verify their status as copers. Uninjured subjects were matched to the noncopers by age, gender, and preinjury activity level. This study was approved by the University of Delaware human subject review board, and written informed consent was obtained from all the subjects.

Evaluation of the muscles.

Axial spin-echo T1-weighted MRIs were taken from the level of the ankle mortise to the iliac crest while the subjects were positioned supine in a 1.5-T SignaLX scanner (General Electric Medical Systems, Milwaukee, WI). The images were done in four sequences: lower leg, knee, thigh, and pelvis; both limbs were imaged at the same time using the scanner's body coil. The imaging protocol was as follows: repetition time, 350 ms; echo time, 9 ms; slice thickness, 10 mm (except in the knee section, where it was 5 mm for more detailed tendon data); gap between slices, 1.5 mm (except in knee section, where it was 1.0 mm) with a 256 × 160 matrix and a field of view that varied with the size of the subject.

The tibialis anterior and the soleus muscles were digitally reconstructed from the MRI images to find the volume and peak CSA of the two muscles. The muscles were digitally reconstructed by tracing their contours on each axial MRI image that was displayed using a digitization tablet and IMOD software (14). The tendons of the muscles were left out of the contour to leave just the muscle for more accurate volume. The contours were then grouped and used to build patient-specific triangle-based mesh surface models of each muscle with Nuages software (11). The muscle volumes were calculated using subroutines from the visualization toolkit (19). The peak CSA was calculated using a trapezoidal integration algorithm that calculated the area enclosed in the contour of muscles on each axial image. The contour of each muscle with the greatest area became its peak CSA.

Each subject was compared with itself to normalize the groups. Uninjured subjects were normalized by comparing each subject's dominant leg with their nondominant leg. Subjects with ACL-deficient legs were normalized by comparing the muscles of the deficient legs with the muscles of the nondeficient legs. Also, to alleviate confounding variables of larger muscles in the dominant leg, the injured subjects were further divided into two groups: those subjects who injured their dominant legs and those who injured their nondominant legs. Within these groups the injured subjects were normalized by comparing their injured legs with their uninjured legs. The mean of the ratio for each group (uninjured, dominant injured copers, nondominant injured copers, dominant injured noncopers, and nondominant injured noncopers) was then found.

Data analysis.

Comparisons were made between the muscles of the injured legs of the copers and noncopers using the normalized injured to uninjured ratios. Groups were compared using a two-sample t-test. To determine whether there was a size difference between the dominant and nondominant leg, a single-tailed z-test was conducted comparing the normalized dominant with nondominant leg ratios of the uninjured subjects to one. Because a size difference was noted (Fig. 1), the groups were divided into those who injured their dominant leg and those who injured their nondominant leg. The dominant injured copers and the dominant injured noncopers were each compared with the uninjured (dominant to nondominant). Finally, the nondominant injured copers and nondominant injured noncopers were separately compared with the uninjured (nondominant to dominant). Groups were compared using two-sample t-tests. Significance was established at P ≤ 0.05 for all comparisons.

F1-3
FIGURE 1:
Ratios of the average volume (V) and cross-sectional area (CSA) of the uninjured dominant tiblialis anterior (Tib) and soleus (sol) muscles to nondominant muscles. Error bars show the standard error of the mean.

In addition to the comparison of the injured versus uninjured ratios, the actual size of the muscles were compared across groups. The muscle size comparisons were carried out to determine whether there was bilateral trophy in a sample. The copers were compared with the unimpaired, the noncopers were compared with the unimpaired, and the copers and noncopers were compared. Each group was compared using a two-sample t-test (signinficance at 0.05).

RESULTS

Complete data sets were collected for all but one subject. The peak CSA of the soleus muscle for one uninjured subject could not be found because of a technical error. As Table 1 shows, for uninjured subjects, the tibialis anterior muscles in the dominant legs were significantly larger then those of the nondominant legs for both the volume (P = 0.039) and CSA (P = 0.006). However, the volume and CSA of the dominant and nondominant soleus muscles for the uninjured subjects were not significantly different from each other (Fig. 1).

T1-3
TABLE 1:
Statistical tests resulting from six different comparisons.

The tibialis anterior muscles of the noncopers were larger than those of the copers. The volume of the tibialis anterior for the noncopers was 6.6% larger (P = 0.001) than in the copers. The CSA was 10.9% greater in the noncopers (P = 0.012). For the soleus, there was no significant difference in the volume and CSA between the two groups (Fig. 2).

F2-3
FIGURE 2:
Ratios of the average volume (V) and cross-sectional area (CSA) of the injured tiblialis anterior (Tib) and soleus (sol) muscles to the uninjured muscles.

For the subjects who injured their dominant legs, there were no significant differences between the copers and uninjured subjects for either the tibialis anterior muscle's volume or CSA (Fig. 3). In contrast, when comparing the uninjured subjects' tibialis anterior with the noncoper's tibialis anterior, we found that the noncopers had significantly larger volumes (P = 0.014), but the CSA did not show a significant difference between the groups. When comparing the soleus muscles of the uninjured subjects with both the copers' and the noncopers' volume, no significant differences were found. The CSA of the copers' soleus showed a significant difference from the uninjured subjects (P = 0.045).

F3-3
FIGURE 3:
Ratios of the average volume (V) and cross-sectional area (CSA) of the uninjured dominant tiblialis anterior (Tib) and soleus (sol) muscles to nondominant muscles, and of the injured to the uninjured muscles for the copers and noncopers who injured their dominant leg.

When comparing the tibialis anterior muscles of subjects who injured their nondominant legs, we again found no significant difference between the copers and the uninjured subjects (Fig. 4). We also found that the noncopers' muscles were significantly larger than those of uninjured people in both the volume (P < 0.001) and the CSA (P < 0.001) of the tibialis anterior. For the soleus muscle, there were no significant differences for the copers and the noncopers compared with the uninjured.

F4-3
FIGURE 4:
Ratios of the average volume (V) and cross-sectional area (CSA) of the uninjured nondominant tiblialis anterior (Tib) and soleus (sol) muscles to dominant muscles, and of the injured to the uninjured muscles for the copers and noncopers who injured their nondominant leg.

A comparison test was done to see whether bilateral atrophy had occurred. There was no significant difference in the size between any groups compared (copers and normals, noncopers and normals, and copers and noncopers), indicating an absence of bilateral atrophy.

DISCUSSION

The results were contrary to the hypothesis that the muscles of the noncopers' injured legs would atrophy. No atrophy of either the tibialis anterior or soleus muscles in either copers and noncopers were observed. We observed that the soleus muscles of both copers and noncopers were not significantly affected by the ACL injury. In contrast, the tibialis anterior muscles were affected differently in each group. As projected, the copers tibialis anterior muscle ratios of injured to noninjured limbs were very similar to the ratios of those of normal subjects and were not significantly different. Yet, the tibialis anterior of the noncopers presented a very surprising result. The tibialis anterior muscles were not smaller in the injured limb, but they were actually larger relative to the noninjured leg.

This increased size is surprising. What may have caused this affect on the tibialis anterior of the noncopers? One possibility could be associated with the knee stiffing that occurred in the injured subjects. Studies have also found that the gait of copers and noncopers differ. Copers move like uninjured patients with no significant difference in knee flexion, whereas noncopers move with less knee flexion, as well as hip and knee stiffening (16,18). Although we are not aware of any studies investigating possible increased ankle stiffening in noncopers, this would be a reasonable expectation based on the general leg stiffening strategy encountered at the other joints of the injured leg. Such a strategy, especially at heel strike, would require greater tibialis anterior moments to prevent and stiffen the downward slap of the foot, which would lead to increased work of the tibialis anterior. This could then lead to the increased size observed. EMG studies have shown a difference in specificity of muscle activation in the tibialis anterior between ACL-deficient and unimpaired subjects. Ciccotti et al. found that the ACL-injured subjects have an increased level of muscle activity in the tibialis anterior compared to unimpaired subjects (5). When the tibialis anterior is constricted, it causes dorsiflexion and inversion of the foot, which causes an outer rotation of the tibia. This outward rotation prior to heel strike may be a compensatory mechanism to stabilize the knee during landing (5). This increase in activity to help stabilize the knee could help explain the increase in size observed in the noncopers. The stiffening strategy does not seem to greatly affect the soleus muscle because the soleus is used primarily in pushing off from the ground. The stiffening strategy is linked to the loading phase and does not occur during push-off; therefore, its affects would not be seen in the muscles that are used during push-off.

In this study, two of the CSA measurements went against the prevailing trends: the tibialis anterior muscle was larger in the injured leg of the noncopers, and there was no difference in the soleus muscle between groups (Table 1). The CSA is a less reliable measurement of muscle size than volume because it is determined by data from a single slice of the muscle. In contrast, the volume takes measurements from the entire muscle and would therefore be less vulnerable to variation. Therefore, we believe that volume is a better indication of the trends occurring in the muscle.

The main reason for conducting this research was to determine how some of the muscles that control the ankle are affected by an ACL injury in copers and noncopers. The copers' ankle muscles were not greatly affected by the ACL injury. The soleus of the noncopers was not affected by the ACL injury, but the tibialis anterior was larger on the injured side than on the uninjured side. These results indicate that there may have been a change in motor control in noncoping subjects.

If rehabilitation of noncopers was to include muscles that control the ankle, these results suggest that the therapy should focus primarily on trying to prevent overactivation of the tibialis anterior and engagement of the stiffening strategy employed by the noncopers. The overactivation of the tibialis anterior could be prevented by teaching the noncopers not to invert their injured ankles and thus cause the outward rotation of their tibias. This might reduce the stiffening strategy of the ankle, and it might force the noncopers to compensate by the activation of other muscles and, perhaps, become more like the copers in their ability to stabilize their knees.

The authors wish to acknowledge Glenn N. Williams, PT, PhD, Peter J. Barrance, PhD, and Christine Tate for their help in acquiring the data and digitally reconstructing the MRI images, and Stuart A. Binder-Macleod, PT, PhD, FAPTA, for his critique of an earlier version of this manuscript. This study was funded by NIH R01-AR46386 and R01-HD38582.

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Keywords:

ANKLE; ASYMMETRY; ATHLETES; MORPHOLOGY; MRI

©2006The American College of Sports Medicine