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Quadriceps Function and Knee Joint Ultrasonography after ACL Reconstruction

PAMUKOFF, DEREK, N.; MONTGOMERY, MELISSA, M.; MOFFIT, TYLER, J.; VAKULA, MICHAEL, N.

Medicine & Science in Sports & Exercise: February 2018 - Volume 50 - Issue 2 - p 211–217
doi: 10.1249/MSS.0000000000001437
CLINICAL SCIENCES

Purpose Individuals with anterior cruciate ligament reconstruction (ACLR) are at greater risk for knee osteoarthritis, partially because of chronic quadriceps dysfunction. Articular cartilage is commonly assessed using magnetic resonance imaging and radiography, but these methods are expensive and lack portability. Ultrasound imaging may provide a cost-effective and portable alternative for imaging the femoral cartilage. The purpose of this study was to compare ultrasonography of the femoral cartilage between the injured and uninjured limbs of individuals with unilateral ACLR, and to examine the association between quadriceps function and ultrasonographic measures of femoral cartilage.

Methods Bilateral femoral cartilage thickness and quadriceps function were assessed in 44 individuals with unilateral ACLR. Quadriceps function was assessed using peak isometric strength, and early (RTD100) and late (RTD200) rate of torque development.

Results Cartilage thickness at the medial femoral condyle (P < 0.001) and femoral cartilage cross-sectional area (P = 0.007) were smaller in the injured compared with the uninjured limb. After accounting for time since ACLR, quadriceps peak isometric strength was associated with cartilage thickness at the medial femoral condyle (r = 0.35, P = 0.02) and femoral cartilage cross-sectional area (r = 0.28, P = 0.04). RTD100 and RTD200 were not associated with femoral cartilage thickness or cross-sectional area.

Conclusions Individuals with ACLR have thinner cartilage in their injured limb compared with uninjured limb, and cartilage thickness is associated with quadriceps function. These results indicate that ultrasonography may be useful for monitoring cartilage health and osteoarthritis progression after ACLR.

Department of Kinesiology, California State University–Fullerton, Fullerton, CA

Address for correspondence: Derek N. Pamukoff, Ph.D., Department of Kinesiology California State University–Fullerton, Fullerton, CA 92831; E-mail: dpamukoff@fullerton.edu.

Submitted for publication April 2017.

Accepted for publication September 2017.

Individuals with anterior cruciate ligament reconstruction (ACLR) are five to seven times more likely to develop knee osteoarthritis (OA), with nearly 50% of patients developing OA within 2 decades (1,2). Importantly, OA is a major contributor to physical disability, in part because of reductions in mobility and physical activity (3). Knee OA is a chronic disorder that affects the entire joint organ (4), but the main characteristic of OA is a reduction in articular cartilage thickness (5). Osteoarthritis is commonly assessed via measurement of joint space narrowing using radiography (6). However, radiographic methods do not assess cartilage morphology (6) and lack portability for ease of assessment. Therefore, novel imaging techniques are necessary to evaluate and monitor changes in articular cartilage after ACLR.

Ultrasonography is a reliable and valid method for quantifying femoral cartilage thickness (7–11). Ultrasonographic methods demonstrate strong agreement when compared with cross-sectional cadaver methods (9) and thickness values obtained from magnetic resonance imaging (MRI) (10). Furthermore, ultrasonography is capable of monitoring knee joint health in individuals who already have OA (11). However, to our knowledge, ultrasonographic methods have not been applied to individuals with ACLR, despite their elevated risk for knee OA. Ultrasonography is a portable and low-cost alternative compared with other imaging methods (MRI and radiography) and could be a useful method to monitor cartilage health and OA progression after ACLR, and to evaluate the efficacy of therapeutic interventions. Furthermore, radiography introduces ionizing radiation (12), which precludes its use in individuals who are pregnant, and contraindications for MRI include individuals who have pacemaker (13). Therefore, ultrasonography may provide a viable alternative for these populations.

The cause of knee OA is multifactorial and can partially be attributed to alterations in neuromuscular function after ACLR (14). Prospective evidence (15) indicates that quadriceps dysfunction contributes to knee OA development. Furthermore, quadriceps dysfunction is associated with radiological changes before clinical manifestations of knee OA (15), and recent evidence indicates that isometric quadriceps strength is associated with cartilage composition assessed via MRI (16). As such, quadriceps dysfunction may contribute to early changes in cartilage that precede knee OA. Individuals with ACLR have chronic quadriceps dysfunction that persists after rehabilitation (14), which contributes to aberrant walking biomechanics that are linked to knee OA (17). Importantly, greater quadriceps strength is associated with thicker femoral cartilage assessed using ultrasonography in individuals who already have knee OA (18). Individuals with ACLR have quadriceps dysfunction in their injured limb compared with uninjured limb (17), and knee OA risk is three times greater in the injured limb compared with uninjured limb (19). However, the relationship between ultrasonographic measures of cartilage morphology and quadriceps dysfunction in individuals with ACLR has yet to be examined.

Therefore, the purpose of this study was to compare ultrasonographic measurements of femoral cartilage morphology (thickness and cross-sectional area) between the injured and uninjured limb of individuals with unilateral ACLR and to evaluate the association between quadriceps dysfunction and ultrasonographic measurements of cartilage morphology. We hypothesized that individuals with unilateral ACLR would have thinner and smaller femoral cartilage in their injured compared with uninjured limbs and that quadriceps dysfunction would be associated with smaller and thinner femoral cartilage in their injured limb.

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METHODS

Experimental design

Data reported here are from a cross-sectional investigation evaluating many factors linked to knee OA after ACLR. Neuromuscular (quadriceps strength), biomechanical (walking, running, and landing), imaging (cartilage and muscle), and self-report surveys (International Knee Documentation Committee Subjective Knee [IKDC] Form) were obtained in two separate testing sessions that were separated by 2 to 7 d. However, only quadriceps function and joint ultrasonography data are reported here, which were obtained in a single session.

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Participants

Forty-four individuals (32 female and 12 male subjects; age, 22.2 ± 2.9 yr; height, 1.71 ± 0.09 m; mass, 71.9 ± 15.7 kg; time since ACLR, 53.9 ± 30.1 months; IKDC Score, 85.7 ± 9.3) with primary unilateral ACLR (21 patellar tendon grafts, 10 hamstring grafts, 13 allograft; 22 with concomitant meniscal repair or meniscectomy) volunteered to participate in this study. To be included, participants were required to be cleared by a physician for return to physical activity and to engage in exercise for at least 30 min three times per week. Participants were excluded for bilateral ACL injury, a history of graft rupture or revision surgery, lower extremity injury within the preceding 6 months before participation, any lower extremity surgery (other than ACLR), or any neurological disorder. An a priori power analysis was conducted using data comparing cartilage thickness between pre-osteoarthritic knees to knees with no joint-space narrowing (20). Assuming a similar effect, it was determined that 39 participants would be necessary to achieve a power of 0.8 (d = 0.65, β = 0.2, α = 0.05). All participants provided written informed consent before participation, and the university’s institutional review board approved all methods.

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Ultrasound assessments

Participants were instructed to avoid exercise the day before and the day of laboratory testing. Upon arrival to the laboratory, participants rested in a non–weight-bearing supine position on a treatment table with their knees in full extension for 30 min to unload the articular cartilage and to minimize the effects of any preceding weight-bearing activity on articular cartilage (8,21). While supine, the individual’s knee was placed in 140° of flexion using a handheld goniometer (9). This position was selected because it allows for clear visualization of the femoral articular cartilage without obstruction from surrounding soft tissue structures. A Logiq E ultrasound system (GE Healthcare, Fairfield, CT) and a 12–5 MHz linear array transducer were used to image the femoral cartilage (depth, 4.5 cm; gain, 50). The probe was placed anteriorly over the distal femoral cartilage of the medial and lateral femoral condyles in the transverse plane and superior border of the patella (7,8). The intercondylar notch was centered on the screen using a transparent grid that was overlaid on the ultrasound screen (8). Three images were obtained for each knee, and knees were imaged in a random order.

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Quadriceps function assessment

After the ultrasound assessment, participants were tested bilaterally for maximal isometric quadriceps strength (peak torque [PT]) and rate of torque development (RTD). These variables were selected because quadriceps PT is associated with self-reported disability in individuals with ACLR (22), and RTD is associated with gait kinetics in individuals with ACLR (17,23). Participants were seated on a dynamometer (HUMAC NORM; CSMi, Stoughton, MA) with straps secured over the leg, thigh, and torso to isolate the quadriceps contribution to knee extension torque. The lever arm was positioned so that the axis of rotation was aligned with the knee joint center, and the ankle strap was 2 cm above the medial malleolus. During isometric assessments, the knee and hip were positioned in 45° and 85° of flexion, respectively, and participants were instructed to keep their arms crossed over their chest. This knee position was selected because previous research indicates that individuals with ACLR demonstrate greater quadriceps dysfunction at 45° compared with other joint positions (24). Before maximal strength assessments, participants completed a series of submaximal contractions at 25%, 50%, 75%, and 100% of perceived maximum to serve as a warm-up and acclimatization to dynamometry. Participants were instructed to extend their knee “as hard and fast as possible” against the dynamometer. Three maximal trials were completed with 60 s rest in between trials. Limbs were tested in a random order, and verbal encouragement was provided for all trials while a monitor displayed visual feedback of the torque signal.

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Data reduction

Ultrasound images were analyzed using ImageJ Software (National Institutes of Health, Bethesda, MD). Thickness was measured at three locations (midpoints of the lateral and medial condyle, and intercondylar notch) by the straight-line distance (mm) drawn from the hyperechoic cartilage–bone interface to the synovial space–cartilage interface (Fig. 1) (8,18). Cartilage cross-sectional area (mm2) was assessed by tracing the border of femoral cartilage (Fig. 2). Each image was measured three times by two different investigators to obtain intrarater and interrater reliability. Additionally, investigators conducting ultrasound image analyses were blinded to limb injury status, and the average of all measurements was used for analysis.

FIGURE 1

FIGURE 1

FIGURE 2

FIGURE 2

Torque data were processed using a custom LabVIEW program (National Instruments, Austin, TX). Isometric torque data were low-pass filtered at 50 Hz. The trial with the highest PT value was used for analysis. From this trial, the slopes of the torque–time curve from 0 to 100 ms and 100–200 ms after contraction onset were used to define early RTD (RTD100) and late RTD (RTD200), respectively (23). These intervals were selected because RTD100 is strongly influenced by neural contributors (e.g., motor unit firing frequency) to torque development, whereas RTD200 is more attributed to cross-sectional area and overall capacity of the muscle to produce strength (25). As such, RTD100 and RTD200 represent different physiological metrics. Contraction onset was determined as the point when the torque signal exceeded three standard deviations of the resting value. Peak torque and RTD data were normalized to body mass for analysis (N·kg−1).

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Statistical analyses

Intrasession (ICC3,1) and interrater (ICC2,k) reliability for ultrasound images were assessed using intraclass correlation (ICC), and ICCs were classified as weak (<0.5), moderate (0.5–0.69), and good (>0.7). Standard error of the measurement (SEM) was calculated to establish measurement precision. Femoral cartilage measurements were compared between the injured and uninjured limbs using paired-samples t tests. Partial correlations (Pearson r) were used to examine the association between quadriceps dysfunction (PT, RTD100, and RTD200) and cartilage morphology (thickness and cross-sectional area) after accounting for time since reconstruction. All assessments were conducted using directional hypotheses as hypotheses were formulated before the start of the study (α = 0.05). Correlation coefficients were interpreted as being weak (r < 0.3), moderate (0.3 < r < 0.7), and strong (r > 0.7). Each variable was assessed for normality via the Shapiro–Wilk test and assessment of skewness and kurtosis. Furthermore, outliers were assessed using box plots. Although not a primary purpose of this study, independent samples t tests were used to compare quadriceps function and cartilage morphology between individuals with and without concomitant meniscal injury. Likewise, one-way analysis of variance was used to examine the influence of graft type.

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RESULTS

All data were confirmed to be normal (P > 0.05), and no outliers were identified. Therefore, all cases were included in analyses. Reliability analyses indicated good reliability for ultrasound measurements (Table 1). Paired samples t tests indicate that the injured limb had thinner cartilage at the medial femoral condyle (t 43 = 6.13, P < 0.001; Table 2) and smaller cross-sectional area (t 43 = 2.84, P = 0.007; Table 2) compared with the uninjured limb. No difference between limbs was found in thickness at the intercondylar notch (t 43 = 1.48, P = 0.14; Table 2) or lateral femoral condyle (t 43 = 0.05, P = 0.95; Table 2).

TABLE 1

TABLE 1

TABLE 2

TABLE 2

Partial correlation analyses indicate that greater quadriceps PT was associated with greater thickness at the medial femoral condyle (r = 0.35, P = 0.02; Table 3) and that greater femoral cartilage cross-sectional area was associated with greater quadriceps PT (r = 0.27, P = 0.04; Table 3). No relationship was found between quadriceps PT and cartilage thickness at the femoral lateral condyle or intercondylar notch (Table 3), and no relationship was found between RTD100 or RTD200 and any measure of cartilage morphology (Table 3).

TABLE 3

TABLE 3

An exploratory analysis found no differences between individuals with and without meniscal injury in cartilage thickness at the medial femoral condyle (1.60 ± 0.44 vs 1.61 ± 0.47 mm, P = 0.97), lateral femoral condyle (1.84 ± 0.34 vs 1.81 ± 0.28 mm, P = 0.74), or intercondylar notch (2.27 ± 0.52 vs 2.06 ± 0.60 mm, P = 0.21). However, we did observe lesser quadriceps PT in individuals with meniscal injury compared with those without (2.16 ± 0.45 vs 2.45 ± 0.61 N·m·kg−1, P = 0.04). No differences were observed between graft types (Table 4).

TABLE 4

TABLE 4

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DISCUSSION

The purpose of this study was to compare femoral cartilage cross-sectional area and thickness between the injured and injured limbs of individuals with ACLR and to examine the association between quadriceps function (PT and RTD) and femoral cartilage thickness and cross-sectional area in the injured limb of individuals with ACLR. The main findings of this study were that the injured limb had lesser femoral cartilage cross-sectional area and thinner cartilage at the medial femoral condyle compared with the uninjured limb. Additionally, weak to moderate correlations were found between quadriceps PT and femoral cartilage cross-sectional area, and thickness at the medial femoral condyle in the injured limb.

Previous studies have used ultrasound imaging to identify features of knee OA and to quantify cartilage thickness in patients with knee OA (11,18,26,27). However, to our knowledge, this is the first study to evaluate femoral cartilage using ultrasound imaging in individuals with ACLR. Recent evidence has identified changes in tibial and femoral cartilage structure as early as 1 yr after ACLR (28). However, this study evaluated the articular cartilage using MRI techniques (T1ρ and T2ρ relaxation time), which quantifies early signs of cartilage breakdown by identifying changes in cartilage structure (proteoglycans, water, and collagen content) (16). Typically, early changes in cartilage structure may occur in the absence of a decline in cartilage thickness (29), and 30% to 70% of all patients with ACLR develop radiographic OA within 5 to 10 yr (1,2). Our sample was 53.9 months (i.e., nearly 5 yr) from reconstruction, and self-reported disability scores (IKDC) indicated some impairment (i.e., <90%) (22). As such, these individuals may be at high risk for OA development, and ultrasonography may be useful to monitor early changes in cartilage thickness in individuals with ACLR. We note that 52% of our sample had meniscal repair or meniscectomy, which may also contribute to early cartilage degeneration. A recent systematic review (30) indicates that concomitant meniscal injury, regardless of location, increases the risk for radiographic knee OA. We did find evidence of greater quadriceps dysfunction in individuals with meniscal injury compared with those without; however, no differences were found in any of the cartilage measurements. Furthermore, we did not image the tibial cartilage, and the length of time since injury may also contribute to the incidence of knee OA after ACLR in individuals with and without concomitant meniscal injury. Future studies should consider ultrasonographic evaluations of articular cartilage in those with and without meniscal injury.

Interestingly, we only observed a difference in cartilage thickness at the medial femoral condyle, which likely explains the difference observed in overall femoral cartilage cross-sectional area. Medial compartment knee OA is much more common compared with lateral compartment knee OA (31) and is largely attributed to joint alignment and the external knee adduction moment during walking (32). However, quadriceps dysfunction may also be associated with medial cartilage loss. For instance, past research indicates that greater vastus medialis cross-sectional area (33) is associated with greater medial cartilage volume (33), and quadriceps strength is greater in individuals without knee OA compared with those without knee OA (34). We did observe weak to moderate correlations between isometric quadriceps strength, and cartilage cross-sectional area and cartilage thickness at the medial femoral condyle. These findings are in agreement with a previous study (18) that found a similar relationship (r = 0.30) between isometric knee extensor strength and cartilage thickness at the medial femoral condyle. This study also found significant relationships between knee extensor strength and cartilage thickness at the lateral femoral condyle and intercondylar notch. However, this study evaluated patients who already had knee OA, and thus, we attribute the difference in findings to a different study sample.

We do note that, although the relationships found between quadriceps strength and cartilage measurements were significant, they were of relative small magnitude. Only 12% of the variance in cartilage thickness at the medial femoral condyle could be explained by quadriceps peak strength. Therefore, future studies should consider other factors that contribute to cartilage thickness. For instance, aberrant walking biomechanics may contribute to greater cartilage degeneration in individuals with ACLR. Quadriceps dysfunction is associated with biomechanical factors during walking that are linked to knee OA such as the knee flexion angle and moment (23,35,36). Interestingly, we did not observe any relationship between cartilage measurements and either measure of RTD. Rate of torque development is also associated with aberrant walking biomechanics such as the vertical loading rate (17), and thus, we hypothesized that it would also be related to cartilage measurements. However, RTD was assessed at a different knee angle (90°) in these studies (17,23), which may explain our lack of significant findings.

As mentioned previously, the association between medial cartilage loss and walking biomechanics is often attributed to the knee adduction moment, which serves as a surrogate indicator of medial compartment loading (37). However, evidence is conflicting regarding the association between quadriceps dysfunction and the knee adduction moment (35,38), which may explain the low correlation found in this study. For instance, Lim et al. (38) found no association between quadriceps strength and the knee adduction moment, but Murray et al. (35) found that 9% of the variance in knee adduction moment could be explained by isokinetic quadriceps power. As such, quantification method of quadriceps dysfunction (i.e., power vs strength) may be relevant when examining the role of the quadriceps in knee OA after ACLR. Alternatively, imbalance between the lateral and medial quadriceps muscles may contribute to preferential loading of the medial compartment (39). Future studies should evaluate the associations between cartilage thickness and co-contraction ratios of the medial and lateral quadriceps.

There are limitations to consider when interpreting the results of this study. First, the cross-sectional design impairs our ability to draw causal conclusions on the effect of quadriceps strength on knee OA. Second, we included participants of all graft types in this study, which may influence long-term joint health. However, current evidence does not support graft type as a risk factor for knee OA after ACLR (40), and we did not observe any differences between graft types. Moreover, the reconstructive procedure does not prevent knee OA (1), and knee OA development may be due to factors associated with the initial ACL injury. Future longitudinal studies are needed to evaluate the effect of graft type on knee OA development and progression. Third, whereas our participants were positioned in a supine non-weight bearing position for 30 min before ultrasound measurements as in previous research (8,21), a recent study (8) indicates a 3.4% ± 5.3% increase in cartilage thickness after 30 min of sitting. However, the difference between limbs in the current study was 27%, and both limbs were subject to the same 30-min resting period. Nonetheless, a longer rest period before ultrasound imaging is recommended in future studies. Finally, ultrasound measurements in this study do not provide an indication of cartilage composition, and changes in cartilage composition may occur before changes in overt cartilage size. Future studies may benefit from measuring the response of cartilage to joint loading (i.e., the change in cartilage thickness) in individuals with and without ACLR, as cartilage deformation may provide a surrogate assessment for cartilage composition.

The results of this investigation suggest that individuals with unilateral ACLR have thinner cartilage at the medial femoral condyle and smaller femoral cartilage cross-sectional area in their injured limb compared with uninjured limb. Moreover, greater quadriceps strength was associated with thicker cartilage and greater cartilage cross-sectional area, but these relationships were relatively small. Overall, these data indicate that ultrasonography may be useful for monitoring femoral cartilage after ACLR. Future studies are needed to evaluate other contributors to cartilage size and the longitudinal relationship between quadriceps function and cartilage degeneration in individuals with ACLR.

This study was supported by the California State University Research, Scholarship, and Creative Activity Incentive Grant Program and the California State Program for Research and Education in Biotechnology New Investigator Grant.

The authors thank Kevin Choe and Skylar Holmes for assistance in this study.

The authors have no professional relationships with companies or manufacturers who would benefit from the results of the present study. The results of the present study do not constitute an endorsement by the American College of Sports Medicine. The results are presented clearly and honestly and without fabrication, falsification, or inappropriate data manipulation.

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Keywords:

OSTEOARTHRITIS; CARTILAGE; MUSCLE; KNEE

© 2018 American College of Sports Medicine