Physiologic Medial Meniscal Extrusion With Loading and Flexion Detected by Ultrasound

Abstract

Background:

Medial meniscal extrusion (MME) is a risk factor for osteoarthritis of the knee and is usually assessed using a supine, unloaded magnetic resonance imaging. However, protocols for examining meniscal extrusion with ultrasound in the literature vary regarding specific flexion angles and the extent of weightbearing during the examination, complicating interpretations of the influence of loading and position on meniscal extrusion.

Hypothesis:

The hypothesis was that loading and increased flexion angles would increase physiologic MME relative to supine and neutral positions.

Study Design:

Descriptive laboratory study.

Methods:

Asymptomatic volunteers with no history of knee pain, injury, or surgery were included. Real-time knee joint angles were obtained by a motion-capture system using retroreflective markers placed on the lower limbs. Ultrasound images of the medial meniscus of both knees were acquired in the coronal plane for supine, single-leg, and double-leg standing positions and with the knee in neutral (0°-5°), 20°, and 45° of flexion. MME was compared across legs, stances, and angles using a repeated-measures mixed-effects linear model, and pairwise comparisons were made using a post hoc Tukey test.

Results:

A total of 21 volunteers (age, 33 ± 12 years; body mass index, 23 ± 2.3 kg/m²; 9 women) participated in the study. MME was significantly lower in the supine position compared with single- and double-leg stances (P < .0001, estimated marginal mean MME: supine = 1.1, 1-leg = 1.3, 2-leg = 1.3), with no significant difference between weightbearing stances. Increasing knee flexion angles were associated with significantly lower extrusion (P < .0001, estimated marginal mean MME: neutral = 1.4; 20° = 1.3; 45° = 1), with extrusion greatest at neutral flexion and lowest at 45° of flexion. There was no significant difference in MME between right and left legs (estimated marginal mean MME = 1.2 for both left and right legs; P = .7255).

Conclusion:

Our study demonstrated that unloaded, supine examinations of MME may be of limited value. Also, including ultrasound assessment under loaded conditions may better reflect the biomechanical function of the meniscus during activities of daily life.

Clinical Relevance:

Examining physiologic meniscal behavior is important to provide context for altered meniscal function in the presence of pathology, which may help inform clinical decisions regarding the management of meniscal degeneration or tears.

Understanding and preventing osteoarthritis is one of the biggest challenges in orthopaedics. Recently, meniscal tears and extrusion have been identified as key risk factors for the progression of knee osteoarthritis.^4,15,16 External displacement of the medial meniscus, or medial meniscal extrusion (MME), is particularly implicated in knee osteoarthritis severity and outcomes; it can be an indirect sign of tears or indicate degenerative changes that influence its biomechanical function. ⁸ There is no standardized method to measure MME. However, it is most commonly defined as the amount of protrusion relative to the edge of the medial tibial plateau on a supine coronal magnetic resonance imaging (MRI) scan, where the knee is unloaded and in slight flexion. ⁸ A threshold of 3 mm of extrusion is typically considered clinically significant, ¹² but meniscal extrusion measured in this position may not accurately reflect physiologic or pathologic meniscal behavior during activities of daily life. Alternative techniques that enable measurement of meniscal function during weightbearing, such as ultrasonography (US), can relate the degree of meniscal extrusion to altered joint mechanics. Meniscal extrusion measurements observed by US are highly correlated with those obtained by MRI in supine, unloaded positions, and in weightbearing positions.^13,18,19 In weightbearing assessments, US has been documented to outperform MRI in measuring MME in patients with knee osteoarthritis, detecting increasing MME with increasing body mass and disease severity. ²⁰ Examining physiologic meniscal behavior is important to provide context for altered meniscal function with aging or pathology, which may help inform clinical decisions regarding the clinical management of meniscal degeneration or tears. ⁷ However, protocols for examining meniscal extrusion with US in the literature vary regarding specific flexion angles and the extent of weightbearing during the examination,^1,3,7,17 complicating interpretations of the influence of loading and position on meniscal extrusion.

This study aimed to systematically examine physiologic meniscal extrusion in both unloaded and loaded states, as well as between knee flexion angles, in asymptomatic volunteers. Motion capture was used with ultrasound to achieve greater objectivity in measuring changes in MME with flexion. The hypothesis was that loading and increased flexion angles would increase physiologic MME relative to supine and neutral positions.

Methods

Study Population

This preliminary, prospective cohort study (evidence level 2) was approved by the Vail Health Hospital Institutional Review Board (IRB) (IRB No. 2022-119-SPRI). All participants gave written informed consent before participating in the study. Participants with asymptomatic knees were recruited from the general population. Exclusion criteria included knee pain, a diagnosed meniscal tear, a history of knee surgery, or a recent knee injury (within 1 month of participating in the study).

US Examination

Retroreflective markers were placed on the distal fibula, joint line, and greater trochanter on the lateral side of both legs, as well as on the lateral right thigh, for real-time assessment of knee flexion angles in a motion capture laboratory (Figure 1, A and B). Flexion angles were determined using an 18-camera motion-capture system at a frequency of 150 Hz (Oqus 700+ series; QTM Connect MATLAB plugin) and presented on a monitor visible to the participant for real-time feedback and correction to keep within 5° of the target angles (Figure 1, B and C). Joint angles and ultrasound images were captured simultaneously.

Figure 1.

(A) Ultrasound images of the medial meniscus were acquired in supine and 1- and 2-leg standing positions. (B) A motion-capture system was used to record joint angles in real time as participants stood with the knee in full extension (0°-5°) and squatted to 20° and 45° of flexion (20° shown). (C) Corresponding real-time flexion angle measurements (black line = recorded flexion angle, blue lines = visual boundaries to guide participant to stay within 5° of target angle). (D) Ultrasound images were captured simultaneously with joint angle measurements. Four points were placed to indicate the medial side of the joint, the joint margin line, and the medial border of the meniscus. A perpendicular line (blue line) was created between the meniscal margin point and the joint margin line (green line) to calculate meniscal extrusion (mm). Readers were blinded to the stance and knee flexion angle used to acquire each image. MCL, medial collateral ligament.

Ultrasound imaging of the medial meniscus of both knees was performed by an orthopaedic surgeon (M.D.H.) with 6 years of experience with musculoskeletal US using an Aplio i800 ultrasound system (Canon Medical Systems). An 18 MHz linear array transducer (i18LX8, Model PLI-1205BX/FS; Canon Medical Systems) was placed in the coronal plane parallel to the anterior part of the superficial medial collateral ligament to measure medial meniscal body extrusion in supine and weightbearing positions using the medial collateral ligament as a landmark (Figure 1D). Participants were first examined in the supine position, with the knee at full extension (0°-5°), and at 20° and 45° of flexion. An example of the ultrasound probe placement for each angle is provided in Figure 2. Then, participants were examined while standing on 2 legs on a dual-belt treadmill equipped with force plates. Participants were instructed to balance their weight between legs and to place their hands on supports for balance as they stood (0°-5° of flexion) and squatted, holding the knee at 20° and 45° of flexion. This procedure was repeated with participants standing on a single leg at a time, alternating between left and right legs between each flexion angle. Three coronal-plane images were acquired at each stance and flexion angle, for a total of 54 images per participant.

Figure 2.

Representative images depicting placement of the ultrasound transducer with the knee at full extension (0°-5°), 20°, and 45° of flexion. The transducer was placed in the coronal plane parallel to the anterior part of the superficial medial collateral ligament to measure medial meniscal body extrusion.

Measurement of Meniscal Extrusion

US images were evaluated by 2 orthopaedic surgeons (M.D.H. and R.D.H.), blinded to stance and flexion angle, using a custom MATLAB script (R2021b; MathWorks). MME was measured as the orthogonal distance from the peripheral border of the meniscal body to a line connecting the margins of the tibial and femoral cortices, using the articular cartilage as a landmark for the femoral cortical edge (Figure 1D). After calibrating the pixel scale using a scale bar on the ultrasound image, 4 points were placed: first to mark the medial side of the joint; 2 points for the tibia and femur to indicate the joint margin line; and a fourth point for the medial margin of the meniscus. A perpendicular line was created between the joint margin line and the meniscal margin point to calculate MME (mm). The 3 images acquired for each stance and flexion angle were measured, and the mean MMEs over the 3 images were used for statistical analysis.

Statistical Analysis

A power analysis was performed, informed by results from Shimozaki et al, ¹⁹ which revealed that for an effect size of 0.32, a power of 0.8, and an α level of .05, a minimum of 18 individuals were required to assess differences in MME between positions. Repeatability in MME was evaluated using an intraclass correlation coefficient (ICC) using a 2-way mixed effects model to test the agreement in MME between the 3 images acquired for each stance and flexion angle and between raters (inter-rater ICC). ICC values of 0 to 0.5 are considered poor, 0.5 to 0.75 are moderate, 0.75 to 0.9 are good, and 0.9 to 1 are excellent. ¹⁰ The mean and 95% CI of MME in each position and flexion angle are reported. Violin plots were used to visualize the distribution in MME for each stance and flexion angle. A repeated-measures mixed-effects linear model fit by maximum likelihood was used to examine the influence of age, leg, stance, and knee flexion angle on MME, accounting for repeated measures within a subject. Both an interaction model and a main effects model were constructed. The main effects model had the lowest Bayesian Information Criterion and was selected for reporting. Model fit and assumptions were assessed by inspecting residual diagnostics; the MME was log-transformed to meet the normality assumption. The estimated marginal means and 95% CIs were reported. Pairwise comparisons were performed using a post hoc Tukey test. Statistical analysis was performed using R Version 4.2.2 (RStudio).

Results

A total of 20 participants were included in the study (age, 33 ± 12 years; BMI, 23 ± 2.3 kg/m²; 9 women). There was moderate agreement in MME measurements between readers (ICC, 0.571 [95% CI, 0.286-0.728]), as well as between repeated images of the same stance and flexion angle (ICC, 0.676 [95% CI, 0.670-0.682]). Repeated measures had an overall coefficient of variation of 12% and a standard deviation of 0.3 mm (range, 0.2-0.4 mm). For the 2-leg weightbearing stance, for example, the intra-measurement standard deviation was 0.4 mm at 0° to 5° of flexion, 0.3 mm at 20° of flexion, and 0.4 mm at 45° of flexion. The mean MME and associated 95% CIs for each stance and knee flexion angle are provided in Table 1.

Table 1

Mean MME for Each Stance and Knee Flexion Angle ^a

	MME, mm
Flexion Angle	Supine	2 Legs	1 Leg
Neutral, 0°-5°	2.8 (2.6-3)	3.1 (3-3.3)	3.3 (3.1-3.5)
20°	2.2 (1.9-2.5)	2.7 (2.6-2.9)	3 (2.8-3.1)
45°	1.3 (1-1.6)	2 (1.8-2.3)	2.2 (2-2.5)

a

Data are presented as mean (95% CI). MME, medial meniscal extrusion

There were significant relationships between MME and age (P = .0013), stance (P < .0001), and flexion angle (P < .0001), but not between MME and leg (P = .7255). The estimated marginal means are provided in Table 2. MME was significantly lower when measured in a supine position compared with MME in single- and double-leg stances; nonetheless, there was no significant difference between the 2 weightbearing stances (Figure 3, A-C and Figure 4). Furthermore, increasing knee flexion angles to 20° and 45° were associated with significantly lower MME (Figure 3, D and E, and Figure 4), with the greatest MME observed in full extension and the lowest in 45° of flexion.

Table 2

Estimated Marginal Means for Each Stance and Knee Flexion Angle ^a

		MME, mm
Flexion angle	Neutral, 0°-5°	1.4 (1.3-1.5)
	20°	1.3 (1.2-1.3)
	45°	1 (0.9-1.1)
Stance	Supine	1.1 (1-1.1)
	1 leg	1.3 (1.2-1.4)
	2 legs	1.3 (1.2-1.4)
Leg		1.2 (1.1-1.3)
Age		1.2 (1.1-1.3)

a

Data are presented as mean (95% CI). MME, medial meniscal extrusion.

Figure 3.

Representative ultrasound images for a 33-year-old male volunteer and associated MME measurements. (A) MME was lowest in the supine position compared with (B) 1-leg and (C) 2-leg standing positions for all flexion angles. Images A to C exhibit the left meniscus at full extension or neutral flexion. MME was greatest in (D) neutral flexion and decreased with (E) increasing flexion to 20° and (F) 45° for all positions. Images D to F exhibit the right meniscus in the supine position. MME, medial meniscal extrusion.

Figure 4.

Violin plots depict the distribution of MME metrics for each flexion angle and stance. There were significant differences in MME with knee flexion angle (*P < .0001). MME at each flexion angle was significantly different than the others; MME was greatest in full extension (neutral flexion) and lowest in 45° of flexion. Extrusion also showed significant differences depending on the stance (^†P < .0001), where MME was lowest in the supine position compared with 1-leg and 2-leg standing positions. MME, medial meniscal extrusion.

Discussion

This study systematically examined MME under several loading and flexion conditions, incorporating ultrasound imaging and motion-capture technology. The major findings of the study demonstrated that, in asymptomatic volunteers, weightbearing and knee flexion independently influenced MME. MME was increased with weightbearing compared with a supine, unloaded position, and with the knee closer to full extension, increased extrusion. There was no difference between 2-leg and 1-leg standing positions.

The work presented here reproduced findings from previous literature on physiologic meniscal extrusion during loading and flexion. MRI and US examinations in the coronal plane have observed greater MME in a 2-leg stance than in supine, unloaded positions in relaxed (slight flexion) and stressed (active leg lift) conditions. ⁵ Similar to findings in this study, physiologic extrusion >3 mm was also observed in weightbearing stances. Using MRI and US, both Shimozaki et al ¹⁹ and Meng et al ¹³ observed that MME was greatest in the 1- and 2-leg upright positions compared with the supine position, and that measures were strongly correlated across modalities. Shimozaki et al ¹⁹ found no differences in MME between upright positions, in agreement with results here, and also observed that there were strong correlations in the extent of meniscal extrusion between imaging modalities for all loading conditions. In this study, a change in MME on US images of 0.5 to 0.8 mm was measured when participants moved from a supine to a 2-leg standing position with 20° of flexion, in line with previous literature reporting changes ranging from 0.5 to 0.8 mm in asymptomatic volunteers under these same conditions.^1,5,17 Knowledge of physiological meniscal extrusion is important to provide context for changes associated with meniscal pathology. In patients with pain, MME under weightbearing correlates with high osteoarthritis grades, whereas nonweightbearing MME does not. ¹⁴ Generalized meniscal degeneration may contribute to the greater amount of change in MME from supine to 2-leg standing positions observed in osteoarthritis cohorts^7,17 or those with knee pathology ⁵ compared with healthy controls. However, the behavior of the torn meniscus has varied in the literature. In the supine position, MME is greater in patients with meniscal root tears than in those with intact menisci. ² MME on supine MRI is 1.12 mm greater in patients with medial meniscal root tears compared with patients with non-root tears and 2.13 mm greater than in those with intact menisci. Furthermore, patients with osteoarthritic knees exhibited 0.73 mm greater MME than those without knee osteoarthritis. ⁶ When loading is introduced, changes in MME from supine to 2-leg standing were around 0.1 mm in patients with meniscal tears but 1 mm in those with intact menisci, suggesting that tears are related to altered meniscal displacement under load. ⁹ These studies emphasize the importance of studying both physiological and pathological meniscal extrusion under loaded conditions to understand meniscal behavior during activities of daily life and with knee pain and pathology. The variability in the measurement technique observed in this study, on the order of 0.3 mm, could complicate the interpretation of loading- and flexion-related extrusion measures if the same technique were used for patients with meniscal tears. However, the measurement variability was lower than the reported changes with loading and flexion in intact menisci and was below clinically relevant differences in MME on supine imaging, as described above. Future work is recommended to better understand changes in MME and displacement with loading and flexion in patients with aging, degenerative, or torn menisci.

This work adds to existing literature by systematically evaluating the contributions of the stance and flexion angle to physiologic MME. Techniques reported in the literature vary in the extent of weightbearing and flexion angles and frequently include conditions involving one or both factors. This work implemented ultrasound imaging in a biomotion laboratory setting to systematically examine the contribution of both loading and flexion to MME. Findings suggest that flexion angle and loading influence MME independently. Knee flexion closer to full extension was associated with more MME. Studies of meniscal behavior during knee flexion have been more limited and variable to date; however, results here in asymptomatic volunteers show similar trends to previous findings in an osteoarthritis population, in which the meniscus retracted as the knee moved from 0° to 90° of flexion in an unloaded, supine position. ¹⁸ There, the lack of a decrease in MME with 90° of flexion was characteristic of patients with a loss of meniscal hoop function. Similarly, increased flexion on supine loaded MRI was associated with lateral and posterior shifts in the position of the meniscal body, whereas an extended position was related to medial and lateral shifts in the meniscus <50% of body weight. ¹¹ While the previously mentioned ultrasound studies in asymptomatic volunteers measured meniscal extrusion in a neutral stance (extension) or at 20° of flexion, Cho et al ³ performed an ultrasound study of meniscal behavior using the Thessaly test that incorporated internal and external rotation. They observed a decrease in extrusion with rotation but no difference between neutral stance and 5° or 20° of flexion. Systematically examining meniscal behavior under load and flexion could help inform the expected meniscal behavior during clinical tests, such as the Thessaly test, that probe specific meniscal pathology. These results report physiological trends in asymptomatic menisci at controlled flexion angles to support further investigation of meniscal behavior with flexion; however, further work is necessary to incorporate other factors, such as internal/external rotation and meniscal pathology. These techniques could also improve knowledge of the role of meniscal function in joint stability and osteoarthritis progression. Meniscal tears and extrusion are important risk factors for the onset and progression of osteoarthritis and may be linked to an altered joint loading environment. Further research will focus on understanding the influence of these pathologies on elevated osteoarthritis risk.

Limitations

The study has important limitations. In this preliminary study, asymptomatic volunteers from the general public were recruited who self-reported with no history of knee or meniscal injury or pain. The tissue state was not confirmed by US or MRI, and no comparison of imaging modalities was performed, as these asymptomatic volunteers had no imaging available. Similarly, no long-standing radiographs were available to examine coronal limb alignment. Further work will examine these influences in a larger population, including asymptomatic and pathologic menisci, such as meniscal root tears. Knee flexion angles were selected to model flexion during activities of daily life, such as walking and climbing stairs; further work will examine greater degrees of flexion, such as 90°, which may be of interest for evaluating meniscal root tears and fixation treatment. The ultrasound probe was placed using anatomic landmarks and followed the medial collateral ligament during knee flexion, which may not have fully captured any posterior translation of the meniscus during flexion. Additionally, knee flexion angles were precisely monitored using motion-capture technology. However, errors in joint angles may have resulted from marker placement on the skin or limb rotation, which were not examined in this study. Nevertheless, this technique offers greater precision than conventional goniometer-based angle measurements or the descriptive terms used in previous literature. Intraobserver ICC was not assessed in this study. The laboratory setup supported the study’s aim of systematically examining the influence of loading and flexion angle to improve understanding of physiologic meniscal behavior to contextualize meniscal pathology, which may be measured using variable protocols in a clinical setting. Translation of this methodology to the clinic would require modification for alternative methods of recording joint angles in real time and is beyond the scope of the study.

Conclusion

Overall, our preliminary study demonstrated that unloaded, supine examinations of MME may be of limited value and that including ultrasound assessments under loaded conditions may better reflect the biomechanical function of the meniscus during activities of daily life.

Examining physiologic trends in asymptomatic meniscal extrusion at controlled flexion angles may provide context for meniscal behavior in cases of pathology.