Osteoarthritis-Related Degeneration Alters the Biomechanical Properties of Human Menisci Before the Articular Cartilage

Abstract

An exact understanding of the interplay between the articulating tissues of the knee joint in relation to the osteoarthritis (OA)-related degeneration process is of considerable interest. Therefore, the aim of the present study was to characterize the biomechanical properties of mildly and severely degenerated human knee joints, including their menisci and tibial and femoral articular cartilage (AC) surfaces. A spatial biomechanical mapping of the articulating knee joint surfaces of 12 mildly and 12 severely degenerated human cadaveric knee joints was assessed using a multiaxial mechanical testing machine. To do so, indentation stress relaxation tests were combined with thickness and water content measurements at the lateral and medial menisci and the AC of the tibial plateau and femoral condyles to calculate the instantaneous modulus (IM), relaxation modulus, relaxation percentage, maximum applied force during the indentation, and the water content. With progressing joint degeneration, we found an increase in the lateral and the medial meniscal instantaneous moduli (p < 0.02), relaxation moduli (p < 0.01), and maximum applied forces (p < 0.01), while for the underlying tibial AC, the IM (p = 0.01) and maximum applied force (p < 0.01) decreased only at the medial compartment. Degeneration had no influence on the relaxation percentage of the soft tissues. While the water content of the menisci did not change with progressing degeneration, the severely degenerated tibial AC contained more water (p < 0.04) compared to the mildly degenerated tibial cartilage. The results of this study indicate that degeneration-related (bio-)mechanical changes seem likely to be first detectable in the menisci before the articular knee joint cartilage is affected. Should these findings be further reinforced by structural and imaging analyses, the treatment and diagnostic paradigms of OA might be modified, focusing on the early detection of meniscal degeneration and its respective treatment, with the final aim to delay osteoarthritis onset.

Keywords: degeneration; equilibrium modulus; instantaneous modulus; knee; mapping; meniscus; thickness; water content.

FIGURE 1

Human cartilage and meniscus sample preparation: (A) Horizontal plane cut at the distal femur. (B) Highlighting the cartilage-to-cartilage contact area at the tibial plateau using a permanent tissue marker. (C) Separated lateral meniscus with its intact anterior and posterior root attachments. (D) Horizontal plane cut at the proximal tibia. Meniscus cast preparation steps: (E) The meniscus was initially embedded at a time point when the polymethylmethacrylate (PMMA) had a rubber-like texture. (F) Insertion of six needles to allow for a later positioning of security sutures. (G) During the exothermic hardening reaction of the PMMA, the meniscus body was temporarily removed. (H) Final meniscus sample including interlinked security sutures and anterior (A) and posterior (P) cast markings.

FIGURE 2

Representative biomechanical mappings of the instantaneous modulus (IM) measurements of mildly and severely degenerated menisci, with all values given in megapascal. Middle row: Box plots (minimum, maximum, median, and 25th and 75th percentiles) of the lateral and medial IM_Meniscus values in megapascal. Lower row: Box plots (minimum, maximum, median, and 25th and 75th percentiles) of the lateral and medial E_t20 values in megapascal. Subdivided anatomical regions are: AH, anterior horn; PI, pars intermedia; PH, posterior horn. Non-parametric statistical analyses: n = 12; *p < 0.05. For reasons of readability, we marked significant differences between the mild and severe degeneration of the medial and lateral sides above the representative biomechanical mappings.

FIGURE 3

Box plots (minimum, maximum, median, and 25th and 75th percentiles) of the relaxation percentages over the maximum stress (Δσ_relax) of the mildly and severely degenerated menisci. Subdivided anatomical regions are: AH, anterior horn; PI, pars intermedia; PH, posterior horn. Non-parametric statistical analyses: n = 12; *p < 0.05.

FIGURE 4

Water content value box plots (minimum, maximum, median, and 25th and 75th percentiles) in percent of the mildly and severely degenerated menisci. Subdivided anatomical regions are: AH, anterior horn; PI, pars intermedia; PH, posterior horn. Non-parametric statistical analyses: n = 12; *p < 0.05.

FIGURE 5

Representative biomechanical mappings of the instantaneous modulus (IM) measurements of the mildly and severely degenerated tibial plateau articular cartilage (AC), with all values given in megapascal. Middle row: Box plots (minimum, maximum, median, and 25th and 75th percentiles) of the lateral and medial IM_{TibialCartilage} values in megapascal. Lower row: Box plots (minimum, maximum, median, and 25th and 75th percentiles) of the lateral and medial E_t20 values in megapascal. Subdivided anatomical regions are: AH, anterior horn; PI, pars intermedia; PH, posterior horn; CtC, cartilage-to-cartilage contact area. Non-parametric statistical analyses: n = 12; *p < 0.05. For reasons of readability, we marked significant differences between the mild and severe degeneration of the medial and lateral sides above the representative biomechanical mappings and also between the CtC and other anatomical compartments only at the legend of the category axis (e.g., CtC*).

FIGURE 6

Box plots (minimum, maximum, median, and 25th and 75th percentiles) of the relaxation percentages over the maximum stress (Δσ_relax) of the mildly and severely degenerated tibial plateau articular cartilage (AC). Subdivided anatomical regions are: AH, anterior horn; PI, pars intermedia; PH, posterior horn; CtC, cartilage-to-cartilage contact area. Non-parametric statistical analyses: n = 12; *p < 0.05.

FIGURE 7

Water content in percent of the mildly and severely degenerated tibial plateau articular cartilage (AC). Box plots (minimum, maximum, median, and 25th and 75th percentiles) of the tibial cartilage water content values in percent. Subdivided anatomical regions are: AH, anterior horn; PI, pars intermedia; PH, posterior horn; CtC, cartilage-to-cartilage contact area. Non-parametric statistical analyses: n = 12; *p < 0.05.

FIGURE 8

Representative maps of the instantaneous modulus (IM) measurements of the mildly degenerated and severely degenerated distal femora, with all values given in megapascal. Middle row: Box plots (minimum, maximum, median, and 25th and 75th percentiles) of the lateral and medial IM_{DistalFemurCartilage} values in megapascal. Lower row: Box plots (minimum, maximum, median, and 25th and 75th percentiles) of the lateral and medial E_t20 values in megapascal. Non-parametric statistical analyses: n = 12.

FIGURE 9

Box plots (minimum, maximum, median, and 25th and 75th percentiles) of the relaxation percentages over the maximum stress (Δσ_relax) of the mildly and severely degenerated distal femur articular cartilage (AC). Non-parametric statistical analyses: n = 12.