Adaptation of Fibril-Reinforced Poroviscoelastic Properties in Rabbit Collateral Ligaments 8 Weeks After Anterior Cruciate Ligament Transection

Abstract

Ligaments of the knee provide stability and prevent excessive motions of the joint. Rupture of the anterior cruciate ligament (ACL), a common sports injury, results in an altered loading environment for other tissues in the joint, likely leading to their mechanical adaptation. In the collateral ligaments, the patterns and mechanisms of biomechanical adaptation following ACL transection (ACLT) remain unknown. We aimed to characterize the adaptation of elastic and viscoelastic properties of the lateral and medial collateral ligaments eight weeks after ACLT. Unilateral ACLT was performed in six rabbits, and collateral ligaments were harvested from transected and contralateral knee joints after eight weeks, and from an intact control group (eight knees from four animals). The cross-sectional areas were measured with micro-computed tomography. Stepwise tensile stress-relaxation testing was conducted up to 6% final strain, and the elastic and viscoelastic properties were characterized with a fibril-reinforced poroviscoelastic material model. We found that the cross-sectional area of the collateral ligaments in the ACL transected knees increased, the nonlinear elastic collagen network modulus of the LCL decreased, and the amount of fast relaxation in the MCL decreased. Our results indicate that rupture of the ACL leads to an early adaptation of the elastic and viscoelastic properties of the collagen fibrillar network in the collateral ligaments. These adaptations may be important to consider when evaluating whole knee joint mechanics after ACL rupture, and the results aid in understanding the consequences of ACL rupture on other tissues.

Keywords: Anterior cruciate ligament transection; Finite element model; Medial/lateral collateral ligament; Rabbit model; Tissue adaptation.

Figure 1

Workflow of the study. (a) Medial (MCL) and lateral collateral ligaments (LCL) were carefully dissected from Anterior Cruciate Ligament-transected (ACLT), contralateral (C-L), and control (CNTRL) rabbit knee joints. b The cross-sectional area was measured using micro-computed tomography (µCT) imaging data. (c) Tensile stress-relaxation experiments of the collateral ligaments were conducted using a micromechanical testing system. (d) A fibril-reinforced poroviscoelastic material model was implemented in a finite element model to replicate each stress-relaxation experiment. (f) The force–time output of the numerical model was fit to the experimental force–time curve measured at the toe region of the stress–strain curve to determine the material properties of each sample.

Figure 2

(a) The cross-sectional area and (b) the stiffness of the medial collateral ligament (MCL, blue) and the lateral collateral ligament (LCL, magenta) samples for the Anterior Cruciate Ligament-transected (ACLT), contralateral (C-L), and control (CNTRL) groups, respectively are shown. The boxplot shows median (horizontal line), 25th and 75th percentile (colored box), and minimum and maximum values (bars). *α < 0.05.

Figure 3

Elastic properties of the medial collateral ligament (MCL, blue) and the lateral collateral ligament (LCL, magenta) samples for the Anterior Cruciate Ligament-transected (ACLT), contralateral (C-L), and control (CNTRL) groups, respectively are shown. (a) Elastic modulus of the non-fibrillar matrix. (b) Nonlinear elastic fibrillar network modulus. The boxplot shows median (horizontal line), 25th and 75th percentile (colored box), and minimum and maximum values (bars). *α < 0.05.

Figure 4

Fast relaxation properties of the medial collateral ligament (MCL, blue) and the lateral collateral ligament (LCL, magenta) samples for the Anterior Cruciate Ligament-transected (ACLT), contralateral (C-L), and control (CNTRL) groups, respectively are shown. (a) The elastic part of the Maxwell element describing the magnitude of fast relaxation or recruitment of viscoelasticity of the fibrillar network. (b) Damping component of the Maxwell element describing fast relaxation of the fibrillar network. The boxplot shows median (horizontal line), 25th and 75th percentile (colored box), and minimum and maximum values (bars). *α < 0.05.

Figure 5

Long-term relaxation properties of the medial collateral ligament (MCL, blue) and the lateral collateral ligament (LCL, magenta) samples for the Anterior Cruciate Ligament transected (ACLT), contralateral (C-L), and control (CNTRL) groups, respectively are shown. (a) The elastic part of the Maxwell element describing the magnitude of long-term relaxation or recruitment of viscoelasticity of the fibrillar network. (b) Damping component of the Maxwell element describing long-term relaxation of the fibrillar network. The boxplot shows median (horizontal line), 25th and 75th percentile (colored box), and minimum and maximum values (bars). *α < 0.05.

Figure 6

Scatter plots between OARSI grades and fibril-reinforced poroviscoelastic properties of collateral ligaments. Statistically significant (Spearman’s) correlations are presented from ACLT group and the OARSI scores. (a) lateral femur and the elastic modulus of the non-fibrillar matrix, (b) patella and the damping component describing fast relaxation of the fibrillar network, and (c) lateral femur and damping component describing long-term relaxation of the fibrillar network.