Mechanical function near defects in an aligned nanofiber composite is preserved by inclusion of disorganized layers: Insight into meniscus structure and function

Abstract

The meniscus is comprised of circumferentially aligned fibers that resist the tensile forces within the meniscus (i.e., hoop stress) that develop during loading of the knee. Although these circumferential fibers are severed by radial meniscal tears, tibial contact stresses do not increase until the tear reaches ~90% of the meniscus width, suggesting that the severed circumferential fibers still bear load and maintain the mechanical functionality of the meniscus. Recent data demonstrates that the interfibrillar matrix can transfer strain energy to disconnected fibrils in tendon fascicles. In the meniscus, interdigitating radial tie fibers, which function to stabilize and bind the circumferential fibers together, are hypothesized to function in a similar manner by transmitting load to severed circumferential fibers near a radial tear. To test this hypothesis, we developed an engineered fibrous analog of the knee meniscus using poly(ε-caprolactone) to create aligned scaffolds with variable amounts of non-aligned elements embedded within the scaffold. We show that the tensile properties of these scaffolds are a function of the ratio of aligned to non-aligned elements, and change in a predictable fashion following a simple mixture model. When measuring the loss of mechanical function in scaffolds with a radial tear, compared to intact scaffolds, the decrease in apparent linear modulus was reduced in scaffolds containing non-aligned layers compared to purely aligned scaffolds. Increased strains in areas adjacent to the defect were also noted in composite scaffolds. These findings indicate that non-aligned (disorganized) elements interspersed within an aligned network can improve overall mechanical function by promoting strain transfer to nearby disconnected fibers. This finding supports the notion that radial tie fibers may similarly promote tear tolerance in the knee meniscus, and will direct changes in clinical practice and provide guidance for tissue engineering strategies.

Impacts of maturation on the micromechanics of the meniscus extracellular matrix

“…The other structural units exhibit differentiated age-dependence. The radial tie fibers and superficial layer share similar structure of radially oriented fibers, and play similar functions of integrating circumferential fiber bundles (Bansal et al, 2017; Skaggs et al, 1994). However, at the fetal stage, radial tie fibers appear to be less developed than superficial layer, as evidenced by the much lower modulus.…”

Synthetic scaffolds for musculoskeletal tissue engineering: cellular responses to fiber parameters

“…37 Aligned fiber scaffolds are formed in a variety of ways: using a rotating disc 38 or mandrel, 39 patterned electrodes, 40 air-gap techniques, 41 a patterned insulator, 42 or high strength ceramic or electromagnets with copper plates. 43 Electrospinning is used to produce prototypical biomaterial scaffolds for tissue engineering for tendon, 44,45 bone, 46 cartilage, 47,48 meniscus, 49 smooth and skeletal 50 muscle, and neural tissue 51,52 and produces highly tunable scaffold structure and architecture. Electrospinning parameters such as voltage, flow rate, distance to the collector, polymer concentration, solution conductivity, solvent, humidity, and temperature determine the fiber characteristics.…”

Structure, function, and defect tolerance with maturation of the radial tie fiber network in the knee meniscus

“…where dispersed nonaligned elements within aligned materials were protective of overall mechanical function. 15 Overall, this study provides new data and insight into the postnatal structural development and maturation of the meniscus RTF network and its impact on the functional characteristics of the tissue.…”

“…Indeed, we recently showed, in a biomaterial model, that the introduction of a disorganized fiber element in an otherwise aligned network could restore strain transfer close to focal defects that interrupted the aligned fiber network. 15 It is possible that the RTF network of the knee meniscus plays a similar role.…”