Increased hydraulic conductance of human articular cartilage and subchondral bone plate with progression of osteoarthritis

Abstract

Objective: Osteoarthritis (OA) is characterized by progressive degeneration of articular cartilage and remodeling of the subchondral bone plate, comprising calcified cartilage and underlying subchondral bone. Calcified cartilage remodeling due to upward invasion by vascular canals or to calcified cartilage erosion may contribute to biomechanical alteration of the osteochondral tissue and its subchondral bone plate component. The study hypothesis was that hydraulic conductance of osteochondral tissue and subchondral bone plate increases with structural changes indicative of increasing stages of OA.

Methods: Osteochondral cores were harvested from the knees of cadaveric tissue donors and from discarded fragments from patients with OA undergoing knee surgery. The osteochondral cores from tissue donors were macroscopically normal, and the cores from patients with OA had partial-thickness or full-thickness erosion to bone. The cores were perfusion-tested to determine the hydraulic conductance, or ease of fluid flow, in their native state and after enzymatic removal of cartilage. Adjacent portions were analyzed by 3-dimensional histology for calcified cartilage, subchondral bone, and subchondral bone plate thickness and vascular canal density.

Results: Hydraulic conductance of native osteochondral tissue and subchondral bone plate was higher (2,700-fold and 3-fold, respectively) in fully eroded samples than in normal samples. The calcified cartilage layer was thicker (1.5-fold) in partially eroded samples than in normal samples but thinner and incomplete in fully eroded samples. Subchondral bone plate vascularity was altered with increasing stages of OA.

Conclusion: During joint loading, increased hydraulic conductance of the osteochondral tissue and subchondral bone plate could have deleterious biomechanical consequences for cartilage. Increased fluid exudation from overlying and opposing cartilage, increased fluid depressurization, and increased cartilage tissue strains could lead to chondrocyte death and cartilage damage.

Figure 1

(A) Schematic diagram of perfusion test setup and representative Darcy plot to estimate hydraulic conductance constant, c. (B) Effect of OA erosion and papain digestion on hydraulic conductance of osteochondral tissue and ScBP. Conductance values after 2h perfusion of normal, partially eroded, and fully eroded osteochondral tissue before and after removal of cartilage by papain digestion. ● = p<0.013; ▲ = p<0.0033.

Figure 2

Normal (A,D), partially eroded (B,E), or fully eroded (C,F) osteochondral samples without (A,B,C) and with (D,E,F) articular cartilage removal by papain digestion

Figure 3

Typical vascular canals penetrating (A) into calcified cartilage in normal ScBP, (B) into deep zone cartilage in partially eroded ScBP, and (C) to the surface of fully eroded ScBP.

Figure 4

Stereological measurements of subchondral bone plate structure. (A) Thickness of calcified cartilage (black) and underlying subchondral bone (white). Total height of each column is ScBP thickness. (B) Number of vessels penetrating the CC/bone interface per cross-sectional area for normal, partially eroded and fully eroded osteochondral samples before and after cartilage removal by papain digestion. ● = p<0.013; ▲ = p<0.0033.

Figure 5

Schematic of normal (A), partially eroded (B), and fully eroded (C) osteochondral tissue and potential deleterious effects of increased ScBP permeability leading to increased fluid loss. Wavy arrows indicate fluid flow within cartilage and also fluid loss from from overlying (B) and opposing (C) articular cartilage during loading. Plus signs indicate magnitude of osteochondral and ScBP hydraulic conductance.