Epiphyseal cartilage vascular architecture at the distal humeral osteochondritis dissecans predilection site in juvenile pigs

Abstract

Failure of endochondral ossification due to interruption of the vascular supply to the epiphyseal cartilage is a critical step in the development of osteochondritis dissecans (OCD). Herein we describe the vascular architecture of the distal humeral epiphyseal cartilage in pigs and identify characteristic features that have been associated with sites predisposed to OCD development across species. Distal humeral specimens were harvested from pigs (n = 5, ages = 1, 10, 18, 30, and, 42 days old) and imaged at 9.4T magnetic resonance imaging (MRI) using a 3D gradient recalled echo sequence. The MRI data were processed using a quantitative susceptibility mapping (QSM) pipeline to visualize the vascular architecture. Specimens were also evaluated histologically to identify the presence of ischemic epiphyseal cartilage necrosis (osteochondrosis [OC]-latens) and associated failure of endochondral ossification (OC-manifesta). The QSM data enabled visualization of two distinct vascular beds arising from the perichondrium at the lateral and medial aspects of the distal humeral epiphysis. Elongated vessels originating from these beds coursed axially to supply the lateral and medial thirds of epiphyseal cartilage. At 18 days of age and older, a shift from perichondrial to transosseous blood supply was noted axially, which appeared more pronounced on the lateral side. This shift coincided with histologic identification of OC-latens (30- and 42-day-old specimens) and OC-manifesta (18- and 42-day-old specimens) lesions in the corresponding regions. The vascular anatomy and its evolution at the distal humeral epiphysis closely resembles that previously reported at predilection sites of knee OCD, suggesting a shared pathophysiology between the knee and elbow joints.

Keywords: MRI; OCD; elbow; epiphyseal vasculature.

Figure 1:

3D reconstructions of the segmented secondary ossification center, epiphyseal cartilage, and the epiphyseal vasculature, depicting the vascular architecture to the distal humeral epiphyseal cartilage in pigs aged 1 to 42 days. Elongated vessels, arising abaxially from the perichondrium, supply the lateral and medial third of the joint, while the central portion of the epiphyseal cartilage is avascular. At 18 days of age and later, at the lateral portion of the distal humerus, blood supply to the axial segment has shifted from vessels originating from the perichondrium to vessels traversing the ossification front (white ellipses). The secondary ossification center of the medial epicondyle (black circles) is apparent at 18, 30, and 42 days of age. Image orientation: Lateral is to the left and anterior (cranial) is to the top.

Figure 2:

Coronal and axial plane minimum intensity projections generated from the 3D QSM images depicting the distal humeral epiphyseal vasculature in pigs aged 1 to 42 days. Elongated vessels arising from the perichondrium coursing axially (black arrows) are apparent both in the medial and lateral thirds of the distal humeral epiphyseal cartilage, while the central third of the epiphyseal cartilage is avascular (black ellipse). Vessels traversing the growth plate (white arrowheads) are present in the 1 and 10-day-old specimens. There is progressive thinning of the epiphyseal cartilage with increasing age. Blooming MRI artifacts (black arrowheads) in the 1- and 18-day-old specimens are apparent. Black insets in the right lower corner identify the region the minimum intensity projections depict. Coronal image orientation: lateral is left and proximal is to the top. Axial image orientation: lateral is left and anterior (cranial) is to the top.

Figure 3:

Axial plane minimum intensity projections generated from the 3D QSM images depicting the vascular supply to the distal humeral growth plate in pigs aged 1 to 42 days. Black dots (black arrows) present in the central portion of the growth plate in the 1- and 10-day-old specimens correspond to vessels traversing the growth plate. At 18 days of age and later, these transphyseal vessels are no longer present. Blooming MRI artifacts (white arrowheads) in the 1-day-old specimen are apparent. Black insets in the right lower corner identify the regions the minimum intensity projections depict. Image orientation: lateral is left and anterior (cranial) is to the top.

Figure 4:

Histologic section (Panel A) depicting an OC manifesta lesion (*) in the medial aspect of the distal humeral epiphyseal cartilage in the 18-day-old piglet. Inset: The OC-manifesta lesion (dotted line) and associated delay of the ossification front (white arrows) along with a vascular profile (black arrowhead) are apparent. The OC-manifesta lesion is also visible in the Corresponding 3D GRE image (Panel B) and 3D QSM minimum intensity projection (Panel C). Vessels supplying the epiphyseal cartilage (black arrows) are clearly identified in the minimal intensity projection (Panel C). A blooming artifact associated with the vascular profile identified in panel A is apparent in the MRI images (black arrowhead) in panels B and C.