A model of the intracortical vascular system of long bones and of its organization: an experimental study in rabbit femur and tibia.

The vascular anatomy of the cortical bone and the canal system are highly correlated, and the former has an important bearing on shape and microscopic lamellar structure, as it is established in the progression of the remodelling process. The classical description of a longitudinal system of canals (Havers') connected by the transversal Volkmann's canals is the generally acknowledged model of the structural organization of the cortex. However, it is remarkably difficult to study the circulation inside the compact bone in detail owing to its hard, calcified matrix, and the methods thus far applied have represented either the bone morphology and the architecture of the canal system or the injected vessel network. In the present study, the intracortical vessel network was injected with black China ink and evidenced by transillumination of full-thickness, decalcified hemicortices. By making use of the depth of field of the microscope objective, the three-dimensional architecture of the network was highlighted and the morphometry of vessel size measurements and a classification of the network nodes according to the number of arms was made possible. These observations were integrated with data obtained by routine histology on decalcified sections relevant to the connections of the intracortical canal system with the outer environment, with regard to the direction of advancement of new canals and with regard to the mode of formation of the system nodes. The formation of the intracortical vessels network involved two processes: the incorporation of the periosteal network and osteonal remodelling, the latter occurring through the advancement of cutting cones followed by their own vascular loop and by concentric lamellar apposition. The two systems could be distinguished by the diameter of the vessels (the former were significantly larger) and by the network architecture (the former convoluted, and the latter longitudinally orientated and straight). Longitudinal vessels could form branches or create connections with the periosteal derived vessels that occasionally meet on the line of their advancement. They were observed entering from either inside the cortex from the metaphyses or from the endosteal surface of the marrow cavity. The combined observations from different methods of study documented a model of intracortical canal and vessel networks formed by two initially independent systems: one derived from the external, periosteal vessels, and one from metaphyseal and marrow vessels. Connections between the two were established with the advancing of cutting cones from the extremities of the diaphysis. Analysis of the system architecture and the modalities of its progressive organization suggested that the direction of advancement of a forming canal does not necessarily correspond to the final blood flow direction of its central vessel.