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Part 1
Physiology![]()
CHAPTER 1
THE PHYSIOLOGY OF BONE CIRCULATION
IAN MCCARTHY
University College London Institute of Orthopaedics
and Musculoskeletal Science
Royal National Orthopaedic Hospital, Brockley Hill, Stanmore, UK
INES REICHERT
Department of Orthopaedic Surgery
Kingās College Hospital, Denmark Hill, London, UK
1.1 Introduction
Maintenance, regular turnover, and repair of bone are critically dependent on a sufficient vascular supply and responsive hemodynamics. Bone circulation obviously acts as a conduit to provide nutrients for cell in bone, but in addition, it has an important role in mineral homeostasis, the control of bone turnover, and the response to injury. Any event such as a fracture or surgical intervention to bone poses a challenge due to disruption of the blood supply, and requires an intact vascular response for successful repair.
1.2 Organization of the Vascular System in Bone
The specific anatomical organization of the vascular system in the skeleton varies from bone to bone, and details have been described.16, 29 There are, however, common underlying principles for the vascular organization in all bones, and these are important for many of the physiological functions of the vascular system. This section, therefore, will provide an overview of the anatomic sources of blood flow to bone, and their hemodynamic interconnections.
Following historical accounts by Langer72 and Lexer,74 there is agreement that the blood supply of bone has three main sources of vessels supplying the cortex of long bones:16, 63 the epiphyseal-metaphyseal arteries, the nutrient artery, and the periosteum.
1.2.1 Medullary circulation
Bone marrow is perfused by blood vessels arising from the one or two nutrient arteries which have pierced the bone. In over 90% of the human tibiae examined by Menck et al. there was one nutrient foramen evident, but in a few cases there were two such foramina.92 The nutrient vessels will not solely supply marrow, but cortical bone as well. In the diaphyseal marrow of tubular long bones, the nutrient artery divides into ascending and descending branches and, together with the medullary branches of the metaphyseal arteries, is responsible for the blood supply to the fatty and haemopoietic bone marrow.
1.2.1.1 Parallel supply of marrow and cortex by the nutrient artery
Lopez-Curto et al. used stereo light-microscopy for three-dimensional examination of the vasculature in the adult dog tibia and showed that the vasculature of the cortex and the medulla did not communicate at an arteriolar or capillary level.80 They concluded that the nutrient artery supplied the marrow and cortex in parallel.
1.2.2 Metaphyseal circulation
The periosteal vascular plexus, the Hunterās vascular circle, around the metaphysis perforates the cortex in a pattern constant throughout the life of an individual. These arteries divide within the metaphyseal area and anastomose with branches of the nutrient artery.142 Anecdotal evidence suggests that the metaphyseal arteries are capable of sufficiently supplying the diaphysis in long bones with congenitally absent nutrient foramina.16 Following the closure of the epiphysis, intraosseous ā in addition to the existing extra-osseous ā anastomoses occur between the metaphyseal and epiphyseal arteries. The vascular network thus formed is referred to as the epiphysio-metaphyseal vascular system.99, 138, 140
1.2.3 Venous system
The arrangement of the venous system of the marrow is different from that of the arterial system. A central venous sinus with a diameter approximately four times that of the nutrient artery, but with a thinner wall, runs medullo-central the full length of the diaphysis.16 The nutrient vein branches off the central venous sinus as well as other emissary vessels and traverses the cortex.15, 80
1.2.4 Periosteal circulation
The periosteum forms a thin surrounding layer of soft tissue which envelopes bone. It is most distinct at the level of the diaphysis and particularly well established in the young organism. A fracture of the juvenile skeleton is often referred to as a āgreenstickā fracture when the periosteal layer has stayed intact. The periosteum forms the interconnection of cortical bone with the musculature and connective tissue. The periosteum consists ultrastructurally of three layers of tissue: close to bone the cambium layer contains osteogenic cells, in the midzone a highly vascular layer contributes to the blood supply of the cortical bone, and in the periphery there is a dense layer of collagen bundles and fibers.45 The periosteum is responsive to injury two-fold: its osteogenic layer forms the peripheral callus in fracture healing and its vascularity acts as reserve supply should the medullary system fail.
Menck et al. have given a detailed account of the anatomy of the arterial supply to the periosteum of the human tibia.92 They dissected 30 legs after the injection of Berlin Blue Gelatine and found crucially that the distal diaphysis is supplied exclusively by semicircular branches of the anterior tibial artery. In contrast, the proximal diaphysis is supplied by periosteal branches of the anterior and posterior tibial artery. As clinically observed, it is in the distal tibia that fracture healing is often impaired.
1.2.5 Structure and blood supply of the diaphyseal cortex
The vasculature in cortical bone utilizes the spaces provided by the longitudinal Haversian system and the transverse Volkmann canals, although the causative relationship is probably the reverse. A description of the structure of compact bone will outline the arrangement of the angioarchitecture of bone.
Cortical bone is structured in a highly organized fashion and intracortical vessels play a central role. The osteon is a term often used interchangeably with the Haversian system and should be preferred if the structure is addressed. The osteon constitutes the basic morphological unit of most of the compact (cortical) bone, together with the circumferential and interstitial lamellae that are deposited at the periosteal and endosteal surfaces.23 The vessels in the osteons were found to be continuous with vessels coursing in endosteal lamellae, most of which pierce the subendosteal lamellae. The network of osteons follows a spiral around the axis of the bone.
A Volkmann canal ā a term for a vascular channel which is not surrounded by concentric lamellae of bone ā forms a radial connecting canal passing through circumferential lamellae.26
1.2.5.1 Ultrastructure of Haversian systems
Cooper et al. performed electronmicroscopic studies on the Haversian system. Within each osteon they found one or two vessels with the ultrastructure of capillaries.26 The vessels are lined by endothelial cells and often connected by a special single-layered membrane. Immediately adjacent, but not forming a complete ring, pericytes were seen. The basement membrane splits to include the pericytes.34 Usually there were unmyelinated and sometimes myelinated nerve fibers 5ā9 Āµm in diameter seen.26
Mature osteons gradually transform into resorption spaces and new osteons will be formed in such spaces. All osteons are demarcated from their neighbors by a jagged-edged cement line which may mark the limit of bone erosion prior to the formation of an osteon.23 Similar basophilic lines also occur in the absence of erosion when bony growth is interrupted and then res...
