Blood Supply of Bone

4.1 Introduction

Bone is a very vascular tissue. Its cells need blood within a short distance, and they die within hours to days when the supply stops. New bone cannot form without new vessels.

For the reconstructive surgeon, the blood supply of bone is the basis of three daily decisions: how much periosteum to strip, whether a bone fragment or graft will survive, and when to choose a vascularized bone flap instead of a graft.

4.2 Arterial supply of a long bone

A long bone has three main arterial systems (Trueta and Morgan 1960; Rhinelander 1974):

Three points about this pattern matter in surgery:

• Flow in the cortex normally runs from inside to outside, from the marrow toward the periosteum.
• The systems are connected. When the nutrient artery is destroyed, for example by a fracture or by reaming for a nail, the periosteal vessels take over more of the cortex and flow can reverse (Rhinelander 1974). A fracture that has lost its nutrient supply then depends on the periosteum and the surrounding muscle.
• The "inner two-thirds and outer one-third" rule is only a guide. It does not mean the outer cortex or the periosteum can be stripped freely when the nutrient artery is intact.

The position of the nutrient foramen varies between bones and between people. In the fibula it is usually near the middle of the shaft. This is why the middle of the fibula is chosen for a flap that will be cut into segments: the segment containing the nutrient artery gets both supplies, and the others survive on the periosteal branches.

4.3 Vessels inside the cortex

Inside the cortex, blood runs in the central (Haversian) canals along the bone and in the perforating (Volkmann) canals across it. The osteocytes are fed from these vessels through the fluid in their canaliculi.

Recent imaging has shown that the cortex of a long bone is crossed by a large number of small vessels running straight from the marrow to the periosteum. In mice, these trans-cortical vessels carry more than 80% of arterial blood and 59% of venous blood leaving the bone, and similar vessels were found in human limb bones (Grüneboom 2019). The inner and outer systems are therefore one connected network, not two separate ones.

4.4 Periosteal and soft tissue supply

The periosteum has its own network of vessels. It is fed by the muscles, fascia and ligaments attached to it. Branches pass from it into the outer cortex. This means:

• A bone fragment that remains attached to muscle or periosteum can stay alive even when it has no medullary supply.
• Stripping periosteum removes this supply, and stripping the muscle off the periosteum removes its feeding vessels.
• In a bone flap, the periosteum and a cuff of muscle are kept on the bone because they carry the vessels.

The fibula is the clearest example. Its nutrient artery and its periosteal branches both come from the peroneal artery. The periosteal branches enter at intervals along the bone through the muscles and the intermuscular septum. When the fibula is cut into segments for a mandible, each segment survives because it keeps its periosteal branches from the peroneal artery, even though only one segment contains the nutrient artery.

4.5 Venous drainage

Blood leaves the marrow through large thin-walled channels (sinusoids) that drain into veins running with the nutrient artery, into veins at the ends of the bone, and into periosteal veins. In the skull, the diploic veins drain the diploë.

A bone flap needs venous outflow as much as arterial inflow. In free flaps, venous thrombosis is more common than arterial thrombosis. In the fibula flap, the two venae comitantes of the peroneal artery drain the bone.

4.6 Blood supply of flat and facial bones

Flat and facial bones are supplied differently from long bones in one important way: most of their blood comes from the soft tissue attached to them, and little or none comes from a nutrient artery.

• A flat bone has no marrow cavity and usually no large nutrient artery.
• Many small vessels enter from the periosteum and from the muscles, mucosa or dura attached to it.
• Inside the bone, these vessels join in the cancellous layer.

This rich supply from the soft tissue is one reason why facial bones heal faster than long bones and are less often infected. It is lost after radiotherapy and in scarred tissue, and in those conditions facial bone heals poorly.

4.7 Blood supply of growing bone

The physis (growth plate) is cartilage and has no vessels of its own. It depends on the vessels on either side:

• Epiphyseal vessels feed the resting and proliferative zones from the epiphyseal side. If they are damaged, the cartilage cells die and growth stops.
• Metaphyseal vessels end in loops at the bottom of the physis. They invade the calcified cartilage and bring the cells that replace it with bone.

This is why a vascularized fibular epiphyseal transfer in a child must be based on the vessel that supplies the proximal fibular epiphysis (the anterior tibial artery). Without that vessel, the physis is carried but does not grow.

The slow flow in the metaphyseal loops of children is also why blood-borne bone infection in children usually starts in the metaphysis.

4.8 New vessels and new bone

New bone forms only where new vessels have grown. This link is called angiogenic-osteogenic coupling.

In mice, a specific type of capillary, called type H, lies next to growing bone and carries the progenitor cells that form it. These vessels decline with age, and restoring them restored bone mass in old mice (Kusumbe 2014; Ramasamy 2014). This is laboratory work; it explains why vessels and bone grow together, but it is not yet a treatment.

Brief hypoxia starts this process. Prolonged ischemia stops it. A fracture with poor blood supply or an irradiated bed produces fibrous tissue or cartilage instead of bone.

4.9 When the blood supply fails

4.9.1 The recipient bed

A free (non-vascularized) bone graft has no blood supply when it is placed. Most of its cells die. It depends on the vessels of the recipient bed to grow into it and bring new cells. The quality of the bed therefore decides whether a free graft survives.

4.9.2 Radiotherapy and osteoradionecrosis

Radiotherapy damages the small vessels and the cells of bone. Marx (1983) described the irradiated bone as hypoxic, hypocellular and hypovascular. In his series, bacteria were only contaminants; the primary problem was tissue that could not repair itself. Minor injury, such as a dental extraction, can then lead to a wound that does not heal and to exposed dead bone: osteoradionecrosis.

This is the main reason why the head and neck reconstructive surgeon uses vascularized bone. A free fibula or iliac crest flap brings its own blood supply into a bed that cannot supply a graft. Advanced osteoradionecrosis of the mandible is treated by resecting the dead bone and replacing it with a vascularized bone flap.

4.10 Vascularized bone flaps

A vascularized bone flap keeps the bone's own vessels, which are joined to vessels at the recipient site. The osteocytes stay alive, so the flap heals to the host bone like a fracture and does not depend on the bed. Each flap is supplied in a different way.

A vascularized flap still needs good fixation, contact with the host bone and good soft tissue closure. Its vessels must stay open: both the artery and the veins.

4.11 Summary

• A long bone is supplied by the nutrient artery, metaphyseal and epiphyseal arteries, and periosteal vessels. Normal flow in the cortex runs from inside to outside.
• The systems are connected by many vessels crossing the cortex. When one is lost, the others take over part of its territory.
• Flat and facial bones depend mainly on the soft tissue attached to them. Keep facial bone attached to its periosteum.
• The mandible relies more on its periosteum with age and loss of teeth. The maxilla survives a Le Fort I osteotomy on its palatal and buccal soft tissue.
• The physis depends on epiphyseal vessels for growth and metaphyseal vessels for ossification.
• New bone forms only where new vessels grow (hypoxia, HIF-1α, VEGF).
• Irradiated bone is hypoxic, hypocellular and hypovascular. It needs vascularized tissue.

References

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