ORTHOPEDICS

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BASIC MAMMALIAN BONE ANATOMY AND HEALING

Dianne Dunning, DVM, MS, DACVS

To fully appreciate bone anatomy and healing in birds one must have an understanding of mammalian bone, because avian and mammalian skeletal systems have more similarities than differences in structure and function. Both skeletal systems provide a rigid and protective framework for most of the soft tissues and internal organs while providing a scaffold for tendon and ligament attachments.4, 15, 18 Additionally, bone serves as an important storehouse for calcium and phosphorus and as a site for fat storage and hematopoiesis.4, 18 BONE COMPOSITION Bone is a specialized form of connective tissue that consists of a matrix, minerals, and cells. Biochemically, it is a blend of organic (35%) and inorganic (65%) material.4 The inorganic or mineral component consists of calcium hydroxyapatite crystals (Ca10[PO4]6[OH]2), which give bone its strength and rigidity and serve as a reservoir for 99% of the bodys calcium, 85% of the bodys phosphorus, and 65% of the bodys sodium and magnesium.4 The structure and composition of individual bones provide the maximum resistance to mechanical stresses while maintaining the least bone mass.25 To accommodate changing mechanical tresses and the demands of calcium and ion homeostasis, all bones in the body are in a dynamic state of growth and resorption throughout life.2, 4, 18 Avian bones have a higher calcium content (e.g., 16.42% in

From the Department of Clinical Medicine, University of Illinois, College of Veterinary Medicine, Urbana, IL VETERINARY CLINICS OF NORTH AMERICA: EXOTIC ANIMAL PRACTICE
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chickens) than do mammalian bones (10%), which may contribute to the thin and brittle nature of avian bones.12, 19, 21 Biomechanical studies in breeder chickens have revealed that bone density and strength increase with age, which may be related to increases in inorganic content and collagen.17 The organic component of bone consists of cells and an extracellular matrix.2, 4 The cells consist of osteoblasts, osteocytes, and osteoclasts.2, 11 Osteoblast and osteocytes are mesenchymal in origin and are called osteoprogenitor cells.2, 4, 18, 25 Osteoblasts are immature bone cells that are responsible for the synthesis and secretion of osteoid, an organic component of the extracellular matrix of bone.2, 4 Osteoid rapidly undergoes mineralization to form bone.2, 4, 18, 28 The osteoblasts become entrapped within the secreted matrix and differentiate into osteocytes. Osteocytes make up most of the bone cell population in adult animals and are responsible for the maintenance of the bony matrix. Osteoclasts are multinucleated cells that are derived from the macrophagemonocyte family and are involved actively in the resorptive process associated with the continuous remodeling of bone.2, 4, 18, 25 The extracellular matrix consists of a ground substance composed of glycoproteins, proteoglycans, and collagen bers and is mineralized. The glycoproteins and proteoglycans are highly anionic complexes that have a high ion-binding capacity and are thought to play an important role in the mineralization of bone and in the xation of the calcium hydroxyapatite crystals to the collagen bers.14 Type 1 collagen forms the backbone of the matrix and accounts for 90% of the organic component.4 Osteoblasts deposit type 1 collagen in either a random or lamellar fashion, depending on whether the bone is trabecular or lamellar in nature.4 Noncollagenous proteins make up the remainder of the organic matrix of bone in the form of cell-adhesion proteins, calcium-binding proteins, mineralization proteins (osteocalcin), enzymes, cytokines, and growth factors (Table 1).4 Of these proteins, osteocalcin is the only protein that is unique to bone.4 STRUCTURE OF BONE There are two types of bone: cortical and cancellous bone. Cortical or compact bone forms the dense walls of the shaft or diaphysis and is the outer protective covering of all bone.15, 25 Compact bone is made up of columns of bone that are parallel to the long axis of the diaphyseal shaft and to the stresses exerted by the normal weight bearing of the bone.4, 14, 18, 19, 25 Each of the columns is composed of concentric layers of bone, known as lamellae, centered around neurovascular channels referred to as Haversian canals.4, 14, 18, 19, 25 The neurovascular canals and their concentric lamellae are referred to commonly as Haversian system (Fig. 1).4, 14, 18, 19, 25 Between each Haversian system are interstitial lamellae, which further support the infrastructure of cortical bone.4, 14, 18, 19, 25 Haversian canals develop from broad channels lined with osteo-

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Table 1. BONE MATRIX PROTEINS Protein Class Collagen Cell-adhesion proteins Type 1 Osteopontin, bronectin, thromboplastin Osteonectin, bone sialoprotein Osteocalcin Collagenase, alkaline phosphatase Example Function Serves as a structural scaffold2, 18 Mediates cellular adhesive interaction; provides collagen crosslinks and platelet aggregation Mediates calcium binding Marker of osteoblastic activity18 Collagenase catalyzes the hydrolysis of peptide bonds in collagen; alkaline phosphatase catalyzes the release of inorganic phosphate from phosphoric esters Control bone cell proliferation, maturation, and metabolism and act as cellular messengers4 Activate proteolytic enzymes important for cture healing18; act as cellular messengers4

Calcium binding proteins Mineralization proteins Enzymes

Growth factors

IGF-1, TGF-, IL-6

Cytokines

Prostaglandin, IL-1, IL-6

Adapted from Contran RS, Kumar V, Collins T: Bones, Joints, and Soft Tissue Tumors. In Contran RS, Kumar V, Collins T (eds): Robbins Pathologic Basis of Disease. Philadelphia, WB Saunders, 1999, pp 12161267; with permission.

blasts. The osteoblasts produce osteoid, which later is mineralized and forms the concentric lamellae. With the deposition of each successive lamellae, the channel narrows and the osteoblasts that become entrapped in lacunae are called osteocytes, which are arranged in concentric rings within the lamella. The osteocytes maintain ne cytoplasmic extensions to neighboring osteocytes via minute interconnecting channels known as canaliculi (Fig. 2). The canaliculi provide passages for the circulation of tissue uid and the diffusion of metabolites and allow rapid communications between osteocytes. Osteocytes are responsible for maintaining calcium homeostasis via the resorption and uptake of mineralized matrix. Calcium levels within the body are inuenced directly by a negative feedback system based on serum calcium concentration and indirectly controlled by hormones that are secreted by the parathyroid and thyroid glands.18, 25 There have been limited microscopic studies performed on cortical bone in birds.13, 19, 2224 Unlike in mammals, mature cortical bone in pigeons contains relatively few Haversian systems.23, 24 Studies have revealed that the cortical bone is arranged in a circumferential lamellar

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Figure 1. The basic unit of compact bone. Mineralized bone is deposited in concentric layers around a central canal containing the neurovascular supply of the Haversian system. Intersitial lamellae provide the supportive infrastructure between each Haversian system. (From Remedios A: Bone and Bone Healing. Vet Clin of North Amer 29:10291044, 1999; with permission.)

pattern in pigeons and a few other species of birds, which may contribute to its brittle nature.23, 24 Cancellous or trabecular (spongy) bone occupies the metaphysis of all long bones.14, 25 Trabecular bone consists of a network of ne, irregular plates called trabeculae that are separated by intercommunicating spaces lled with bone marrow and hematopoietic cells.25 The lining of the trabeculae is covered by endosteum, which contains osteoprogenitor cells.25 Cancellous bone is scarce or nonexistent in certain at bones of the skull and pelvis in mammals and birds.4, 15 Furthermore, bones of the skull, vertebrae, pelvis, sternum, ribs, the humerus, and sometimes the femur in birds have minimal trabecular bone owing to their pneumatic nature9, 14, 19 In immature animals, the medullary cavities of most bones contain active bone marrow, which is responsible for the production of red blood cells. Active bone marrow consists of two main components: a supportive reticulin framework and a system of interconnected blood sinusoids that drains toward the central vein. Hematopoiesis occurs within the reticulin framework. Once red cell development is complete or almost complete, the cells move into the sinusoids and are released into the general circulation. In the adult animal, active marrow is restricted to the metaphysis and the medullary cavities of the diaphysis are lled with inactive marrow, which is largely comprised of fat.25 A connective tissue layer called the periosteum covers nonarticular

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Figure 2. Each osteocyte is surrounded by calcied matrix. Long cytoplasmic processes extend between lacunae, which maintain cell to cell contact and provide passages for circulation of tissue uid and diffusion of metabolites. (From Remedios A: Bone and Bone Healing. Vet Clin of North Amer 29:10291044, 1999; with permission.)

cortical bone. Muscles, tendons, and ligaments insert into and originate in this dense brous connective tissue. A delicate connective tissue layer called the endosteum covers the inner surface of the medullary cavity. The endosteum and periosteum in mammals contain osteogenic cells that are responsible for growth, remodeling, and repair of bone fractures.25 In direct contrast to mammals, the endosteum and periosteum in adult birds seem relatively quiescent. In the skeletally mature pigeon humerus, the periosteum consists of a dense layer of tissue, which contains few osteoprogenitor cells. Likewise, avian endosteum contains few osteospecialized cells. Histomorphometry studies on the pigeon further support the lack of biologic activity of the periosteal and endosteal envelopes, revealing the minimal uptake of uorescent labeling, which is an indication of low levels of resorption/formation in the intact bone.24 A layer of hyaline cartilage that is composed of chondrocytes and an extracellular matrix protects the articular surfaces of the epiphysis.25 Hyaline cartilage plays a vital role in the function of articular joints by

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absorbing stresses, distributing mechanical loads, and resisting deformation. BONE GROWTH AND DEVELOPMENT Two classes of bone are recognized based on histogenesis: at bone (ossa plana), which arises from intramembranous ossication,11, 15 and long bone (ossa longa), which is derived primarily from endochondral ossication. Interestingly, the development and growth of long bones actually involves both types of ossication.15 Intramembranous ossication occurs directly within the mesenchymal tissue in specic centers of ossication. Osteoblasts, derived from primitive mesenchymal cells, begin synthesizing and secreting osteoid, which becomes mineralized. As the osteoid is deposited, the osteoblasts become entrapped within lacunae in the matrix; however, they maintain cytoplasmic extensions within canaliculi that allow for cell-to-cell contact. Osteoprogenitor cells divide and multiply, producing more osteoblasts, which continue to lay down additional bone. Progressive bone formation allows the separate centers of ossication to coalesce and fuse. Initially, bone formed by intramembranous ossication appears trabecular in nature. The randomly arranged conguration of cells, collagen bers, and osteoid are soon remodeled by osteoclasts, allowing the ordered osteoblastic deposition of compact and trabecular bone.2, 25 In endochondral ossication, mesenchymal cells rst differentiate into cartilage. A small model of the long bone is formed from hyaline cartilage. Then, within the shaft of cartilage, the cartilage cells hypertrophy and undergo degradation and mineralization.2, 15 This creates what is referred to as a primary center of ossication.2, 14, 25 Osteoclast-type cells remove the mineralized cartilage, which allows the ingrowth of blood vessels that carry osteoprogenitor cells.2, 15 Simultaneously, the perichondrium that surrounds the cartilage shaft develops osteogenic potential and becomes the periosteum.14, 25 The periosteum lays down a thin layer of bone around the surface of the shaft, and primitive mesenchymal cells and blood vessels invade the spaces within the shaft after the degeneration of the chondrocytes.2, 14, 25 The primitive mesenchymal cells differentiate into the osteoblasts and hematopoietic cells of the bone marrow.25 The osteoblasts line the mineralized cartilage scaffolding and begin to produce trabecular bone.25 The epiphyses form separate, secondary centers of ossication, and the interface between the epiphyses and the shaft of the bone form the epiphyseal plate (also called the growth plate). Long bone growth is the direct result of continual, rapid proliferation of cartilage at the epiphyseal plate, which subsequently mineralizes and is replaced by bone (Table 2). At sexual maturity, most mammals undergo hormonal changes that result in the cessation of growth and fusion of the growth plate.4, 14, 25 Endochondral ossication in birds is different from that in mammals in several ways. Although the nomenclature used to describe the zones

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Table 2. EPIPHYSEAL GROWTH PLATE ZONES IN MAMMALS Zone Zone of reserve cartilage Zone of proliferation Zone of maturation Zone of hypertrophy and calcication Zone of cartilage degeneration Zone of osteogenesis Cellular Population Consists of hyaline cartilage that is organized in cellular clusters25 Consists of clusters of cartilage cells that undergo mitotic proliferation25 Cell division ceases, and the chondrocytes begin to enlarge25 Cellular enlargement continues, and the surrounding matrix begins to mineralize25 Chondrocytes begin to deteriorate; vascular channels invade and osteogenic cells set up residence19, 25 Osteogenic cells differentiate into osteoblasts and begin bone formation25

of the epiphyseal plate varies from publication to publication, there is general agreement to the number of zones (Table 3). The zone of proliferation is relatively wider in many avian epiphyseal plates than it is in mammalian growth plates. Additionally, cells in the zone of hypertrophy are not arranged in orderly columns nor are they invaded systematically by vascular channel, which leaves clusters of chondrocytes surrounded by mineralized matrix. Finally, the growth plate in birds is vascularized by two sets of vessels, from the epiphysis and the metaphysis. This contrasts with the epiphyseal blood supply in mammals, which is supplied directly by one vessel from the epiphysis.19 NEUROVASCULAR SUPPLY TO BONE The basic components of the medullary blood supply are the nutrient artery and the proximal and distal metaphyseal arteries. The nutrient artery and metaphyseal arteries anastomose with one another at each end of the medullary cavity and are responsible for the excellent blood supply and healing capabilities of the metaphysis. The nutrient artery enters the bone along the diaphysis and usually is accompanied by a major fascial attachment of muscle. It traverses the cortical bone without
Table 3. EPIPHYSEAL GROWTH PLATE ZONES IN BIRDS Zone Zone of proliferation Zone of prehypertrophy Zone of hypertrophy Comments Also known as the proliferating and maturing zone and the proliferating prehypertrophied zone Also known as the uncalcied hypertrophic zone and the hypertrophied zone Also known as the calcied hypertrophic zone and the degenerating hypertrophied zone

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arborizing and enters into the medullary cavity. Once in the medulla, the nutrient vessel bifurcates into ascending and descending tributaries, which arborize and penetrate the endosteum. The nutrient and metaphyseal arteries provide approximately two thirds of the blood supply of long bones, with the rest supplied by the muscle attachments of the periosteum.4, 24, 26 Intramedullary arterial pressure is higher than in the periosteum and maintains the centrifugal ow of blood.26 The afferent vessels enter the bone and form neurovascular channels known as Haversian canals or osteons (see Fig. 1). These neurovascular bundles interconnect with one another and with the endosteum and periosteum via Volkmanns canals, which traverse the Haversian systems longitudinally. The Haversian vessels supply oxygen and important nutrients to the osteocytes via canaliculi.18, 25 Venous drainage of blood occurs primarily in a centripetal fashion.18, 26 In mature and immature mammals, the cortex and medullary cavity are drained separately. Medullary venous blood is drained into sinusoids that coalesce into a central venous sinus. The central venous sinus then forms the nutrient vein, which exits the cortex at the same site as the nutrient artery and drains into the systemic circulation. Cortical venous blood ow is also centripetal, toward the periosteum, where it is drained into periosteal venules then coalesces into larger periosteal veins before entering the systemic circulation.18 The blood supply in immature bone is similar to that in adult bone, with a few minor exceptions. In immature animals, the periosteal blood supply is substantial and is responsible for most of the appositional bone growth. Once an animal reaches maturity, this abundant blood supply atrophies. In all mammals, except for neonatal foals, the physis provides a barrier that separates the physeal and the epiphyseal blood supply. This is an area of active endochondral growth that receives a rich vascular supply from a network of vessels called the epiphyseometaphyseal arcade.18 Birds also have an intramedullary blood supply in pneumatic and marrow-lled bones. As in mammals, the nutrient and metaphyseal arteries in birds provide most of the blood supply to the marrow-lled bones (e.g., radius, ulna).24 In the pneumatic bones, such as the humerus, however, the arborization is less extensive.24 Generally, most of the blood supply originates from the medullary cavity, with no appreciable periosteal circulation present along the diaphysis.24 The lack of periosteal circulation may be attributed to the lack of soft tissue coverage.21 Angiographic analysis in pigeons and other species of birds has revealed fewer Haversian systems in the humerus, which may account for its more brittle nature.24 Additionally, the decreased number of Haversian systems in birds, with their central vascular channels, suggests a cortical blood supply that is less important in fracture healing and is biologically active.24 Accordingly, the osteon and its accompanying blood vessel may have less of a role in bone remodeling and repair.24 As with mammals, immature birds have biologically more active marrow cavities with

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increased vascularization and hematopoietic capacity. Angiographic studies of immature pigeons have revealed that the intramedullary blood supply of the humerus bones is similar to that of the nonpneumatic bones.24 Lymphatic ducts are present in the periosteum and within the medullary cavity itself.4 The nervous supply to bone is primarily sensory, carrying only afferent impulses of pain to brain.4 Although denitive studies of the lymphatic and nervous systems to bone have not been performed in birds, they are assumed to be similar. BIOLOGY OF BONE HEALING Although the biology of bone healing in birds is similar to that in mammals, it often is complicated by the lack of soft tissue coverage, the presence of brittle pneumatic bones (see Dr. Tullys article for more information on this), and the intense distracting forces of the pectoral ight muscles.22 The rate of fracture healing depends on the displacement of the fracture fragments, the amount of damage to the blood supply, the presence of infection, and the amount of motion at the fracture site.12 There are essentially two classes of fracture healing: primary (direct) and secondary (indirect). Primary fracture healing occurs in instances where there is low interfragmentary strain. This usually occurs only when the fracture fragments are reduced anatomically and stabilized and when the fragments are placed under interfragmentary compression, usually with a dynamic compression plate. In this circumstance, there is direct formation of lamellar bone across the fracture line and no evidence of callous formation.1, 11, 16, 18, 20 Depending on the distance between the fracture fragments there are two methods of primary healing: contact and gap. Contact healing occurs when there is a defect of less than 0.01 mm. In this situation, new lamellar bone is formed directly across the fracture line, parallel to the long axis of the bone. Haversian remodeling is immediate, with osteoclastic cutting cones crossing the fracture line and bringing perivascular osteoprogenitor cells that differentiate into osteoid-producing osteoblasts. If the fracture gap is greater than 0.01 mm but less than 0.50 mm, primary bone healing still may occur in the form of gap healing. In gap healing, endosteal and periosteal cells produce lamellar bone, which is deposited perpendicular to the long axis of the bone. The perpendicular lamellar bone is remodeled later by Haversian systems into the proper longitudinal orientation.11, 16, 18, 20 Primary healing in birds is preferable but difcult to achieve. Plates are ideal for promoting primary healing and thus produce the fastest rate of union with the smallest callus, which allows an early return to function (Fig. 3).13 Small plating systems are available and lend themselves well to the avian species. Practices with a high avian case load should consider this option because it may provide the best prognosis

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Figure 3. Comminuted femoral fracture owing to gunshot injury repaired by way of a platerod combination. (Courtesy of S. Kerwin, DVM, MS, Associate Professor, Louisiana State University, School of Veterinary Medicine, Baton Rouge, Louisiana.)

for the avian fractures. The disadvantages of plating are the initial cost of instrumentation and the learning curve. As mentioned previously, bird cortices are brittle and plate application is technically unforgiving. Secondary bone healing occurs when there is (1) a lack of rigid internal xation and compression, and (2) complex or comminuted fractures in which the bony column cannot be reconstructed. This type of healing is a common end product of less stable forms of internal xation (e.g., pin, cerclage), external xation, and external coaptation with casts or splits. It is also the end product of untreated fractures, which are seen commonly in wild animals and birds and in most cases result in malunion of the fracture fragments. The hallmark of secondary bone healing is callous formation, which is directly proportional to the amount of motion present between the fracture fragments. Technically speaking, almost all fractures heal via second intention, because it is difcult to eradicate motion completely even with internal plate xation.1, 10, 11, 18, 20, 22 Secondary bone healing is divided into three phases: the inamma-

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tory phase, the reparative phase, and the remodeling phase.1, 10, 11, 18, 20, 22 The division between these phases is somewhat arbitrary and there is overlap; however, for discussion purposes, they are informative. The inammatory phase begins immediately after the trauma of a fracture.1, 10, 11, 18, 20, 22 In most cases, fractures are associated with an immediate and profound alteration in blood supply to the bone.1, 11, 18, 26 Depending on the kinetic energy associated with the fracture, the medullary and periosteal blood supply both may be served. A hematoma forms within the soft tissues and envelopes the fracture fragments.1, 11, 18, 26 Disruption of the vascular supply to the bone causes ischemic cell death and necrosis of the osteocytes at the apices of the fracture fragments.1, 11, 18, 26 In response to these vascular changes, the fracture site becomes hypoxic and acidotic.1, 11, 18, 26 Inammatory cells arrive on the scene and begin the process of phagocytosis.1, 11, 18, 26 Neutrophils are the rst to arrive, followed by macrophages in 3 to 5 days if infection is not present.57 The presence of bacteria and foreign material prolongs the inammatory phase by weeks to months, depending on severity of the infection or contamination.57 The vascular system responds to tissue ischemia and inammation within hours of the fracture by enhancing ow to the medullary cavity and periosteum.5, 11, 20 New transient extraosseus blood ow emerges from the injured soft tissue adjacent to the fracture site.5, 11, 20 These new blood vessels supply osteoprogenitor cells, which aid in the construction of the fracture callus.5, 11, 20 The ability of the blood supply to revascularize the fracture completely is related directly to whether motion is controlled at the fracture site.20 The reparative phase is heralded by the organization of the hematoma and the formation of granulation tissue. The fracture environment becomes more cell friendly, with a gradual shift in the pH toward the neutral or alkalotic range. Mesenchymal cells invade the site from the periosteum, endosteum, and bone marrow and begin brous callus formation, which is mechanically stiffer than the hematoma or the granulation tissue. The brous callus consists predominately of type III collagen that is produced by broblasts during the rst week of injury. Mesenchymal cells that are recruited by bone-morphogenic proteins differentiate into chondrocytes and produce a cartilage matrix. In a process similar to endochondral ossication, the cartilage callus is replaced via vascular invasion, cartilage mineralization, and bone formation.1, 11, 18, 20 The remodeling phase is characterized by the slow conversion of the bony callus, which is made up of trabecular bone, to compact bone. Osteoclasts resorb the trabecular bone and deposit the lamellar bone in a manner that is biomechanically compatible with the forces acting on the long bone. This appropriate adaptation of bone to the forces of weight bearing is known as Wolffs law. Over time, the compact bone of the cortex is restored completely and the medullary cavity is reestablished.1, 11, 18, 20 Many growth factors have been shown to inuence bone heal-

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g.3, 8, 18 Most of the recent research has focused on several major growth factors: platelet-derived growth factor, insulin-like growth factor 1, transforming growth factor , bone-morphogenic proteins, and broblast growth factor.18 A full discussion of each of these is outside the scope of this article, and the reader is referred to several excellent reviews for further information.3, 9, 18

FAILURE OF FRACTURE REPAIR Fracture healing usually is monitored by periodic radiographic reassessment. A delayed union is dened as the slowed progression of fracture healing beyond the usual expected timeframe.1, 5, 7 A fracture is termed a nonunion if it does not heal within an expected timeframe and does not show radiographic signs of bony activity.1, 5, 7 The causes of delayed union and nonunion are numerous, but most commonly involve motion at the fracture site, infection, and poor blood supply.1, 5, 7 Other possible causes of delayed union or nonunion include metabolic or nutritional disturbances, which are seen more commonly in avians than in mammals, neoplasia, and advanced age.2, 7, 11, 18 By far the most common cause of failure of fracture repair in mammals and birds is inadequate xation.1, 5, 7 Inadequate xation allows for excessive motion at the fracture site, which impedes vascular invasion and angiogenesis.1, 5, 7 A fracture callus is formed; however, it may not be able to bridge the fracture gap without supplemental support.1, 5, 7, 18 Excessive callous formation in birds may inhibit ight function by interfering with joint mobility and soft tissue adhesions.23 Furthermore, prolonged nonunion may lead to a false articulation between fracture fragments, which is called a pseudojoint.1, 5, 7, 18 Severe soft tissue injury associated with fractures of the distal extremities is also a common impairment to fracture healing. The kinetic energy associated with comminuted fractures often is associated with severe impairment to the vascular supply, which delays healing, especially if the fracture is not stabilized immediately.23 Posttraumatic osteomyelitis is dened as inammation of the bone and most commonly is caused by bacterial infection, although fungal and viral agents also may be involved. This condition usually develops after the direct inoculation of bacteria at the time of fracture or during the fracture xation. Despite the high incidence of contamination in open and comminuted fractures in both birds and mammals, osteomyelitis develops in relatively few cases. Factors that increase the likelihood of infection include excessive soft tissue injury, periosteal stripping of the muscular attachments to the bone, and inadequate patient preparation before surgery. Fractures can heal in the face of infection, albeit slowly; however, securing fragment stability is imperative because the combination of motion and infection can lead to disastrous results.5, 7

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SUMMARY The goal of any method of fracture repair should be the early return to function of the patient with minimum postoperative morbidity. This is accomplished most optimally by having a basic understanding of the biology of bone healing and by being familiar with the musculoskeletal system of the species before attempting fracture repair. Applying the fundamental principles of mammalian bone anatomy and physiology to the bird ensures the best prognosis possible and minimizes postoperative complications in the avian patient. References
1. Brown SG, Kramers PC: Indirect (secondary) bone healing. In Bojrab MJ (ed): Disease Mechanisms in Small Animal Surgery, ed 2. Philadelphia, Lea & Febiger, 1993, pp 671 677 2. Contran RS, Kumar V, Collins T: Bones, joints, and soft tissue tumors. In Contran RS, Kumar V, Collins T (eds): Robbins Pathologic Basis of Disease. Philadelphia, WB Saunders, 1999, pp 12161267 3. Dubreuil P, Abribat T, Broxup B, et al: Long-term growth hormone-releasing factor administration on growth hormone, insulin-like growth factor-I concentrations, and bone healing in the beagle. Can J Vet Res 60:713, 1996 4. Evans HE: The skeleton. In Evans HE (ed): Millers Anatomy of the Dog, ed 3. Philadelphia, WB Saunders, 1993, p 122 5. Herron MR: Fracture disease. In Bojrab MJ (ed): isease Mechanisms in Small Animal Surgery, ed 2. Philadelphia, Lea & Febiger, 1993, pp 697699 6. Herron MR: Osteomyelitis. In Bojrab MJ (ed): Disease Mechanisms in Small Animal Surgery, ed 2. Philadelphia, Lea & Febiger, 1993, pp 692696 7. Hoee WD: Delayed fracture union, nonunion, and malunion. In Bojrab MJ (ed): Disease Mechanisms in Small Animal Surgery, ed 2. Philadelphia, Lea & Febiger, 1993, pp 689691 8. Kirker-Head CA: Recombinant bone morphogenic proteins: Novel substances for enhancing bone healing. Vet Surg 24:408419, 1995 9. Lawton MPC. Basic anatomy, physiology, and nutrition. In Tulley TN Jr, Lawton MPC, Dorrestein GM (eds): Avian Medicine. Oxford, Butterworth Heinemann, 2000, pp 125 10. MacCoy DM, Haschek WM: Healing of transverse humeral fractures in pigeons treated with ethylene oxide-sterilized, dry-stored, onlay cortical xenografts and allografts. AJVR 49:106111, 1988 11. Mann FA, Payne JT: Bone healing. Semin Vet Med Surg (Small Animal) 4:312321, 1989 12. Martin HD, Ritchie BW: Orthopedic surgical techniques. In Ritchie BW, Harrison GJ, Harrison LR (eds): Avian Medicine: Principles and Applications. Lake Worth, Florida, Wingers Publishing, 1994, pp 11371169 13. Newton CD, Zeitlin S: Avian fracture healing. JAVMA 170:620625, 1977 14. Nickel R, Schummer A, Seiferle E, et al: Passive locomotor apparatus, the skeletal system. In Nickel R, Schummer A, Seiferle E (eds): Anatomy of the Domestic Birds. Berlin, Verlag Paul Parey, 1977, pp 325 15. Nickel R, Schummer A, Wille K-H, et al: Passive locomotor system, skeletal system. In Nickel R, Schummer A, Seiferle E, et al (eds): The Locomotor System of the Domestic Mammals, vol 1. Berlin, Springer-Verlag, 1986, pp 9161 16. Perren SM: Primary bone healing. In Bojrab MJ (ed): Disease Mechanisms in Small Animal Surgery, ed 2. Philadelphia, Lea & Febiger, 1993, pp 663670 17. Rath NC, Balog JM, Huff WE, et al: Compariative differences in the composition and biomechanical properties of tibiae of seven- and seventy-two-week-old male and female broiler breeder chickens. Poultry Sci 78:12321239, 1999

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18. Remedios A: Bone and bone healing. Vet Clin North Am 29:10291044, 1999 19. Riddell C: Skeletal system. In Riddell C (ed): Avian Histopathology, ed 2. Kennett Square, American Association of Avian Pathologists, 1996, pp 4560 20. Skerry TM: Fracture healing. In Coughlan AR, Miller A (eds): BSAVA Manual of Small Animal Fracture Repair and Management. Cheltenham, England, British Small Animal Veterinary Association, 1998, pp 2934 21. Wan PY, Adair HS, Patton CS, et al: Comparison of bone healing using polydioxanone and stainless steel intramedullary pins in transverse, midhumeral osteotomies in pigeons (Columbia livia). J Zoo Wildlife Med 25:264269, 1994 22. Wander KW, Schwarz PD, James SP, et al: Fracture healing after stabilization with intramedullary xenograft cortical bone pins: A study in pigeons. Vet Surg 29:237244, 2000 23. West PG, Rowland GR, Budsberg SC, et al: Histomorphometric and angiographic analysis of bones healing in the humerus of pigeons. American Journal of Veterinary Research 57:10101015, 1996 24. West PG, Rowland GR, Budsberg SC, et al: Histomorphometric and angiographic analysis of the humerus in pigeons. AJVR 57:982986, 1996 25. Wheater PR, Burkett HG, Daniels VG: Skeletal tissues. In Wheater PR, Burkett HG (eds): Functional Histology: A Text and Colour Atlas, ed 2. Edinburgh, Scotland, Churchill Livingstone, 1987, pp 142160 26. Wilson JR: Vascular supply to normal bone and healing fractures. Semin Vet Med Surg (Small Animal) 6:2638, 1991 Address reprint requests to Dianne Dunning, DVM, MS, DACVS Assistant Professor University of Illinois College of Veterinary Medicine 1008 West Hazelwood Drive Urbana, Illinois 61802 e-mail: ddunning@cvm.uiuc.edu.