Spine Fusion: Anatomy and Biomechanics of Bone-Bone Interface

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Chapter 17 Spine Fusion

Anatomy and Biomechanics of Bone-Bone Interface

In the late 19th century, Sir William Macewen firmly established bone grafting as a treatment option for replacing missing bone and enhancing bone formation. His interest in bone grafting led him to perform allografts and autografts in his patients.1 In the United States, spine fusion was first reported in the early 1900s by Albee2 for the treatment of Pott disease and by Hibbs,3 who used fusion surgery to halt the progression of scoliotic deformity. Since that time the indications for and number of spine fusions have increased. In fact, the numbers doubled between 1980 to 1990,4 with an increase of 77% between 1996 and 2001.5 Spine arthrodesis is now one of the most common surgical procedures performed in the United States.

Unfortunately, a number of complications have been associated with spine fusion. Pseudarthrosis can occur in as many as 35% to 40% of multilevel lumbar fusions.6 Donor site morbidity can also be considerable.7 To achieve successful bony fusion, minimize complications, and achieve a good functional outcome, it is important to understand the various structural, biologic, and biomechanical aspects of bone fusion.

Bone grafts involve transplanting bone tissue from one site to another in order to obtain bone fusion. The terms used for describing them are usually derived from the bone’s origin, anatomic placement, or composition. Autograft is a transplanted tissue within the same individual; allografts are tissues coming from a genetically different individual of the same species; xenografts are tissues transplanted from one species to a member of a different species; isograft is tissue obtained from a monozygotic twin. A graft transplanted to an anatomically appropriate site is defined as orthotopic, whereas if it is transplanted to an anatomically dissimilar site, it is termed heterotopic. Grafts are also categorized by composition as cortical, cancellous, corticocancellous, or osteochondral.8

Anatomy of the Bone-Bone Interface

Histologic Components

On a gross level, all bones are composed of two basic components: cortical (compact) bone and cancellous (trabecular) bone. Cortical bone is a dense, solid mass, except for its microscopic channels, and contains parallel stacks of curved sheets called lamellae, which are separated by bands of interlamellar cement. Regularly spaced throughout the lamellae are small cavities, or lacunae. Lacunae are interconnected by thin, tubular channels called canaliculi. Entrapped bone cells (osteocytes) are located in the lacunae, and their long, cytoplasmic processes occupy canaliculi. The cell processes within canaliculi communicate by gap junctions, with processes of osteocytes lying in adjacent lacunae. Canaliculi open to extracellular fluid at bone surfaces, thus forming an anastomosing network for the nutrition and metabolic activity of the osteocytes. Cortical bone possesses a volume fraction of pores less than 30% and has an apparent density of up to about 2 g/mL. Its compressive strength is approximately 10-fold that for a similar volume of cancellous bone.

Cancellous bone is porous and appears as a lattice of rods, plates, and arches individually known as trabeculae. It has a greater surface area and can be readily influenced by adjacent bone marrow cells. Because of this structural difference, cancellous bone has a higher metabolic activity and responds more readily to changes in mechanical loads.9

Cortical and cancellous bone may consist of woven (primary) or lamellar (secondary) bone. Woven bone forms the embryonic skeleton and is then resorbed and replaced by mature bone as the skeleton develops.10 In the adult, woven bone is found only in pathologic conditions, such as fracture healing and in tumors. Woven and lamellar bones differ in formation, composition, organization, and mechanical properties. Woven bone has an irregular pattern of collagen fibers, contains approximately four times as many osteocytes per unit volume, and has a rapid rate of deposition and turnover. The osteocytes of woven bone vary in orientation, and the mineralization of woven bone follows an irregular pattern in which mineral deposits vary in size and in their relationship to collagen fibrils. In contrast, the osteocytes of lamellar bone are relatively uniform, with their principle axis oriented parallel to that of other cells and to the collagen fibrils of the matrix. The collagen fibrils of lamellar bone lie in tightly organized, parallel sheets, with uniform distribution of mineral within the matrix.11,12

The irregular structure of woven bone makes it more flexible, more easily deformed, and weaker than lamellar bone.9 For these reasons the restoration of normal mechanical properties to bone tissue at the site of a healing fracture requires eventual replacement of the woven bone of the fracture callus with mature lamellar bone.11

Biomechanical Properties of Graft Material

In vivo, the mechanical performance of a bone graft is a function of the intrinsic property of the graft and the properties of the graft-host interface.13 Intrinsic properties of a graft are related to its geometry and composition and include its fracture toughness, yield strength, and elastic modulus.8

In a clinical setting, where the graft has geometric and mechanical properties similar to the host bone, it may function almost immediately.14 Nevertheless, in the case of inferior bone graft mechanical properties, the construct should be designed with additional graft material or incorporate internal fixation until remodeling occurs and the graft can provide adequate load-bearing function.14 A graft’s load-bearing capacity is achieved after complete biologic incorporation by the host, which is related to the mechanical and biologic properties of the graft-host interface.

Iliac crest wedges are the most commonly used graft material. The percentages of cortical and cancellous bone remain constant at 41% and 59%, respectively, regardless of the total cross-sectional area of the wedge. Donor age also does not affect this physical parameter.15

To reduce the immune response and also as methods of preservation and sterilization, allografts undergo certain modifications. These modifications have a profound effect on the biomechanical properties of the graft. Freezing has minimal effects compared with freeze-drying, which significantly reduces both the yield strength and stiffness of the bone graft.16 Autoclaving produces a dose-dependent decrease in strength and stiffness.17 The relationship between gamma radiation and mechanical properties has yet to be established at doses between 0 and 25 kGy (standard dose). But it becomes dose-dependent at 25 kGy for cortical bone or 60 kGy for cancellous bone.18 Complete demineralization of the bone graft results in loss of almost all of its mechanical properties. Comparison testing of various graft materials shows allograft or fresh-frozen cancellous bone to be the weakest, failing at 863 N of compression. Air-dried, ethylene oxide-sterilized, tricortical bone failed at an average load of 2308 N, and fresh-frozen, tricortical allograft bone failed at an average load of 2257 N. Rehydrated iliac crest wedges are more deformable than freeze-dried wedges.19 During loading, freeze-dried wedges fail dramatically, fracturing into many small pieces; this occurrence is secondary to its brittle nature. Rehydrated wedges fail with a circumferential fracture along the side of the wedge where the cortical bone is thinnest. It has been recommended that freeze-dried wedges be rehydrated in a vacuum before clinical use.19 When water or saline is added to the vacuum-sealed container holding the wedge, the wedges gain 100% of their wet weight within 5 minutes of addition of the fluid. Graft collapse occurred more frequently with freeze-dried allografts (30%) than with autografts in anterior cervical fusions.

The loads at the lumbar spine have been well documented in various positions and levels of activity.20 Either autograft or allograft iliac crest wedges are biomechanically sound in an interbody fusion of the lumbar spine, since such fusions would provide load-bearing capacities approximately fourfold greater than would be applied in vivo. Specimens from the anterosuperior iliac spine could bear substantially greater axial loads (average 3230 N) compared with specimens from the posterosuperior iliac spine (average 1458 N).21 Fibular strut grafts are the strongest and have been shown to have a compressive strength of 5070 N.22 However, their cross-sectional area, which is important in preventing telescoping of the graft, is much smaller. In interbody fusion, the cross-sectional area of the graft should be substantially greater than 30% of the end plate to provide a margin of safety.23

Incorporation of Bone Graft

Bone graft incorporation is a prolonged process with a sequence of complicated steps involving the interrelationship of the graft and host. This ultimately leads to the envelopment of a complex of necrotic old bone with viable new bone.24 The complex develops through resorption of the necrotic old bone with viable new bone being laid down. The incorporation of the bone graft is a dynamic process involving the following processes: osteoinduction, osteoconduction along with the availability of osteogenic cells, and the structural integrity, which provides mechanical support.14,19,25,26 This ultimately leads to the replacement of the graft by host bone in a predictable pattern under the influences of load bearing.14,27

At the beginning, the inflammatory response at the host-graft interface results in migration of inflammatory cells and fibroblasts into the bone graft. In addition, the developing hematoma enhances the release of both cytokines and growth factors. Osteoinduction is the process whereby a tissue is influenced to form osteogenic elements through chemotaxis, mitosis, and differentiation of the host osteoprogenitor cells. Induction requires an inducing stimulus, such as a piece of bone or an osteogenic cell, and an environment favorable for osteogenesis. Osteoconduction is the process by which capillaries, perivascular tissue, and osteoprogenitor cells from the recipient bed grow into the graft. It can occur within a framework of nonbiologic materials or nonviable biologic materials. In viable bone grafts, osteoconduction is facilitated by osteoinductive processes and therefore occurs more rapidly than in nonviable or nonbiologic materials.28 Ultimately, this process results in the resorption of the original graft tissue and replacement with new host bone. Remodeling is a response to weight bearing.

Differences in Cancellous and Cortical Bone Graft Incorporation

Cancellous grafts are revascularized more rapidly and completely than cortical grafts. The open trabecular pattern of cancellous bone facilitates vessel ingrowth. Revascularization has been reported to begin within a few hours after grafting29 and may be complete by 2 weeks. In contrast, the dense structure of cortical bone prevents neovascular penetration during the first several weeks after grafting, and hence revascularization of cortical bone may take several months. Because of the dense architectural structure of cortical bone, new vessel incorporation follows preexisting haversian and Volkmann canals.30

Several differences exist between the cellular process of repair in cancellous and cortical grafts. With cancellous grafts, primitive mesenchymal cells that originate in the trabeculae may differentiate directly into osteoblasts, thereby resulting in relatively early new bone formation. The new bone forms on the dead trabeculae of the graft. This is followed by a resorptive phase. Cancellous bone initially undergoes an appositional new bone formation phase called creeping substitution, which is the process of new tissue invading along channels made by invasive blood vessels or along preexisting channels in the transplanted bone.31 The necrotic areas within the cancellous bone graft eventually are entirely resorbed by osteoblastic activity and totally replaced with new viable bone. As the revascularization of cancellous bone graft proceeds, primitive mesenchymal cells differentiate into osteogenic cells. These osteogenic cells form osteoblasts that line the edges of dead trabeculae and deposit a seam of osteoid that is annealed to, and eventually surrounds, a central core of dead bone. This process of alignment of osteoblasts on existing bone surfaces, with the synthesis of osteoid in successive layers to form lamellae, is termed appositional bone formation. Thus initially, there is an increase in the size of the graft. Cancellous grafts tend to repair completely with time. The areas of entrapped necrotic bone are resorbed by osteoclasts. In time the cancellous bone graft is completely replaced by viable new bone.

Cortical grafts must undergo osteoclastic resorption before osteoblastic new bone formation occurs. In cortical grafts the repair process is initiated by osteoclasts with preferential early resorption of the external cortical surface. Osteoblasts appear only after bone resorption has begun, and the initial deposition of osteoid usually occurs in resorbed areas. Cortical grafts remain as admixtures of necrotic and viable bone. In cortical grafts, revascularization is primarily the result of vascular infiltration through Volkmann and haversian canals.19 Osteoclasts initiate resorption of bone approximately 2 weeks after vascularization. Resorption is maximal at 6 weeks, and then gradually the graft recovers normal strength by 1 year. New bone is formed and seals off the remaining necrotic bone from further encroachment beginning at around 12 weeks. Thus if a biopsy specimen is obtained from a cortical graft years after placement, it demonstrates an admixture of necrotic and viable bone.

Biomechanics of Graft Incorporation

Porosity is a dominant factor in determining the material properties of bone. It is directly related to the stiffness of the tissue and yield of strength.13,14,32 Therefore, any change in porosity result in important effects on the bone graft material properties. Cortical bone grafts initially may have as little as 5% to 10% porosity, whereas cancellous grafts may be as high as 70% to 80%. This explains the material strength of cancellous graft, which is roughly equivalent to 4% of that of cortical bone.13

Cancellous grafts are incorporated by an early appositional phase. New bone formation onto the necrotic trabeculae of the graft tissue leads to an early increase in graft strength. It has been shown that necrotic bone maintains its mechanical strength.30 Cancellous grafts therefore initially strengthen with the addition of new bone. As the necrotic cores are resorbed, the mechanical strength of the graft area normalizes.

Cortical bone grafts first undergo osteoclastic bone resorption, which significantly increases graft porosity and thus decreases the graft strength. In the canine model of autogenous cortical transplant, the greatest compromise in mechanical strength occurs at 12 weeks30 (Fig. 17-1). The strength returns to normal between 1 and 2 years after transplantation. Human data suggest that cortical grafts lose approximately half their biomechanical strength during the first 6 months—a decline that persists for another 6 months.33 This process is related to osteoclastic graft resorption and is slowly reversed during the second year after implantation. These observations correlate with the highest incidence of mechanical graft failure between 6 and 8 months after transplantation. If the graft is allogenic, this process is further prolonged. Hence it is important to protect segmental grafts during the critical phase when the resorptive phase outstrips the appositional phase. This is usually accomplished by load sharing with spinal instrumentation or a spinal orthosis.

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FIGURE 17-1 Graph illustrating the quantitative temporal interrelationships between the physical integrity and the biologic processes of repair within a segmental autogenous cortical bone transplant. The initial persistence of strength (0–4 weeks after transplantation) indicates the subsequent loss was caused by reparative processes rather than any intrinsic weakness in the material. The sudden loss in strength at 6 weeks is caused by the increased internal porosity. From 6 to 12 weeks, the decrease in mechanical strength is reduced by 50%. The level of porosity continues to increase until week 12 because of the temporal lag in the apposition of new bone formation. At 24 weeks, there is no significant improvement in strength, despite the beginning reduction in the porosity of the transplant and maturation of the callus. At 48 weeks, however, the physical integrity of the transplant has returned toward normal, primarily as the result of decreased material porosity, since the amount of callus has not increased. By 2 years, the physical integrity of the transplant has returned toward normal, primarily as a result of decreased material porosity, since the amount of callus has not increased. By 2 years, the physical integrity of the transplant and the internal porosity of the remaining transplanted material are normal. The biologic completeness of repair (i.e., approximately 50% of the graft is viable) is not significant, because mechanical strength has been retained. The admixture of necrotic and viable bone remains for the life of the individual’s skeletal metabolic activity.

(From Burchardt H: Biology of cortical bone graft incorporation. In Friedlaender GE, Mankin HJ, Sell KW, editors: Osteochondral allografts: biology, banking, and clinical applications, Boston, 1983, Little, Brown, p 55.)

Temporal Profile of Graft Incorporation

During the first week after grafting, both cancellous and cortical grafts have similar histologic features. Both are surrounded by coagulated blood, and the graft is the focus of a tissue response characterized by vascular buds infiltrating the grafted bed. By the second week, fibrous granulation tissue becomes increasingly dominant in the graft bed, the number of inflammatory cells decrease, and osteoclastic activity increases. Within the confines of the graft, osteocytic autolysis proceeds, resulting from anoxia and injury by surgery, with necrosis delineated by vacant lacunae. Some cells, however, survive by diffusion of nutrients from surrounding host tissues. Creeping substitution of cortical bone grafts progresses transversely and parallel to the long axis of the transplanted segment. Thus the repair is found to be greater at the graft-host junctions.34

A study done in rabbits35 showed the sequence of events during the process of dorsolateral intertransverse fusion. Three phases were identified. Phase 1 represents the early reparative phase (1–3 weeks). It consists of hematoma formation and granulation tissue. There is minimal ossification. Phase 2 represents the middle reparative phase (4–5 weeks), when the fusion solidifies. Finally, phase 3 represents the late remodeling phase (6–10 weeks).35

Both membranous and enchondral ossification play a role in the fusion process. Membranous ossification is the predominant mechanism that begins at the termini of the fusion mass and emanates from the decorticated transverse process. The central portion of the fusion mass, where the vascular supply is poorer and movement is greater, heals by cartilage formation and enchondral ossification.