Osteointegration (Osseointegration)

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Chapter 19 Osteointegration (Osseointegration)

Daisuke Togawa, Thomas W. Bauer, Edward C. Benzel,

Recent advances in spine surgery have led to expanded use of synthetic biomaterials. The interface between host bone and a synthetic device has an important influence on the clinical efficacy of that device. These interfaces have been described as abutting (e.g., interbody bone graft, interbody cement), penetrating (e.g., nail, staple, screw), gripping (e.g., hook, wire), conforming (e.g., polymethylmethacrylate), and osteointegrating (e.g., some types of metal and ceramics).¹ The word osteointegration is derived from the Latin word integratus and the Greek osteon, meaning renewing or making new bone. However, because the prefix osseo- is also derived from the Latin for bone,² the term osseointegration is often (or preferably) used instead of osteointegration.

Since Brånemark, a Swedish dentist, introduced the term osseointegration to describe the process by which some oral implants interface with bone,³ this term has been widely used in the dental and orthopaedic arenas. Brånemark originally defined osseointegration as “direct structural and functional connection between ordered, living bone and the surface of a load carrying implant.”³ During the past 30 years, however, the term osseointegration has been used in a number of scientific publications regarding both structural (morphologic) and functional (physiologic) senses. Various factors influence this process at the implant-bone interface, including preparation of the surrounding bone, the surface preparation and sterilization procedures to remove organic residues from the implant, surface topography, overall implant design and composition, and load transmission.

Direct bone apposition to an implant suggests attachment of the implant to the bone over the entire contact surface, allowing load transfer from the implant to bone over a large surface area. Most surgeons expect direct bone apposition for interbody fusion devices, artificial discs, pedicle screws, and various spacers. However, it remains unclear how often, and to what extent, this is achieved.

Osteoconductivity

An osteoconductive material promotes bone apposition along its surface. The term osteoconduction is not absolute and is best understood in the context of a comparison in which variables of the substrate material, porosity, surface geometry, and surface chemistry are highly controlled and defined.⁴ For example, when matched by size, shape, and surface texture, hydroxyapatite is more osteoconductive than titanium, but titanium is more osteoconductive than a similar segment of cobalt-chromium alloy, or stainless steel; and rough stainless steel is more osteoconductive than polished stainless steel. Thus, several different factors influence the extent to which osteoblasts bind to a surface and produce bone matrix.

Biomaterials

Metals

Metals have been used in various forms as implants, including stainless steels, cobalt-based alloys, pure titanium, and titanium-based alloys. Each metal has different characteristics and behaves differently in vivo. For example, titanium alloys differ from stainless steel by having less resistance to abrasive wear, but provide better corrosion resistance, biocompatibility, less MRI distortion, and increased modulus of elasticity. Because of these advantages, titanium alloy is often used for orthopaedic and spine implants. As described by Wolff’s law, bone grows in response to applied stress and often is resorbed if a mechanical stimulus is lacking.⁵ Note, however, that the stiffness of many metals may shield the underlying bone from stress. Alloys with elastic moduli less than that of stainless steel, such as Ti6Al4V, have been successfully used in fracture fixation, but stress shielding is still observed.^6,⁷ At the implant-bone interface, most of these metals demonstrate variable osteoconductivity. Titanium implants generally have a better biocompatibility and osteoconductivity than many other metals, and their surface chemistry and texture are more influential during bone ingrowth.

Surface Texture

Early investigations were undertaken by Smith in the 1960s, using a porous surface ceramic.⁸ Currently, a wide variety of surface textures have been utilized to help achieve bone ingrowth into prosthetic devices in both dental and orthopaedic implant applications. Three dimensionally porous surfaces of sintered beads or wire, roughened surfaces created by etching the implant surface, and rough surfaces created by the application of metal by plasma spray or other methods have been tested in a number of animal and clinical studies⁹^–¹² (Figs. 19-1 and 19-2). For example, Friedman et al. tested various biomaterials with different surfaces in the rabbit femur and showed that the shear strength and bone apposition of implants with arc-deposited titanium coating and with one and three layers of cobalt-chromium beads were significantly greater than those of implants with plasma-sprayed cobalt-chromium texture and grid-blasted titanium alloy.¹³ Moreover, previous studies have suggested that the metal surface texture of a biomaterial can influence cell attachment and bone apposition. Martin et al. showed that surface texture affects cell attachment as well as cell morphology, proliferation, and differentiation.¹⁴ Thomas and Cook showed that roughened implants yielded more direct bone apposition in vivo than smooth implants of the same materials.¹⁵ Similarly, Turner et al. demonstrated greater bone apposition to titanium canine hip implants with an average texture of 45 μm than implants with texture of 8, 4, and 1 μm.¹⁶

FIGURE 19-1 A, Gross view. B, Direct bone apposition to metal hip implant. Direct bone apposition (BA) and healthy bone marrow (BM) are observed without an intervening layer of fibrous tissue on this experimental canine femoral titanium implant (Ti; surface: arc apatitic titanium).

(From Togawa D, Bauer TW, Mochida Y, et al: Bone apposition to three femoral stem surfaces in canine total hip arthroplasty. Transactions of the 27th Annual Meeting of the Society for Biomaterials, 251, 2001.)

FIGURE 19-2 A, Gross view. B, Direct bone apposition to hydroxyapatite (HA)-coated titanium implant. HA-coated titanium femoral stems (Ti) show extensive bone apposition (BA) compared with non–HA-coated stems (canine total hip arthroplasty model).

Excellent clinical results for joint arthroplasty have been reported with several surface treatments.^10,¹¹ However, the optimal surface texture for each implant remains controversial. A number of manufacturers continue to investigate new surfaces in an attempt to improve fixation and lower cost. Thus, a surface topography that incorporates such surface modifications can alter the tissue and/or cell interactions with bone and appears to affect biomechanical interactions as well.¹⁷

Other Materials

Various other biomaterials have been used at the bone-implant interface for spine surgery, including polymethylmethacrylate (PMMA), calcium phosphate cement, ceramics (hydroxyapatite, bioactive glasses), and polymers (polylactic acid [PLA], polyglycolic acid [PGA], hydrogels, carbon fiber-reinforced polymer, and polyetheretherketone [PEEK]). All foreign materials induce some response when implanted in a host; so strictly speaking, all materials are bioactive. This response is often inflammatory, but some materials induce relatively little inflammation and instead promote bone formation by osteogenic, osteoconductive, or osteoinductive processes. Although PMMA and carbon have excellent biocompatibility, both are less osteoconductive than calcium phosphates or some metals. PMMA has been used for years to help stabilize pathologic fractures, but its exothermic curing and poor osteoconductivity are disadvantages for some clinical applications. Carbon fiber-reinforced polymer and PEEK can yield wear debris,¹⁸^–²¹ but in the spine, carbon fiber-reinforced polymer has been used as an interbody stabilization device and has been associated with clinically successful outcomes without significant particle-induced osteolysis.^22,²³ Nevertheless, there is no evidence that these cages have direct bone apposition around them.

Hydroxyapatite (HA) is an osteoconductive calcium phosphate that can be prepared as granules, blocks, or a coating on implants.²⁴ When placed in a suitable host site, HA is osteoconductive and has some compressive strength, but in general blocks of sintered HA are difficult to machine. In addition, they are brittle and very slow to resorb. Injectable cements are composed of either calcium phosphates or bioglass derivatives. The calcium phosphate cements are highly osteoconductive, develop about 55 MPa compressive strength, cure isothermically, are very slow to resorb, and very weak in tension and shear. The bioglass cements are not as osteoconductive, but offer greater shear strength.²⁵ Bioabsorbable materials like PLA and PGA, are less osteoconductive in general, but since Kulkarni et al. introduced resorbable polymers for use in surgical implants, these materials have been used successfully in selected applications.²⁶^–³⁰ The use of resorbable polymers in spine surgery has only been advocated recently. The main theoretical advantage of a resorbable material is that it confers initial and intermediate stability without having any of such long-term complications as stress shielding or migration of the implant, but this requires degradation of the implant at a rate that coincides with new bone formation. The gradual degradation of bioabsorbable spinal implants can theoretically allow axial loads that were initially borne by the implant to be progressively transferred to the bone.³¹ Another advantage of such materials is that they do not interfere with radiographic studies. Resorbable polymers have been used as plates and interbody fusion devices,³²^–³⁴ but again there is little histologic evidence of direct bone apposition to the implant, and the rate of degradation has not always been coupled with new bone formation.

Surgical Applications

Osseointegration of spinal implants is desirable for many clinical applications, and a variety of biomaterials have been used in spine surgery to achieve that result.

Interbody Fusion

Interbody fusion devices are widely used for spinal arthrodesis and have demonstrated their clinical effectiveness for various degenerative disorders of the spine. Numerous types of spinal fusion cages have been developed from titanium and carbon fiber-reinforced or bioabsorbable polymer composites.³⁵^–³⁹ They also have been created in many shapes: horizontal cylinders; vertical rings; or mesh, rectangular, and open boxes. All can be packed with bone graft or graft materials to promote interbody fusion. Variations in cage design in the extent of the end plate, material stiffness, and other characteristics may be factors affecting success. Successful spinal fusion with interbody cage devices has been radiographically confirmed in a number of clinical studies.^22,^38,^40,⁴¹ The results of some animal studies have shown histologic evidence of bone graft incorporation and good connectivity between the bone inside the cages and adjacent vertebral bodies.^36,⁴²^–⁴⁴ The extent of direct bone apposition to clinically satisfactory cages is unknown, but clinically failed cages show no direct bone apposition, even when viable bone is present in the center of the cages^21,⁴⁵ (Figs. 19-3 and 19-4).

FIGURE 19-3 No direct bone apposition to metal cage. This clinically failed metal cage (A) contained viable bone (VB) extending through the openings along one side (B). The bone must have connected to bone outside the cage, but there is no direct bone apposition to the metal of the cage. Instead, fibrous tissue (FT) and fibrocartilage (FC) surround each strut of metal.

(From Togawa D, Bauer TW, Lieberman IH, et al: Lumbar intervertebral body fusion cages—histological evaluation of clinically failed cages retrieved from humans. J Bone Joint Surg [Am] 86:70–79, 2004.)

FIGURE 19-4 No direct bone apposition to carbon fiber-reinforced polymer. This clinically failed carbon fiber-reinforced polymer cage (A) retrieved from the cervical spine showed no direct bone apposition to the carbon fiber polymer (C) (B), even if most of the bone inside the cage was viable bone (VB). The viable bone extends through the lateral hole, but fibrous tissue (FT) separates bone from the cage.

(From Togawa D, Bauer TW: The histology of human retrieved body fusion cages: good bone graft incorporation and few particles. Transactions of the 47th Annual Meeting of the Orthopaedic Research Society, San Francisco, 950, 2001.)