albrektsson 1983 jpd

Direct bone anchorage of dental implants

Tomas Albrektsson, M.D., Ph.D.* University of Gijteborg and the Institute for Applied Biotechnology, Gateborg, Sweden

T he insertion of any given foreign material in a bone site is a multifaceted problem that involves the implant, the adjacent tissue, and the interface between implant and tissue. Implant parameters of concern include chemical composition, surface conditions, and mechanical factors such as yield strength, tensile strength, and elongation. The tissue’s reaction depends on its unique capacity to adapt itself to various external stimuli and its ongoing vitality. It is also essential that the tissue remain in the closest proximity to the implant. The interfacial behavior between implant and tissue is determined not only by the nature of the implant and the state of the iissue per se, but also by the technique of inserting and loading the implant. This review summarizes the biologic aspects of achieving integration of titanium implants in host bone tissue.

OSSEOINTEGRATION

There are few in vivo possibilities to analyze the subsequent bone integration once the implant is inserted. Some information is gained from the clinical evaluation, including radiographic examination, which if repeated at various stages of the osseointegration process, may indicate the condensation of bone along the implant exterior. While this is considered to be one sign of true bone anchorage,’ it does not provide information of cellular details and is therefore of limited value for the biologic assessment of osseointegration. Experimental studies with a titanium implant, the optical chamber, have provided information about the nature of bone anchorage on the tissue level. Such information is not obtainable in clinical evaluations. Another important source of information is a histologic and ultrastructural analysis of implants that had to be removed from patients in spite of an undisturbed anchorage functj on.

The long-term success of any implant system depends on the biocompatibility of the materials used

Presented at the Toronto Conference on Osseointegration in Clinical Dentistry, Toronm, Ont., Canada.

*Laboratory of Experimental Biology, Department of Anatomy.

THE JOURNAL OF PROSTHETIC DENTISTRY

and the condition of the tissue bed before and at the time of the installation. An initially healthy tissue may easily be transformed into a necrotic state if a surgical technique that does not ensure minimal tissue violence is used. Another risk lies in early loading of the implant. Brinemark et a1.2-4 showed that if all these factors are controlled, load-bearing osseointegrated dental implants are possible and a predictable long- term functioning of such implants can be achieved routinely.

THE OPTICAL CHAMBER FOR IN VIVO STUDIES OF IMPLANT INTEGRATION

Bone is a living, dynamic tissue with an abundant supply of blood vessels and undergoes constant remodeling. Under resting conditions about 11% of the cardiac output is distributed to the hard tissues of the body. 5,6 A method for the study of implant-tissue integration should encompass in situ investigations of bone remodeling as well as of vascular reactions. The only described method that allows for such investigations is the optical titanium chamber (Fig. 1). The chamber is a hollow screw where parts of the hard tissue that anchors the implant can be transilluminated through an optical system (Fig. 2). The chamber technique permits repeated studies of a defined bone tissue compartment with direct analyses of the osseointegration process. Immediately after insertion of the chamber, for example, in the rabbit tibia, there is rapid vascular activity and bone turnover induced in the border zone. The primary vessels are always observed in the chamber before bone ingrowth starts. These vessels first appear as capillary loops that gradually become more mature, and a well-developed vascular network is generally seen at about 3 weeks after implant insertion. The bone-healing response starts during the first week, peaks around 3 to 4 weeks, and arrives at a relative steady state with only minor bone remodeling 6 to 8 weeks after implant insertion. Follow-up studies of the same animal one or more years later reveal that although some condensation of the bone and some reorientation of the vessels had occurred, the general picture of bone and vascular

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Fig. 1. Optical bone chamber is a hollow implant of pure titanium. Two glass rods separated by a space 100 pm wide are glued inside chamber. After chamber insertion in an animal, long bone tissue will grow to anchor chamber and simultaneously penetrate through space between glass rods. This penetrating bone may be transilluminated in a vital microscope enabling in situ and in vivo investigations of bone and vessels. In schematic enlarged section representing microscopic picture, bone tissue is indicated by spider cells and vessels by arrows.

architecture remained largely unchanged from what was seen at 6 to 8 weeks (Fig. 3).

This series of events constitutes the osseointegration of an implant and may be regularly observed, provided that correct handling of the implant and the tissues is guaranteed. On the other hand, a surgically traumatic insertion technique elicits a different response. The initial vascularization of the implant border zone is poor, and bone invasion is inferior or even absent. There is a complete connective tissue anchorage with subsequent implant loss, or a partial bone tissue remodeling that never quite catches up with what is observed at the osseointegrated titanium implant site. The chamber may remain in the bone site, but 1 year after implant insertion there is still poor vascularization and dead, unperfused bone is observed (Fig. 4). These results clearly indicate the importance of an early establishment of blood flow and osteogenesis for

the reliable integration of an implant. Whatever the stimulus is for bone repair, it seems to be compromised if the initial healing is disturbed by traumatic surgery. Later recovery is then dubious, and the risk for connective tissue formation and premature loss of the implant is considerably increased.

HISTOLOGIC AND ULTRASTRUCTURAL ANALYSES OF THE IMPLANT-BONE INTERFACE

The studies of Branemark et al.2,3 on the interface zone of ground sections and histologic specimen of both canine and human clinical material showed that the bone was bordering the implant without an interposed connective tissue layer. This finding was in contrast to the general opinion at the time, which stated that an interface zone of connective tissue is unavoidable around metallic implants.’ In a lo-year follow-up of

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DIRECT BONE ANCHORAGE OF DENTAL IMPLANTS

clinical dental implants, the concept of osseointegration was defined as a direct contact between haversian bone and implant at the light microscopic level.4 Today we know that this direct bone-to-implant contact occurs even at the ultrastructural level. Albrektsson et al.* examined the interface zone between tissue and titanium of clinical dental implants, which at the time of removal had been fixed prosthesis loaded in vivo for up to 7% years. The implants were taken out for reasons not associated with the bone anchorage. Their bone integration had remained undisturbed, and there were no clinical signs of loosening. Scanning electron microscopy (SEM) showed a very close spatial relationship between titanium and bone. The pattern of anchorage of collagen filaments to titanium appeared to be similar to that of Sharpey’s fibers to bone. An intact bone- implant interface was analyzed by transmission electron microscopy (TEM), again revealing a direct bone-to-implant interface contact.

The same implants were also examined by Auger electron spectroscopy. It was found that the oxide layer of the titanium implants had grown from a thickness of about 50 A to about 2,000 A after fixed prosthesis loading for 6 years. The oxide had incorporated phosphorus, calcium, and sulfur while implanted, and this was interpreted by McQueen et a1.9 as an indication of interaction with the body tissues.

BIOCOMPATIBILITY

Bone tissue may react in different ways when an implant is inserted. If the implanted material is incom- patible, for example, copper, a thick connective tissue capsule is formed around the implant and rapid rejection will occur.“~ Less toxic materials such as certain types of stainless steels will be enveloped by a thinner connective tissue layer,6 which with time, however, may thicken, leading to loosening of the implant. More compatible materials may be anchored in the bone without an interposed connective tissue layer. In the case of Vitallium,” gold,12 and other types of stainless steels,‘” the type of bone in the border zone of the implant is of a disordered character. Mature haversian bone is found only at some distance from the metal surface. The long-term functional capacity of extracorporeal substitutes that become anchored in disordered bone is not quite clear. The absence of well-oriented bone does indicate, however, that the material is not fully accepted and that rejection may occur with time due to corrosive or other toxic effects of the materials used.

Ordered haversian bone in the interface all around the implant is a clear indication of tissue acceptance. There have been indications of such a direct bone

connection with alkali-poor ceramic implants6 and with implants of pure titanium.4~*~‘3 Various types of implant coatings, such as bioglass14 or tricalcium phosphate, I5 have been developed to create surfaces that are said to be well tolerated. However, no one has actually shown that bioglass or tricalcium phosphate are in any way clinically preferable to pure titanium. The unique biocompatibility of titanium may be explained on the basis of the tightly adherent oxide layer, built up of a combination of TiO, TiOz, Tiz03, and T&O,, which immediately forms on the metal’s surface. In experimental studies well-organized bone has been demon- strated around titanium implants at a resolution level of 30 to 40 A (Fig. 5).12 The interface situation created around titanium implants may resemble that seen around ceramic implants. The latter material also shows excellent biocompatibility, but it is brittle and may function less adequately if loaded in a complete fixed prosthesis over long periods of time.

The fact that titanium may be regarded as a most suitable material for implantation does not necessarily mean that titanium alloys, for example, Ti-6Al-4V, are equally well tolerated by bone tissue. The biocompatibility of an alloy may differ from that of the pure metal, although I am not aware of any comparative study between the interfacial behavior of titanium and titanium alloy.

A bone-anchored dental implant must penetrate mucogingival tissues. An in vitro study by Could et alI6 revealed the formation of hemidesmosomes on titanium surfaces. Histologic evidence from gingival tissues around functioning titanium dental implants removed after 7 years of load-bearing also indicates the presence of a hemidesmosome-like attachment between titanium and epithelial cells.* The formation of hemidesmosomes is a clear indication that the soft tissues of the oral cavity accept titanium oxide as being tissue compatible.

CONDITION OF THE TISSUE BED

The optimal bony or hard tissue bed is one free from infections and providing enough bone for implant incorporation. It is also as a rule possible to insert implants in extremely resorbed mandibles. In the maxillae, on the other hand, about 10% of an unsel- ected material of edentulous patients will have to be bone grafted before dental prostheses can be safely anchored. Brinemark et al.,’ Breine and Branemark,” and Lindstriim et al.‘* have used a two-stage procedure with so-called preformed grafts obtained from the iliac or tibia1 bone and reported favorable clinical results. In some patients implants were inserted and allowed to heal in situ at the donor site and after grafting were

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used as anchorage for dental fixed partial dentures at the host site. However, whenever possible, grafting should be avoided. In the upper jaw, penetration of the walls of the nasal and sinus cavities may occur in some patients. Brinemark et a1.19 presented clinical material indicating success figures for such penetrating implants as similar to those of other upper jaw implants, that is, around 80% success rates.

Some of Brinemark’s bone graft patients were irradiated following cancer surgery. Experimentally, little is known about the capacity for bone healing if implants are inserted in an irradiated bed. Jacobsson et al.” studied titanium implants in the rabbit tibia and showed that irradiation in therapeutic doses (single administration of 15 to 25 Gy) did not lead to implant loss over a follow-up period of 1 year. Another question is whether an implant may be integrated in a previously irradiated bed. The studies of Jacobsson et a1.2o have shown that an irradiation dose of 15 Gy* immediately prior to implantation leads to failure. This does not necessarily imply that implants cannot be successfully bone integrated some months after irradiation. The cells most susceptible to irradiation injury are the rapidly dividing active cells that, after bone surgery, will start developing in an osteogenic direction. Accord- ing to Brinemark,” even irradiation in diagnostic doses may prove harmful to the rapidly turning over cell population. Therefore, it cannot automatically be regarded as safe to perform conventional roentgen examinations immediately after implantation. Brine- mark recommends that radiographic examinations be avoided during ,the first months after implantation if the aim is to achieve and maintain a direct integration of the prosthesis in haversian bone.

SURGICAL TECHNIQUE

As a result of all surgical preparations of hard tissue, a necrotic border zone will develop due to the cutting of blood vessels, frictional heat development, and vibra- tion trauma. The smaller this necrotic zone, the more rapid and complete the repair that will follow, as was shown in the experimental bone chamber study described earlier. Bone and adjacent soft tissues are interconnected with respect to blood flow and are partly dependent on the same supply of undifferen- tiated cells for repair.22 Careful and gentle tissue handling is essential during the entire surgical preparation, not only when cutting bone.

It has recently been shown that bone tissue is much more sensitive to heat trauma than was previously

*l Gy = 100 rad.

258

believed. The critical temperature for hard tissue necrosis is not 56” C, as postulated by several authors,23,24 but rather 47” C. When the latter temperature was applied for 1 to 5 minutes in a rabbit tibia1 experimental model, bone and tissue necrosis occurred.25*26 These findings emphasize the importance of careful cooling during bone surgery and the need to avoid ultra-high-speed drilling. It is well known that the temperatures found at bone surgery even in the presence of a coolant may well exceed 60” C.27,2* However, external cooling from at least two sources and the avoidance of an uninterrupted through-the- bone preparation will considerably limit the thermal trauma. Internally cooled burs have also been intro- duced but with the problem of plugging of the irrigation canals with debris in some situations. Other suggested means of minimizing the surgical damage at bone preparation are summarized by Lindstriim et al.‘* and include views on a suitable instrument topography, on the cutting edge of the tool, and on the drilling techniques. At the most critical steps in the surgical procedure, as tapping the hole for the threaded implant, Brinemark uses an electrical machine that works with adequate torque at low rotatory speeds (15 to 30 rpm). At drilling, the use of a rotatory speed of only 15 to 30 rpm together, with adequate cooling produces no heat-caused injury. However, not only is the rotatory speed of the machine important, but also the, angular rate at the periphery of the bur, which is dependent on the diameter of the cutting tool. In summary, at dental implant insertion a strict surgical routine ensuring minimal tissue violence is imperative for long-term success.2-4* 29

LOADING OF THE IMPLANT

Dead bone, as found in the border zone around a newly inserted implant, is a poor anchor site for a prosthesis. This dead bone in favorable patients will be subjected. to remodeling and. will become replaced with new-built haversian bone. From the load point of view, the first months following implant installation are particularly critical. Overloading during this vulnera- ble phase may compromise the balance between osteogenesis and bone resorption, leading to connective tissue formation. The holding power of bone screws has been shown to weaken considerably if early loading and movements are allowed.30*3’ In a clinical situation at least 3 months of undisturbed healing should elapse before any implant is individually loaded. This period of unloading allows for the differentiation of primitive mesenchymal cells to bone-forming ones and for the

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DIRECT RONE ANCHORAGE OF DFNTAI. IMPLANTS

Fig.. 2. A, Low-power view of haversian canals (*) containing vessels and fat cells in living tibia1 bone of rabbit. B, Detail of A. Arrows are pointing at individual osteocyte lacunae. C, Detail of A. High-power view of a venula. D, High-power view of two osteocyte lacunae with living cells. Vacuoles are seen in lacunae, but other cellular details are not visible in unstained tissue. Arrows point at canaliculi.

Fig. 3. Typical bone growth pattern in a chamber inserted with a gentle surgical technique. A, At 4 weeks after chamber installation, two bone tongues are seen appsoaching each other. B, At 8 weeks bone tongues are in contact. Vessels are seen in typical canals in bone. C, At 52 weeks general picture is similar although not identical to one seen 44 weeks before. bone tissue, dotted; vessels, with arrows; and connective tissue proper, white.


ALBREKTSSON

Fig. 4. Typical events after chamber installation by means of traumatic surgery, in this case high-speed drilling. A, If bone invests chamber at all, there is usually only a minor amount of hard tissue. B, At 8 weeks picture does not significantly differ from what was seen at 4 weeks. C, One year after c@mber insertion there are few vessels and only a minor amount of bone.in chamber.

Fig. 5. Bone (B) to titanium (73) interface in a rabbit tibia implant that was loaded for 3 months. Hydroxy- apatite crystals are seen in direct contact with titanium. Resolution level of direct bone-to-titanium contact is 30 to 50 A, which excludes interposed soft tissue layers. (Magnification X100,000.)

initial callus formation and creeping substitution that are necessary to achieve primary stability of the implant in the bone site. ” The bone remodeling process responsible for the healing-in of the implant continues after the implant is connected to a dental fixed prosthe-

sis some 3 to 6 months after installation. Haversian bone, with capability of adapting to new load situations by remodeling, will finally anchor the implant in the jaw. The load-dependent gradual bone anchorage of a titanium implant follows the same laws that govern fracture healing.32* 33

After osseointegration of the implants, there are no specific restrictions on the loading. Patients with osseointegrated titanium fixtures have been shown to have similar maximal bite force and chewing capacity levels as patients with intact dentitions.34

Another advantage of avoiding early loading is the presence of an intact mucoperiosteum to cover the implant after its insertion. These mucoperiosteal layers act as a barrier toward downgrowth of granulation tissue during the phase of bone demineralization.

CONCLUSIONS

Generally speaking, a connective tissue anchorage of dental implants is an indication of failure.4 The achievement of a solid bone anchorage for a dental implant can lead to predictable long-term clinical results. This appears to depend on the control of the surgical trauma, the condition of tissue bed, implant loading conditions, and the biocompatibility of the material used. In this manner a meticulous clinical approach can ensure a lasting and successful bone integration of an extracorporeal substitute.

REFERENCES 1. Brinemark, P-I., and Strid, K-G.: Computerbased analysis oi

dental implant roentgenograms. (In press.) 2. Brinemark, P-I., Breine, U., Adell, R., Hansson, B-O.

Lindstriim, J., and Ohlsson, A.: Intraosseous anchorage 01

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Branemark, P-I., Adell, R., Albrektsson, T., Lekholm, U., Lindsttim, J., and Rockier, B.: Osseointegrated fixtures penetrating the bone towards the nasal cavity and the maxillary sinus. J PROSTHET DENT (To be submitted.) Jacobsson, M., Albrektsson, T., and Turesson, I.: Effect of irradiation on bone tissue. A vital microscopic study. Brinemark, P-I.: Unpublished data, 1979. Hulth, A.: Fracture healing. A concept of competing healing factors. Acta Orthop Stand 51:5, 1980. Rhinelander, F. W., Nelson, C. L., Stewart, R. D., and Stewart, C. L.: Experimental reaming of the proximal femur and acrylic cement implantation. Clin Orthop 141:74, 1979. Green, C. A., and Matthews, L. S.: The thermal effects of skeletal fixation pin replacement in human bone. 27th Annual ORS, Las Vegas, No. 103, 1981. Eriksson, A., Albrektsson, T., Grane, B., and McQueen, D.: Thermal injury to bone. A vital microscopic description of heat effects. Int J Oral Surg (In press.) Eriksson, A., and Albrektsson, T.: Temperature threshold levels for heat-induced bone tissue injury: A vital-microscopic study in the rabbit. J PROSTHET DENT 50:101, 1983. Tetsch, P.: Development of raised temperature after osteoto- mies. J Maxillofac Surg 2141, 1974. Lavelle, C., and Wedgwood, D.: Effect of internal irrigation on frictional heat generated from bone. J Oral Surg 38:499, 1980. Adell, R., Lekholm, U., Rockier, B., and Brinemark, P-I.: A 15-year study of osseointegrated implants in the treatment of the edentulous jaw. Int J Oral Surg. Uhthoff, H. K.: Mechanical factors influencing the holding power of screws in compact bone. J Bone Joint Surg [Br] 55~633, 1973. Schatzker, J, G., Horne, J. G., and Summer-Smith, G.: The effect of movement on the holding power of screws in bone. Clin Orthop 111:257, 1975. Albrektsson, T.: Healing of Bone Grafts. Thesis, University of Giiteborg, 1979. Albrektsson, T.: Frakturliikningsteorier. Astra-Syntex (In press.) Haraldson, T.: Functional Evaluation of Bridges on Osseointe- grated Implants in the Edentulous Jaw. Thesis, University of Giiteborg, 1979.

Reprinf requests to: DR. GEORGE A. ZARB UNIVERSITY OF TORONTO FACULTY OF DENTISTRY 124 EDWARD ST. TORONTO, ONT. M5G lG6 CANADA


albrektsson 1983 jpd

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