Dental implant design-Effect on bone remodeling R.M. Pilliar,* D. A. Deporter, P. A. Watson, and N.Valiquette MRC Dental Implant Program, University of Toronto, Faculty of Dentistry, Toronto, Ontario, Canada, M5G 1G6 Bone remodeling around three different endossesous dental implant designs placed in dog mandibles was studied using radiography during lengthy periods of function and by histology after animal sacrifice. The three designs investigated were (a) threaded (c.P. titanium), (b) fully porous-coated (titanium alloy), and (c) partially porous-coated (titanium alloy). The implants were kept in function for either 32 weeks (fully porous-coated) or 73 to 77 weeks (partially porous-

coated and threaded). The studies indicated that some crestal bone loss occurred for both the threaded and partially porous-coated implants while no significant bone loss was seen with fully porous-coated implants in the absence of plaque-associated infection. It is suggested that these observed differences are a result of the different stress states that develop in bone surrounding the three designs underlying the importance of implant design on bone remodeling.

INTRODUCTION

Resorption of crestal bone around endosseous dental implants appears to occur to a degree with all currently used implants. Nevertheless, most of these appear successful clinically, at least for the periods of patient followup that have been reported to date. The so-called "osseointegrated" implant developed by Branemark and his coworkers' has had the longest reported history of use in humans, and even with this highly successful implant system continuous loss of crestal bone is reported. Up to 1 mm or so of bone height adjacent to the implant is lost in the first year of function (as determined by radiographic examination of the mesial and distal aspects of the implants) with an approximate 0.1 mm per year loss subsequently.' For the reported periods of use (up to 15 years), these implants have performed adequately despite this loss of bone.3However, this cumulative bone loss remains a concern for the long-term success of dental implants in general. The success of endosseous implants currently in clinical use requires their reliable fixation in the jaw bone through rigid fixation or so-called "osseointegration." This implies a need for adequate healthy bone in direct contact with or in very close proximity to the surface of the implant. Extensive bone loss during implant *To whom correspondence should be addressed. Journal of Biomedical Materials Research, Vol. 25, 467-483 (1991) CCC 0021-9304/91/040467-17$4.00 0 1991 John Wiley & Sons, Inc.

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function could result in implant instability and failure. Bone loss superiorly with retention of bone and implant fixation at the apex only would also render the implant more susceptible to mechanical (fatigue) fracture because of the increased bending stresses that would act on the implant in this situation. A similar concern has been noted for orthopedic implants such as hip and knee joint replacements that might lose support proximally while remaining well fixed di~tally.~ The possible causes of crestal bone loss include (a) local tissue infection because of bacteria from the oral cavity migrating along the implant-tissue interface and (b) abnormal mechanical stresses acting on the crestal bone around the implant, either very low stresses resulting in bone loss due to disuse atrophy or very high stresses causing microfracture and subsequent resorption of the bone contacting the implant. In addition, the formation of fibrous tissue initially in the wound site as a natural healing phenomenon can occur. However, this should not of itself lead to continued and sustained bone loss months and years after implant placement as has been reported with endosseous dental implants. In this paper we report on two independent animal studies involving dogs in which the long-term changes in the alveolar bone around endosseous dental implants have been monitored using radiography. The results suggest that bone loss can occur next to the coronal aspect of dental implants because of abnormal stress states acting on the bone in this region. EXPERIMENTAL METHODS

Implant design

Three different implant designs were studied. Two of these were Ti6A14V implants with porous powder metal-made surface coatings over either the entire implant component surface (fully porous-coated or FPC implants) or over the apical two-thirds of the implant component only (partially porouscoated or PPC implants).We have described these implants in other reports.58 Briefly, the porous coating is formed by sintering Ti6A14V alloy powder (44 to 150 pm size range) to a machined implant core made from the same alloy. By vacuum sintering at 1250C for 2 h (vacuum = to mm Hg), a wellbonded porous coating (35 to 40 volume % porosity, 80 to 100 pm average pore size) results. The two porous-coated implant designs studied are shown in Figure 1. The FPC system not only had a porous coating over the entire length and base of the implant component (I in Fig. 1)but also on the apical one-third of the collar component (C in Fig. 1).As reported elsewhere: concerns related to problems of entrapment of bacteria, particularly in the porous coating on the collar component, and transfer of bacterial microrganisms to the tissues supporting the implant led to the use in our later animal studies of the PPC design. Both these designs were intended to become rigidly fixed in the mandible by bone growth into the porous surface coating. The two-stage implantation procedure used in these studies invariably

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7 2 m m

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Figure 1. Schematic drawings of the fully porous-coated (FCP) and partially porous-coated (PPC) endosseous dental implants. I, implanted component; C, collar component. Not shown are the collar retaining screws that are used for connecting the two components, the coping (that is attached to the collar and is made an integral part of the bridge), and the temporary cover screw (that is placed into the implant during the healing period).

resulted in bone ingrowth in a relatively short time period (by 4 weeks). Histological examination of tissue-implant sections for the FPC implants after animal sacrifice at about 32 weeks showed evidence of infection with varying degrees of crestal bone loss for 22 of the 32 implants placed in the 4 dogs (4 implants/dog) in that study. The tissues around the remaining 10 implants appeared infection-free and corresponded to no apparent loss of crestal bone around those implants. As reported previously, it was concluded that the loss of crestal bone around the 22 implants was in response to bacterial plaque that had become entrapped within the porous coating. It should be noted that the examples of infection-free tissues occurred for implants in all 4 dogs so that specific animals did not appear more resistant to plaque build-up and infection but instead, plaque accumulation appeared to be related to chance interaction of implants and oral bacteria either at the time of placement of the second stage (the transgingival component) or shortly after due to entrappment of bacteria in the oral cavity within exposed porous regions. In a second independent study7 PPC and threaded implants were placed in similar sites to those used with the FPC implants, (mandibular premolar in dogs). These were maintained in function for longer periods (73 to 77 weeks). For all three designs, implant performance was followed through regular clinical examinations and radiographic studies as described below. Following sacrifice, implant-tissue sections were prepared for histology. For the PPC and threaded implants, there was no suggestion of excess plaque buildup leading to tissue infection around the implants. In order to study the effect of factors other than those related to plaque build-up and consequent tissue in-

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fection on crestal bone loss around dental implants, the FPC implants that did not appear to be associated with tissue infection have been included in this report. We have assumed that the major difference between the FPC and PPC implants for this subgroup (no tissue infection) would be the nature of the implant-to-bone fixation at the coronal third of the implants. The PPC implant systems were similar in shape and dimensions to the FPC implants but the porous coating was restricted to the apical two-thirds of the implant component only. A 2-mm length of the superior region of the implant component (the coronal third) had a smooth surface (as-machined, surface roughness = 1.75 pm) and, therefore, bone ingrowth was only possible over the apical 4-mm length. While the FPC implants allowed bone ingrowth and good force transfer between the implant and surrounding bone, this was not possible with the PPC implants. It should be noted that similar procedures for site preparation and animal rehabilitation were used for these two designs. The third implant design studied was a screw-threaded system that was intended to mimic the threaded design used by Branemark and co-workers. It was made from c.p.titanium rather than Ti6A14V alloy in order to simulate the Branemark implant. The implant used in our dog studies is shown in Figure 2. The overall length of this implant was the same as the FPC and PPC implants as was the collar diameter. The major difference between the threaded and porous-coated designs, other than the obvious surface features, was the cylindrical shape of the threaded implant versus the tapered or truncated conical shape of the porous-coated implants. This conical shape was preferred for the porous-coated implants because it facilitated tight initial placement of the implant in the prepared site in the jaw bone (i.e., the compo-

- 1 mm Figure 2. Photograph of the partially porous-coated and threaded implants with collar components attached.

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nent is self-seating). The necessary condition for bone ingrowth, namely lack of or, at most, limited implant micromotion relative to the host bone4we felt would be more readily achieved with this tapered conical implant shape. The threaded implants in addition to being of a different design, were implanted using somewhat different site preparation methods (preparation of a tapped implantation site). All other treatment procedures were exactly the same as for the PPC implants.

Animal model and surgery For our animal studies, inbred adult beagles ranging in initial weight from 11 to 20 kg were used. All animals had their third and fourth mandibular premolar teeth removed at least 6 months prior to implant insertion. Following this healing period, the mandibles were prepared to receive 4 implants, 2 on either side of the mandible. The placement procedure has been described in detail el~ewhere~-~ but, in summary, it involved raising a region of the mucoperiosteum along an approximate 3 cm length using a lingually based fullthickness pedicle flap. Two pilot holes were drilled normal to the alveolar ridge surface on either side of the mandible with care being taken to properly align these holes relative to the crest of the bone and as nearly parallel to each other as possible. The holes were spaced about 1 cm apart. Finally, an implant-shaped burr was used to prepare the sites for the porous-coated implants while a threaded tap was used to prepare the threaded implant sites. Following site preparation, the porous-coated implants were placed snugly in position using a Tef lon-headed driver and the self-tapping threaded components were screwed into the slightly undersized, tapped holes. The mucoperiosteal flap was repositioned over the implanted components and sutured. The implant components were placed so that their superior aspects were just below the surface of the surrounding bone. In some cases this necessitated surgical reduction of knife-edged crestal ridges to provide a sufficiently wide, flat region of bone to accept the implant. The buried implant components were left in this nonfunctional mode for 4 to 8 weeks (as described below) after which a small incision was made through the mucosal tissue above the implant, the healing cap that had been placed on the implant component at implantation was removed, and the collar component was attached. The mucosal tissue was sutured tightly against the collar and a week later two custom-made prosthetic appliances bridging the two pairs of implants on either side of the mandible were added bringing the implants into function. The observations reported in this paper are based on radiographic examination of the dog mandibles at regular intervals during the period in which the implants were functional. The examinations were made with the aid of either a custom-made film holder that was fitted over adjacent teeth (first experiment) or attached directly to the collar component of the implant system (second experiment). This ensured reproducible positioning of radiographs from one time period to the next for comparison of radiographs for any one implant after different times in function. Care was also taken to keep exposure times, x-ray intensities, and film processing conditions constant.

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Two separate experiments, as indicated above, were conducted. The first experiment made use of the FPC implants only placed in 4 dogs. The implants on one side of the mandible were kept nonfunctional for 8 weeks while the contralateral pair of implants was made functional after just 4 weeks. Eight dogs were used with 32 implants. Because of the infection that occurred in association with 22 of these implant^,^ the study was terminated at 32 weeks of function rather than the intended 72 weeks. The second experiment used the PPC and threaded implants and these were placed in 6 dogs. Two PPC implants were placed on one side of the mandible in each dog while two threaded implants were placed in the contralateral sites. These implants were kept in function for 73 to 77 weeks at which time the animals were sacrificed and specimens for histological studies were prepared. The results of the histological analyses have been reported elsewhere.*Radiographs were taken at regular intervals as described below.

Radiographic assessment Radiographs were taken immediately after bridge placement, at 2-week intervals for up to 2 months and then at monthly intervals (approximately) for the FPC implants to the time of animal sacrifice at 32 weeks. The PPC and threaded implants were examined at the time of bridge placement, 2 and 6 weeks later, and then at 2 monthly intervals for the duration of the study (73 to 77 weeks in €unction).To allow comparison of bone density from one examination period to the next, film exposure and processing conditions were kept constant. A video camera was used to display the x-ray images onto a television monitor. The monitor was adjusted to give equal contrast of a specified “reference” area on the film from one time period to the next for any one implant site. The ”reference”area selected was a region of bone a small distance from the implant (see Fig, 3). It was assumed that this ”reference” re-

Standardization

Figure 3. Schematic illustration of radiograph of PPC implants in situ showing resorption of crestal bone adjacent to the implants and the area near the implant that was used for standardizing the density of the x-ray films on the television monitor.

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gion of bone would not have changed in density significantly from one examination period to the next. The television image gave the profile of the alveolar ridge next to the implant. The positions of apparent contact of crestal bone with the mesial and distal aspects of the implant were determined by making line tracings of the bone profiles and implants from the television screen. These tracings were superimposed for any one implant thereby providing a picture of the change in bone profile with time in function. Figure 4 shows a schematic illustration of a PPC implant with the bone profile traces observed at the different x-ray examination periods. For the three designs, the height of the bone from the base of the implant to the position of bone contact with the mesial and distal surfaces of the implant at each x-ray examination time was measured (B in Fig. 4). To compare the average response of bone remodelling for all the implants in the three design groups, the difference in bone height from its position at each x-ray period (B in Fig. 4) and its initial position at the time the implants became functional (A in Fig. 4) was normalized against this initial bone height. This normalization procedure accounted for the initial positioning of the implant, a factor we considered important in our analysis. The ratio of change in bone heighthnitial bone height (B-A)/A is referred to as the Bone Height Index (BHI) (see Fig. 4). The televised x-ray image was approximately X15 the actual implant size but for each radiographic image, an exact magnification factor was determined using the collar diameter as a reference. Therefore, absolute bone heights were determined. Mean values and standard deviations of BHI were determined for each time in function for the three designs. Line graphs indicating implant performance in terms of bone remodeling for each design were generated from this data.

BHI

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Figure 4. Schematic illustration of bone profile traces viewed at four time periods for the PPC implants.

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Histological assessment After animal sacrifice, histological sections of the implant-tissue interface region were prepared using techniques described elsewhere.’ A number of mesiaVdista1 and buccaVlingua1 sections were prepared and examined from all the implants. Of specific significance to this study was the relationship between the radiographically determined bone height and the measurements made directly from the mesial/distal histological sections for the PPC and threaded implants. Unfortunately, sufficient mesial/distal sections were not prepared from the FPC samples from our earlier study so that a correlation of the x-ray and histology measurements could only be made for the PPC and threaded implants. This was done using the final radiographs taken just prior to sacrifice and the histological sections. RESULTS

Fully porous-coated implants The tissue response to the FPC implants has been reported previo~sly.~ For the conditions used in the study, bone ingrowth into the surface porosity occurred within 4 weeks after implantation. Those FPC implant sites that did not show signs of infection (as assessed histologically) showed virtually no bone loss during the 32-week period of function (Fig. 5). One-way analysis of variance indicated that there was no significant difference in BHI with time in function for this design, although comparison of the mean values of BHI for the different times, suggested a trend to increased bone height with time.

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Time in Function (weeks) Figure 5. Bone height index (BHI) (mean and S.D.) versus time in function for the fully porous-coated implants.

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Partially porous-coated implants Histological examination of these implants showed good bone ingrowth into the porous-coated regions (Fig. 6). In the region adjacent to the machined coronal portion, a small amount of bone appeared closely adapted to some of the implants. For the most part, this region was surrounded by fibrous tissue. The radiographs reflected the histological findings. Figure 7 shows a plot of BHI versus time in function for the PPC design. One-way analysis of variance indicated that there was a significant change in BHI with time for this design, at least until 56 weeks (p < 0.05). Multiple comparison tests (Fisher PLSD) further showed that no significant differences in BHI occurred for the measurements taken at 56/64, and 74 weeks (p < 0.05) suggesting that by 56 weeks, the bone had remodeled to a new equilibrium profile. The horizontal line shown in Figure 7 at BHI = -0.278 + /-0.06 corresponds to the value of BHI for bone resorption to the level of the machined surface-to-porous coat junction. Figure 7 suggests that any bone loss that occurs in the first

Figure 6. Ground section of bone/PPC implant interface region stained with Stevenel's Blue and Van Gieson's picrofuchsin showing bone ingrowth.

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Time in Function (weeks) Figure 7. Bone height index (BHI) (mean and S. D.) versus time in function for the partially porous-coated implants. The horizontal line corresponds to the position of the smooth-to-porous coating junction.

year or so is limited to the smooth region of the implant. The greatest change in bone height occurred within the first 12 weeks or so of function.

Threaded implants The threaded implants were all "osseointegrated with bone having formed in close apposition to the threaded implant surface (Fig. 8). The BHI versus time in function plot is shown in Figure 9. Analysis of variance confirmed that a change in BHI had occurred with time for this design also. Multiple comparison analysis indicated that for this design, bone loss occurred for the first 20-week period or so of function but no significant changes in BHI occurred subsequently ( p < 0.05). Histological examination showed that the new equilibrium position for the threaded implant system corresponded to a point just apical to the first thread on the implant.

Radiographic versus histologic assessment For the threaded and PPC implants, measurements of the position of bone in contact with the distal and mesial aspects of the implant were made radiographically just prior to sacrifice and, subsequently, by direct examination of histological sections. The two sets of measurements for the PPC implants are presented in Figure 10 and indicate a reasonably good correlation between the two sets of measurements. The radiographic method gives a slightly greater value of bone height. The figure suggests that radiographic and histologic assessments are in better agreement for the PPC implants.

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Figure 8. Ground section of bonelthreaded implant interface region stained with Stevenel's Blue and Van Gieson's picrofuchsin.

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Time in Function (weeks) Figure 9. Bone height index (BHI) (mean and S. D.) versus time in function for the threaded implants.

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Figure 10. A comparison of measurements of bone height from the base of the implants to the position of contact of crestal bone and implant surfaces determined from the radiological and histological data.

DISCUSSION

A striking result from these studies was the observed difference in tissue response to the FPC (noninfected subgroup) and PPC implants. While no significant bone loss was observed around the coronal region of the FPC implants included in this study, some bone loss, albeit limited in extent and time over which it occurred, was observed with all the PPC implants. This observation was anticipated and was the basis for our initial choice of the fully porous-coated implant design for the long-term function experiments. We abandoned this design in favor of the PPC design only after problems with infection of some of the FPC implants became apparent? Previous studies using porous-coated implants for orthopedic applications had shown that bone ingrowth would allow effective transfer of mechanical forces between implants and juxtaposed bone." It was observed that bone was retained and even formed preferentially next to porous-coated regions of implants." The observation of a trend toward increased bone height with time for some of the FPC implants suggested such an effect of the porous coat on the coronal region of the FPC implant component and the apical third of the collar component. We believe that this effective transfer of stress to the crestal bone was responsible for the maintenance of bone in this region during the period of implant function.

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The bone remodeling observed with the PPC implants was quite different than with the FPC implants. With the PPC design we observed significant loss of bone for about the first 54 weeks of function. We believe that this bone loss is related to the lack of effective mechanical coupling between the machined (smooth) coronal region of the implant and surrounding bone. This would result in less effective transfer of tensile and shear stresses between implant and bone in this region for the PPC implants compared with FPC implants. As a result, abnormally low stresses would act on the bone next to the "smooth" region resulting in bone loss because of disuse atrophy. With continued bone loss, stresses in the remaining bone would increase until bone loss ceased and a new equilibrium structure formed. This apparently occurred by 54 weeks of function with the PPC implants, An explanation often invoked to explain crestal bone loss around dental implants related to biomechanical effects, involves very high stress concentrations leading to bone breakdown (microfracture) and resorption. A number of finite element studies of different dental implant designs have suggested that very high compressive stresses can develop just at the crestal boneimplant j u n ~ t i o n . ' ~However, -~~ other finite element studies have suggested the development of lower than normal stresses in the bone juxtaposing the implant in this region.16-19Our own finite element analysis using a twodimensional model has supported the development of lower stresses in the crestal bone region for PPC implants compared with FPC implants?' However, this analysis as well as those presented by others is limited by the assumptions made for the study. At least our preliminary finite element study was consistent with the hypothesis that lower than normal stresses caused bone loss around the PPC implants. The possibility that vertical and horizontal force components acting on the implants can result in high stress concentrations locally and that this can cause bone loss was considered. The different response observed with the FPC and PPC implants could be explained by the increased restraint due to bone ingrowth of the coronal region of the FPC implants providing greater resistance to both vertical and horizontal forces. As a result, somewhat lower compressive stresses would develop in the crestal bone around the FPC implants compared with the PPC implants and this could be significant in preventing bone overloading, microfracture and resorption. The results of our finite element studies have not supported this hypothesis, Threaded implants were also observed to lose bone during the first 20 weeks or so of function. Again, bone loss could have been due to very low stresses causing disuse atrophy or very high stresses resulting in mechanical fracture (microfracture) and resorption of bone. Assuming loss because of understressing, a similar argument to that presented for the PPC implants can be used to explain the establishment of a new equilibrium bone profile at 20 weeks or so. To explain this limited bone loss over 20 weeks because of overloading requires a more complex explanation since bone resorption at the most coronal thread site should lead to high stress concentrations at the next available bone-interfacing thread so that a progressive loss of bone would occur, all other factors remaining constant, until the implant loosened

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completely. This does not appear to happen. Examination of bone-implant histological sections corresponding to 74 week periods of function for the threaded implants showed that a more or less continuous shell of bone develops around these implants. Often this shell of bone forms under the base of the implant providing added support. Presumably this bone forms in response to the loads acting on the implants. Thus, the support provided through formation of bone against the implant would increase with time and the stresses within bone next to the most coronally positioned thread would be reduced thereby preventing continued bone loss through overstressing. It could be that the very different times noted to establish a new equilibrium bone profile (54 weeks for the PPC implants and 20 weeks for the threaded implants) is due to two different mechanisms causing crestal bone loss for the two designs, understressing causing disuse atrophy and limited bone loss for the partially porous-coated implants and initial overstressing resulting in mechanical breakdown and loss of some bone for the threaded implants. A number of reports have described the occurrence of crestal bone loss around dental implants in animals and h ~ m a n s ? Some ~ - ~ ~of the animal studies involved porous-coated implants. Of note was the study reported by Peterson et a1.2’ in which partially porous-coated CoCrMo implants were placed in dog mandibles for periods up to 2 years. A large percentage of the implants failed, probably because of the single-stage implantation technique used and the fact that rather large implants were placed in fresh extraction sites. Those that did not fail, however, showed a similar response to that noted in our study, namely, the resorption of bone just to the smooth-toporous coat junction. The implants used by Peterson were cylindrical in shape compared to our tapered implants. Human radiographic studies of patients with Branemark threaded implants have been reported by at least two independent gro~ps.2,~ There appears to be general agreement that in the first year of function, approximately 1.2 to 1.6 mm of bone is lost followed by a much slower rate of loss in subsequent years, namely 0.10 to 0.13 mm/year. This results in bone resorption in the first year to the region between the first and second thread position. This is similar to the observation made in our dog study. Other factors that might have caused the crestal bone loss in our studies include modification of local blood supply (because of the implant) or trauma resulting from the second-stage surgical procedure. However, these do not readily explain the observed differences between the FPC, on the one hand, and PPC and threaded implants on the other in which these other factors were virtually equal. Our studies have shown that both the threaded and porous-coated designs are prone to some crestal bone loss most probably because of the mechanical forces acting on the bone around the coronal region of the implants and the effect that these forces have on stresses within the bone and associated resorption or formation of bone. However, it should be noted that despite the observed bone loss, both the threaded and PPC designs appeared to perform satisfactorily as determined by clinical assessment for the Wmonth period of function used in this study.

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Although we can relate the loss of crestal bone to the altered stress state of bone in these regions, we cannot, at this time, describe this phenomenon in a quantitative manner. A number of studies dealing with bone remodeling around implants have been rep~rted'~-~' with some studies having attempted a quantitative description of the phenomenon. Bone loss might be due to factors other than mechanical, some of which have already been noted. Interference with blood supply,3' release of degradation products from the implant material triggering a resorption resp0nse,3~or, possibly, infection of the tissues during implant component placement as observed in association with some of the FPC implants in our earlier studies7are other possibilities. These cannot readily explain the differences observed between the three implant designs tested in our experiments.A significant differencein vasculature or extent of surgical trauma is not likely, especially for the FPC versus PPC implants. The summary of the radiology and histology bone height measurements presented in Figure 10, indicates that the threaded implants retained bone to a higher height against the implants than did the PPC implants. However, it appears that the final equilibrium position of the crestal bone is related for both designs to specific implant features, namely, the position of the superior threads for the threaded implants and the position of the smooth-to-porouscoat junction for the PPC implants. CONCLUSIONS

From these studies, it appears that modification of the loads transferred to crestal bone around endosseous dental implants as determined by the design of the implant can cause significant changes to bone structure. Through appropriate implant design, these changes can be limited so as to not compromise implant performance. For porous-coated dental implants, bone loss can be avoided by extending the porous coat coverage of the implant coronally but at the risk of increasing the probability of implant site infection, an unacceptable trade-off. These factors must be considered in the design of effective porous-coated endosseous dental implants. This study was funded by the Medical Research Council of Canada through a Program Grant. The authors would also like to acknowledge the technical assistance of K. Parisien and D. Abdulla.

References 1. P.-I. Branemark, B.-0. Hansson, R. Adell, U. Breine, J. Lindstrom, 0. Hallen, and A. Ohman, "Osseointegrated implants in the treatment of edentulous jaw. Experience from a 10-year period,"Scand. J. Plast. Reconstr. Surg. Sup& 16 (1977). 2. J.F. Cox and G.A. Zarb, "The longitudinal clinical efficacy of osseointegrated dental implants: A 3-year report," Int. 1. Oral Maxillofacial Implants, 2(2), 91-100 (1987). 3. R. Adell, U.Lekholm, B. Rockler, and P.4. Branemark, "A 15-year study of osseointegrated implants in the treatment of the edentulous jaw," Int. J. Oral Surg., 10, 387-416 (1981).

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6.

7.

8. 9. 10. 11. 12.

13.

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Received December, 1989 Accepted October 22, 1990