859

Dental Roland M.

Implants:

A Review

Meffert, * Burton Langer,f and Michael E. Fritz*

The present article is a review presenting an update on the field of dental implants since the World Workshop in Clinical Periodontics in July 1989. Areas that are discussed include following: 1. Biomaterials and the implant interface, and the interaction of these with the environment. 2. Periodontal considerations including data supporting a perimucosal seal of implant to soft tissue and discussion of the endosseous interface between the bone and the implant. 3. Newer techniques of diagnostic imaging and their determination of bone types are related to the future practice of dental implants. 4. Implant selection and the surgical techniques involved in implant placement. 5. Current ideas of implant prosthodontics, implant maintenance, and the treatment of implant failures. 6. Finally, the use of dental implants in the United States and Sweden. J Periodontol 1992; 63:859-870.

Key Words: Biocompatible materials; dental implants; osseointegration; radiography,

imaging techniques

This is a review article presenting an update on the field of dental implants since the World Workshop in Clinical Periodontics in July, 1989. Some "classic" articles published prior to the World Workshop are included to provide a complete overview. The paper is organized into the following sections: 1) biomaterials and the interface; 2) periodontal considerations; 3) diagnostic imaging techniques and pre-operative determination of bone type; 4) implant

Table 1.

Metals and

9) implants in private United States practice and do they differ from the Swedish experience? This review article will report strictly on endosseous implants, most notably root-form and plate-form (blade) implants.

Biomaterials for Dental

Implants'

alloys

Ti and Ti-Al-V Co-Cr-Mo Fe-Cr-Ni

Titanium and titanium aluminum vanadium Cobalt chromium molybdenum Iron chromium nickel

Ceramics and carbon

ALO,

Ca,o(P04)6(OH)2HA Ca3(P04)2 TCP

selection; 5) surgical techniques; 6) implant prosthodontics and esthetics; 7) implant maintenance; 8) implant failure;

and

Synthetic

C and C-Si

Aluminum oxide Calcium phosphate hydroxyapatite Calcium phosphate tricalcium phosphate Carbon and carbon silicon

Polymers PMMA PTFE PE PSF 6

Polymethylmethacrylate Polytetrafluoroethylene Polyethylene Polysulfone

Reproduced with permission.

BIOMATERIALS AND THE INTERFACE

Since the introduction by Professor Branemark of the term "osseointegration," there has been a great deal of confusion in the dental literature regarding this term and the nature of bone adaptation to an endosseous dental implant.1 Currently the terms most in use are osseointegration, which connotes a bone adaptation to the implant and is most utilized in connection with root form dental implants or fixtures, and "fibro-osseous integration"2 which describes the interposition of a peri-implant ligament between the bone and the implant resulting in a possible substantial load reduction in the bone. Plate-form (blade) implants fall into •Department of Periodontology, University of Texas Health Science Center, San Antonio, TX. Private Practice, New York, NY. •Emory University, School of Medicine, Atlanta, GA.

this latter category. Present guidelines of the Council of Dental Materials of the American Dental Association for acceptance for endosseous implants do not specify which bone adaptation is required or recommended.3 In our opinion, however, it is essential to understand the surface chemistry of the implant before a rational decision can be made as to the validity of either concept. As recently described in a review article by Lemons,4 there are three basic types of synthetic biomaterials for dental implants: metals and alloys, ceramics and carbon, and

polymers (Table 1). Biomaterials are usually classified according to their material properties, their actions in the tissues, or their primary area of surgical application. For example, regarding material properties, biomaterials are compared acœrding to elastic moduh

860 or

DENTAL IMPLANTS

tensile

strength,

and

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J Periodontol November 1992

A REVIEW

are

ranked

accordingly. Currently,

titanium or titanium-aluminum-vanadium alloys are the metallic materials of choice for endosseous implants. Commercially-pure titanium has a predictable interaction with the environment. It oxidizes upon contact with air or tissue fluids thus minimizing corrosion. It has a low density which gives it a high-strength-to-weight ratio and can be

successfully alloyed particularly with aluminum (6%) and (4%). Aluminum increases the strength and decreases the weight of the material and vanadium acts as an aluminum scavenger, presumably preventing corrosion. Some of the new implants utilize a titanium or titanium alloy substructure coated with a thin layer of either calcium phosphate ceramic, hydroxyapatite, or a plasma spray technique. Tricalcium phosphate or hydroxyapatite coatings are designed to produce a bio-active surface promoting bone growth and inducing a direct bond between the implant and the hard tissues.5'6 This phenomenon has been called biointegration. Commercially-pure titanium or titanium alloyed implant surfaces form and maintain an oxide layer without apparent break-down or corrosion under physiological conditions.7 9 It is this relatively thick titanium oxide layer that determines the implant-tissue interaction rather than the metal itself. vanadium

There are two distinctive interfaces described with titanium metal dental implants. First, the peri-mucosal interface where soft tissue meets the implant; and second, the endosseous interface where alveolar bone contacts the implant. In a recent article by Donley et al.,10 the reviewed literature suggests that a portion of the crevicular epithelial cells adjacent to a titanium implant can be expected to form a hemidesmosomal type of attachment to the implant surface similar to that of a natural tooth. The authors, in reviewing the literature, describe a number of theoretically possible relationships between the attached portion of the epithelium and the implant surface, notably the fact that the attached epithelium can extend along the abutment surface without approaching the abutment-fixture junction. Based on a comprehensive review of the literature, Meffert7 has also suggested that the junctional hemidesmosomal arrangement may not be predictable in a metallic system. Lekholm et al., however, have discussed the fact that the seal is mostly probably viable and adequate in function based on the fact that there were minimal histologie inflammatory reactions in the underlying connective tissues in cross-sectional and longitudinal human studies.11 Regarding the connective tissue attachment to the implant, it would appear that collagen fibers form a tight cuff around the implant abutment. Histology by Hobo et al. appears to indicate that approximately a 2 mm connective tissue band acted as a resistant barrier.12 There have been reports in the literature that the use of plasma spray promotes connective tissue adherence with fibers inserted functionally at 90° into the plasma sprayed surface of the

implants.13,14 Bone adaptation

to

titanium

or

titanium

alloy implants

has been reviewed in several articles.1'4'8'9,15 Successful bone adaptation to the implant surface appears to be very much related to the original premise of Eriksson, who described a lack of heat generation during drilling as the predominant predictor for osseointegration.16 Recent studies describing the placement of both round and flat unloaded implants in monkey mandibles under controlled drilling conditions showed that both achieved osseointegration.17 The use of hydroxyapatite or tricalcium phosphate-coated implants has also been described in the literature to demonstrate direct bone attachment to the hydroxyapatite surface as early as one month post-operatively, and according to the proponents of HA-coated implants, to demonstrate the most normal soft tissue anatomy in terms of lack of apical migration of the junctional epithelium and lack of inflammation.5-6'18 In a recent histological study conducted 10 months post-operatively on dogs, a layer of dense lamellar bone formed on the HA coating surrounding over 90% of implant surface, while the authors report that the uncoated implants show a much lower percentage of the surface closely adapting to bone.5 Similar results have been obtained by others utilizing a different hydroxyapatite-coated dental implant.19 Much more research, especially long-term studies, must be done in this area before anything definitive can be determined however. The original premise of osseointegrated systems, whether on a coated or non-coated implant, was described with the use of implants which were entirely endosseous and not per-gingival until the second or connecting stage. Newer data have come from Buser et al.20 indicating that a plasmasprayed titanium implant which is per-gingival in placement can exhibit anatomy similar to that of the original Branemark implant. In summary, the literature to date concurs that coated, non-coated, or plasma-sprayed implants all have the capacity to achieve osseointegration, if appropriate surgical techniques are involved. There may, in fact, be quantitative differences as to the amount of osseointegration with each particular type of surface and also the rapidity of osseointegration may vary with different materials.21

PERIODONTAL CONSIDERATIONS FOR ENDOSSEOUS IMPLANTOLOGY In the light of our knowledge of biomaterials and the implant interface, a prerequisite to a successful endosseous dental implant should be obtaining a perimucosal seal of the soft tissue to the implant surface. Failure to achieve or maintain this seal results in the apical migration of the epithelium into the bone/implant interface and possible complete encapsulation of the endosseous or root portion of the

implant system.

In natural dentition, the junctional epithelium provides a seal at the base of the sulcus against the penetration of chemical and bacterial substances. If the seal is disrupted and/or the fibers apical to the epithelium are lysed or destroyed, the epithelium migrates apically, forming a peri-

Volume 63 Number 11

odontal pocket after cleavage of the soft tissue from the radicular surface. Since there is no cementum or fiber insertion of the surface of an endosseous implant, the perimucosal seal may be extremely important. If it is lost, the "periodontal pocket" can extend to the osseous structures. The question of whether or not a perimucosal seal is possible with the endosseous dental implant was reviewed in the World Workshop7 and the conclusion was that it is achievable with many surfaces.10,22-27 If junctional epithelial attachment to the implant or abutment is not predictable, can it be modified? Using a series of laboratory animals, von Recum et al.26 used collagen and fibronectin to promote fibroblastic proliferation and attachment. His premise was based on the work of Kleinman et al.25 which demonstrated that collagen-bound fibronectin provided an excellent substratum for cell attachment in vitro. Von Recum and colleagues found that the collagen did not enhance attachment, but the fibronectin actually retarded healing when applied at the rate of 0.5 mm a day in humans and 2.0 mm a week in the animal model and will predictably end up at the osseous crest if not impeded. In a

14-day study, however, Lowenberg et al.27 reported good

results using a bovine collagen on titanium alloy (TigA^V) to enhance fibroblastic attachment and mitotic activity. Using the demineralized root slice as a control, the authors demonstrated a collagen-coated alloy demonstrated the same attachment as the root slice. No attachment was demonstrated on the uncoated alloy. Ongoing studies are exploring the possibility of coating the substrate with laminin since Seitz29 et al.30 described predictable adhesion of epithelial cells to bioglass when the surface was treated with laminin. Other possibilities may include the use of "barrier materials" and guided tissue regeneration (GTR) in which substances such as Teflon millipore filters or resorbable collagen materials are placed between the surgical flap and the implant interface to exclude apically proliferating epithelium and gingival connective tissue elements from the substrate surface. This, theoretically, would allow the wound to be populated by deeper undifferentiated cells. New concepts regarding GTR are discussed below under Surgical Techniques. In summary, if the seal breaks down and/or is not present, a "pocket" exists and the area is subject to periodontaltype disease. The proponents of the two theories of implant retention and stabilization (fibro-osseous vs. osseointegration) are entirely at odds regarding the behavior of bone during loading of tissue maintenance as related to function. According to Weiss30, key differences lie between function and hypofunction, or between submerging the endosseous portion of the implant for 3 to 6 months (as advocated by Branemark et al.1), or protecting it in a hypofunctional mode from the day of insertion until it is placed in full function 1 to 2 months after the initial surgery. Weiss2 agrees that an afunctional, submerged system will allow for direct bone apposition (osseointegration), but feels

MEFFERT, LANGER,

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861

submerging the implant will actually result in retarded healing and failure when it is placed in full function from that an

afunctional mode. Branemark et al.1 theorize that the

implant must be protected from function and envision a healing phase of 0 to 12 months. During this time new bone is formed close to the immobile, resting implant. A remodeling phase of 3 to 18 months ensues when the implant is exposed to masticatory forces. After 18 months, there is a balance between the forces acting on the implant and the remodeling capacities of the anchoring bone. In support of this premise, the work of Adell,31 in which bone loss of 1 to 1.5 mm occurs during the first year (as a result of the surgical trauma) and subsequent marginal bone loss after the first year of 0.05 to 0.1 mm annually is cited. Exactly, what does happen when an implant is placed in bone? Roberts15 and co-workers report that a bridging callus originates within a few mm from the implant site and a lattice of woven bone reaches the implant surface in approximately 6 weeks. It is their contention that this bridging callus requires complete stability and immobilization and has very little load-carrying capability. The lattice structure of woven bone becomes filled with well-organized lamellae and this does not achieve maximum load-carrying capability in the human in less than 18 weeks. A maximum compact/ composite bone interface is achieved in humans in approximately 1 year.

The work of Roberts et al.15 would seem to correlate very closely with the rationale of Branemark. Maximum load-carrying capability is achieved in 4 to 5 months; Branemark advocates immobilizing the system for 3 to 6 months before placing it in function. Conversely, the theory of Weiss,2,30 proposing the system be placed in full function in a 1- to 2-month time frame, long before load-carrying capability is reached, appears open to question. With the above in mind, what may cause the formation of a connective tissue interface? In the authors' opinion, a lack of osseointegration (other than overheating the bone during surgery) may be the result of any of the following situations: 1. The system is prematurely loaded (earlier than 3 to 6

months). 2. Apical migration of epithelium into the interface, followed by connective tissue elements. 3. The implant is placed with too much pressure. Linkow

and Wertman32 propose that the failure of the endosseous implant starts from within and not from the outside and that the system must lie passively in the implant site without any pressure. Weiss2,30 advocated making the implant site slightly smaller than the implant so it is placed with a frictional fit. 4. The implant does not exactly fit the site. The important aspect of load transfer from implant to bone is the absence of relative movement between implant and bone. What will happen if there is a connective tissue interface? If the implant is mobile, the connective tissue encapsulation continues to expand in width and mobility increases. If the

862

DENTAL IMPLANTS

-

A REVIEW

J Periodontol November 1992

is non-mobile and the width of the interface is to function. This is estrue if the implant design incorporates a mesh or

future implant research. From the results published, it would appear that the Branemark categorization has merit. Short implants placed in spongy bone have a tendency to fail more readily than longer implants in denser bone.

DIAGNOSTIC IMAGING TECHNIQUES AND PREOPERATIVE DETERMINATION OF BONE TYPE In their initial treatise on osseointegrated implants, Branemark et al.1 described various classifications of bone, based largely on intuitive reasoning. They speculated that implant failure or success could well be related to the type of bone present. Since the initial writings, there has been a remarkable upsurge in techniques of head and neck radiology, most notably the use of CT scanning in the pre-operative assessment of the maxillal and mandible for endosseous implant surgery.33-35 Using these techniques, it is now possible to determine on a highly predictable basis whether or not there is inadequate height and width of bone, the presence of undercuts, and the location of vital structures such as the mandibular nerve or maxillary sinus leading to correction of these conditions. Finally, CT can determine inappropriate implant sites where newer techniques must be utilized to increase bone width and density before implant placement can be considered. Recently Jeffcoat et al.35 noted that a CT scan, when used with appropriate new computer software provides the following features: 1. Ability to try different lengths and styles of implants and select the optimal implant for the situation. 2. Freedom to place the implant in 3-dimensional space. The software should allow the implant to rotate and tilt on any axis. 3. Display of the selected implant position from several different viewpoints, which shows the clinician that it is possible to place the selected implants in a parallel manner to facilitate the prosthetic reconstruction. 4. Aids for planning alveoloplasty. This feature will help to determine how much bone must be removed. An example is the reduction of a narrow ridge to sufficient ridge width to support the selected implant. Such software has now been produced, and with the use of CT scanning, should revolutionize dental implant placement in the next decade. Subtraction radiology, presently in a more experimental stage, is a potential diagnostic tool for patient monitoring.3639 Digital subtraction radiology may be one of the most sensitive, non-invasive methods for assessing several changes in peri-implant tissue and also for providing information on osseointegration. For a very comprehensive review of the theory and practice of subtraction radiology and the critical assessment of alveolar bone, the reader is directed to a recent paper by Hausmann.36 Since the initial discussion of pre-operatfve bone types in alveolar bone by Branemark and his colleagues,1 there have been reports describing the success or failure rate of integrated fixtures in various bone types.40,41 At this time, these data are certainly not complete and the subject will be an avenue of

IMPLANT SELECTION A paper by English presents an overview of currently available implant hardware.42 The author lists the following 10 categories of endosseous implants: ramus frame, pin implant, disk implant, single tooth plateform, mandibular

implant

minimal, the implant will continue

pecially design.

basket

plateform, maxillary plateform, cylindrical bullet, cylindrical basket, cylindrical screw, and cylindrical fin. Each

of these systems is available from a number of manufacturers. In spite of claims that an implant works better in this or that area, there are really no data to support these statements. A recent recommendation to the FDA by a dental panel indicates, in fact, that the only valid data at present are that screw-type implants can be utilized in the mandibular anterior segment with high success rates. Whether this recommendation will be accepted is not known at the time of this report. SURGICAL TECHNIQUES The surgical protocol described in osseointegration involved the placement of incisions in the buccal vestibule similar to that used in the Le Forte I osteotomy.1 The objective of this approach was to obtain maximum exposure of the surgical site with its adjacent anatomical structures, plus keeping the incision and sutures away from the site of the fixture, thus avoiding possible bacterial seepage into the site and premature fixture exposure. Untoward postoperative sequelae, such as exaggerated edema, ecchymosis, and difficulty in replacing a removable prosthesis, resulted in the search for a less traumatic approach. The overlapped flap was developed to minimize these complications, while adhering to the biological requirement of the Swedish investigators.43 The procedure was originally designed for the maxilla, where the bulk of tissue facilitated its use; however, it soon became a modality for the mandible. Preservation of keratinized tissue and vestibular depth was optimized. Limitations of the procedure were in areas of thin tissue hindering a split thickness approach. Other modifications soon followed which simplified the surgical procedure for both the clinician and the patient. The objectives of fixture health; i.e., maximizing the blood supply around the implant and adequate tissue coverage over the implant, were a priority. Entrance of a non-submerged, but unloaded, implant also added a new aspect to the surgical necessity of complete tissue coverage.44 Bone enhancement techniques such as the placement of membranes have modified the total tissue coverage requirement and in many cases added an additional surgical procedure. Lazzara showed the extraction of a tooth and the successful installation of a fixture using a membrane exposed to the oral environment.45 Removal was advocated 6 to 8 weeks followed by a normal maturation period of 4

Volume 63 Number 11

uncovering. The results were within the normal parameters of osseointegration. Becker et al.46,47 also showed successful osseointegration, but advocated leaving the membrane under the tissue for the full term of healing, thus avoiding a third surgery. Other investigators48-53 also reported the successful use of membranes to create bone growth on the buccal surface of a resorbed mandibular ridge and advocate a 2-stage procedure. Other bone regeneration procedures have been reported (unpublished data) using autogenous bone taken from intraoral sites or a remote source such as the iliac crest. Freezedried allografts have gained wide popularity and have been used with and without membranes. The results seem promising but are not time tested and will require close observation under normal loading situations. Sinus elevation procedures described outside the periodontal literature have recently been reported as a viable means to expand the receptor sites of implants. The techniques are variable, depending on the amount of bone required. In situations requiring small amounts of bone, the sinus membrane can be lifted in an attempt to allow the implant to engage the denser bone bordering the interior border of the sinus and, hopefully, allowing new bone to grow over the apical end of the implant. This does not always happen and it is surgically difficult to lift the membrane without puncturing it. If successful, the amount of new bone to be gained would be in the order of 1 to 2 mm. A second approach, and one used with a high degree of success for larger amounts of bone, is the external sinus infracture.54 56 Using this technique and implanting either autogenous or freeze-dried bone, the amount of new bone may be considerable.57 Combinations of bone and synthetics or synthetics alone have been used by many clinicians who claim success, but statistical evaluation is lacking. Both the quality of the bone and the long-lasting results of osseointegration are promising, but inconclusive and will require careful scrutiny. A third approach, which is a combination of the two previous procedures, involves an internal infracture of the interior wall of the sinus with the membrane attached to the bone. The bone-membrane combination may give additional osteoblastic induction for new bone formation rather than just elevating the sinus membrane. Again, long-term results are lacking and will require close observation.58 The importance of keratinized gingiva around coated implants was emphasized by Kirsch and Menteg.59 It was believed that keratinized tissue was more resistant to "periimplantitis" and thus progressive bone loss. Long-term results from the Branemark Clinic did not corroborate these findings, but reported that the lack of the attached tissue had little or no bearing on the success of the bone around the fixture.60 This discrepancy is discussed below in the Implant Maintenance section. It is generally accepted that patients will have an easier task of oral hygiene if they are brushing against keratinized tissue. Cosmetics will also be enhanced if the tissue surto 6 months before final

M EFFERT,

LANGER,

FRITZ

863

rounding the implant is keratinized. Consequently a variety of augmentation procedures such as the subepithelial connective tissue graft61 and synthetic augmentation materials62 are being utilized to enhance these deficiencies and to repair damaged anatomical topography. The uncovering procedure which was described as an excisional core of tissue removed from the top of the implant has also been modified to facilitate finding the buried implants and to preserve and move keratinized tissue into desired locations.63 These modifications were a natural progression of procedures taken from other periodontal therapies such as the apically repositioned, split thickness, and laterally repositioned flaps.

IMPLANT PROSTHODONTICS AND ESTHETICS The prosthetic phase of the original implant patients were well defined since a majority were full denture situations. This changed dramatically with the introduction of osseointegration into partially edentulous dentitions. Consideration of the difference between the movement of teeth with a periodontal ligament and implants with a direct contact to bone created a dilemma. Should implants be connected to teeth? Should they stand alone? Are attachments and stress breakers necessary to compensate for differences between the two entities? The situations became increasingly more complex as implants were used to supplement failing dentitions. The cases in which implants were being used in partially endentulous patients were rather well defined in a multicenter study.64 66 Most clinicians recommended keeping the implant bridges separate from the teeth, especially if the teeth were healthy, but there are no data to support this hypothesis. The situation is complicated further if there are an insufficient number of implants to supply a missing segment of the dentition, or if the abutment teeth are mobile. Kirsch and Ackermann popularized the use of the intramobile element to compensate for this disparity of movement.67 Kay has suggested the use of implants with an intramobile element as a stabilizing abutment in periodontal prostheses.68 Rangert et al. demonstrated that, even though it was believed that osseointegrated fixtures functioned with little or no perceptible movement, the attachment of the abutment to the implant and the gold cylinder to the abutment allowed a deflection that was similar to the intramobile element.69 Whether this movement was in harmony with the movement of teeth was not resolved. Unquestionably, the major hazard of joining implants to teeth was the possibility of overloading the implants ultimately leading to "disintegration." Changes in periodontal treatment planning described by Langer and Sullivan70,71 have also suggested that the combination of periodontal soft tissue management and prosthetic principles of occlusal reconstruction might have a beneficial effect on the success and preservation of osseointegration in "fixture assisted dental reconstruction" cases. According to the proponents of fibro-osseointegration, the movement described above can be

864

DENTAL IMPLANTS

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J Periodontol November 1992

A REVIEW

buffered by the fibrous membrane.2,30 It is clear that data comparing the two systems during loading are needed be-

fore the issue can be resolved. As the dental profession became somewhat disenchanted with acid etched bridges because of their short duration, the single tooth implant emerged as the likely successor. Jemt et al. demonstrated a high success rate in a multicenter study of single tooth implant replacements.72,73 The major obstacles cited were loosening of the set screws and cosmetic irregularities. The esthetic problem has been reduced surgically by the use of tissue augmentation procedures such as the subepithelial connective tissue graft61 and controlled tissue expansion62 and implantation of collagen and hydroxyapatite. Prosthetically, introduction of the UCLA abutment by Lewis et al.74 eliminated the metal collar at the gingival margin. However, problems with casting irregularities and a gold interface with titanium within the gingival sulcus bothered many clinicians. Development of the single tooth abutment has also camouflaged the metal collar and kept a pure titanium interface within the sulcus. Although the single crown is usually not retrievable, as in most osseointegrated prostheses, an abutment can be screwed into position using forces of up to 32 Ncm thus virtually ensuring its lasting position.73 Other single tooth replacements are retained with frictional fit or interlocks. Hybrid cases in which abutment teeth are retained to hold a transitional fixed bridge are becoming more popular. The teeth retain the profile of the alveolus and are often helpful in providing an esthetic restoration. A fixed provisional restoration is beneficial to the patient who wishes to replace the prosthesis immediately after fixture installation. Removable appliances are difficult to wear after surgery and transmit forces directly to the newly healing fixtures. Retained teeth which are periodontally sound also can be used to absorb eccentric forces in patients with severe parafunctional habit patterns and thereby protect implants. The negative aspect of saving teeth is that they limit the possible number and location of prospective implant sites. These "saveable" teeth are often located in areas with the greatest supply of available bone for implants. Prosthetically, they can complicate the impression and try-in stage of the restoration.75 Weaving implants and teeth together can create great difficulty in the final prosthetic design and often frustrates the most accomthe ability plished prosthodontist. Yet, in certain cases, to combine the two entities are essential.76 78 Developing the technology to add implants to existing restorations and the further refinement of esthetic needs will undoubtedly be major future prosthetic breakthroughs. IMPLANT MAINTENANCE If the dental implant is at risk from lack of predictable soft tissue attachment at the transgingival area and the oral hygiene is ineffective or less than optimum, how can it be maintained? "Candidates" for dental implant(s) usually have

history of less than ideal home care which has resulted in a partially or wholly edentulous state. After surgery, they may develop a fear of home care procedures used around the implant neck or may become over zealous in implementing the home care procedures. The result in either situation can increase the possibility of failure. Because implant superstructures are often very bulky and overcontoured with ledges, shelves, etc., traditional home care procedures are sometimes ineffective. The bacterial flora in adult Periodontitis and peri-implantitis seems to have great similarities.79,80 Increased levels of subgingival spirochetes have been associated with endosseous dental implants considered to be failing due to advancing pocket formation. Marked gingival inflammation and progressive bone loss occur in well-maintained and clinically stable implants, while spirochetes were rarely encountered in subgingival plaque. Failing dental implant sites were characterized by microbiota consisting primarily of Gram-negative anaerobic rods, chiefly Bacteroides and Fusobacterium spp. which were infrequently found in healthy sites. Becker et al. used clinical and DNA-probe analysis to evaluate 36 failing implant sites in 13 patients.81 They reported that failing implants had mobility, peri-implant radiolucencies, and probing depths greater than 6 mm in 58% of the sites. Moderate levels of A. actinomycetemcomitans, P. intermedia, and P. gingivalis were detected with the DNA probes, bacteria that are considered the primary organisms present in adult Periodontitis. Is there a difference in the bacterial morphotypes when implants are present in the partially edentulous mouth versus the fully edentulous implant mouth? Apse et al.82 found few differences in the microflora between implants and teeth in partially edentulous patients, but a marked decrease in the number of periodontal pathogens in implant crevices in the fully edentulous implant case.82 Quirynen and Listgarten studied 24 partially edentulous implant patients. When they compared the percentage of coccoid forms, motile rods, spirochetes, and other bacteria in implant pockets versus natural teeth crevices, the results were 65.8, 2.3, 2.1, and 29.8 and 55.6, 4.9, 3.6, 34.9 respectively.83 When comparing the morphotypes in the fully edentulous implant case, significant differences appeared. There were more coccoid cells (71.3%), fewer motile rods (0.4%) and no spirochetes a

(0.0%).

If the implant in a partially edentulous mouth is at more "risk" for peri-implantitis than that in the fully edentulous mouth, the rationale of Wennstrom and Lindhe may readily be explained.23,24 They speculated that keratinized tissue was not necessarily a prerequisite for gingival health and that movable mucosa around the trans-epithelial extension of an endosseous implant is not necessarily a vulnerable situation. They used the prospective and retrospective studies of Branemark with an over 90% success rate in terms of fixture survival and in which the marginal tissue was keratinized gingiva in only 67% and 51% of the facial and lingual surfaces respectively to support this premise. In a

Volume 63 Number 11

clinical report of 2,284 implants, Kirsch and reported a failure rate of 2.2% and attributed the main cause of failure to insufficient width of attached gingiva or insufficient mucogingival attachment. The difference in the two studies may be that the retrospective and prospective studies of Branemark were in fully edentulous cases and 1,746, or 76.4%, of the implants in Kirsch's study were in partially edentulous mouths. With no predictable epithelial attachment and less-than-optimum home care procedures, the soft tissue/implant interface is a very vulnerable area and at risk to gingival pathology. Keratinized tissue should be created with mucogingival surgical techniques prior to implant placement, if not present in adequate amounts. Possibly the worst time to gain attached gingiva via soft tissue grafting would be after the superstructure is inserted, because of lack of the adaptation or attachment of the soft tissue to the metallic abutment. If bacteria are significantly associated with ailing or failing dental implants, what hygiene techniques, instrumentation, and possibly antimicrobials should be used in the maintenance of the dental implant? Thomson-Neal et al. evaluated the effects of different prophylactic modalities on different implant surfaces, such as commercially pure titanium, titanium alloy and hydroxyapatite-coated titanium, and found that the titanium and hydroxyapatite-coated surfaces were scarred and pitted in a random fashion with metal or ultrasonic instruments, whereas antimicrobials and hand or motorized tooth brushes produced very little change in surface appearance from the original unused surfaces.85 They found rubber-cup polishing with a fine abrasive paste the safest modality when performed by a hygienist or dentist in the dental office. In a study of the effects of various oral hygiene instruments and materials on titanium abutments, Rapley et al. found that the inter-dental brush, plastic sealer, or rubber cup left a surface as smooth as the control, whereas the surface was severely roughened by ultrasonic instrumentation and metal sealers.85 Fox et al. scaled titanium abutments with titanium-tipped, stainless steel, and plastic curets; in summary, the plastic instruments produced an insignificant alteration of the titanium implant surface following instrumentation, while metal instruments significantly altered the surface.86 8 8 ^, the titanium-tipped curet produced a rougher surface than the stainless steel instrument. Is this surface roughening of any consequence? Commercial firms are marketing plastic instruments for facilitating home care procedures, but, in our opinion, these are difficult to use in terms of access and are designed obviously for supragingival use only. The plastic tip is soft, very flexible and is not suited to remove calculus to any degree. It is possible that some of the plastic will "rub off" on the abutment which would not be desirable. Plastic and Teflon-coated curets designed for subgingival access are now being proposed. Most recently, instruments coated with a layer of gold have been available. The premise is that the gold alloy is softer than titanium and will not scratch the

10-year

Ackermann62

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abutment surface in contra-distinction to the harder stainless steel and titanium nitride instruments. Plastic probes should be used at the gingival/implant interface, but in the authors' opinion, should only be used if there is pathology evident. Probing studies in dental implants are largely irrelevant unless the superstructure is removed, allowing probing parallel to the long axis of the fixture. Since the Thomson-Neal study84 showed a minimum alteration of the surface with the application of antimicrobials, an effective means of soft tissue maintenance around the dental implant might be the use of a topical mouthwash containing commercially available compounds such as phenolic agents,5 plant alkaloids,11 or Chlorhexidine gluconate.* Most dentists placing implants use the ADA-approved Chlorhexidine gluconate because of its demonstrated binding action to soft and hard tissues in the oral cavity. It has also demonstrated close to a 100% bacterial kill in a 0.12% concentration, up to 5 hours after a 30-second rinse.87 Optimum home care at the gingival/implant junction, may be accomplished by the use of an interdental brush, hand or motorized. It is advisable to use a hand brush with a plastic- or Teflon-coated shaft to minimize trauma and scratching. It is also effective to use an antimicrobial with either hand or motorized brushes for maximum contact of the agent with the implant and soft tissue surfaces. Patients may use the rinse as directed by the manufacturer. Since Chlorhexidine may cause staining in some individuals, patients with multiple composites or tooth-colored filling materials may prefer to use a cotton swab dipped in the antimicrobial and applied to the site. In our experience, it is advisable to dip the hand or motorized brush head in the solution with subsequent application to the implant head and neck. Some patients use a floss or shoe string dipped into the antimicrobial for care around the implant "neck." All of these procedures should be used daily and at the soft tissue/implant interface. Irrigation can be used if pathological changes are present. It has been our clinical experience that the daily use of topically-applied antimicrobials effectively negates the need for any instrumentation, since plaque will not form and the absence of plaque will mean the absence of calculus. IMPLANT FAILURES The ultimate goal of periodontal therapy is restoration and regeneration of a functional attachment apparatus, and the objective of the clinician using bone grafting materials is new attachment, bone, cementum, and periodontal ligament. Unfortunately, this does not always occur in natural dentition and, obviously, does not take place when repairing a dental implant. The objectives in restoring the ailing, failing dental implant to a state of health are to achieve a

'Listerine, Warner-Lambert Co., Morris Plains, NJ. "Viadent, Viadent, Inc., Fort Collins, CO. 'Peridex, Procter & Gamble Co., Cincinnati, OH.

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A REVIEW

sulcus of decreased depth and possibly promote some type of osseous regeneration. The failing implant may evidence bone loss, pocketing, bleeding upon probing, purulence, and indications that the bone loss patterns are progressing.85 The failed implant has mobility, a dull sound when percussed, and a peri-implant radiolucency radiographically.88 The ailing and failing implant may be treated; the failed implant must be removed, since it is nonfunctional and bone loss will continue. One of the first problems is treating the implant surface. The failing implant surface is contaminated with endotoxin and as long as endotoxin is present, there can be no biologic repair. As noted above, the subgingival flora associated with dental implants has been shown to be very similar to that associated with natural teeth.79"82 Chemotherapeutic agents such as Chlorhexidine gluconate, stannous fluoride, and tetracycline are all antimicrobials and/or antibiotics which theoretically would not only kill the periodontopathic bacteria but remove endotoxin from a root/implant surface. Zablotsky et al. evaluated chemotherapheutic agents' abilities to remove radioactive labeled lipopolysaccharide (LPS) endotoxin from hydroxyapatite-coated surfaces.89 They found that tetracycline did not have much effect in removing the LPS endotoxin when used in a concentration of 50 mgm/ cc (pH 2 or 3), but it did significantly alter the inner and outermost Ca/P ratios of the hydroxyapatite coating. Hydrogen peroxide did not remove LPS to any degree; and both Chlorhexidine gluconate and stannous fluoride seemed to bind, rather than remove, the LPS to the coated surface. The speculation is that both Chlorhexidine and hydroxyapatite are highly charged and there may be an interaction which would bind the LPS to the hydroxyapatite surface; the same may be true of stannous fluoride. Zablotsky et al. concluded that the treatment of choice for removing endotoxin from the hydroxyapatite-coated surface is citric acid (pH 1, 40% concentration), applied to the surface for 30 to 60 seconds. A longer application time of 2 to 3 minutes significantly altered the thickness of the HA and there seemed to be a weakening of the hydroxyapatite substrate. A modified plastic ultrasonic tip1 also removed endotoxin to a great degree; further research is indicated in this area, especially on titanium or titanium alloy surfaces. This study89 also demonstrated that, although tetracycline was contra-indicated and relatively ineffective in detoxification of a hydroxyapatite-coated substance, it was effective on a metallic surface. Lozada et al. used a high pressure sodium bicarbonate cleaning device** to achieve a clean, smooth surface, followed by detoxification with Chloramine and grafting with demineralized freeze-dried bone to treat an ailing threaded-type implant.90 Although there is the possibility that an air abrasive instrument could remove endotoxin, it might be contra-indicated in the surgical site due to possible

introduction of emboli. Chloramine did not remove LPS degree.89 Wittrig et al. found that tetracycline, citric and the modified plastic ultrasonic1 tip allowed for acid, fibroblastic coverage and growth than that seen on greater treated with strips hydrogen peroxide, stannous fluoride, Chlorhexidine and polymyxin B, gluconate.91 In this study, there was 68% surface coverage with tetracycline-treated hydroxyapatite strips and 55% surface area covered when treated with citric acid. Considering the slight difference in area covered after treatment with tetracycline and citric acid and the significant alteration of the Ca/P ratio with the antibiotic, it might be best to use citric acid, not only for detoxification but for attempted biologic repair. After the implant surface is decontaminated, one of the objectives would be regeneration or obliteration of the osseous defect with grafting material or GTR, or a combination of both. GTR has been used in recent years, not only to cover exposed threads or surfaces of an implant, an implant placed in a fresh extraction site, and premature exposure of an implant fixture, but in repair of the failing implant to protect the grafted material and to keep it in place. Non-resorbable membrane material composed of polytetrafluoroethylene (PTFE)tf is the most commonly used barrier material at this time. Zablotsky et al. created surgical dehiscences in dogs associated with hydroxyapatite-coated and commercially pure titanium implants, covered the experimental sites with PTFE, and noted marked coverage (up to 95% of the dehisced test implants in 4 weeks).92 More recently, resorbable materials have been used to treat implant defects. Demineralized freezedried lamellar cortical bone strips, freeze-dried dura mater, and cross-linked bovine collagen are examples of bio-resorbable materials used as barriers. In an 8-week study with dogs, Sevor et al. created dehiscences over hydroxyapatitecoated and grit-blasted titanium implants and covered the experimental sites with a resorbable collagen.93 They report a 78% bone coverage over the HA-coated systems (compared to 33% when no membrane was used) and a 52% coverage over the grit-blasted fixtures (compared to 26% without membrane).93 Unlike the non-resorbable PTFE, the cross-linked bovine flexor tendon collagen resorbs in approximately 6 to 7 weeks, stays hard for 4 weeks, and does not have to be removed. The protocol below is based on extensive clinical experience currently used by one of the authors (RM) to repair the failing implant: 1. If there is an active infection with purulence, bleeding etc., the tissue must be reflected and the defect degranulated with hand instrumentation. If the implant is coated, the hydroxyapatite is contaminated and must be removed until the metallic substrate is exposed. The surface is detoxified with tetracycline paste (250 mgm mixed with saline in a dappen dish) applied to the implant surface for 2 to 3 min-

'Cavitron, Dentsply Corp., York, PA. **Prophyjet, Dentsply Corp., York, PA.

"Perio-Barrier #4, Colla-Tec

to any

"GTAM",

W.L. Gore and

Associates, Flagstaff, AZ. Corp., Plainsboro, NJ.

Volume 63 Number 11 a cotton pledget or camel's hair brush. The tetis left on the surface and the defect grafted with either non-resorbable hydroxyapatite or freeze-dried bone. If the implant fixture is not hydroxyapatite-coated, the defect is degranulated, the tetracycline applied to detoxify and the site grafted as above. 2. If there is no active infection and the hydroxyapatitecoated surface looks relatively intact (non-œntaminated with no pitting, cracking, résorption or change in color), it is possible to detoxify the surface with citric acid, pH 1 (40%) for 30 to 60 seconds, applied with a camel's hair brush. The area is flushed and irrigated and grafted with either hydroxyapatite or freeze-dried bone. The citric acid detoxifies or freshens the surface, accomplishing a surface demineralization of the hydroxyapatite-coated surface. Citric acid is not indicated for use on the metallic substrate fixtures since its action is large demineralization along with detoxification; it has been used for this purpose for many years in periodontal therapeutic procedures. 3. The rationale of grafting with either hydroxyapatite or freeze-dried bone lies in the effectiveness of cleaning or detoxification. If the surface is clean and detoxified and all areas of the fixture have been visualized, it is possible to graft with demineralized freeze-dried bone to achieve a biologic healing. If the surface is not clean and detoxified due to vents, holes in the fixture, or tortuous osseous defects not amenable to instrumentation, it is advisable to graft with an alloplast such as hydroxyapatite to achieve a physical "fill" of the defect to minimize pocket depth. Biologic healing will not take place against a contaminated implant surface so a resorbable material, to be replaced by bone, may not be indicated in such a case. 4. The rationale of using GTR as a "barrier" lies in the need to keep the grafting material in place to prevent exfoliation of the allograft or alloplast. Since the stability of the implant lies in the bone-to-implant contact (osseointegration) at the non-involved portion of the fixture, a 10 to 12 week time frame is probably sufficient to allow maturation of the grafted material in the peri-implant defect. Complete regeneration of the lost osseous structures is probably not possible; the defect is repaired to maintain function and to enhance hygiene considerations and

utes

with

racycline

techniques. It is possible to treat and retain the ailing, failing implant, although a statistical analysis of treatment success is lacking

at this time. The cause of continued

destruction must be identified and rectified in the case of the failing implant to arrest the disease process. A mobile or failed implant must be removed since it is not functioning as designed. There is some controversy among investigators whether the bladetype can function with slight mobility patterns, but the cylindrical or screw-type fixture must be immobile the day of insertion, the day of exposure (if 2-stage), and at subsequent re-evaluation or maintenance checks. Studies are in progress to determine the efficacy of the various allografts and alloplasts; at this time both resorbable

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and non-resorbable hydroxyapatites are available and used clinically. New xenografts are gaining increased attention, and the possibility of using these materials in combination with each other is being studied. The failures of screw type commercially-pure titanium or titanium alloyed implants have been attributed by some to functional

overload, rather than the presence of bacterial

plaque. These failures also may be due to differences in the various types and configurations of implants, as well as the fit and design of the prostheses. Carefully controlled studies examining these parameters are needed in the literature. OSSEOINTEGRATION IN THE UNITED STATES PRIVATE PRACTICE When osseointegration was introduced into North America by P.I. Branemark and his co-workers, it was impossible to predict its impact on American dentistry. Now approximately 10 years later, it has become an integral part of

therapy.

Our reluctance in periodontics to use implants prior to 1983 came from the lack of scientific evidence and biologic parameters by which the value and safety could be judged. This, of course, has changed dramatically as witnessed by our current enthusiasm. Our goal was to emulate the Swedish results and possibly even improve on them. Was this a fair assumption? Let us go back to the situation in Gothenburg, Sweden and see how it compares with our environment in private practice. Is it similar? The Swedish implant teams were a network of surgeons and restorative dentists working in close proximity. Both were well trained in various phases of osseointegration and realized that they were breaking new ground. Most of the treatment regimens were subsidized by government funding and thus were not under financial pressures. Whether the teams treated 50 or 200 patients had little effect on their personal remuneration. As a result, careful therapeutic modalities and maintenance routines could be administered. Subsequent well-documented protocols and parameters of success could be substantiated. Ill-conceived treatment would invariably surface and ultimately be remedied. The situation in the United States in private practice is entirely different. Although, as in Sweden, one clinician installs the implants, while another restores them, they are rarely involved in a group environment. While this is not always a hindrance, there often is lack of continuity in the sequence of therapy. If conditions are optimum and bone quality and quantity is favorable, very few untoward complications will develop. However, if the conditions are less than ideal, the need for carefully executed surgical and prosthetic procedures may mean the difference between success and failure. One illustration is the patient with a complete maxillary denture or partial prosthesis who has received implants, and is ready for second stage treatment. Most people wish to wear their prosthesis, especially if they are not going to be

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DENTAL IMPLANTS

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by their restorative dentist that day. Therefore their removable appliance is either relined or relieved so that it fits over their implants; at a later date, the patient is scheduled for impressions to fabricate a metal framework. Yet, probably one of the most destructive phases of osseointegration is the period of time between the uncovering stage and the placement of the framework. The removable appliance causes severe lateral forces on each of the uncovered implants, which in cases of poor bone quality can destroy immature bone. In a closely-knit environment, as we find in the Swedish setting, this can easily be avoided by scheduling the patient with the restorative dentist immediately after the uncovering, thus avoiding this lag phase. Continuity and communication with the laboratory technician is also crucial; this was available in Sweden, but not always in the United States. Even if the practitioners communicated well enough to coordinate their schedules, many would find it impossible to get the necessary laboratory work completed in the desired time. One must reflect on the high failure rate reported when implants were placed in type 4 bone40,41 when compared to the Swedish statistics, which also warned about poor quality bone but did not cite their results.94 Could there be differences in the manner of treatment or case selection? Is it possible that if the cases with poor bone quality and insufficient height were treated with bone grafts rather than placing short (7 mm) implants, would they stand the forces of occlusion? This does not seem to be the case since even the small fixtures did not fail in the same proportions reported by the American clinicians. The size and number of fixtures in a given area is an area of future intensive seen

investigation.

investigators were working with a single in its purest form predominantly in fully edentulous mouths, whereas American private practitioners are using many systems and combining them in order to accommodate their restorative dentists. It is interesting to note that the results of Parel and Tjellstrom95 on osseointegration and facial prosthesis showed similar results in the United States and in Sweden with some minor variations. Again, the studies were done in different countries but in controlled environments rather than in private practice. The amalgamation of many types of implants and ideas in the United States in private practice have initiated many of the changes described in earlier sections of this paper; the treatment timetable has been accelerated and new dimensions of surgical expertise have been added. As stated above, the concept of immediate extraction and fixture placement has gained momentum in private practices. Cosmetic enhancement, as well as many of the prosthetic solutions for the edentulous and partially edentulous dentitions, have been developed by both the Swedish and American systems. Since protocol is not inviolate in practice, it is not illogical to think that many new applications and innovations will continue to emanate from both. It is, however, The Swedish

implant system

J Periodontol November 1992

A REVIEW

safe to say that the two experiences (Swedish and the United States private practice system) exhibit many differences.

Acknowledgment

This investigation was supported in part by NIH grant RR00165 from the National Center for Research Resources to the Yerkes Regional Primate Research Center and NIH grant DE08917. The Yerkes Center is fully accredited by the American Association of Laboratory Animal Care. Special thanks are due to Ms. Sharon B. Nichols for her typing of this manuscript and coordinating the submission of papers by the authors. REFERENCES 1. Branemark PI, Zarb GA, Albrektsson T. Tissue Integrated Prostheses. Chicago: Quintessence; 1985. 2. Weiss CM. A comparative analysis of fibro-osteal and osteal integration and other variables that affect long term bone maintenance around dental implants. / Oral Implant 1987; 13:169-214. 3. Stanford JW. Acceptance Program for Endosseous Implants: A service of ADA Membership. IntJ Oral Maxillofac Implant 1991; 6:1518. 4. Lemons, JE. Dental implant biomaterials. J Am Dent Assoc 1990; 121:716-719. 5. de Putter C, de Lange GL, de Groot . Perimucosal dental implants of dense hydroxylapatite: Fixation in alveolar bone. In: Proceedings of the International Congress on Tissue Integration in Oral and Maxillofacial Reconstruction, May 1985, Brussels. (Excerpta Medica, Current Practice Series #29) 389-394. 6. Denissen HW, Veldhuis AAH, van den Hooff A. Hydroxylapatite titanium implants. Proceedings of the International Congress on Tissue Integration in Oral and Maxillofacial Reconstruction, May 1985, Brussels. (Excerpta Medica, Current Practice Series #29) 399—tt)5. 7. Meffert R. The soft tissue interface in dental implantology. Implantologist 1986; 5:55-58. 8. Meffert R. Implant therapy. In: Proceedings of the World Workshop in Clinical Periodontics. Chicago: The American Academy of Periodontology; 1989: VIII-l-VIII-10. 9. Meffert RM, Block MS, Kent JN. What is osseointegration. Int J Periodontics Restorative Dent 1987; 7(4):9-21. 10. Donley TG, Gillette WB, Roudedush RL. Titanium endosseous implant soft tissue interface: A literature review. J Periodontol 1991; 62:155-160. 11. Lekholm U, Adell R, Lindhe J, et al. Marginal tissue reaction at osseointegrated titanium fixtures. II. A cross-sectional retrospective study. Int J Oral Maxillofac Surg 1986; 15:53-61. 12. Hobo S, Ichida E, Garcia LT. Osseointegration and Occlusa! Rehabilitation. Chicago: Quintessence: 1989: 33-54. 13. Schroeder A, van der Zypen E, Stich H, Sutter F. The reaction of bone connective tissue and epithelium to endosteal implants with titanium-sprayed surfaces. J Maxillofac Surg 1981; 9:15-25. 14. Buser D, Warrer K, Karring T. Formation of a periodontal ligament around titanium implants. J Periodontol 1990; 61:597-601. 15. Roberts WE, Turley PK, Brezniak N, Fielder, PJ. Bone physiology and metabolism. J Calif Dent Assoc 1987; 15:54-63. 16. Eriksson RA, Alberktsson T. The effect of heat on bone regeneration. J Oral Maxillofac Surg 1984; 42:701-711. 17. Koth DL, Lemons JE, Braswell LD, Fritz ME. Root and plate form tissue interfaces from dogs and primates. J Dent Res 1992 (Spec. -

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Volume 63 Number 11 Reconstruction. May 1985, Brussels, (Excerpta Medica, Current Practice Series #29) 278-287. 19. Kent JN, Block MS, Finger IM, Guerra L, Larsen H, Misiek DJ. Biointegrated hydroxylapatite-coated dental implants: 5-year clinical observations. J Am Dent Assoc 1990; 121:138-144. 20. Buser DA, Schroeder A, Sutter F, Lang NP. The new concept of hollow-cylinder and hollow-screw implants: Part 2. Clinical aspects, indications and early clinical results. Int J Oral Maxillofac Implant 1988; 3:173-181. 21. Albrektsson T, Sennerby L. State of the art in oral implants. J Clin Periodontol 1991; 18:474-48. 22. Schroeder A, Van der Zypen E, Stich H. The reactions of bone, connective tissue, and epithelium to endosteal implants with titaniumsprayed surfaces. / Oral Maxillofac Surg 1981; 39:15-25. 23. Wennstrom J. Keratinized and attached gingiva. Regenerative potential and significance for periodontal health [Thesis] University of Goteborg, Sweden; 1982. 24. Wennstrom J, Lindhe J. Plaque-induced gingival inflammation in the absence of attached gingiva in dogs. / Clin Periodontol 1983; 10:266276. 25. Jansen JA. Ultrastructural study of epithelial cell attachment to implant materials. / Dent Res 1985; 64:891-896. 26. Von Recum AF, Schreuders PD, Powers, DL. Basic healing phenomena around permanent percutaneous implants. In: Proceedings of the International Congress of Tissue Integration in Oral and Maxillofacial Reconstruction. May 1985, Brussels. (Excerpt Medica Current Clinical Practice Series #29) : 159-169. 27. Lowenberg BF, Aubin JE, DePorter DA, Sodek J, Melcher AH. Attachment, migration and orientation of human gingival fibroblasts to collagen-coated, surface-demineralized and non-demineralized dentin in vitro. J Dent Res 1985; 64:1106-1110. 28. Kleinman HK, Klebe RJ, Martin GR. Role of collagenous matrices in adhesion and growth of cells. / Cell Biol 1981; 88:473^185. 29. Seitz TL, Noonan KD, Hench LL, Noonan NE. Effect of fibronectin on the adhesion of an established cell line to a surface reactive material. J Biomed Mater Res 1982; 16:195-207. 30. Weiss CM. Tissue integration of dental endosseous implants. Description and comparative analysis of fibro-osseous and osseo-integration systems. J Oral Implant 1986; 12:169-214. 31. Adell R. Marginal tissue reactions at osseointegrated titanium fixtures. I. A three-year longitudinal prospective study. IntJ Oral Maxillofac Surg 1986; 15:39-52. 32. Linkow LI, Wertman E. Re-entry implants and their procedures. / Oral Implant 1986; 12:590-626. 33. Rothman SLG, Chaftez N, Rhodes ML, Schwartz MS. CT in the preoperative assessment of the mandible and maxilla for endosseous implant surgery (Work in Progress). Radiology 1988; 168:171-175. 34. James RA, Lozada JL, and Truitt HP. Computer tomography (CT) applications in implant Dentistry. J Oral Implant 1991; 17:10-15. 35. Jeffcoat M, Jeffcoat RL, Reddy MS, Berland L. Planning interactive implant treatment with 3-D computed tomography. J Am Dent Assoc

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36. Hausmann E. A contemporary perspective on techniques for the clinical assessment of alveolar bone. J. Periodontol 1990; 61:149-156. 37. Bragger U, Burgin W, Ing D, Lang NP, Buser D. Digital subtraction radiography for the assessment of changes in peri-implant bone density. IntJ Oral Maxillofac Implants 1991; 6:160-166. 38. Jeffcoat MK, Williams RC, Reddy MS, English R, Goldhaber P. Flurbiprofen treatment on Periodontitis: Effect on alveolar bone height and metabolism. J Periodont Res 1987; 22:396-402. 39. Jeffcoat MK, Page R, Reddy MS, et al. Use of digital radiography to demonstrate the potential of naproxen as an adjunct in the treatment of rapidly progressive Periodontitis. J Periodont Res 1990; 25(415-

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40. Jaffin RA, Berman CL. Predictability of implants in bone of differing quality. / Periodontol 1991; 62:2-4. 41. Engquist B, Beigendal T, Kallist T. A retrospective multicenter eval-

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Langer , Langer L. The overlapped flap:

A surgical modification fixture installation. Int J Periodontics Restorative Dent 1990; 10:209-215. 44. Buser D, Weber HP, Lang NP. Tissue integration of non-submerged implants: One year results of a prospective study with 100 hollowcylinder and hollow-screw implants. Clin Oral Implant Res 1990; 1:33^10. 45. Lazzara RJ. Immediate implant placement into extraction sites: Surgical and restorative advantages. Int J Periodontics Restorative Dent 1989; 9:333-343. 46. Becker W, Becker BE, Handlesman M, et al. Bone formation at dehisced dental implant sites treated with implant augmentation material: A pilot study in dogs. Int J Periodontics Restorative Dent 1990; 10:93-101. 47. Becker W, Becker BE. Guided tissue regeneration for implants placed into extraction sockets and for implant dehiscences: Surgical techniques and case reports. Int J Periodontics Restorative Dent 1990; 10:377-391. 48. Dahlin C, Sennerby L, Lekholm U, Linde A, Nyman S. Generation of new bone around titanium implants using a membrane technique: An experimental study in rabbits. Int J Oral Maxillofac Implant 1989; 4:19-25. 49. Nyman S, Lang NP, Buser D, Bragger U. Bone regeneration adjacent to titanium dental implants using guided tissue regeneration: A report of two cases. Int J Oral Maxillofac Implant 1990; 5:9-14. 50. Buser D, Bragger U, Lang NP, Nyman S. Regeneration and enlargement of jaw bone using guided tissue regeneration. Clin Oral Implant Res 1990; 1:22-32. 51. Kan S, Ruben MP, Bloom AA, Mardam-Bey W, Boffa M. Regeneration of periodontal ligament using resorbable and nonresorbable membranes: Clinical, histological, and histometric study in dogs. Int J Periodontics Restorative Dent 1991; 11:59-69. 52. Dahlin C, Lekholm U, Linde A. Membrane-induced bone augmentation at titanium implants. A report on ten fixtures followed from 1 to 3 years after loading. Int J Periodontics Restorative Dent 1991; 11:273-281. 53. Balshi T, Hernandez R, Cutler R, Hertzog C. Treatment of osseous defects using Vicryl mesh (Polyglactin 910) and the Branemark implant: A case report. Int J Oral Maxillofac Implant 1991; 6:87-91. 54. Boyne PJ, James RA. Grafting of the maxillary sinus floor with autogenous marrow and bone. J Oral Surg 1980; 38:613-616. 55. Wood RM, Moore DL. Grafting of the maxillary sinus with intraorally harvested autogenous bone prior to implant placement. Int J Oral Maxillofac Implant 1988; 3:209-211. 56. Tarum H. Maxillary and sinus implant reconstruction. Dent Clin North Am 1986; 30:207-229. 57. Zweig BE, Hebel M, Itkin AB. Maxillary sinus repositioning and grafting: An aid to implant placement. J NJ Dent Assoc 1991; 62:3032. 58. Smiler DG, Holmes RE. Sinus lift procedure using porous hydroxylapatite: A preliminary clinical report. / Oral Implant 1987; 13:239253. 59. Kirsch A, Menteg PJ. The IMZ endosseous two phase implant system: A complete oral rehabilitation treatment concept. Oral Implant 1986; 13:576-589. 60. Strub JR, Gaberthuel TW, Grander U. The role of attached gingiva in the health of peri-implant tissue in dogs: Part 1. Clinical findings. Int J Periodontics Restorative Dent 1991; 11:317-333. 61. Langer , Calagna L. The subepithelial connective tissue graft. J Prosthet Dent 1980; 44:363-367. 62. Bahat O, Handelsman M. Controlled tissue expansion in reconstructive periodontal surgery. Int J Periodontics Restorative Dent 1991; 11:33-47.

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iodontics Restorative Dent 1989; 9:85-105. van Steenberghe D, Lekholm U, Bolender C, et al. The applicability of osseointegrated oral implants in the rehabilitation of partial edentulism: A prospective multicenter study on 558 fixtures. Int J Oral Maxillofac Implant 1990; 5:272-281. 65. van Steenberghe D. A retrospective multicenter evaluation of the survival rate of osseointegrated fixtures and supported bridges in the treatment of partial edentulism. / Prosthet Dent 1989; 61:217-223. 66. Jemt T, Lekholm U, Ragnor A. Osseointegrated implants in the treatment of partially edentulous patients: A preliminary study of 876 consecutively placed fixtures. Int J Oral Maxillofac Implant 1989; 4:211-217. 67. Kirsch A, Ackermann KL. The IMZ osteointegrated implant system. Dent Clinic North Am 1989; 33:733-791. 68. Kay HB. Osseointegration Beyond tooth replacement: The intramobile cylinder (UMZ) as a stabilizing abutment in periodontal prosthesis. Int J Periodontics Restorative Dent 1989; 9:395^115. 69. Rangert , Jemt , Jorneus L. Forces and moments on Branemark implants. Int J Oral Maxillofac Implant 1989; 4:241-247. 70. Langer , Sullivan DY. Osseointegration: Its impact on the interrelationship of periodontics and restorative dentistry: Part II. Int J Periodontics Restorative Dent 1989; 9:165-183. 71. Langer , Sullivan DY. Osseointegration: Its impact on the interrelationship of periodontics and restorative dentistry. Part III. Periodontal prosthesis redefined. Int J Oral Periodontics Restorative Dent 1989; 9:241-261. 72. Jemt T, Lekholm U, Grondahl K. A 3-year follow-up study of early single implant restorations Ad Modum Branemark. Int J Periodontics Restorative Dent 1990; 10:341-349. 73. Jemt T, Laney W, Harris D, et al. Osseointegrated implants for single tooth replacement: A 1-year report from a multicenter prospective study. Int J Oral Maxillofac Implant 1991; 6:29-36. 74. Lewis S, Avera S, Engleman M, Beumer J. The restoration of improperly inclined osseointegrated implants. Int J Oral Maxillofac Implant 1989; 4:147-152. 75. Lothigius E, Smedberg JI, De Buck V, Nilner K. A new design for a hybrid prosthesis supported by osseointegrated implants: Part I technical aspects. Int J Oral Maxillofac Implant 1991; 6:80-86. 76. Chapman RJ, Kirsch A. Variations in occlusal forces with a resilient internal implant shock absorber. Int J Oral Maxillofac Implants 1990; 5:369-374. 77. Astrand P, Borg , Günne J, Morgan O. Combination of natural teeth and osseointegrated implants as prosthesis abutments: A 2-year longitudinal study. Int J Oral Maxillofac Implant 1991; 6:305-312. 78. Scher ELC. The use of osseointegrated implants in long-span fixed partial prosthesis: A case report. Int J Oral Maxillofac Implant 1991; 6:351-353. 79. Mombelli A, van Osten MAC, Schurch E, Lang NP. The microbiota associated with successful or failing osseointegrated titanium implants. Oral Microbiol Immunol 1987; 2:145-152. 80. Malmstrom HS, Fritz ME, Timmis DP, Van Dyke TE. Osseointegrated treatment of a patient with rapidly progressive Periodontitis: A case report. / Periodontol 1990; 61:300-304. 81. Becker W, Becker B, Newman M, Nyman S. Clinical and micro-

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biologic findings that may contribute to dental implant failure. Int J Oral Maxillofac Implant 1990; 5:31-38. Apse P, Ellen RP, Overall CM, Zarb GA. Microbiota and crevicular fluid collagenase activity in the osseointegrated dental implant sulcus: A comparison of sites in edentulous and partially edentulous patients. J Periodont Res

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1989; 24:96-105.

Quirynen M, Listgarten

MA. The distribution of bacterial

morpho-

types around natural teeth and titanium implants ad modum Brane-

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Send reprint requests to: Dr. Michael E. Fritz, Emory University School Medicine, 1462 Clifton Road, N.E., Room 300, Atlanta, GA 30322. Accepted for publication May 1, 1992.