CHAPTER 11 PERI-IMPLANT SOFT TISSUES
To be functionally useful, dental implants have to pierce the oral mucosa and enter the oral cavity, thus establishing a transmucosal connection between the external environment and the inner parts of the body. To avoid bacterial penetration that could jeopardize either initial healing or long-term behavior of implants, the early formation of a longstanding, effective barrier capable of biologically protecting the peri-implant structures is mandatory to prevent oral bacteria and their products from penetrating into the body.1–7
Establishment of this critical soft tissue barrier is the result of wound healing that establishes an effective interface between living tissues and a foreign body. The soft tissue barrier (also called biological width) has been evaluated in animals and found to have a dimension of about 3 mm in the apico-coronal direction. The interface consists of two zones, one of epithelium that covers about 2 mm of the surface and one devoted to connective tissue adhesion.
After installation of the transmucosal implant component, the healing of the connective tissue wound involves four distinct processes: (1) formation and (hopefully) adhesion of a fibrin clot to the implant surface, (2) adsorption of extracellular matrix proteins and subsequently of connective tissue cells to the implant surface, (3) transformation of the clot into granulation tissue, and (4) migration of epithelial cells on top of the fibrin clot/granulation tissue.8,9
Through its capacity to proliferate and to move on surfaces, the epithelium found at the border of the incision crosses over the bridge of the fibrin clot/granulation tissue that rapidly starts forming after implant/abutment installation. Upon reaching the surface of the implanted component, it moves in the corono-apical direction, giving rise to a junctional epithelium about 2 mm long.10,11 In the initial healing phases, the quality and stability of the fibrin clot adhesion to the surface of the transmucosal components probably play a role in the formation and positioning of the junctional epithelium.12
The presence of granulation tissue adhering to the surface of transmucosal implant components is considered the principal factor that stops the epithelium from moving further apically.13 The role of the connective tissue in preventing epithelium downgrowth has been clearly demonstrated in animal models.14,15 Berglundh et al.16 also speculated that the epithelium stops migrating in an apical direction because of the interaction between the soft tissue and the layer of titanium oxide. It seems that mature connective tissue interferes more effectively than granulation tissue with epithelial downgrowth.17
Once the epithelial cells have reached the implant surface, their attachment occurs directly via a basal lamina (<200 nm) and the formation of hemidesmosomes.18–24 Hemidesmosomes may already be formed at 2-3 three days of healing.25
It is generally recognized that the epithelium lining the peri-implant sulcus is similar to the junctional epithelium adjacent to teeth: it shares many structural, ultrastructural, and functional characteristics with the corresponding gingival tissue. Studies conducted in humans26–27 indicate that the epithelium surrounding dental implants possesses patterns of differentiation and function similar to gingival epithelium.
In contrast, connective tissue attachment to implant components is different from the attachments observed for teeth. In periodontal tissues, cementum lines the root until enamel is reached, thus offering a substrate in which bundles of collagen fibers can deeply insert.28 These bundles reinforce the gingiva and provide the high cohesive strength to the dentogingival attachment that is necessary for maintaining its architecture and integrity at repeated trauma due to mastication.
With endosteal dental implants, due to the absence of cementum and to the solid nature of transmucosal implant components, there is no true anchorage of supra-alveolar connective tissue, but only a brittle adhesion.29–32 As a consequence, the connective tissue adhesion at implant has a poor mechanical resistance compared to that of natural teeth. In other words, the gingiva at implants can hardly be qualified as attached.
Because the connective tissue interface is considered of paramount importance in supporting the epithelium and blocking its apical migration, this lack of mechanical resistance can endanger the prognosis of dental implants. Tearing at the connective tissue/implant interface could occur as a consequence of mastication or a lack of soft tissue stability, which could then induce an apical migration of the junctional epithelium, bone resorption, and pocket formation or gingival recessions.33
Despite comparable histological dimensions of the soft tissue compartments (junctional epithelium and connective tissue interface) at teeth and implants, it has been shown that when a probe pressure of 0.5 N is used in dogs, the probe tip penetrates on average 0.7 mm deeper at implant sites.34 The histological sections with probes in situ evidenced that around implants, the tip of the probe ended apically to the junctional epithelium, close to the bone crest, explaining why the clinical probing depth is higher. This is in accordance with the results of Gray et al.35 in baboons.
In humans, it was confirmed that 0.5-1.4 mm deeper measurements are generally found at implants.36–38 These results are the consequence of the brittle adhesion of connective tissue at implant components, illustrating that at implants the probe tip ends somewhere in the connective tissue and that the significance of probing at implants and at teeth is different.
Several studies have examined changes in soft tissue levels after implant placement.36–40 Despite significant differences in experimental designs, a vast majority of studies conclude that a gingival recession grossly varying from 0.6-1.5 mm is unavoidable.
No significant difference could be determined between the 2-stage and the 1-stage surgical approaches41nor between one- or two-piece implants.42,43 One clinical study44 reported 1.3-mm recession from 1 month to 1 year, then an additional loss of 0.4 from 1-3 years. Another45 found 1.6 mm of mean recession at the mandible versus 0.9 mm at the maxilla. In contrast, some authors found much lower levels of recession.46–49 It is important to note that these studies started measuring the soft tissue recession only 1 month,50,51 6 weeks,52 or even 3-5 months53 after mucosal piercing. This is most probably of major impact, since the clinical study of Small and Tarnow54 demonstrated that 50% of the recession is obtained after only 1 month and 90% after 3 months, with a stable level reached at 9 months. This was later confirmed in another clinical study by Kan et al.55
The reaction of cells and tissues to implanted foreign bodies depends on the material’s properties and its behavior on contact with the body fluids. It is mandatory to place at the transmucosal level a biocompatible material to which tissues can adhere.
It must be noted that the chemical composition of the bulk material is sometimes significantly different from that of the surface that is at the interface with the living tissues: some materials demonstrate a surface oxidation (such as titanium, which exhibits a surface layer of titanium oxide), whereas the mode of preparation or of sterilization of others will result in chemical contamination of the surface.
Commercially pure titanium is the only material that has proven his biocompatibility toward the soft tissues in long-term clinical studies. Some favorable clinical data have become available for zirconium and aluminum oxide. In contrast, animal studies have shown that dental porcelain or gold is less biocompatible and should be avoided. Materials such as resins and composites cannot be recommended.
The ultimate goal of cleaning procedures should be to remove the contaminants and restore the elemental composition of the surface oxide without changing the surface topography, either after the fabrication process, after handling in the dental laboratory, or when transgingival components are reused.
Although specific protocols have been developed, it proves to be rather difficult to effectively clean a contaminated titanium surface, most probably because of the strong binding of proteins and amino acids.56,57 This could negatively alter the biocompatibility.
Vezeau et al.58 and Keller et al.59 evaluated the surface changes and effects of common sterilization methods. Results indicated that steam autoclave sterilization contaminated and altered the titanium surface, resulting in decreased levels of cell attachment and spreading in vitro. Several studies60,61 have also shown that saliva has deleterious and almost irreversible effects on cell adhesion in vivo.
It should be noted that it is most unlikely to alter the composition of the transmucosal part of one-piece implants, which will therefore always be biocompatible with currently commercially available one-piece systems.
In a one-piece implant the transmucosal component facing the soft tissues makes part of the implant. In a two-piece implant the transmucosal component dedicated at soft tissue integration is a separate part from the implant body. The interface between the transmucosal component and the implant is generally located in the neighborhood of the alveolar bone level.
Comparative studies were performed in dogs to determine the influence of implant design on soft tissue integration. Abrahamsson et al.62 demonstrated that the dimensions of the junctional epithelium and of the connective tissue are similar on one-piece implants and on two-piece implants. In addition, their position relative to the bone crest was also comparable, with the soft tissue integration located on the smooth implant’s neck on one-piece implants and at the abutment level on two-piece implants. Using the same experimental conditions, but after 6 months of undisturbed plaque accumulation, it was shown63 that the extent of the plaque-related inflammatory infiltrate was comparable around one- and two-piece implants.
Using experimental implants with either a one-piece or a two-piece design, Hermann et al.64 showed significantly higher apical migration of the soft tissues and marginal bone resorption with two-piece implants, suggesting a role for the subgingival position of the abutment/implant interface (so-called microgap) on tissue remodeling. It must be noted that all two-piece implants in this experiment were clinically and histologically surrounded by an intense inflammatory process. This is in strong opposition with several animal studies65–76 in which a soft tissue integration occurred at the abutment level.
In another experiment by the same group, it was demonstrated that the size of the microgap between implants and abutments has little influence on marginal bone remodeling, whereas micromovements of the abutments induce a significant bone loss, independent of the microgap’s size. This strongly suggests that the mechanical disruption of the soft tissue interface is of importance.
An inflammatory cell infiltrate has been demonstrated at two-piece implants, in the close vicinity of the abutment/implant interface.77 This infiltrate does not impair the formation of effective soft tissue integration and seems to be present at implant systems with an external implant/abutment connection as well as at systems with an internal morse taper connection, but not at one-piece implants.77
In some experiments using commercially available implants, the infiltrate proved to be very limited in size (<0.5 mm) and was not linked to a higher bone loss as compared to one-piece implants, whereas Broggini et al.78 linked the 0.5-mm inflammatory infiltrate seen in their samples with experimental implants to a higher bone loss than at one-piece implants.
It has been shown that the seal provided by a locking taper connection at the implant/abutment interface effectively impairs bacterial leakage. But it has not been clearly shown that the bacterial contamination of the internal components of some two-piece implant systems79 is responsible for the inflammatory cell infiltrate seen at the abutment/implant interface.
An intentional or unintentional disconnection of abutments is possible at two-piece implants. Based on results by Hermann et al., an unintentional abutment loosening will lead to a disruption of the soft tissue integration and to increased bone remodeling.64
It also has been shown that repeated intentional abutment disconnection and reconnection after alcoholic disinfection induce an apical repositioning of the soft tissues and marginal bone resorption80; a single shift of a healing abutment and replacement by a final abutment proved to induce no marginal bone remodeling.81
Several studies have examined changes in soft tissue levels after implant placement.82,83 Despite significant differences in experimental designs, a vast majority of studies conclude that a gingival recession grossly varying from 0.6-1.5 mm is unavoidable. All these studies used transmucosal components with divergent designs.
In contrast, favorable results have been described with slightly concave abutments. By using abutments that have a diameter narrower than their two-piece implants, Cooper et al. showed a mean vertical gain of 0.34 mm of soft tissue.
More recently, Rompen et al. showed that with concave, gingivally converging abutment components the frequency and magnitude of recessions can be dramatically reduced. In contrast with existing data from the literature showing that a 0.5-1.5-mm recession must be expected on a majority of implants, 87% of their cases showed facial soft tissue stability or gain, while recessions (13% of the sites) were never greater than 0.5 mm. These results remained stable from the time of placement of the definitive restoration to 12, 18, and 24 months, suggesting that using inwardly narrowed transmucosal profiles for implant components allows for more predictable soft tissue stability in aesthetic areas than divergent profiles.
The hypothesis is that the positive soft tissue behavior with the particular transmucosal design evaluated in the present study is linked to a combination of three primary factors. First, the circumferential macrogroove creates a void chamber in which a blood clot forms and that provides space for soft tissue regeneration. The result is a nonsurgical, localized thickening of the soft tissues. Second, the highly curved profile allows increased soft tissue-to-implant interface length, facilitating a biological seal of 3 mm despite a shorter crown-to-implant distance. Third, after maturation of the soft tissues, a ring-like seal (Figure 11-1) is created that could stabilize the connective tissue adhesion and functionally mimic the effect of Sharpey’s fibers at teeth (Figure 11-2).