Rational management of soft peri-implant tissues

Introduction

Although the method of attachment of an osseointegrated implant is, by definition, quite different from that of a natural tooth, the situation which exists between the peri-implant mucosa and the superficial periodontal tissues is sufficiently analogous for us to consider that the conditions required to maintain peri-implant health are the same as those for periodontal health. These analogies involve the nature of the soft tissues as much as the aetiology and pathogenesis of bacteria-induced inflammatory diseases which, progressing apically, can compromise the prognosis of a functioning implant in the same way as it does a tooth. The aim of this article is to examine these analogies and, from experience gained from treating periodontal diseases, to suggest a rational approach to peri-implant mucosal problems.

Nature of the peri-implant mucosa

The nature of the soft tissues surrounding the attachment of an osseointegrated titanium implant has been the subject of several histological studies in both man and animals. In a preliminary study on dogs, ^{Berglundh et al. (1991)} sought to compare the structures of the peri-implant mucosa with those of the gingiva. They demonstrated that the two tissues had microscopic features in common. They both have a keratinised epithelium in continuity with a junctional epithelium which is approximately 2 mm long. This junctional epithelium is itself separated from alveolar bone by a zone of connective tissue approximately 1 mm wide.

The main difference lies in the composition of this supra-crestal connective tissue. The peri-implant connective tissue more closely resembles that of a scar tissue with fewer fibroblasts and more collagen. The major difference involves the orientation of the collagen fibres which, instead of being inserted perpendicularly into cementum, are directed parallel to the titanium surface. Other studies, comparing the soft tissues in relationship to the various surface finishes of the implant attachments and according to whether surgery was undertaken in two stages or one (^{Abrahamsson et al., 1996}, 1997), have shown that the existence of this attachment apparatus, comprising a junctional epithelium and a zone of connective tissue, is a constant feature which can provide a protection for osseointegration.

Assessment of the dimensions of this peri-implant mucosal attachment was the object of another study on dogs (^{Berglundh and Lindhe, 1996}), the conclusions of which recalled the concept, commonly expressed in periodontology, of incompressible biological space (^{Gargiulo et al., 1961}). According to this study, the peri-implant biological space is approximately 3 mm. Encroachment into this space, from the time the implant is exposed, will lead to bone loss after 6 months healing.

Role of the peri-implant mucosa

Secondary implant failures, involving osseointegrated implants in function, are due to marginal inflammation, mechanical overload or to a combination of the two (^{Tonetti and Schmid, 1994}). The term mucositis has been proposed to describe the reversible inflammatory reaction of the peri-implant soft tissues and the term peri-implantitis to define the process of infection which leads to the progressive loss of bone in an apical direction around an implant in function.

Numerous experimental studies have sought to establish a parallel between peri-implant diseases and periodontal diseases. In a study undertaken in dogs, ^{Berglundh et al. (1992)}, in comparing inflammatory infiltrates, have found that the initial host response to bacterial plaque is the same around implants and around teeth. In an attempt to confirm the aetiological role of bacterial plaque in causing alterations to the peri-implant soft tissues in man, ^{Pontoriero et al. (1994)} used the experimental gingivitis protocol of ^{Löe et al. (1965)}. In a study using dogs, using ligatures to induce experimental periodontitis, ^{Lindhe et al. (1992)} showed that for the same degree of exposure to infection, the clinical and radiographic signs of tissue destruction were more pronounced around the implants than around teeth and that the lesion extends as far as the medullary bone around the implants, whereas around the teeth, there were intact gingival fibres separating bone from the subgingival environment.

The clinical implications of these experimental studies leads us now to believe that the success of implant treatment lies, as in periodontology, in the effective control of bacterial plaque which in turn is facilitated by a favourable tissue morphology. There is no scientific data to indicate that the height of the keratinised peri-implant mucosa influences the prognosis of osseointegrated implants (^{Schou et al., 1992}). From the reports of the most authoritative retrospective long term studies, one can even say that the presence of keratinised tissue is not necessary for the maintenance of functional implants (^{Adell et al., 1981} ; ^{Albrektsson et al., 1986}).

In a clinical evaluation of the health of soft tissues around 141 functional Brånemark implants, ^{Wennström et al. (1994)} showed that the presence of keratinised mucosa had no influence on plaque control or the presence of inflammation determined by bleeding on probing (^{fig. 1}). The conclusions from this study reflect those of periodontal studies on the role that keratinised gingiva plays in the maintenance of gingival health (^{Lang and Löe, 1972} ; ^{Wennström, 1987}).

Nevertheless, the multiplicity of indications for implant therapy in partially edentulous cases and the necessity, for aesthetic reasons of concealing the margins of the titanium prosthesis may call these principles into question and justify the need to increase the height of keratinised mucosa. In fact, we know that the clinical consequences of inflammation due to a prosthetic restoration are not the same, depending on the nature of the marginal tissues. In a study on dogs ^{Wennström and Lindhe (1983)} showed that plaque induced inflammation around implants induced hyperplasia where there was keratinised gingiva but recession in the absence of gingiva. Clinically, a hyperplastic reaction is less likely to compromise the aesthetic result and seems more likely to be reversible than a recession which is extending to involve the deeper tissues.

In a study of experimental peri-implantitis in monkeys, ^{Warrer et al. (1995)} showed that an absence of keratinised mucosa around implants increased the susceptibility of the peri-implant tissues to recession and loss of attachment. According to ^{Listgarten et al. (1992)}, placing implants in an area of mobile non-keratinised mucosa could not only influence the orientation of the collagen fibres of the supra-crestal connective tissue but also facilitate rupture of the peri-implant epithelial attachment.

The need to ensure maximum stability at the boundaries of the mucosal margins encourages us, in implantology as in conventional dentistry, to prefer an adequate height of keratinised mucosa. But, in order for it to play an effective role in providing a stable barrier, this keratinised mucosa must be attached to the underlying bone. Clinical experience shows that those sites, where there is an absence of keratinised mucosa combined with a peri-implant bone dehiscence, are particularly susceptible to the development of rapid mucosal recession.

For empirical reasons and with reference to the principles expressed for pre-prosthetic periodontal surgery (^{Maynard and Wilson, 1979}), one can consider that the ideal clinical situation is that which provides a height of keratinised peri-implant mucosa of at least 5 mm which ensures 3 mm attached and 2 mm free mucosa.

Increasing the height of the keratinised mucosa

Surgical techniques for increasing the height of attached keratinised mucosa around implants are indicated in order to ensure stability of the marginal tissues as well as to eliminate the risk of recession or loss of attachment (^{fig. 2a} et ^2b).

These techniques can also be useful to correct unfavourable anatomical situations, to eliminate frenal pull or to deepen the vestibular sulcus, all of which have the aim of facilitating plaque control and thus eliminating the risk of marginal inflammation. However, in the majority of cases the lack of keratinised mucosa can be avoided by carefully selecting the line of incision at the time of fitting the implants or even by preliminary preparation of the site with a gingival graft.

In the case of implants which are buried (using the two stage operating technique), the need to extend the period of burial throughout the whole of the osseointegration period, often leads to a reduction in vestibular depth and tissue contraction with an associated reduction in keratinised mucosa.

The preparation of the peri-implant soft tissues is undertaken at the time of the second operation, when the implants are exposed. Here again, the choice of the lines of incision is a determining factor and one must be constantly aware of the need to preserve an adequate amount of keratinised mucosa around the implant.

In order to place the required tissues in position, a partial thickness apically repositioned flap can effectively be used at the time of exposure of the implants (^{fig. 3}, ^3b, ^3c, ^3d and ^3e). In the most unfavourable cases, a free gingival graft from the palate can be used either at the time of exposure of the implants or later (^{fig. 4}, ^4b, ^4c, ^4d and ^4e).

Problems with the peri-implant mucosa involve the lingual surfaces as much as the buccal surfaces in both the mandible and the maxilla (^{fig. 5}, ^5b, ^5c, ^5d and ^5e). Equally, they involve the posterior segments where access for tooth cleaning is difficult and the anterior regions where stability of the margins is essential in order to ensure an aesthetic result. As in periodontology, these surgical techniques cannot be satisfactorily undertaken until after soft tissue inflammation has been effectively brought under control.

The choice of operative technique depends above all on the amount of tissue available in the area and its quality, but in addition, it depends on the accessibility for surgery in the area concerned. The clinical results speak for themselves but up to the present time there have been no studies to confirm the reliability of these techniques over the long term, nor their efficacy in maintaining implants in function.

Conclusion

As in the case of natural teeth supporting fixed prostheses, the height of keratinised mucosa around osseointegrated implants is important to facilitate plaque control, assist the maintenance of soft tissue health and ensure the stability of the tissue margins. Nowadays, we can consider that the indications for increasing the height of peri-implant keratinised mucosa are the same as those in periodontology. As to the surgical techniques currently in use, they are inspired mainly by muco-gingival surgical techniques, the advantages and disadvantages of which are well known. Free gingival grafts from the palate are an easy way to increase the height of keratinised mucosa around exposed implants. Nevertheless, in the majority of cases, this treatment for the peri-implant soft tissues, which imposes an extra surgical procedure on the patient, can be avoided by taking care to preserve the available keratinised mucosa and to position it correctly at the time of fitting the implants and during their exposure.

BIBLIOGRAPHIE

• ABRAHAMSSON I, BERGLUNDH T, WENNSTRÖM J, LINDHE J. The peri-implant hard and solft tissues characteristics at different implant systems. A comparative study in dogs. Clin Oral Implant Res 1996;7:212-220.
• ADELL R, LEKHOLM U, ROCKLER B, BRÅNEMARK PI. A 15-years study of osseointegrated implants in the treatment of edentulous jaw. Int J Oral Surg 1981;6:387-399.
• ALBREKTSSON T, ZARB G, WORTHINGTON P, ERIKSSON RA. The long-term efficacy of currently used dental implants : A review and proposed criteria of success. In J Oral Maxillofac Implant 1986;1:11-25.
• BERGLUNDH T, LINDHE J, ERICSSON I, MARINELLO CP, LILJENBERG B, THOMSEN P. The soft tissue barrier at implants and teeth. Clin Oral Implant Res 1991;2:81-90.
• BERGLUNDH T, LINDHE J, MARINELLO C, ERICSSON I, LILJENBERG B. Soft tissue reaction to de novo plaque formation on implants and teeth. An experimental study in the dog. Clin Oral Implant Res 1992;3:1-8.
• BERGLUNDH T, LINDHE J. Dimension of peri-implant mucosa. Biological width revisited. J Clin Periodontol 1996;23:971-973.
• GARGIULO AW, WENTZ F, ORBAN B. Dimensions and relations of the dento-gingival junction in humans. J Periodontol 1961;32:261.
• LANG NP, LÖE H. The relationship between the width of keratinized gingiva and gingival health. J Periodontol 1972;43:623-627.
• LINDHE J, BERGLUNDH T, ERICSSON I, LILJENBERG B, MARINELLO C. Experimental breakdown of peri-implant and periodontal tissues. Clin Oral Implant Res 1992;3:9-16.
• LISTGARTEN MA, LANG HP, SCHROEDER HE, SCHROEDER A. Periodontal tissues and their counterparts around endosseous implants. Clin Oral Implant Res 1992;2:1-19.
• LÖE H, THEILADE E, JENSEN SB. Experimental gingivitis in man. J Periodontol 1965;36:177-187.
• MAYNARD JG, WILSON RD. Physiologic dimensions of the periodontium significant to the restorative dentist. J Periodontol 1979;50:170-179.
• PONTORIERO R, TONELLI MP, CARNEVALE G, MOMBELLI A, NYMAN SR, LANG NP. Experimental induced peri-implant mucositis. A clinical study in humans. Clin Oral Implant Res 1994;5:254-259.
• SCHOU S, HOLMSTRUP P, HJORTING-HANSEN E, LANG NP. Plaque-induced marginal tissue reactions of osseointegrated oral implants : a review of the literature. Clin Oral Implant Res 1992;3:149-161.
• TONETTI MS, SCHMID J. Pathogenesis of implant failures. Periodontology 2000 1994;3:127-138.
• WARRER K, BUSER D, LANG NP, KARRING T. Plaque-induced peri-implantitis in the presence or absence of keratinized mucosa. An experimental study in monkeys. Clin Oral Implant Res 1995;6:131-138.
• WENNSTRÖM JL, LINDHE J. Plaque-induced gingival inflammation in the absence of attached gingiva in dogs. J Clin Periodontol 1983;10:266-276.
• WENNSTRÖM JL. Lack of association between width of attached gingiva and development of soft tissue recession. A 5-year longitudinal study. J Clin Periodontol 1987;14:181-184.
• WENNSTRÖM JL, BENGAZI F, LEKHOLM U. The influence of the masticatory mucosa on the peri-implant soft tissue condition. Clin Oral Implant Res 1994;5:1-8.