July/August 2013, Volume 34, Issue 7
Published by AEGIS Communications
Peri-Implant and Periodontal Tissues: A Review of Differences and Similarities
The health and vitality of an osseointegrated implant depends on the surrounding supporting tissues, which not only anchor the implant to the bone but also have the important function of providing a protective seal. The aim of this article is to provide a basic understanding of differences and similarities between the periodontal and peri-implant tissues at the histologic, clinical, and immunologic levels; it is essential to know these differences and similarities during the clinical handling of these similar-looking tissues. The comparative features are of clinical relevance because it is critical to understand the behavior of the soft tissue found around the tooth and implant. This knowledge is vital from the preliminary stage of treatment planning through prosthetic rehabilitation.
The functional usefulness of oral implants lies in the fact that piercing the gingival or oral mucosa of the oral cavity establishes a transmucosal connection between the external environment and the inner dental implant. The term osseointegration refers to the direct bone contact to the alloplastic metallic implant. Titanium, which has excellent biocompatibility properties in physiologic conditions, has been the most commonly used biometal for implants.1 The soft tissue around the implant, ie, peri-implant mucosa, is similar in many ways to the gingiva found around the tooth. The aim of this review article is to highlight the clinical, biochemical, histologic, and other features of the two similar-looking tissues—the gingival and peri-implant mucosa—which also exhibit several areas of dissimilarity.
Peri-implant mucosa is composed of well-keratinized oral epithelium, sulcular epithelium, and junctional epithelium, as well as underlying connective tissue. Between the implant surface and the epithelial cells are hemidesmosomes and basal lamina.2 The soft-tissue interface is made up of the epithelium and the underlying connective tissue, which includes the biologic zone known as the “biologic width,” referring to the height of the dentogingival attachment apparatus encircling the tooth. The term “biologic width” is based on the work of Gargiulo et al, who described the dimensions of the dentogingival junction in human cadavers.3 The average dimension of 2.04 mm (1.07 mm + 0.97 mm) is comprised of supra-alveolar connective tissue and junctional epithelial attachment. Functionally, in a clinical sense, there must not be any encroachment within 2 mm of the bone that surrounds the tooth. That a similar relationship of bone to overlying soft tissues exists around implants and changes in this relationship may be one of the reasons for the early crestal bone loss.4
The proliferative capacity of the junctional epithelium leads to the rapid migration of the epithelial cells as soon as the fibrin clot/granulation tissue starts forming at the implant installation. Once the cells reach the implant surface, their attachment occurs rapidly through the basal lamina and the hemidesmosomes.5 Another possible attachment modality hypothesized is an indirect epithelium-to-implant contact.6 The peri-implant sulcus shares the structural, ultrastructural, and functional characteristics with the gingival tissues. Human studies have demonstrated that epithelium surrounding dental implants possesses similar patterns of differentiation and function to gingival tissues.7 The presence of granulation tissue adhering to the surface of the transmucosal components is considered the principal factor that stops the epithelium from migrating down apically.8 Berglundh speculated that the reason the epithelium does not migrate down apically is likely due to the interaction between the titanium and the soft tissue.9
Connective tissue adhesion of the healing wounds involves the following: formation and adhesion of the fibrin clot to the implant surface; adsorption of the fibrin clot to the implant surface; adsorption of the extracellular matrix (ECM) proteins and connective tissue cells to the implant surface; transformation of the clot into granulation tissue; and migration of epithelial cells on top of the fibrin clot/granulation tissue.10 The connective tissue zone next to the implant surface is primarily divided into two parts. The first is a 50-µm inner zone that is rich in fibers; resembling scar tissue, several scattered fibroblasts in close contact with the titanium surface maintain the seal between the peri-implant bone and the oral environment.11,12 The remaining part of the connective tissue comprises fibers running in different directions, along with the cellular elements and blood vessels.11 Connective tissue cells and the collagen fiber bundles are separated from the TiO2 surface with a 20-nm-wide proteoglycan layer.13 Table 1 presents the salient features of similarity and dissimilarity between the peri-implant and periodontal tissues.9,11,14-37
Periodontal probing is one of the basic diagnostic tools used to measure clinical attachment level (CAL), pocket depth, and width of the attached gingiva.38 The probing depth is the distance between the gingival margin and the depth of the probe tip penetration into the pocket.39 Increased probing depth and loss of clinical attachment are pathognomonic of periodontal disease.40 Peri-implant probing provides an assessment of different parameters such as bleeding on probing, suppuration, and exudation from the sulcus and peri-implant tissues.37 Studies have shown that, when used, probe pressure of 0.5 N penetrates an average of 0.7 mm deeper at implant sites.41 Clinical probing depth is higher around implants versus teeth, as the probe tip ends apically to the junctional epithelium into the connective tissue close to the bone crest.42 Bleeding on probing is a more reliable sign of inflammation around a tooth but is less reliable around implants. Probing depth penetration around teeth has been found to be < 3 mm as opposed to 2.5 mm to 4 mm around implants.
In natural teeth, the nonkeratinized junctional epithelium attaches to the enamel surface via the internal basal lamina and desmosomes along the entire length of the junctional epithelium; however, the attachment of the peri-implant epithelium to the implant surface is confined to the apical region only. Fibers run a parallel course to the implant surface, as observed in human subjects.17 Yet several other authors have found fibers to be running in different directions. A perpendicular direction was also found with implants harboring porous surfaces.37,43 The orientation seems to be dependent on the quality of the mucosa, which tend to be parallel in alveolar mucosa and perpendicularly directed in keratinized mucosa. Fibers are perpendicularly inserted into the cementum around the tooth. Apart from the orientation of the fibers, there exists a significant difference between the connective tissue around the tooth and abutment. The dentogingival collagen fibers are firmly inserted into the cementum and the bone and in a perpendicular or oblique direction, thus serving as a barrier to the epithelial migration and the impending bacterial invasion.44 The connective tissue adhesion with implants has a poor mechanical resistance as compared to the natural tooth.25
There appears to be a resilient connection between bone, periodontal ligament, and cementum around a tooth. However, a rigid connection appears in the form of functional ankylosis/osseointegration due to the lack of periodontal ligament around the implant. Absence of resiliency somewhat leads to the direct transmission of the loads to the bone–implant interface, and no compensatory tooth movements can accommodate the occlusal disharmony. The lack of periodontal ligament also precludes the use of implants in growing individuals. The highly sensitive receptors present within the periodontal ligament are responsible for the propioceptive and tactile sensitivity around the tooth. Absence of the periodontal ligament leads to reduced tactile sensation and reflex function around implants.15 The adaptive capacity of the periodontal ligament allows the tooth movements, but the orthodontic movements cannot be undertaken with implants.
Diagnostic criteria for detection of peri-implant health and for monitoring the progression of disease are similar to that for periodontal disease. The gingival/mucosal tissues constitute the primary defense mechanism against microbial infections. The conversion of the junctional epithelium to the pocket epithelium is considered to be the key to the progression of gingivitis/peri-mucositis to periodontitis/peri-implantitis. When performing visual inspection of peri-implant soft tissue, signs of disease include color alteration, swelling, thickness, and bleeding on probing, all clinical indices used for the evaluation of gingival disease. Inflammatory lesions may be present in the absence of the visual signs of inflammation. The peri-implant crevice is surgically created and is not developed as it is for natural teeth. Pocket depth is determined by many factors such as abutment height, depth of fixture countersinking at stage 1 surgery, and the amount of tissue thinning during stage 2 surgery.11 Structural differences between the peri-implant and periodontal tissue dictate the probing pattern around the implants as well. The parallel disposition of the collagen fibers to the implant surface and the absence of the connective tissue insertion cause the probe to go beyond the epithelial seal and results in injury to the connective tissue.45
Sulcular fluid around the gingiva is called gingival crevicular fluid (GCF), and that which is around the implant is known as peri-implant sulcus fluid (PISF). Gingival crevicular fluid is a healthy serum transudate in a healthy free gingiva, and during inflammation GCF is converted into an inflammatory exudate originating from the vessels of the gingival plexus and is recognized as apart of the gingival defense system. GCF is rich in leucocytes, especially polymorphonuclear leukocytes (PMN), and is attracted by a chemotactic gradient of bacterial or host origin. It is also rich in host-derived molecules from blood as well as substances from microorganisms of the dental plaque. The GCF flow requires permeability-induced initiators of inflammation. About 65 different infection-induced enzymes and their inhibitors and regulators have been found.32
PISF is an inflammatory exudate originating from the vessels of the gingival plexus and is similar to GCF. It contains the host-derived enzymes and their inhibitors and host-response modifiers and some tissue breakdown products. PISF volume, along with the increased enzymatic activity, has been suggested to be elevated during inflammation, which confirms the diagnostic potential of PISF in peri-implant inflammation. Table 2 summarizes the gingival crevicular fluid and peri-implant sulcular fluid components.32
GCF functions to continuously flush the dentogingival crevice and release antimicrobial components of serum such as antibodies and complement enzymes. In disease, the crevicular fluid flow increases 30 times more than in health.
The biologic inflammatory response of the tissues around the tooth and implant depend largely on their histologic framework. Implants contain a dense network of collagen fibers that originate from the alveolar bone crest to the gingival margin in a parallel fashion, in contrast to teeth, where the fibers are perpendicular. The fibers in implants appear very large and follow a circular arrangement around the implant neck. Fiber-to-metal surface contact has generally not been observed. There are studies, however, that have observed direct fibrous attachment to the titanium surface.25 The length of the supra-alveolar connective tissue in implants is also significantly larger than that of teeth. Teeth have multiple collagen bundle fibers that run in various directions to various adjacent structures. Studies based on the response of the tooth and implants to experimental breakdown have revealed the differences in the nature of the breakdown. Ligature-assisted subgingival plaque formation inducing the periodontal and peri-implant lesion formation in beagle dogs revealed more pronounced clinical and radiographic signs of destruction around implants than teeth. Furthermore, the size of the soft-tissue lesion was found to be larger around the implants than teeth and extended into the bone marrow.33 Yet another study described the host-response results of longstanding plaque and gingivitis and revealed an inflammatory cell infiltrate that extended more apical into the peri-implant mucosa (~ 1.5 mm) than the gingiva (~ 0.9 mm).24
Histomorphometric studies have revealed that implants and teeth have a comparable ratio of collagen, vessels, and plasma cells, whereas implants have lower proportions of lymphocytes, macrophages, and PMNs. Hence, implants render a weak biologic barrier to prevent the apical migration of inflammatory cells compared to teeth.21 Revealing results were demonstrated in a study to show the effects of the microbial response on the inflammatory markers myeloperoxidase (MPO) and nitrite in healthy and diseased teeth and implant sites. MPO and nitrite levels were stable in the GCF at healthy and diseased sites, whereas the PISF levels were found to be raised with MPO and nitrite levels.46
When exposed in the oral cavity through the transmucosal abutment, an osseointegrated implant provides a favorable surface for bacterial colonization. This further leads to the selective adsorption of the salivary proteins, peptides, etc, and rapid formation of the pellicle.24 Biofilm formation around the implant is similar to that formed around teeth.47 The composition of the pellicle formed around implants lacks the low molecular mucins commonly found on the enamel in natural teeth, which may lead to the qualitative difference in the early biofilm formation around the implant. This possibly contributes to the low plaque formation around implants.48 However, these differences do not seem to influence the bacterial composition of the early biofilms formed on the implant surface. Biofilm formation on the implant is influenced by the properties of the surface to be colonized, including chemical composition, surface roughness, and surface free energy.49
Many studies have pointed out the comparative rates and the composition of the microbiota associated with health and disease as associated with teeth and implants.50-52 Classic differences in the microbial profile of the peri-implant flora in certain in-vitro studies reveal an affinity of Staphylococcus aureus for the titanium surface, but it is not a common microflora around teeth.30 A host response to the bacterial challenge is known to develop irrespective of the implant system,53 while the initial host response to the bacterial challenge in the peri-implant mucosa is similar to that found in the gingiva. However, the longstanding inflammation does have a more pronounced response in the peri-implant tissues than in gingiva, leading to the significant apical extension of the inflammatory infiltrate in the mucosa and increased size of the lesion as compared to the gingival.47 The Sixth European Workshop on Periodontology 2008 defines peri-implant diseases as inflammatory lesions that develop in the tissues around the implant and consisting of two entities: peri-implant mucositis and peri-implantitis. Peri-implant mucositis is the reversible inflammatory reaction in the soft tissues surrounding the functioning implant, whereas peri-implantitis is defined as the inflammation in the mucosa characterized by loss of supporting bone around an implant in function.54
Histopathologic data of the human case series have described the inflammatory lesions as comprising the B cells and plasma cells, suggesting that peri-implantitis and periodontitis lesions are similar.55,56 Despite the fact that peri-implantitis and periodontitis develop similarly, the dynamics of this process could be different. Because the periodontitis lesion is walled off by the intact supracrestal connective tissue fiber compartment, the penetration of the infiltrates into the bone marrow is generally not evident. However, because the peri-implantitis lesion progresses without the presence of the connective tissue compartment, it often progresses rapidly into the marrow.46,57 Periodontitis and peri-implantitis share common risk factors, such as poor oral hygiene, tobacco consumption, and diabetes mellitus. Cross-sectional analyses have evaluated the risk indicators for peri-implantitis to be poor oral hygiene, history of periodontitis, tobacco consumption, diabetes mellitus, alcohol consumption, and genetic traits.58
Microflora Around Implants
The microbiota on implants in edentulous and partially edentulous patients and in patients with a history of periodontal disease varies. Studies have stated that the microbiota obtained from colonizing clinically healthy implant fixtures in fully edentulous subjects are similar to the microbiota associated with healthy periodontal sites in periodontally healthy subjects.59 It was suggested that extraction of all teeth results in elimination of the Porphromonas gingivalis and Aggregatibacter actinomycetemcomitans from the oral microbiota.60
In partially edentulous subjects the developing microbiota around implants is similar to that of naturally occurring teeth.61 This microflora—85% of which are identified as gram-positive cocci—inhabit immediately after installation of the implant. Microbial colonization and the ensuing inflammatory reaction in the peri-implant tissues might be analogous to the key events in the pathogenesis of periodontitis. The literature comparing the microbiota around implants in fully edentulous and partially edentulous mouths stated a higher percentage and frequency of the black pigment bacteroids, fewer coccoids and motile rods, and high frequency of the P gingivalis and P intermedia on implant surfaces in partially edentulous subjects.62,63 The microbiota of the remaining teeth serve as the primary source of the putative pathogens. This reveals that the microbial state of the remaining teeth influences the fate of the newly incorporated implants.64 Microbiota on implants in subjects with a history of periodontal disease are similar in nature to those found in the periodontal pockets around teeth.65 It would seem likely that susceptibility to periodontitis may translate to peri-implantitis. Several reviews have reported a history of treated periodontitis as a risk indicator for implant outcomes with statistically significant results.66-68
The healing response of the tissues around implants varies from that of the natural tooth.69 Implants exhibit a poor vascular supply compared to teeth. Following implant insertion, tissue repair requires development of the vasculature at the site of injury for the delivery of oxygen and nutrients and the removal of cell debris for a complete healing process.70 Berglundh reported that implants placed following flap elevation resulted in a poor vascular supply between the junctional epithelium and marginal bone.9 Ericcson explained that the poor vascular supply in the peri-implant mucosa may be the reason for the extensive progression of plaque-associated inflammation.24
Mucoperiosteal flap elevation results in postoperative bone resorption.71 The amount of the tissue injury is known to influence the speed and quality of healing.72 Small, clean, and closed wounds heal more quickly with little scar formation, whereas large wounds heal slowly and with significant scarring. Flapless surgery perhaps has the added benefit of providing a better vascular supply and retaining the vitality of the supracrestal connective tissue around the implant compared to raised soft-tissue flaps, which may inadvertently lead to cutting and damaging the supraperiosteal vessels, which apparently are the sole source of blood supply around implants.22 The surrounding mucosa after the flapless procedure has smaller, cleaner, and more closed wounds than the flap procedure. The flapless procedure preserves the connective tissue vascularization when no flaps are reflected. The supracrestal connective tissue lateral to the implant surface is supplied by the branches of the supraperiosteal vessels. When soft-tissue flaps are reflected, the branches of the supraperiosteal vessels can be cut or damaged.
Due to the similar etiologies for periodontitis and peri-implant infections, the therapeutic approach also appears to be similar—ie, anti-infective. Periodontal treatment and the long-term results are promising, as compared to implants.73 Since existing periodontal lesions can become a reservoir of pathogens to colonize implant surface, it is imperative that the periodontitis be successfully treated and controlled before implant placement. Periodontal treatment involves the debridement of the contaminated root surfaces, and the treatment of peri-implantitis focuses on the decontamination of the implant surface. Despite the surface roughness and configuration, decontamination of the titanium surface poses inherent problems and can probably not be achieved by debridement alone. Animal studies have demonstrated that there is no superiority of one decontamination protocol versus the other.74
Periodontitis is the main cause of tooth loss in adults. Hence, it is assumed that a greater number of patients receiving implants have a history of periodontal disease. As in cases of periodontitis, peri-implant infections take several years to develop. The pathogenesis of the two diseases depends on the presence of biofilm-containing pathogens. The microbiota in periodontitis primarily comprises gram-negative bacteria; however, increasing evidence suggests that S aureus may be an important pathogen in the initiation of some cases of peri-implantitis.53 The subgingival microflora is initially derived from the supragingival plaque and becomes more anaerobic as the oxygen pressure is reduced. Microbiota associated with both healthy and failing implants are similar to those observed in both healthy and diseased periodontium around teeth. The indigenous oral bacteria on the remaining teeth serve as the reservoir for colonization on the implant surface, which explains the similarity of the biofilm composition around the teeth and the implant in the same individual.65
A more pronounced inflammatory response is expressed in peri-implant mucosal tissues than in the dentogingival unit because of the structural differences of the tissues (vascularity and fibroblast-to-collagen ratios). Periodontal probing is one of the diagnostic tools used to measure pocket depth, clinical attachment level, gingival marginal location, and the width of gingiva. Peri-implant probing depth seems to be related to the thickness and type of the mucosa circumscribing the abutment. Alveolar mucosa is generally associated with deeper probing depths, whereas a keratinized collar around the abutment is usually accompanied by shallower depths.75 The pocket depth around an implant is determined by several factors: abutment height, depth of the fixture countersinking at stage 1 surgery, and amount of the tissue thinning at the stage 2 surgical procedure.11 The surface texture irregularities, shape of the implant, and configuration of the restoration may influence the path of the probe tip.76 Peri-implant probing is more sensitive to force variation than periodontal probing. Conventional probing of 0.25 N does not damage the peri-implant tissues.58
Decontamination of the implant surface located either in a submucosal or under surgical access represents the most pertinent challenge for the predictable treatment outcomes.35 Substantial literature correlates the opportunistic infective nature of periodontitis and peri-implantitis and the possible similarities and dissimilarities.77 Hence, future studies should aim at nonsurgical modalities for treatment of peri-implantitis, ie, decontamination, antibiotics, etc. The probable association between the risk indicators needs to be explored further.
ABOUT THE AUTHORS
Sangeeta Dhir, BDS, MDS
Professor, Department of Periodontics & Implantology, Sudha Rustagi College of Dental Sciences and Research, Faridabad, Haryana, India
Lanka Mahesh, BDS, MDS
Private Practice, New Delhi, India
Gregori M. Kurtzman, DDS, MAGD
Private Practice, Silver Spring, Maryland
KL Vandana, BDS, MDS
Professor, Department of Periodontics, College of Dental Sciences, Davangere, Karnataka, India
1. Räisänen L, Könönen M, Juhanoja J, et al. Expression of the cell adhesion complexes in epithelial cells seeded on the biomaterial surfaces. J Biomed Mater Res. 2000;49(1):79-87.
2. James RA, Schultz RL. Hemidesmosomes and the adhesion of the junctional epithelial cells to metal implants—a prelimnary report. Oral Implantol. 1974;4(3):294-302.
3. Gargiulo AW, Wentz FM, Orban B. Dimensions and relations of the dentogingival junction in humans. J Periodontol. 1961;32(3):261-267.
4. Oh TJ, Yoon J, Misch CE, Wang HL. The causes of early implant bone loss: myth or science? J Periodontol. 2002;73(3):322-333.
5. Listgarten MA, Lai CH. Ultrastructure of the intact interface between an endosseous epoxy resin dental implant and the host tissues. J Biol Buccale. 1975;3(1):13-28.
6. Kawahara H, Kawahara D, Mimura Y, et al. Morphologic studies on the biologic seal of titanium dental implants. Report II. In vivo study on the defending mechanism of epithelial adhesion/attachment against invasive factors. Int J Oral Maxillofac Implants.1998;13(4):465-473.
7. Liljenberg B, Gualini F, Berglundh T, et al. Some characteristics of the ridge mucosa before and after implant installation. A prospective study in humans. J Clin Periodontol. 1996;23(11):1008-1013.
8. Listgarten MA. Soft and hard tissue response to endosseous implants. Anat Rec. 1996;245(2):410-425.
9. Berglundh T, Lindhe J, Ericcson I, et al. The soft tissue barrier at implants and teeth. Clin Oral Implant Res.1991;2(2):81-90.
10. Meyle J. Cell adhesion and spreading on different implant surfaces. In: Lang N, Lindhe J, Karring T, eds. Proceedings of the 3rd European Workshop on Periodontology. Berlin, Germany: Quintessence Publishing; 1999:55-72.
11. Buser D, Weber HP. Soft tissue reactions to non-submerged unloaded titanium implants in beagle dogs. J Periodontol. 1992;63(3):225-235.
12. Abrahamsson I, Berglundh T, Wennström J, Lindhe J. The peri-implant hard and soft tissues at different implant systems. A comparative study in the dog. Clin Oral Implants Res. 1996;7(3):212-219.
13. Hansson HA , Albrektsson T, Brånemark P. Structural aspects of the interface between tissue and titanium implants. J Prosthet Dent. 1983;50(1):108-113.
14. Lindhe J, Meyle J. Peri-implant diseases: Consesnsus Report of the sixth European Workshop on Periodontology. J Clin Periodontol. 2008;35(8 suppl):282-285.
15. Jacobs R, van Steenberghe D. Role of periodontal ligament receptors in the tactile function of teeth: a review. J Periodontal Res. 1994;29(3):153-167.
16. Atsuta I, Yamaza T, Yoshinara M, et al. Changes in the distribution of laminin-5 during peri-implant epithelium formation after immediate titanium implantation in rats. Biomaterials. 2005;26(14):1751-1760.
17. Ericcsson I, Lindhe J. Probing depth at implants and teeth. An experimental study in the dog. J Clin Periodontol.1993;20(9):623-627.
18. Cochran DL, Hermann JS, Schenk RK, et al. Biologic width around titanium implants. A histometric analysis of the implant-gingival junction around unloaded and loaded nonsubmerged implants in the canine mandible. J Periodontol. 1997;68(2):186-198.
19. Ramfjord SP. Indices for prevalence and incidence of periodontal disease. J Periodontol. 1959;30:51-59.
20. Romanos GE, Schröter-Kermani C, Weingart D, Strub JR. Health human periodontal versus peri-implant gingival tissues: an immunohistochemical differentiation of the extracellular matrix. Int J Oral Maxillofac Implants. 1995;10(6):750-758.
21. Ericsson I, Berglundh T, Marinello C, et al. Long-standing plaque and gingivitis at implants and teeth in the dog. Clin Oral Implants Res. 1992;3(3):99-103.
22. Berglundh T, Lindhe J, Jonsson K, Ericsson I. The topography of the vascular systems in the periodontal and the peri-implant tissues in the dog. J Clin Periodontol. 1994;21(3):189-193.
23. Salcetti JM, Moriarty JD, Cooper LF, et al. The clinical, microbial, and host response characteristics of the failing implant. Int J Oral Maxillofac Implants. 1997;12(1):32-42.
24. Kohavi D, Klinger A, Steinberg D, Sela MN. Adsorption of the salivary proteins onto prosthetic titanium components. J Prosthet Dent. 1995;74(5):531-534.
25. Hermann JS, Buser D, Schenk RK, et al. Biologic width around one- and two-piece titanium implants. Clin Oral Implants Res. 2001;12(6):559-571.
26. Brånemark PI , Hansson BO, Adell R, et al. Osseointegrated implants in the treatment of the edentulous jaw. Experience from a 10-year period. Scand J Plast Reconstr Surg Suppl. 1977;16:1-132.
27. Ximénez-Fyvie LA, Haffajee AD, Socransky SS. Comparison of the microbiota of supra- and subgingival plaque in health and periodontitis. J Clin Periodontol. 2000;27(9): 648-657.
28. Shibli JA, Melo L, Ferrari DS, et al. Composition of the supra- and subgingival biofilm of subjects with healthy and diseased implants. Clin Oral Implants Res. 2008:19(10):975-982.
29. Slots J, Rams TE. New views on periodontal microbiota in special patient categories. J Clin Periodontol. 1991;18(6):411-420.
30. Renvert S, Lindhal C, Renvert H, Perrson GR. Clinical and microbiologic analysis of subjects treated with Brånemark and AstraTech implants: a 7-year follow-up study. Clin Oral Implants Res. 2008;19(4):342-347.
31. Pradeep AR, Karthikeyan BV. Peri-implant papilla reconstruction: realities and limitations. J Periodontol. 2006;77(3):534-544.
32. Armitage GC. Development of a classification system for periodontal diseases and conditions. Ann Periodontol. 1999;4(1):1-6.
33. Lindhe J, Berglundh T, Ericsson I, et al. Experimental breakdown of peri-implant and periodontal tissues. A study in the beagle dog. Clin Oral Implants Res. 1992;3(1):9-16.
34. Heitz-Mayfield LJ. Disease progression: identification of high-risk groups and individuals for periodntitis. J Clin Periodontol. 2005;32(6 suppl):196-209.
35. Heitz-Mayfield LJ, Lang NP. Comparative biology of chronic and aggressive periodontitis vs. peri-implantitis. Periodontol 2000. 2010;53:167-181.
36. Op Heij DG, Opdebeeck H, van Steenberghe D, Quirynen M. Age as compromising factor for implant insertion. Periodontol 2000. 2003;33:172-184.
37. Akagawa Y, Takata T, Matsumoto T, et al. Correlation between clinical and histological evaluations of the peri-implant gingiva around the single-crystal sapphire endosseous implant. J Oral Rehabil. 1989;16(6):581-587.
38. American Academy of Periodontology. Glossary of Periodontal Terms. 4th ed. Chicago, IL: American Academy of Periodontology; 2001.
39. Hermann F, Lerner H, Palti A. Factors influencing the preservation of the periimplant marginal bone. Implant Dent. 2007;16(2):165-175.
40. Chow YC, Wang HL. Factors and techniques influencing the peri-implant papillae. Implant Dent. 2010;19(3):208-219.
41. Armitage GC, Svanberg GK, Löe H. Microscopic evaluation of the clinical measurements of connective tissue attachment levels. J Clin Periodontol. 1977;4(3):173-190.
42. Mombelli A, Lang NP. Clinical parameters for evaluation of dental implants. Periodontol 2000. 1994;4:81-86.
43. Schroeder A, van der Zypen E, Stich H, Sutter F. The reactions of bone, connective tissue, and epithelium to endosteal implants with titanium-sprayed surfaces. J Maxillofac Surg. 1981;9(1):15-25.
44. Stern IB. Current concepts of the dentogingival junction: the epithelial and connective tissue attachments to the tooth. J Periodontol. 1981;52(9):465-476.
45. Ikeda H, Yamaza T, Yoshinari M, et al. Ultrastructural and immunoelectron microscopic studies of peri-implant epithelium-implant (Ti-6Al-4V) interface of rat maxilla. J Periodontol. 2000;71(6):961-973.
46. Tözüm TF, Akman AC, Yamalik N, et al. Analysis of the inflammatory process around endosseous dental implants and natural teeth: myeloperoxidase level and nitric oxide metabolism. Intl J Oral Maxillofac Implants. 2007;22(6):969-979.
47. Shibli JA, Melo L, Ferrari DS. Composition of supra- and subgingival biofilm of subjects with healthy and diseased implants. Clin Oral Implants Res. 2008;19(10):975-982.
48. Steinberg D, Klinger A, Kohavi D, Sela MN. Adsorption of the human salivary proteins to tianium powder. I. Adsorption of human salivary albumin. Biomaterials. 1995;16(17):1339-1343.
49. Teughels W, Van Assche N, Sliepen I, Quirynen M. Effect of material characteristics and/or surface topography on biofilm development. Clinl Oral Implants Res. 2006;17(2 suppl):68-81.
50. Agerbaek MR, Lang NP, Persson GR. Comparisons of bacterial patterns present at implant and tooth sites in subjects on supportive periodontal therapy. I. Impact of clinical variables, gender and smoking. Clin Oral Implants Res. 2006;17(1):18-24.
51. Pontoriero R, Tonelli MP, Carnevale G, et al. Experimentally induced peri-implant mucositis. A clinical study in humans. Clin Oral Implants Res. 1994;5(4):254-259.
52. Quirynen M, Listgarten MA. Distribution of the bacterial morphotypes around natural teeth and titanium implants ad modum Brånemark. Clin Oral Implants Res. 1990;1(1):8-12.
53. Abrahamsson I, Berglundh T, Lindhe J. Soft tissue response to plaque formation at different implant system. A comparative study in the dog. Clin Oral Implants Res. 1998;9(2):73-79.
54. Zitzmann NU, Berglundh T. Definition and prevalence of the peri-implant diseases. J Clin Periodontol. 2008;35(8 suppl):286-291.
55. Berglundh T, Gislason O, Lekholm U, et al. Histopathological observations of human periimplantitis lesions. J Clin Periodontol. 2004;31(5):341-347.
56. Gualini F, Berglundh T. Immunohistochemical characteristics of inflammatory lesions at implants. J Clin Periodontol. 2003;30(1):14-18.
57. Seymour GJ, Powell RN, Davies WI. The immunopathogenesis of progressive chronic inflammatory periodontal disease. J Oral Pathol. 1979;8(5):249-265.
58. Heitz-Mayfield LJ. Peri-implant diseases: diagnosis and risk indicators. J Clin Periodontol. 2008;35(8 suppl):292-304.
59. Socransky SS, Haffajee AD. Periodontal microbial ecology. Periodontol 2000. 2003;38:135-187.
60. Danser MM, van Winkelhoff AJ, van der Velden U. Periodontal bacteria colonizing oral mucous membranes in edentulous patients wearing dental implant. J Periodontol. 1997;68(3):209-216.
61. Mombelli A, Buser D, Lang NP. Colonization of the osseointegrated titanium implants in edentulous patients. Early results. Oral Microbiol Immunol. 1988;3(3):113-120.
62. Hultin M, Boström L, Gustafsson A. Neutrophil response and microbiological findings around teeth and dental implants. J Periodontol. 1998;69(12):1413-1418.
63. Kalykakis GK, Mojon P, Nisengard R, et al. Clinical and microbial findings on osseo-integrated implants; comparisons between partially dentate and edentulous subjects. Eur J Prosthodont Restor Dent. 1998;6(4):155-159.
64. 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 Periodontal Res. 1989;24(2):96-105.
65. Mombelli A, Marxer M, Gaberthüel T, et al. The microbiota of the osseointegrated implants in patients with a history of periodontal disease. J Clin Periodontol. 1995;22(2):124-130.
66. Karoussis IK, Kotsovilis S, Fourmousis I. A comprehensive and critical review of dental implant prognosis in periodontally compromised partially edentulous patients. Clin Oral Implants Res. 2007;18(6):669-679.
67. Roos-Jansåker AM, Renvert H, Lindahl C, Renvert S. Nine- to fourteen-year follow-up implant treatment. Part III: factors associated with peri-implant lesions. J Clin Periodontol. 2006;33(4):296-301.
68. Leonhardt A, Renvert S, Dahlén G. Microbial findings at failing implants. Clin Oral Implants Res. 1999;10(5):339-345.
69. Etter TH, Håkanson I, Lang NP, et al. Healing after standardized clinical probing of the peri-implant soft tissue seal: a histomorphometric study in dogs. Clin Oral Implants Res. 2002;13(6):571-580.
70. Arnold F, West DC. Angiogenesis in wound healing. Pharmacol Ther. 1991;52(3):407-422.
71. Wilderman MN, Pennel BM, King K, Barron JM. Histogenesis of repair following osseous surgery. J Periodontol. 1970;41(10):551-565.
72. Sabiston DC. Textbook of Surgery: The Biological Basis of Modern Surgical Practice. 15th ed. Philadelphia, PA: W.B. Saunders; 1997:207-220.
73. Lindhe J, Nyman S. Long-term maintenance of patients treated for advanced periodontal disease. J Clin Periodontol. 1984;11(8):504-514.
74. Schou S, Holmstrup P, Jørgensen T. Implant surface preparation in the surgical treatment of experimental peri-implantitis with autogenous bone graft and ePTFE membrane. Clin Oral Implants Res. 2003;14(4):412-422.
75. Atassi F. Periimplant probing: positives and negatives. Implant Dent. 2002;11(4):356-362.
76. Bauman GR, Mills M, Rapley JW, Hallmon WH. Clinical parameters of evaluation during implant maintenance. Int J Oral Maxillofac Implants. 1992;7(2):220–227.
77. Palacci P. Perio-Implant Soft Tissue Management. Chicago, IL: Quintessence Publishing; 2004.